From TgO/GABA-AT, GABA, and T-263 Mutant to Conception of Toxoplasma

Lykins, Joseph; Moschitto, Matthew J.; Zhou, Ying; Filippova, Ekaterina V.; Le, Hoang V.; Tomita, Tadakimi; Fox, Barbara A.; Bzik, David J.; Su, Chunlei; Rajagopala, Seesandra V.; Flores, Kristin; Spano, Furio; Woods, Stuart; Roberts, Craig W.; Hua, Cong; El Bissati, Kamal; Wheeler, Kelsey M.; Dovgin, Sarah; Muench, Stephen P.; McPhillie, Martin; Fishwick, Colin W.G.; Anderson, Wayne F.; Lee, Patricia J.; Hickman, Mark; Weiss, Louis M.; Dubey, Jitender P.; Lorenzi, Hernan A.; Silverman, Richard B.; McLeod, Rima L.

doi:10.1016/j.isci.2023.108477

From TgO/GABA-AT, GABA, and T-263 Mutant to Conception of Toxoplasma

Journal Article · Wed Nov 15 23:00:00 EST 2023 · iScience

DOI:https://doi.org/10.1016/j.isci.2023.108477· OSTI ID:2470129

Lykins, Joseph ^[1]; Moschitto, Matthew J. ^[2]; Zhou, Ying ^[3]; Filippova, Ekaterina V. ^[4]; Le, Hoang V. ^[5]; Tomita, Tadakimi ^[6]; Fox, Barbara A. ^[7]; Bzik, David J. ^[7]; Su, Chunlei ^[8]; Rajagopala, Seesandra V. ^[9]; Flores, Kristin ^[10]; Spano, Furio ^[11]; Woods, Stuart ^[12]; Roberts, Craig W. ^[12]; Hua, Cong ^[3]; El Bissati, Kamal ^[3]; Wheeler, Kelsey M. ^[13]; Dovgin, Sarah ^[14]; ^[15]; ^[15] more »

Univ. of Chicago, IL (United States); Boston Univ., MA (United States)
Northwestern Univ., Evanston, IL (United States); Rutgers Univ., Piscataway, NJ (United States)
Univ. of Chicago, IL (United States)
Northwestern Univ., Chicago, IL (United States); Univ. of Chicago, IL (United States)
Northwestern Univ., Evanston, IL (United States); National Institutes of Health (NIH), Bethesda, MD (United States)
Albert Einstein College of Medicine, Bronx, NY (United States)
Geisel School of Medicine at Dartmouth, Lebanon, NH (United States)
Univ. of Tennessee, Knoxville, TN (United States)
J. Craig Venter Institute, Inc., Rockville, MD (United States); Vanderbilt Univ., Nashville, TN (United States). Medical Center
Northwestern Univ., Chicago, IL (United States)
Istituto Superiore di Sanità, Rome (Italy)
Univ. of Strathclyde, Glasgow, Scotland (United Kingdom)
Univ. of Chicago, IL (United States); Massachusetts General Hospital, Boston, MA (United States)
Univ. of Chicago, IL (United States); Case Western Reserve Univ., Cleveland, OH (United States)
University of Leeds (United Kingdom)
Feinberg School of Medicine, Chicago, IL (United States); Northwestern Univ., Chicago, IL (United States)
Walter Reed Army Institute of Research, Silver Spring, MD (United States)
US Dept. of Agriculture (USDA), Beltsville, MD (United States). Agricultural Research Service (ARS)
J. Craig Venter Institute, Inc., Rockville, MD (United States)
Northwestern Univ., Evanston, IL (United States); Northwestern Univ., Chicago, IL (United States)

Toxoplasma gondii causes morbidity, mortality, and disseminates widely via cat sexual stages. Here, we find T. gondii ornithine aminotransferase (OAT) is conserved across phyla. We solve TgO/GABA-AT structures with bound inactivators at 1.55 Å and identify an inactivator selective for TgO/GABA-AT over human OAT and GABA-AT. However, abrogating TgO/GABA-AT genetically does not diminish replication, virulence, cyst-formation, or eliminate cat’s oocyst shedding. Increased sporozoite/merozoite TgO/GABA-AT expression led to our study of a mutagenized clone with oocyst formation blocked, arresting after forming male and female gametes, with “Rosetta stone”-like mutations in genes expressed in merozoites. Mutations are similar to those in organisms from plants to mammals, causing defects in conception and zygote formation, affecting merozoite capacitation, pH/ionicity/sodium-GABA concentrations, drawing attention to cyclic AMP/PKA, and genes enhancing energy or substrate formation in TgO/GABA-AT-related-pathways. These candidates potentially influence merozoite’s capacity to make gametes that fuse to become zygotes, thereby contaminating environments and causing disease.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 2470129

Journal Information:: iScience, Journal Name: iScience Journal Issue: 1 Vol. 27; ISSN 2589-0042

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (218)

Ornithine Aminotransferase versus GABA Aminotransferase: Implications for the Design of New Anticancer Drugs: ORNITHINE AMINOTRANSFERASE VS. GABA AMINOTRANSFERASE Lee, Hyunbeom; Juncosa, Jose I.; Silverman, Richard B. Medicinal Research Reviews, Vol. 35, Issue 2 https://doi.org/10.1002/med.21328	journal	August 2014
Crystal structure of human recombinant ornithine aminotransferase Shen, Betty W.; Hennig, Michael; Hohenester, Erhard Journal of Molecular Biology, Vol. 277, Issue 1 https://doi.org/10.1006/jmbi.1997.1583	journal	March 1998
Crystal structure of human ornithine aminotransferase complexed with the highly specific and potent inhibitor 5-fluoromethylornithine 1 1 1Edited by R. Huber Storici, Paola; Capitani, Guido; Müller, Rita Journal of Molecular Biology, Vol. 285, Issue 1 https://doi.org/10.1006/jmbi.1998.2289	journal	January 1999
Crystal structures of Toxoplasma gondii adenosine kinase reveal a novel catalytic mechanism and prodrug binding Schumacher, Maria A.; Scott, Daniel M.; Mathews, Iripam I. Journal of Molecular Biology, Vol. 298, Issue 5 https://doi.org/10.1006/jmbi.2000.3753	journal	May 2000
Differential expression of two plant-like enolases with distinct enzymatic and antigenic properties during stage conversion of the protozoan parasite Toxoplasma gondii Dzierszinski, Florence; Mortuaire, Marlene; Dendouga, Najoua Journal of Molecular Biology, Vol. 309, Issue 5 https://doi.org/10.1006/jmbi.2001.4730	journal	June 2001
Sorghum mitochondrial orf25 and a related chimeric configuration of a male-sterile cytoplasm Van Tang, Hoang; Pring, Daryl R.; Muza, Figuhr R. Current Genetics, Vol. 29, Issue 3 https://doi.org/10.1007/BF02221557	journal	February 1996
Malaria parasites utilize two essential plasma membrane fusogens for gamete fertilization Kumar, Sudhir; Valansi, Clari; Haile, Meseret T. Cellular and Molecular Life Sciences, Vol. 79, Issue 11 https://doi.org/10.1007/s00018-022-04583-w	journal	October 2022
Evolution of Plant-Like Crystalline Storage Polysaccharide in the Protozoan Parasite Toxoplasma gondii Argues for a Red Alga Ancestry Coppin, Alexandra; Varr�, Jean-St�phane; Lienard, Luc Journal of Molecular Evolution, Vol. 60, Issue 2 https://doi.org/10.1007/s00239-004-0185-6	journal	February 2005
The SLC6 transporters: perspectives on structure, functions, regulation, and models for transporter dysfunction Rudnick, Gary; Krämer, Reinhard; Blakely, Randy D. Pflügers Archiv - European Journal of Physiology, Vol. 466, Issue 1 https://doi.org/10.1007/s00424-013-1410-1	journal	December 2013
Transposable elements in Coffea (Gentianales: Rubiacea) transcripts and their role in the origin of protein diversity in flowering plants Lopes, Fabrício Ramon; Carazzolle, Marcelo Falsarella; Pereira, Gonçalo Amarante Guimarães Molecular Genetics and Genomics, Vol. 279, Issue 4 https://doi.org/10.1007/s00438-008-0319-4	journal	January 2008
Sperm DNA integrity assays: diagnostic and prognostic challenges and implications in management of infertility Shamsi, Monis Bilal; Imam, Syed Nazar; Dada, Rima Journal of Assisted Reproduction and Genetics, Vol. 28, Issue 11 https://doi.org/10.1007/s10815-011-9631-8	journal	September 2011
Single nucleotide polymorphism rs527236194 of the cytochrome B gene (MT-CYB) is associated with alterations in sperm parameters Gromenko, Yulia Yu.; Galimov, Kamil S.; Gilyazova, Irina R. Molecular Biology Reports, Vol. 50, Issue 12 https://doi.org/10.1007/s11033-023-08849-9	journal	November 2023
Male sterility systems in wheat and opportunities for hybrid wheat development Singh, Sudhir P.; Srivastava, Rakesh; Kumar, Jitendra Acta Physiologiae Plantarum, Vol. 37, Issue 1 https://doi.org/10.1007/s11738-014-1713-7	journal	November 2014
MYB transcription factor genes as regulators for plant responses: an overview Ambawat, Supriya; Sharma, Poonam; Yadav, Neelam R. Physiology and Molecular Biology of Plants, Vol. 19, Issue 3 https://doi.org/10.1007/s12298-013-0179-1	journal	April 2013
Management of Congenital Toxoplasmosis McLeod, Rima; Lykins, Joseph; Gwendolyn Noble, A. Current Pediatrics Reports, Vol. 2, Issue 3 https://doi.org/10.1007/s40124-014-0055-7	journal	July 2014
Building Programs to Eradicate Toxoplasmosis Part I: Introduction and Overview Felín, Mariangela Soberón; Wang, Kanix; Moreira, Aliya Current Pediatrics Reports, Vol. 10, Issue 3 https://doi.org/10.1007/s40124-022-00269-w	journal	August 2022
Toxoplasma gondii: Isolation and preliminary characterization of temperature-sensitive mutants Pfefferkorn, E. R.; Pfefferkorn, Lorraine G. Experimental Parasitology, Vol. 39, Issue 3 https://doi.org/10.1016/0014-4894(76)90040-0	journal	June 1976
Toxoplasma gondii: The enzymic defect of a mutant resistant to 5-fluorodeoxyuridine Pfefferkorn, E. R. Experimental Parasitology, Vol. 44, Issue 1 https://doi.org/10.1016/0014-4894(78)90077-2	journal	February 1978
Toxoplasma gondii: Genetic crosses reveal phenotypic suppression of hydroxyurea resistance by fluorodeoxyuridine resistance Pfefferkorn, E. R.; Kasper, Lloyd H. Experimental Parasitology, Vol. 55, Issue 2 https://doi.org/10.1016/0014-4894(83)90015-2	journal	April 1983
[10] Mechanism-based enzyme inactivators Silverman, Richard B. Methods in Enzymology, Vol. 249, p. 240-283 https://doi.org/10.1016/0076-6879(95)49038-8	book	January 1995
A Drosophila model for xeroderma pigmentosum and Cockayne's syndrome: haywire encodes the fly homolog of ERCC3, a human excision repair gene Mounkes, Leslie C.; Jones, Richard S.; Liang, Bee-Choo Cell, Vol. 71, Issue 6 https://doi.org/10.1016/0092-8674(92)90389-T	journal	December 1992
The effect of methionine on the accumulation of ornithine by chinese hamster cells in culture Baich, A. Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 756, Issue 2 https://doi.org/10.1016/0304-4165(83)90097-1	journal	March 1983
Alteration of synaptic membrane cholesterol/phospholipid ratio using a lipid transfer protein. Effect on gamma-aminobutyric acid uptake. North, P.; Fleischer, S. Journal of Biological Chemistry, Vol. 258, Issue 2 https://doi.org/10.1016/S0021-9258(18)33185-5	journal	January 1983
Characterization of the ornithine aminotransferase from Plasmodium falciparum Gafan, Colin; Wilson, Judith; Berger, Louise C. Molecular and Biochemical Parasitology, Vol. 118, Issue 1 https://doi.org/10.1016/S0166-6851(01)00357-7	journal	November 2001
Surprising similarities in structure comparison Gibrat, Jean-Francois; Madej, Thomas; Bryant, Stephen H. Current Opinion in Structural Biology, Vol. 6, Issue 3 https://doi.org/10.1016/S0959-440X(96)80058-3	journal	June 1996
Isolation and characterization of the product of inactivation of γ-aminobutyric acid aminotransferase by gabaculine Fu, Mengmeng; Silverman, Richard B. Bioorganic & Medicinal Chemistry, Vol. 7, Issue 8 https://doi.org/10.1016/S0968-0896(99)00081-4	journal	August 1999
Human ornithine aminotransferase complexed with L-canaline and gabaculine: structural basis for substrate recognition Shah, Sapan A.; Shen, Betty W.; Brünger, Axel T. Structure, Vol. 5, Issue 8 https://doi.org/10.1016/S0969-2126(97)00258-X	journal	August 1997
Structure of Escherichia coli ribokinase in complex with ribose and dinucleotide determined to 1.8 å resolution: insights into a new family of kinase structures Sigrell, Jill A.; Cameron, Alexander D.; Jones, T. Alwyn Structure, Vol. 6, Issue 2 https://doi.org/10.1016/S0969-2126(98)00020-3	journal	February 1998
The molecular basis of cytoplasmic male sterility and fertility restoration Schnable, P. Trends in Plant Science, Vol. 3, Issue 5 https://doi.org/10.1016/S1360-1385(98)01235-7	journal	May 1998
Targeting polyamines of parasitic protozoa in chemotherapy Müller, Sylke; Coombs, Graham H.; Walter, Rolf D. Trends in Parasitology, Vol. 17, Issue 5 https://doi.org/10.1016/S1471-4922(01)01908-0	journal	May 2001
Toxoplasma gondii and sex: essential or optional extra? Ferguson, David J. P. Trends in Parasitology, Vol. 18, Issue 8 https://doi.org/10.1016/S1471-4922(02)02330-9	journal	August 2002
Mutations in TTC29, Encoding an Evolutionarily Conserved Axonemal Protein, Result in Asthenozoospermia and Male Infertility Lorès, Patrick; Dacheux, Denis; Kherraf, Zine-Eddine The American Journal of Human Genetics, Vol. 105, Issue 6 https://doi.org/10.1016/j.ajhg.2019.10.007	journal	December 2019
Bi-allelic Mutations in TTC29 Cause Male Subfertility with Asthenoteratospermia in Humans and Mice Liu, Chunyu; He, Xiaojin; Liu, Wangjie The American Journal of Human Genetics, Vol. 105, Issue 6 https://doi.org/10.1016/j.ajhg.2019.10.010	journal	December 2019
PKA, PP1, and DC1 phosphorylation mediate alcohol-induced ciliary dysfunction in Chlamydomonas reinhardtii Yang, Fan; Scarbrough, Chasity; Sisson, Joseph H. Alcohol, Vol. 75 https://doi.org/10.1016/j.alcohol.2018.05.001	journal	March 2019
Central role of soluble adenylyl cyclase and cAMP in sperm physiology Buffone, Mariano G.; Wertheimer, Eva V.; Visconti, Pablo E. Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, Vol. 1842, Issue 12 https://doi.org/10.1016/j.bbadis.2014.07.013	journal	December 2014
CRISPR/Cas9-Derived Mutations Both Inhibit HIV-1 Replication and Accelerate Viral Escape Wang, Zhen; Pan, Qinghua; Gendron, Patrick Cell Reports, Vol. 15, Issue 3 https://doi.org/10.1016/j.celrep.2016.03.042	journal	April 2016
Mitochondrial Metabolism of Glucose and Glutamine Is Required for Intracellular Growth of Toxoplasma gondii MacRae, James I.; Sheiner, Lilach; Nahid, Amsha Cell Host & Microbe, Vol. 12, Issue 5 https://doi.org/10.1016/j.chom.2012.09.013	journal	November 2012
A case report on the efficacy of vigabatrin analogue (1 S , 3 S )-3-amino-4-difluoromethylenyl-1-cyclopentanoic acid (CPP-115) in a patient with infantile spasms Doumlele, Kyra; Conway, Erin; Hedlund, Julie Epilepsy & Behavior Case Reports, Vol. 6 https://doi.org/10.1016/j.ebcr.2016.08.002	journal	January 2016
Characterization and mutation analysis of the human FORMIN-2 (FMN2) gene in women with unexplained infertility Ryley, David A.; Wu, Hsin-Hung; Leader, Benjamin Fertility and Sterility, Vol. 83, Issue 5 https://doi.org/10.1016/j.fertnstert.2004.10.051	journal	May 2005
Redox Regulation of Plasmodium falciparum Ornithine δ-Aminotransferase Jortzik, Esther; Fritz-Wolf, Karin; Sturm, Nicole Journal of Molecular Biology, Vol. 402, Issue 2 https://doi.org/10.1016/j.jmb.2010.07.039	journal	September 2010
TSS-seq of Toxoplasma gondii sporozoites revealed a novel motif in stage-specific promoters Kidaka, Taishi; Sugi, Tatsuki; Hayashida, Kyoko Infection, Genetics and Evolution, Vol. 98 https://doi.org/10.1016/j.meegid.2022.105213	journal	March 2022
Development of dual fluorescent stage specific reporter strain of Toxoplasma gondii to follow tachyzoite and bradyzoite development in vitro and in vivo Paredes-Santos, T. C.; Tomita, T.; Yan Fen, M. Microbes and Infection, Vol. 18, Issue 1 https://doi.org/10.1016/j.micinf.2015.09.016	journal	January 2016
Transcriptional ups and downs: patterns of gene expression in the life cycle of Toxoplasma gondii Sharma, Janak; Rodriguez, Paula; Roy, Proyasha Microbes and Infection, Vol. 22, Issue 10 https://doi.org/10.1016/j.micinf.2020.09.001	journal	November 2020
Improved techniques for endogenous epitope tagging and gene deletion in Toxoplasma gondii Upadhya, Rajendra; Kim, Kami; Hogue-Angeletti, Ruth Journal of Microbiological Methods, Vol. 85, Issue 2 https://doi.org/10.1016/j.mimet.2011.02.001	journal	May 2011
Genome-scale protein expression and structural biology of Plasmodium falciparum and related Apicomplexan organisms Vedadi, Masoud; Lew, Jocelyne; Artz, Jennifer Molecular and Biochemical Parasitology, Vol. 151, Issue 1 https://doi.org/10.1016/j.molbiopara.2006.10.011	journal	January 2007
Structure of the Hsp110:Hsc70 Nucleotide Exchange Machine Schuermann, Jonathan P.; Jiang, Jianwen; Cuellar, Jorge Molecular Cell, Vol. 31, Issue 2 https://doi.org/10.1016/j.molcel.2008.05.006	journal	July 2008
Spontaneous cystogenesis in vitro of a Brazilian strain of Toxoplasma gondii Paredes-Santos, T. C.; Martins-Duarte, E. S.; Vitor, R. W. A. Parasitology International, Vol. 62, Issue 2 https://doi.org/10.1016/j.parint.2012.12.003	journal	April 2013
Commit and Transmit: Molecular Players in Plasmodium Sexual Development and Zygote Differentiation Guttery, David S.; Roques, Magali; Holder, Anthony A. Trends in Parasitology, Vol. 31, Issue 12 https://doi.org/10.1016/j.pt.2015.08.002	journal	December 2015
Spermatogenesis, DNA damage and DNA repair mechanisms in male infertility Gunes, Sezgin; Al-Sadaan, Maha; Agarwal, Ashok Reproductive BioMedicine Online, Vol. 31, Issue 3 https://doi.org/10.1016/j.rbmo.2015.06.010	journal	September 2015
Ras-related proteins (Rab) play significant roles in sperm motility and capacitation status Bae, Jeong-Won; Yi, Jun Koo; Jeong, Eun-Ju Reproductive Biology, Vol. 22, Issue 2 https://doi.org/10.1016/j.repbio.2022.100617	journal	June 2022
Increasing the structural coverage of tuberculosis drug targets Baugh, Loren; Phan, Isabelle; Begley, Darren W. Tuberculosis, Vol. 95, Issue 2 https://doi.org/10.1016/j.tube.2014.12.003	journal	March 2015
Unexpected oocyst shedding by cats fed Toxoplasma gondii tachyzoites: In vivo stage conversion and strain variation Dubey, J. P. Veterinary Parasitology, Vol. 133, Issue 4 https://doi.org/10.1016/j.vetpar.2005.06.007	journal	November 2005
Schizogony and gametogony of oocyst-deficient T-263 strain of Toxoplasma gondii Dubey, J. P. Veterinary Parasitology, Vol. 245 https://doi.org/10.1016/j.vetpar.2017.05.024	journal	October 2017
All about toxoplasmosis in cats: the last decade Dubey, J. P.; Cerqueira-Cézar, C. K.; Murata, F. H. A. Veterinary Parasitology, Vol. 283 https://doi.org/10.1016/j.vetpar.2020.109145	journal	July 2020
Cul4A is essential for spermatogenesis and male fertility Kopanja, Dragana; Roy, Nilotpal; Stoyanova, Tanya Developmental Biology, Vol. 352, Issue 2 https://doi.org/10.1016/j.ydbio.2011.01.028	journal	April 2011
SLC6 family transporter SNF-10 is required for protease-mediated activation of sperm motility in C. elegans Fenker, Kristin E.; Hansen, Angela A.; Chong, Conrad A. Developmental Biology, Vol. 393, Issue 1 https://doi.org/10.1016/j.ydbio.2014.06.001	journal	September 2014
Type I and type II fatty acid biosynthesis inEimeria tenella: enoyl reductase activity and structure Lu, J. Z.; Muench, S. P.; Allary, M. Parasitology, Vol. 134, Issue 14 https://doi.org/10.1017/S0031182007003319	journal	August 2007
Moving towards an integrated approach to molecular detection and identification ofToxoplasma gondii Su, C.; Shwab, E. K.; Zhou, P. Parasitology, Vol. 137, Issue 1 https://doi.org/10.1017/S0031182009991065	journal	September 2009
Suppression of Hepatocellular Carcinoma by Inhibition of Overexpressed Ornithine Aminotransferase Zigmond, Ehud; Ya’acov, Ami Ben; Lee, Hyunbeom ACS Medicinal Chemistry Letters, Vol. 6, Issue 8 https://doi.org/10.1021/acsmedchemlett.5b00153	journal	June 2015
Mechanism of the irreversible inhibition of γ-aminobutyric acid-α-ketoglutaric acid transaminase by the neurotoxin gabaculine Rando, R. R. Biochemistry, Vol. 16, Issue 21 https://doi.org/10.1021/bi00640a012	journal	October 1977
Membrane Cholesterol Modulates Serotonin Transporter Activity ^† Scanlon, Siobhan M.; Williams, D. Clive; Schloss, Patrick Biochemistry, Vol. 40, Issue 35 https://doi.org/10.1021/bi010730z	journal	September 2001
Crystal Structures of Unbound and Aminooxyacetate-Bound Escherichia coli γ-Aminobutyrate Aminotransferase ^† Liu, Wenshe; Peterson, Peter E.; Carter, Richard J. Biochemistry, Vol. 43, Issue 34 https://doi.org/10.1021/bi049218e	journal	August 2004
Mechanisms of Inactivation of γ-Aminobutyric Acid Aminotransferase by 4-Amino-5-fluoro-5-hexenoic Acid Silverman, Richard B.; Bichler, Katherine A.; Leon, Andrew J. Journal of the American Chemical Society, Vol. 118, Issue 6 https://doi.org/10.1021/ja9527885	journal	January 1996
Design and Mechanism of Tetrahydrothiophene-Based γ-Aminobutyric Acid Aminotransferase Inactivators Le, Hoang V.; Hawker, Dustin D.; Wu, Rui Journal of the American Chemical Society, Vol. 137, Issue 13 https://doi.org/10.1021/jacs.5b01155	journal	March 2015
Design and Mechanism of ( S )-3-Amino-4-(difluoromethylenyl)cyclopent-1-ene-1-carboxylic Acid, a Highly Potent γ-Aminobutyric Acid Aminotransferase Inactivator for the Treatment of Addiction Juncosa, Jose I.; Takaya, Kenji; Le, Hoang V. Journal of the American Chemical Society, Vol. 140, Issue 6 https://doi.org/10.1021/jacs.7b10965	journal	January 2018
Mechanism of Inactivation of Ornithine Aminotransferase by (1 S ,3 S )-3-Amino-4-(hexafluoropropan-2-ylidenyl)cyclopentane-1-carboxylic Acid Moschitto, Matthew J.; Doubleday, Peter F.; Catlin, Daniel S. Journal of the American Chemical Society, Vol. 141, Issue 27 https://doi.org/10.1021/jacs.9b03254	journal	June 2019
Fluorinated Conformationally Restricted γ-Aminobutyric Acid Aminotransferase Inhibitors Lu, Hejun; Silverman, Richard B. Journal of Medicinal Chemistry, Vol. 49, Issue 25 https://doi.org/10.1021/jm0608715	journal	November 2006
The 2011 E. B. Hershberg Award for Important Discoveries in Medicinally Active Substances: (1 S ,3 S )-3-Amino-4-difluoromethylenyl-1-cyclopentanoic Acid (CPP-115), a GABA Aminotransferase Inactivator and New Treatment for Drug Addiction and Infantile Spasms Silverman, Richard B. Journal of Medicinal Chemistry, Vol. 55, Issue 2 https://doi.org/10.1021/jm201650r	journal	January 2012
X-ray structure of dopamine transporter elucidates antidepressant mechanism Penmatsa, Aravind; Wang, Kevin H.; Gouaux, Eric Nature, Vol. 503, Issue 7474 https://doi.org/10.1038/nature12533	journal	September 2013
Formin-2, polyploidy, hypofertility and positioning of the meiotic spindle in mouse oocytes Leader, Benjamin; Lim, Hyunjung; Carabatsos, Mary Jo Nature Cell Biology, Vol. 4, Issue 12 https://doi.org/10.1038/ncb880	journal	November 2002
Local admixture of amplified and diversified secreted pathogenesis determinants shapes mosaic Toxoplasma gondii genomes Lorenzi, Hernan; Khan, Asis; Behnke, Michael S. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms10147	journal	January 2016
Genome sequencing sheds light on emerging drug resistance in malaria parasites Neafsey, Daniel E. Nature Genetics, Vol. 45, Issue 6 https://doi.org/10.1038/ng.2648	journal	May 2013
Mutations at the mitochondrial DNA polymerase (POLG) locus associated with male infertility Rovio, Anja T.; Marchington, David R.; Donat, Susanne Nature Genetics, Vol. 29, Issue 3 https://doi.org/10.1038/ng759	journal	October 2001
Fiji: an open-source platform for biological-image analysis Schindelin, Johannes; Arganda-Carreras, Ignacio; Frise, Erwin Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2019	journal	June 2012
Genomic-scale prioritization of drug targets: the TDR Targets database Agüero, Fernán; Al-Lazikani, Bissan; Aslett, Martin Nature Reviews Drug Discovery, Vol. 7, Issue 11 https://doi.org/10.1038/nrd2684	journal	October 2008
The resurgence of covalent drugs Singh, Juswinder; Petter, Russell C.; Baillie, Thomas A. Nature Reviews Drug Discovery, Vol. 10, Issue 4 https://doi.org/10.1038/nrd3410	journal	April 2011
Rare mutations in the complement regulatory gene CSMD1 are associated with male and female infertility Lee, Arthur S.; Rusch, Jannette; Lima, Ana C. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12522-w	journal	October 2019
The genetic basis of sex determination in grapes Massonnet, Mélanie; Cochetel, Noé; Minio, Andrea Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-16700-z	journal	June 2020
A unique Toxoplasma gondii haplotype accompanied the global expansion of cats Galal, Lokman; Ariey, Frédéric; Gouilh, Meriadeg Ar Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-33556-7	journal	October 2022
A MORC-driven transcriptional switch controls Toxoplasma developmental trajectories and sexual commitment Farhat, Dayana C.; Swale, Christopher; Dard, Céline Nature Microbiology, Vol. 5, Issue 4 https://doi.org/10.1038/s41564-020-0674-4	journal	February 2020
An experimental genetically attenuated live vaccine to prevent transmission of Toxoplasma gondii by cats Ramakrishnan, Chandra; Maier, Simone; Walker, Robert A. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-018-37671-8	journal	February 2019
New paradigms for understanding and step changes in treating active and chronic, persistent apicomplexan infections McPhillie, Martin; Zhou, Ying; El Bissati, Kamal Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep29179	journal	July 2016
Unique substrate specificity of ornithine aminotransferase from Toxoplasma gondii Astegno, Alessandra; Maresi, Elena; Bertoldi, Mariarita Biochemical Journal, Vol. 474, Issue 6 https://doi.org/10.1042/BCJ20161021	journal	March 2017
Polyamine homoeostasis as a drug target in pathogenic protozoa: peculiarities and possibilities Birkholtz, Lyn-Marie; Williams, Marni; Niemand, Jandeli Biochemical Journal, Vol. 438, Issue 2 https://doi.org/10.1042/BJ20110362	journal	August 2011
Novel signalling mechanism and clinical applications of sperm-specific PLCζ Nomikos, Michail Biochemical Society Transactions, Vol. 43, Issue 3 https://doi.org/10.1042/BST20140291	journal	June 2015
Mechanism of Pyrimethamine-Induced Megaloblastosis in Human Bone Marrow Waxman, Samuel; Herbert, Victor New England Journal of Medicine, Vol. 280, Issue 24 https://doi.org/10.1056/NEJM196906122802402	journal	June 1969
In silico activity profiling reveals the mechanism of action of antimalarials discovered in a high-throughput screen Plouffe, David; Brinker, Achim; McNamara, Case Proceedings of the National Academy of Sciences, Vol. 105, Issue 26 https://doi.org/10.1073/pnas.0802982105	journal	June 2008
Globally diverse Toxoplasma gondii isolates comprise six major clades originating from a small number of distinct ancestral lineages Su, Chunlei; Khan, Asis; Zhou, Peng Proceedings of the National Academy of Sciences, Vol. 109, Issue 15 https://doi.org/10.1073/pnas.1203190109	journal	March 2012
Formation of interference-sensitive meiotic cross-overs requires sufficient DNA leading-strand elongation Huang, Jiyue; Cheng, Zhihao; Wang, Cong Proceedings of the National Academy of Sciences, Vol. 112, Issue 40 https://doi.org/10.1073/pnas.1507165112	journal	September 2015
Structures of the cGMP-dependent protein kinase in malaria parasites reveal a unique structural relay mechanism for activation El Bakkouri, Majida; Kouidmi, Imène; Wernimont, Amy K. Proceedings of the National Academy of Sciences, Vol. 116, Issue 28 https://doi.org/10.1073/pnas.1905558116	journal	June 2019
Gyrate atrophy of the choroid and retina: deficiency of ornithine aminotransferase in transformed lymphocytes. Valle, D.; Kaiser-Kupfer, M. I.; Del Valle, L. A. Proceedings of the National Academy of Sciences, Vol. 74, Issue 11 https://doi.org/10.1073/pnas.74.11.5159	journal	November 1977
Targeted gene disruption of Hsp70-2 results in failed meiosis, germ cell apoptosis, and male infertility. Dix, D. J.; Allen, J. W.; Collins, B. W. Proceedings of the National Academy of Sciences, Vol. 93, Issue 8 https://doi.org/10.1073/pnas.93.8.3264	journal	April 1996
The Protozoan Parasite Toxoplasma gondii Expresses Two Functional Plant-like Glycolytic Enzymes: IMPLICATIONS FOR EVOLUTIONARY ORIGIN OF APICOMPLEXANS Dzierszinski, Florence; Popescu, Octavian; Toursel, Catherine Journal of Biological Chemistry, Vol. 274, Issue 35 https://doi.org/10.1074/jbc.274.35.24888	journal	August 1999
Membrane Cholesterol Modulates the Outward Facing Conformation of the Dopamine Transporter and Alters Cocaine Binding Hong, Weimin C.; Amara, Susan G. Journal of Biological Chemistry, Vol. 285, Issue 42 https://doi.org/10.1074/jbc.M110.150565	journal	October 2010
Essential Role of the EF-hand Domain in Targeting Sperm Phospholipase Cζ to Membrane Phosphatidylinositol 4,5-Bisphosphate (PIP2) Nomikos, Michail; Sanders, Jessica R.; Parthimos, Dimitris Journal of Biological Chemistry, Vol. 290, Issue 49 https://doi.org/10.1074/jbc.M115.658443	journal	December 2015
Determinants of Substrate Specificity in ω-Aminotransferases Markova, Michaela; Peneff, Caroline; Hewlins, Michael J. E. Journal of Biological Chemistry, Vol. 280, Issue 43 https://doi.org/10.1074/jbc.M506977200	journal	August 2005
Modification of Crocodile Spermatozoa Refutes the Tenet That Post-testicular Sperm Maturation Is Restricted To Mammals* Nixon, Brett; Johnston, Stephen D.; Skerrett-Byrne, David A. Molecular & Cellular Proteomics, Vol. 18 https://doi.org/10.1074/mcp.RA118.000904	journal	March 2019
Activation of GABA_AReceptor/Cl⁻Channel and Capacitation in Rat Spermatozoa: HCO₃⁻and Cl⁻are Essential Jin, Jian-Yuan; Chen, Wen-Ying; Zhou, Cheng Xi Systems Biology in Reproductive Medicine, Vol. 55, Issue 2-3 https://doi.org/10.1080/19396360802626648	journal	January 2009
SNF-10 connects male-derived signals to the onset of sperm motility inC. elegans Fenker, Kristin E.; Stanfield, Gillian M. Worm, Vol. 4, Issue 1 https://doi.org/10.1080/21624054.2014.1003002	journal	January 2015
Drosophila Cappuccino alleles provide insight into formin mechanism and role in oogenesis Yoo, Haneul; Roth-Johnson, Elizabeth A.; Bor, Batbileg Molecular Biology of the Cell, Vol. 26, Issue 10 https://doi.org/10.1091/mbc.E14-11-1558	journal	May 2015
Unrecognized Ingestion of Toxoplasma gondii Oocysts Leads to Congenital Toxoplasmosis and Causes Epidemics in North America Boyer, K.; Hill, D.; Mui, E. Clinical Infectious Diseases, Vol. 53, Issue 11 https://doi.org/10.1093/cid/cir667	journal	October 2011
Adverse Cutaneous Reactions to Pyrimethamine/Sulfadiazine and Pyrimethamine/Clindamycin in Patients with AIDS and Toxoplasmic Encephalitis Caumes, E.; Bocquet, H.; Guermonprez, G. Clinical Infectious Diseases, Vol. 21, Issue 3 https://doi.org/10.1093/clinids/21.3.656	journal	September 1995
Cytoplasmic Male Sterility-Associated Chimeric Open Reading Frames Identified by Mitochondrial Genome Sequencing of Four Cajanus Genotypes Tuteja, R.; Saxena, R. K.; Davila, J. DNA Research, Vol. 20, Issue 5 https://doi.org/10.1093/dnares/dst025	journal	June 2013
Frequent polymorphism of the mitochondrial DNA polymerase gamma gene (POLG) in patients with normal spermiograms and unexplained subfertility Jensen, M. Human Reproduction, Vol. 19, Issue 1 https://doi.org/10.1093/humrep/deh038	journal	January 2004
Hyper-osmotic condition enhances protein tyrosine phosphorylation and zona pellucida binding capacity of human sperm Liu, D. Y.; Clarke, G. N.; Baker, H. W. G. Human Reproduction, Vol. 21, Issue 3 https://doi.org/10.1093/humrep/dei364	journal	October 2005
Tyrosine phosphorylation on capacitated human sperm tail detected by immunofluorescence correlates strongly with sperm–zona pellucida (ZP) binding but not with the ZP-induced acrosome reaction Liu, D. Y.; Clarke, G. N.; Baker, H. W. G. Human Reproduction, Vol. 21, Issue 4 https://doi.org/10.1093/humrep/dei435	journal	January 2006
Hybrid breeding in wheat: technologies to improve hybrid wheat seed production Whitford, Ryan; Fleury, Delphine; Reif, Jochen C. Journal of Experimental Botany, Vol. 64, Issue 18 https://doi.org/10.1093/jxb/ert333	journal	October 2013
Functional disparity between human PAWP and PLCζ in the generation of Ca²⁺oscillations for oocyte activation Nomikos, Michail; Sanders, Jessica R.; Kashir, Junaid Molecular Human Reproduction, Vol. 21, Issue 9 https://doi.org/10.1093/molehr/gav034	journal	June 2015
Ligation-independent cloning of PCR products (LIC-PCR) Aslanidis, Charalampos; de Jong, Pieter J. Nucleic Acids Research, Vol. 18, Issue 20 https://doi.org/10.1093/nar/18.20.6069	journal	January 1990
ProFunc: a server for predicting protein function from 3D structure Laskowski, R. A.; Watson, J. D.; Thornton, J. M. Nucleic Acids Research, Vol. 33, Issue Web Server https://doi.org/10.1093/nar/gki414	journal	July 2005
A specific loop in human DNA polymerase mu allows switching between creative and DNA-instructed synthesis Juárez, Raquel; Ruiz, José F.; McElhinny, Stephanie A. Nick Nucleic Acids Research, Vol. 34, Issue 16 https://doi.org/10.1093/nar/gkl457	journal	September 2006
MolProbity: all-atom contacts and structure validation for proteins and nucleic acids Davis, I. W.; Leaver-Fay, A.; Chen, V. B. Nucleic Acids Research, Vol. 35, Issue Web Server https://doi.org/10.1093/nar/gkm216	journal	May 2007
Dali server: conservation mapping in 3D Holm, Liisa; Rosenstrï¿½m, Pï¿½ivi Nucleic Acids Research, Vol. 38, Issue suppl_2 https://doi.org/10.1093/nar/gkq366	journal	May 2010
TDR Targets: a chemogenomics resource for neglected diseases Magarinos, M. P.; Carmona, S. J.; Crowther, G. J. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1053	journal	November 2011
MMDB and VAST+: tracking structural similarities between macromolecular complexes Madej, Thomas; Lanczycki, Christopher J.; Zhang, Dachuan Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1208	journal	December 2013
Molecular dissection of complex agronomic traits of rice: a team effort by Chinese scientists in recent years Zuo, Jianru; Li, Jiayang National Science Review, Vol. 1, Issue 2 https://doi.org/10.1093/nsr/nwt004	journal	June 2014
Severe Sulfadiazine Hypersensitivity in a Child with Reactivated Congenital Toxoplasmic Chorioretinitis McLeod, Rima; Khan, Asif Rashid; Noble, Gwendolyn A. The Pediatric Infectious Disease Journal, Vol. 25, Issue 3 https://doi.org/10.1097/01.inf.0000202070.59190.9a	journal	March 2006
DNA mismatch repair and infertility Mukherjee, Sarmistha; Ridgeway, Alex D.; Lamb, Dolores J. Current Opinion in Urology, Vol. 20, Issue 6 https://doi.org/10.1097/MOU.0b013e32833f1c21	journal	November 2010
Origins of Eukaryotic Sexual Reproduction Goodenough, U.; Heitman, J. Cold Spring Harbor Perspectives in Biology, Vol. 6, Issue 3 https://doi.org/10.1101/cshperspect.a016154	journal	March 2014
The conserved plant sterility gene HAP2 functions after attachment of fusogenic membranes in Chlamydomonas and Plasmodium gametes Liu, Y.; Tewari, R.; Ning, J. Genes & Development, Vol. 22, Issue 8 https://doi.org/10.1101/gad.1656508	journal	March 2008
Assembly and Motility of Eukaryotic Cilia and Flagella. Lessons from Chlamydomonas reinhardtii Silflow, Carolyn D.; Lefebvre, Paul A. Plant Physiology, Vol. 127, Issue 4 https://doi.org/10.1104/pp.010807	journal	December 2001
A Phosphofructokinase B-Type Carbohydrate Kinase Family Protein, NARA5, for Massive Expressions of Plastid-Encoded Photosynthetic Genes in Arabidopsis Ogawa, Taro; Nishimura, Kenji; Aoki, Takehiko Plant Physiology, Vol. 151, Issue 1 https://doi.org/10.1104/pp.109.139683	journal	July 2009
Male Sterility in Maize after Transient Heat Stress during the Tetrad Stage of Pollen Development Begcy, Kevin; Nosenko, Tetyana; Zhou, Liang-Zi Plant Physiology, Vol. 181, Issue 2 https://doi.org/10.1104/pp.19.00707	journal	August 2019
Plus and Minus Sexual Agglutinins from Chlamydomonas reinhardtii Ferris, Patrick J.; Waffenschmidt, Sabine; Umen, James G. The Plant Cell, Vol. 17, Issue 2 https://doi.org/10.1105/tpc.104.028035	journal	February 2005
TLSMD web server for the generation of multi-group TLS models Painter, Jay; Merritt, Ethan A. Journal of Applied Crystallography, Vol. 39, Issue 1 https://doi.org/10.1107/S0021889805038987	journal	January 2006
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
Optimal description of a protein structure in terms of multiple groups undergoing TLS motion Painter, Jay; Merritt, Ethan A. Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 4 https://doi.org/10.1107/S0907444906005270	journal	March 2006
HKL -3000: the integration of data reduction and structure solution – from diffraction images to an initial model in minutes Minor, Wladek; Cymborowski, Marcin; Otwinowski, Zbyszek Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 8 https://doi.org/10.1107/S0907444906019949	journal	July 2006
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
REFMAC 5 for the refinement of macromolecular crystal structures Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911001314	journal	March 2011
Presenting your structures: the CCP 4 mg molecular-graphics software McNicholas, S.; Potterton, E.; Wilson, K. S. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911007281	journal	March 2011
Exogenous gamma‐aminobutyric acid addition enhances porcine sperm acrosome reaction Kurata, Shouhei; Umezu, Kohei; Takamori, Hironori Animal Science Journal, Vol. 93, Issue 1 https://doi.org/10.1111/asj.13744	journal	January 2022
A novel homozygous CFAP65 mutation in humans causes male infertility with multiple morphological abnormalities of the sperm flagella Zhang, Xueguang; Shen, Ying; Wang, Xiang Clinical Genetics, Vol. 96, Issue 6 https://doi.org/10.1111/cge.13644	journal	October 2019
Immunity against sexual stage Plasmodium falciparum and Plasmodium vivax parasites Jong, Roos M.; Tebeje, Surafel K.; Meerstein‐Kessel, Lisette Immunological Reviews, Vol. 293, Issue 1 https://doi.org/10.1111/imr.12828	journal	December 2019
Characterization of a novel organelle in Toxoplasma gondii with similar composition and function to the plant vacuole: Toxoplasma gondii plant-like vacuole Miranda, Kildare; Pace, Douglas A.; Cintron, Roxana Molecular Microbiology, Vol. 76, Issue 6 https://doi.org/10.1111/j.1365-2958.2010.07165.x	journal	April 2010
Aminotransferases: demonstration of homology and division into evolutionary subgroups Mehta, Perdeep K.; Hale, Terence I.; Christen, Philipp European Journal of Biochemistry, Vol. 214, Issue 2 https://doi.org/10.1111/j.1432-1033.1993.tb17953.x	journal	June 1993
The interplay between drug resistance and fitness in malaria parasites Rosenthal, Philip J. Molecular Microbiology, Vol. 89, Issue 6 https://doi.org/10.1111/mmi.12349	journal	August 2013
Disruption of the GABA shunt affects mitochondrial respiration and virulence in the cereal pathogen Fusarium graminearum Bönnighausen, Jakob; Gebhard, Daniel; Kröger, Cathrin Molecular Microbiology, Vol. 98, Issue 6 https://doi.org/10.1111/mmi.13203	journal	October 2015
Genetics and biology of cytoplasmic male sterility and its applications in forage and turf grass breeding Islam, Md. Shofiqul; Studer, Bruno; Møller, Ian Max Plant Breeding, Vol. 133, Issue 3 https://doi.org/10.1111/pbr.12155	journal	February 2014
Systematic identification of long non‐coding RNAs during pollen development and fertilization in Brassica rapa Huang, Li; Dong, Heng; Zhou, Dong The Plant Journal, Vol. 96, Issue 1 https://doi.org/10.1111/tpj.14016	journal	August 2018
Toxoplasma gondii in Cats: Fecal Stages Identified as Coccidian Oocysts Frenkel, J. K.; Dubey, J. P.; Miller, N. L. Science, Vol. 167, Issue 3919 https://doi.org/10.1126/science.167.3919.893	journal	February 1970
Soluble Adenylyl Cyclase as an Evolutionarily Conserved Bicarbonate Sensor Chen, Y. Science, Vol. 289, Issue 5479 https://doi.org/10.1126/science.289.5479.625	journal	July 2000
Gene Replacement in Toxoplasma gondii with Chloramphenicol Acetyltransferase as Selectable Marker Kim, Kami; Soldati, Dominique; Boothroyd, John C. Science, Vol. 262, Issue 5135 https://doi.org/10.1126/science.8235614	journal	November 1993
Assessment and Continued Validation of the Malaria SYBR Green I-Based Fluorescence Assay for Use in Malaria Drug Screening Johnson, Jacob D.; Dennull, Richard A.; Gerena, Lucia Antimicrobial Agents and Chemotherapy, Vol. 51, Issue 6 https://doi.org/10.1128/AAC.01607-06	journal	June 2007
Type II Toxoplasma gondiiKU80Knockout Strains Enable Functional Analysis of Genes Required for Cyst Development and Latent Infection Fox, Barbara A.; Falla, Alejandra; Rommereim, Leah M. Eukaryotic Cell, Vol. 10, Issue 9 https://doi.org/10.1128/EC.00297-10	journal	September 2011
Maternal Inheritance and Stage-Specific Variation of the Apicoplast in Toxoplasma gondii during Development in the Intermediate and Definitive Host Ferguson, David J. P.; Henriquez, Fiona L.; Kirisits, Michael J. Eukaryotic Cell, Vol. 4, Issue 4 https://doi.org/10.1128/EC.4.4.814-826.2005	journal	April 2005
Pyrimidine Pathway-Dependent and -Independent Functions of the Toxoplasma gondii Mitochondrial Dihydroorotate Dehydrogenase Hortua Triana, Miryam Andrea; Cajiao Herrera, Daniela; Zimmermann, Barbara H. Infection and Immunity, Vol. 84, Issue 10 https://doi.org/10.1128/IAI.00187-16	journal	October 2016
Cyclic Nucleotide Signaling in Toxoplasma gondii Bradyzoite Differentiation Kirkman, Laura A.; Weiss, Louis M.; Kim, Kami Infection and Immunity, Vol. 69, Issue 1 https://doi.org/10.1128/IAI.69.1.148-153.2001	journal	January 2001
Hydrocephalus, Situs Inversus, Chronic Sinusitis, and Male Infertility in DNA Polymerase λ-Deficient Mice: Possible Implication for the Pathogenesis of Immotile Cilia Syndrome Kobayashi, Yosuke; Watanabe, Miho; Okada, Yuki Molecular and Cellular Biology, Vol. 22, Issue 8 https://doi.org/10.1128/MCB.22.8.2769-2776.2002	journal	April 2002
The Toxoplasma gondii Rhoptry Kinome Is Essential for Chronic Infection Fox, Barbara A.; Rommereim, Leah M.; Guevara, Rebekah B. mBio, Vol. 7, Issue 3 https://doi.org/10.1128/mBio.00193-16	journal	May 2016
Efficient Gene Disruption in Diverse Strains of Toxoplasma gondii Using CRISPR/CAS9 Shen, Bang; Brown, Kevin M.; Lee, Tobie D. mBio, Vol. 5, Issue 3 https://doi.org/10.1128/mBio.01114-14	journal	May 2014
Novel Approaches Reveal that Toxoplasma gondii Bradyzoites within Tissue Cysts Are Dynamic and Replicating EntitiesIn Vivo Watts, Elizabeth; Zhao, Yihua; Dhara, Animesh mBio, Vol. 6, Issue 5 https://doi.org/10.1128/mBio.01155-15	journal	October 2015
Plasmodium falciparum Calcium-Dependent Protein Kinase 4 is Critical for Male Gametogenesis and Transmission to the Mosquito Vector Kumar, Sudhir; Haile, Meseret T.; Hoopmann, Michael R. mBio, Vol. 12, Issue 6 https://doi.org/10.1128/mBio.02575-21	journal	December 2021
Identification of gene expression profile during fertilization in Brassica campestris subsp. chinensis Jiang, Jingjing; Jiang, Jianxia; Qiu, Lin Genome, Vol. 56, Issue 1 https://doi.org/10.1139/gen-2012-0088	journal	January 2013
Molecular Genetics of Sexuality in Chlamydomonas Goodenough, U. W.; Armbrust, E. V.; Campbell, A. M. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 46, Issue 1 https://doi.org/10.1146/annurev.pp.46.060195.000321	journal	June 1995
GABA as an inhibitory neurotransmitter in human cerebral cortex McCormick, D. A. Journal of Neurophysiology, Vol. 62, Issue 5 https://doi.org/10.1152/jn.1989.62.5.1018	journal	November 1989
Global proteomic analysis of the oocyst/sporozoite of Toxoplasma gondiireveals commitment to a host-independent lifestyle Possenti, Alessia; Fratini, Federica; Fantozzi, Luca BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-183	journal	March 2013
The plastid-localized pfkB-type carbohydrate kinases FRUCTOKINASE-LIKE 1 and 2 are essential for growth and development of Arabidopsis thaliana Gilkerson, Jonathan; Perez-Ruiz, Juan; Chory, Joanne BMC Plant Biology, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2229-12-102	journal	January 2012
Molecular characterization and application of a novel cytoplasmic male sterility-associated mitochondrial sequence in rice Tan, Yanping; Xu, Xin; Wang, Chuntai BMC Genetics, Vol. 16, Issue 1 https://doi.org/10.1186/s12863-015-0205-0	journal	April 2015
Asexual expansion of Toxoplasma gondii merozoites is distinct from tachyzoites and entails expression of non-overlapping gene families to attach, invade, and replicate within feline enterocytes Hehl, Adrian B.; Basso, Walter U.; Lippuner, Christoph BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-1225-x	journal	February 2015
Transcriptomic and proteomic analysis reveals mechanisms of low pollen-pistil compatibility during water lily cross breeding Sun, Chun-Qing; Chen, Fa-Di; Teng, Nian-Jun BMC Plant Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s12870-019-2166-3	journal	December 2019
Transcriptome profiling of differentially expressed genes in cytoplasmic male-sterile line and its fertility restorer line in pigeon pea (Cajanus cajan L.) Saxena, Swati; Sahu, Sarika; Kaila, Tanvi BMC Plant Biology, Vol. 20, Issue 1 https://doi.org/10.1186/s12870-020-2284-y	journal	February 2020
Changes in m6A RNA methylation are associated with male sterility in wolfberry Zhao, Jiawen; Zhang, Chujun; Li, Sifan BMC Plant Biology, Vol. 23, Issue 1 https://doi.org/10.1186/s12870-023-04458-7	journal	September 2023
Small RNAs, spermatogenesis, and male infertility: a decade of retrospect Joshi, Meghali; Sethi, Shruti; Mehta, Poonam Reproductive Biology and Endocrinology, Vol. 21, Issue 1 https://doi.org/10.1186/s12958-023-01155-w	journal	November 2023
Quantitative proteomics of the tobacco pollen tube secretome identifies novel pollen tube guidance proteins important for fertilization Hafidh, Said; Potěšil, David; Fíla, Jan Genome Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s13059-016-0928-x	journal	May 2016
Analysis of the mechanism by which calcium negatively regulates the tyrosine phosphorylation cascade associated with sperm capacitation Baker, Mark A.; Hetherington, Louise; Ecroyd, Heath Journal of Cell Science, Vol. 117, Issue 2 https://doi.org/10.1242/jcs.00842	journal	January 2004
Identification of SRC as a key PKA-stimulated tyrosine kinase involved in the capacitation-associated hyperactivation of murine spermatozoa Baker, Mark A.; Hetherington, Louise; Aitken, R. John Journal of Cell Science, Vol. 119, Issue 15 https://doi.org/10.1242/jcs.03055	journal	August 2006
Capacitation of mouse sperm is modulated by gamma-aminobutyric acid (GABA) concentration Kurata, Shouhei; Hiradate, Yuuki; Umezu, Kohei Journal of Reproduction and Development, Vol. 65, Issue 4 https://doi.org/10.1262/jrd.2019-008	journal	January 2019
Regulation of Rat Tetratricopeptide Repeat Domain 29 Gene Expression by Follicle-Stimulating Hormone Ohta, Masanori; Ohyama, Kenji; Asano, Atsushi Bioscience, Biotechnology, and Biochemistry, Vol. 76, Issue 8 https://doi.org/10.1271/bbb.120293	journal	August 2012
Intestinal delta-6-desaturase activity determines host range for Toxoplasma sexual reproduction Martorelli Di Genova, Bruno; Wilson, Sarah K.; Dubey, J. P. PLOS Biology, Vol. 17, Issue 8 https://doi.org/10.1371/journal.pbio.3000364	journal	August 2019
A New and Unified Nomenclature for Male Fertility Restorer (RF) Proteins in Higher Plants Kotchoni, Simeon O.; Jimenez-Lopez, Jose C.; Gachomo, Emma W. PLoS ONE, Vol. 5, Issue 12 https://doi.org/10.1371/journal.pone.0015906	journal	December 2010
The Functional Domain of GCS1-Based Gamete Fusion Resides in the Amino Terminus in Plant and Parasite Species Mori, Toshiyuki; Hirai, Makoto; Kuroiwa, Tsuneyoshi PLoS ONE, Vol. 5, Issue 12 https://doi.org/10.1371/journal.pone.0015957	journal	December 2010
Identification of Toxoplasma gondii cAMP Dependent Protein Kinase and Its Role in the Tachyzoite Growth Kurokawa, Hitomi; Kato, Kentaro; Iwanaga, Tatsuya PLoS ONE, Vol. 6, Issue 7 https://doi.org/10.1371/journal.pone.0022492	journal	July 2011
Proteomic Analysis of Fractionated Toxoplasma Oocysts Reveals Clues to Their Environmental Resistance Fritz, Heather M.; Bowyer, Paul W.; Bogyo, Matthew PLoS ONE, Vol. 7, Issue 1 https://doi.org/10.1371/journal.pone.0029955	journal	January 2012
Transcriptomic Analysis of Toxoplasma Development Reveals Many Novel Functions and Structures Specific to Sporozoites and Oocysts Fritz, Heather M.; Buchholz, Kerry R.; Chen, Xiucui PLoS ONE, Vol. 7, Issue 2 https://doi.org/10.1371/journal.pone.0029998	journal	February 2012
EFCAB2 is a novel calcium-binding protein in mouse testis and sperm Shawki, Hossam H.; Ishikawa-Yamauchi, Yu; Kawashima, Akihiro PLOS ONE, Vol. 14, Issue 4 https://doi.org/10.1371/journal.pone.0214687	journal	April 2019
Stage-Specific Changes in Plasmodium Metabolism Required for Differentiation and Adaptation to Different Host and Vector Environments Srivastava, Anubhav; Philip, Nisha; Hughes, Katie R. PLOS Pathogens, Vol. 12, Issue 12 https://doi.org/10.1371/journal.ppat.1006094	journal	December 2016
The aromatic amino acid hydroxylase genes AAH1 and AAH2 in Toxoplasma gondii contribute to transmission in the cat Wang, Zi T.; Verma, Shiv K.; Dubey, Jitender P. PLOS Pathogens, Vol. 13, Issue 3 https://doi.org/10.1371/journal.ppat.1006272	journal	March 2017
Transcriptional repression by ApiAP2 factors is central to chronic toxoplasmosis Radke, Joshua B.; Worth, Danielle; Hong, David PLOS Pathogens, Vol. 14, Issue 5 https://doi.org/10.1371/journal.ppat.1007035	journal	May 2018
Arabidopsis hapless Mutations Define Essential Gametophytic Functions Johnson, Mark A.; von Besser, Kiera; Zhou, Qing Genetics, Vol. 168, Issue 2 https://doi.org/10.1534/genetics.104.029447	journal	October 2004
Analysis of Transposon Insertion Mutants Highlights the Diversity of Mechanisms Underlying Male Progamic Development in Arabidopsis Lalanne, Eric; Michaelidis, Christos; Moore, James M. Genetics, Vol. 167, Issue 4 https://doi.org/10.1534/genetics.104.030270	journal	August 2004
Unexplained Male infertility: diagnosis and Management Hamada, Alaa; Esteves, Sandro C.; Nizza, Mark International braz j urol, Vol. 38, Issue 5 https://doi.org/10.1590/S1677-55382012000500002	journal	October 2012
DNA Polymerases and Human Diseases Sweasy, Joann B.; Lauper, Julia M.; Eckert, Kristin A. Radiation Research, Vol. 166, Issue 5 https://doi.org/10.1667/RR0706.1	journal	November 2006
Factors and pathways involved in capacitation: how are they regulated? Jin, Shi-Kai; Yang, Wan-Xi Oncotarget, Vol. 8, Issue 2 https://doi.org/10.18632/oncotarget.12274	journal	September 2016
Stability of Cytoplasmic Male Sterility in Maize under Different Environmental Conditions Weider, Christophe; Stamp, Peter; Christov, Nikolai Crop Science, Vol. 49, Issue 1 https://doi.org/10.2135/cropsci2007.12.0694	journal	January 2009
Polyamine Metabolism as Chemotherapeutic Target in Protozoan Parasites Bacchi, C.; Yarlett, N. Mini-Reviews in Medicinal Chemistry, Vol. 2, Issue 6 https://doi.org/10.2174/1389557023405549	journal	December 2002
Remarkable Longevity of Dilute Sperm in a Free-Spawning Colonial Ascidian Johnson, Sheri L.; Yund, Philip O. The Biological Bulletin, Vol. 206, Issue 3 https://doi.org/10.2307/1543638	journal	June 2004
Immunization of Cats against Shedding of Toxoplasma Oocysts Frenkel, J. K.; Smith, Donald D. The Journal of Parasitology, Vol. 68, Issue 5 https://doi.org/10.2307/3280978	journal	October 1982
Immunization of Cats with Tissue Cysts, Bradyzoites, and Tachyzoites of the T-263 Strain of Toxoplasma gondii Freyre, A.; Choromanski, L.; Fishback, J. L. The Journal of Parasitology, Vol. 79, Issue 5 https://doi.org/10.2307/3283610	journal	October 1993
Duration of Immunity to Shedding of Toxoplasma gondii Oocysts by Cats Dubey, J. P. The Journal of Parasitology, Vol. 81, Issue 3 https://doi.org/10.2307/3283823	journal	June 1995
Toxoplasma gondii Oocyst Survival under Defined Temperatures Dubey, J. P. The Journal of Parasitology, Vol. 84, Issue 4 https://doi.org/10.2307/3284606	journal	August 1998
A Field Trial of the Effectiveness of a Feline Toxoplasma gondii Vaccine in Reducing T. gondii Exposure for Swine Mateus-Pinilla, Nohra E.; Dubey, J. P.; Choromanski, Leszek The Journal of Parasitology, Vol. 85, Issue 5 https://doi.org/10.2307/3285821	journal	October 1999
Effects of Different Conditions on Duration of Infectivity of Toxoplasma gondii Oocysts Yilmaz, Salih M.; Hopkins, Sewell H. The Journal of Parasitology, Vol. 58, Issue 5 https://doi.org/10.2307/3286589	journal	October 1972
Tissue Distribution and Functional Analysis of Sushi Domain-Containing Protein 4 Tu, Zhidan; Cohen, Mark; Bu, Hong The American Journal of Pathology, Vol. 176, Issue 5 https://doi.org/10.2353/ajpath.2010.091036	journal	May 2010
Prospective vaccine prepared from a new mutant of Toxoplasma gondii for use in cats Frenkel, J. K.; Pfefferkorn, E. R.; Smith, D. D. American Journal of Veterinary Research, Vol. 52, Issue 5 https://doi.org/10.2460/ajvr.1991.52.05.759	journal	May 1991
Detection of Toxoplasma gondii-like oocysts in cat feces and estimates of the environmental oocyst burden Dabritz, Haydee A.; Miller, Melissa A.; Atwill, E. Robert Journal of the American Veterinary Medical Association, Vol. 231, Issue 11 https://doi.org/10.2460/javma.231.11.1676	journal	December 2007
The global burden of congenital toxoplasmosis: a systematic review Torgerson, Paul R.; Mastroiacovo, Pierpaolo Bulletin of the World Health Organization, Vol. 91, Issue 7 https://doi.org/10.2471/BLT.12.111732	journal	May 2013
Foodborne Illness Acquired in the United States—Major Pathogens Scallan, Elaine; Hoekstra, Robert M.; Angulo, Frederick J. Emerging Infectious Diseases, Vol. 17, Issue 1 https://doi.org/10.3201/eid1701.P11101	journal	January 2011
Molecular Basis of Human Sperm Capacitation Puga Molina, Lis C.; Luque, Guillermina M.; Balestrini, Paula A. Frontiers in Cell and Developmental Biology, Vol. 6 https://doi.org/10.3389/fcell.2018.00072	journal	July 2018
Proteomic Changes in Human Sperm During Sequential in vitro Capacitation and Acrosome Reaction Castillo, Judit; Bogle, Orleigh Adeleccia; Jodar, Meritxell Frontiers in Cell and Developmental Biology, Vol. 7 https://doi.org/10.3389/fcell.2019.00295	journal	November 2019
Signaling Enzymes Required for Sperm Maturation and Fertilization in Mammals Dey, Souvik; Brothag, Cameron; Vijayaraghavan, Srinivasan Frontiers in Cell and Developmental Biology, Vol. 7 https://doi.org/10.3389/fcell.2019.00341	journal	December 2019
A Putative Plasmodium RNA-Binding Protein Plays a Critical Role in Female Gamete Fertility and Parasite Transmission to the Mosquito Vector Kumar, Sudhir; Abatiyow, Biley A.; Haile, Meseret T. Frontiers in Cell and Developmental Biology, Vol. 10 https://doi.org/10.3389/fcell.2022.825247	journal	April 2022
CSGID Solves Structures and Identifies Phenotypes for Five Enzymes in Toxoplasma gondii Lykins, Joseph D.; Filippova, Ekaterina V.; Halavaty, Andrei S. Frontiers in Cellular and Infection Microbiology, Vol. 8 https://doi.org/10.3389/fcimb.2018.00352	journal	October 2018
The Structural and Molecular Underpinnings of Gametogenesis in Toxoplasma gondii Tomasina, Ramiro; Francia, María E. Frontiers in Cellular and Infection Microbiology, Vol. 10 https://doi.org/10.3389/fcimb.2020.608291	journal	December 2020
Single Cell Transcriptomes of In Vitro Bradyzoite Infected Cells Reveals Toxoplasma gondii Stage Dependent Host Cell Alterations Sugi, Tatsuki; Tomita, Tadakimi; Kidaka, Taishi Frontiers in Cellular and Infection Microbiology, Vol. 12 https://doi.org/10.3389/fcimb.2022.848693	journal	March 2022
Role of proline and GABA in sexual reproduction of angiosperms Biancucci, Marco; Mattioli, Roberto; Forlani, Giuseppe Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00680	journal	September 2015
The Importance of Oxidative Stress in Determining the Functionality of Mammalian Spermatozoa: A Two-Edged Sword Aitken, Robert J.; Drevet, Joel R. Antioxidants, Vol. 9, Issue 2 https://doi.org/10.3390/antiox9020111	journal	January 2020
Comparative Proteomic Analysis of Mature Pollen in Triploid and Diploid Populus deltoides Zhang, Xiao-Ling; Zhang, Jin; Guo, Ying-Hua International Journal of Molecular Sciences, Vol. 17, Issue 9 https://doi.org/10.3390/ijms17091475	journal	September 2016
Using Transcriptome Analysis to Screen for Key Genes and Pathways Related to Cytoplasmic Male Sterility in Cotton (Gossypium hirsutum L.) Li, Yuqing; Qin, Tengfei; Wei, Chunyan International Journal of Molecular Sciences, Vol. 20, Issue 20 https://doi.org/10.3390/ijms20205120	journal	October 2019
Molecular Biology of Spermatogenesis: Novel Targets of Apparently Idiopathic Male Infertility Cannarella, Rossella; Condorelli, Rosita A.; Mongioì, Laura M. International Journal of Molecular Sciences, Vol. 21, Issue 5 https://doi.org/10.3390/ijms21051728	journal	March 2020
Genetic Manipulation in Δku80 Strains for Functional Genomic Analysis of Toxoplasma gondii Rommereim, Leah M.; Hortua Triana, Miryam A.; Falla, Alejandra Journal of Visualized Experiments, Issue 77 https://doi.org/10.3791/50598	journal	July 2013
CSMD1 Is a Novel Multiple Domain Complement-Regulatory Protein Highly Expressed in the Central Nervous System and Epithelial Tissues Kraus, Damian M.; Elliott, Gary S.; Chute, Hilary The Journal of Immunology, Vol. 176, Issue 7 https://doi.org/10.4049/jimmunol.176.7.4419	journal	April 2006
Major regulatory mechanisms involved in sperm motility Sousa, Mário; Pereira, Rute; Sá, Rosália Asian Journal of Andrology, Vol. 19, Issue 1 https://doi.org/10.4103/1008-682X.167716	journal	January 2017
Soil Survival of Toxoplasma Oocysts in Kansas and Costa Rica Frenkel, J. K.; Ruiz, A.; Chinchilla, M. The American Journal of Tropical Medicine and Hygiene, Vol. 24, Issue 3 https://doi.org/10.4269/ajtmh.1975.24.439	journal	May 1975
Spinal Cord Lesions in Congenital Toxoplasmosis Demonstrated with Neuroimaging, Including Their Successful Treatment in an Adult Burrowes, Delilah; Boyer, Kenneth; Swisher, Charles N. Journal of Neuroparasitology, Vol. 3 https://doi.org/10.4303/jnp/235533	journal	January 2012

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From TgO/GABA-AT, GABA, and T-263 Mutant to Conception of Toxoplasma

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