Synthesizing and Salvaging NAD+: Lessons Learned from Chlamydomonas reinhardtii

Lin, Huawen; Kwan, Alan L.; Dutcher, Susan K.

doi:10.1371/journal.pgen.1001105

Synthesizing and Salvaging NAD+: Lessons Learned from Chlamydomonas reinhardtii

Journal Article · Thu Sep 09 00:00:00 EDT 2010 · PLoS Genetics

DOI:https://doi.org/10.1371/journal.pgen.1001105· OSTI ID:1627286

Lin, Huawen ^[1]; Kwan, Alan L. ^[2]; Dutcher, Susan K. ^[3]

Washington Univ., St. Louis, MO (United States). School of Medicine. Dept. of Genetics; DOE/OSTI
Washington Univ., St. Louis, MO (United States). Dept. of Computer Science and Engineering
Washington Univ., St. Louis, MO (United States). School of Medicine. Dept. of Genetics

The essential coenzyme nicotinamide adenine dinucleotide (NAD+ ) plays important roles in metabolic reactions and cell regulation in all organisms. Bacteria, fungi, plants, and animals use different pathways to synthesize NAD+ . Our molecular and genetic data demonstrate that in the unicellular green alga Chlamydomonas NAD+ is synthesized from aspartate (de novo synthesis), as in plants, or nicotinamide, as in mammals (salvage synthesis). The de novo pathway requires five different enzymes: L-aspartate oxidase (ASO), quinolinate synthetase (QS), quinolate phosphoribosyltransferase (QPT), nicotinate/ nicotinamide mononucleotide adenylyltransferase (NMNAT), and NAD+ synthetase (NS). Sequence similarity searches, gene isolation and sequencing of mutant loci indicate that mutations in each enzyme result in a nicotinamide-requiring mutant phenotype in the previously isolated nic mutants. We rescued the mutant phenotype by the introduction of BAC DNA (nic2- 1 and nic13-1) or plasmids with cloned genes (nic1-1 and nic15-1) into the mutants. NMNAT, which is also in the de novo pathway, and nicotinamide phosphoribosyltransferase (NAMPT) constitute the nicotinamide-dependent salvage pathway. A mutation in NAMPT (npt1-1) has no obvious growth defect and is not nicotinamide-dependent. However, double mutant strains with the npt1-1 mutation and any of the nic mutations are inviable. When the de novo pathway is inactive, the salvage pathway is essential to Chlamydomonas for the synthesis of NAD+ . A homolog of the human SIRT6-like gene, SRT2, is upregulated in the NS mutant, which shows a longer vegetative life span than wild-type cells. Our results suggest that Chlamydomonas is an excellent model system to study NAD+ metabolism and cell longevity.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1627286

Journal Information:: PLoS Genetics, Journal Name: PLoS Genetics Journal Issue: 9 Vol. 6; ISSN 1553-7404

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (104)

Reconstructing eukaryotic NAD metabolism Rongvaux, Anthony; Andris, Fabienne; Van Gool, Fr�d�ric BioEssays, Vol. 25, Issue 7 https://doi.org/10.1002/bies.10297	journal	June 2003
Biochemical Mutants of Chlamydomonas Reinhardi Eversole, Russell A. American Journal of Botany, Vol. 43, Issue 6 https://doi.org/10.1002/j.1537-2197.1956.tb10508.x	journal	June 1956
Predotar: A tool for rapidly screening proteomes forN-terminal targeting sequences Small, Ian; Peeters, Nemo; Legeai, Fabrice PROTEOMICS, Vol. 4, Issue 6 https://doi.org/10.1002/pmic.200300776	journal	June 2004
Phylogenetic Classification of Prokaryotic and Eukaryotic Sir2-like Proteins Frye, Roy A. Biochemical and Biophysical Research Communications, Vol. 273, Issue 2 https://doi.org/10.1006/bbrc.2000.3000	journal	July 2000
Predicting Subcellular Localization of Proteins Based on their N-terminal Amino Acid Sequence Emanuelsson, Olof; Nielsen, Henrik; Brunak, Søren Journal of Molecular Biology, Vol. 300, Issue 4 https://doi.org/10.1006/jmbi.2000.3903	journal	July 2000
A genetic analysis of linkage group I of Chlamydomonas reinhardi Ebersold, W. T.; Levine, R. P. Zeitschrift f�r Vererbungslehre, Vol. 90, Issue 1 https://doi.org/10.1007/bf00888575	journal	January 1959
Purification of Thermus aquaticus DNA polymerase expressed in Escherichia coli Engelke, David R.; Krikos, Alexandra; Bruck, Mary E. Analytical Biochemistry, Vol. 191, Issue 2 https://doi.org/10.1016/0003-2697(90)90238-5	journal	December 1990
Genomic Instability and Aging-like Phenotype in the Absence of Mammalian SIRT6 Mostoslavsky, Raul; Chua, Katrin F.; Lombard, David B. Cell, Vol. 124, Issue 2 https://doi.org/10.1016/j.cell.2005.11.044	journal	January 2006
Vitamins and Aging: Pathways to NAD+ Synthesis Denu, John M. Cell, Vol. 129, Issue 3 https://doi.org/10.1016/j.cell.2007.04.023	journal	May 2007
On the Road to Bacterial Cell Death Wright, Gerard D. Cell, Vol. 130, Issue 5 https://doi.org/10.1016/j.cell.2007.08.023	journal	September 2007
SIRT1 Regulates Circadian Clock Gene Expression through PER2 Deacetylation Asher, Gad; Gatfield, David; Stratmann, Markus Cell, Vol. 134, Issue 2 https://doi.org/10.1016/j.cell.2008.06.050	journal	July 2008
Aging: A Sirtuin Shake-Up? Vijg, Jan; Maslov, Alexander Y.; Suh, Yousin Cell, Vol. 135, Issue 5 https://doi.org/10.1016/j.cell.2008.11.008	journal	November 2008
The Histone Deacetylase Sirt6 Regulates Glucose Homeostasis via Hif1α Zhong, Lei; D'Urso, Agustina; Toiber, Debra Cell, Vol. 140, Issue 2 https://doi.org/10.1016/j.cell.2009.12.041	journal	January 2010
How to Find “Missing” Genes Gerlt, John A. Chemistry & Biology, Vol. 10, Issue 12 https://doi.org/10.1016/j.chembiol.2003.12.008	journal	December 2003
Nampt/PBEF/Visfatin Regulates Insulin Secretion in β Cells as a Systemic NAD Biosynthetic Enzyme Revollo, Javier R.; Körner, Antje; Mills, Kathryn F. Cell Metabolism, Vol. 6, Issue 5 https://doi.org/10.1016/j.cmet.2007.09.003	journal	November 2007
Structural and Kinetic Characterization of Quinolinate Phosphoribosyltransferase (hQPRTase) from Homo sapiens Liu, Huanting; Woznica, Kerry; Catton, Gemma Journal of Molecular Biology, Vol. 373, Issue 3 https://doi.org/10.1016/j.jmb.2007.08.043	journal	October 2007
NAD+ metabolism in health and disease Belenky, Peter; Bogan, Katrina L.; Brenner, Charles Trends in Biochemical Sciences, Vol. 32, Issue 1 https://doi.org/10.1016/j.tibs.2006.11.006	journal	January 2007
Reversal by Tryptophane of the Biological Effects of 3-Acetylpyridine Woolley, D. W. Journal of Biological Chemistry, Vol. 162, Issue 1 https://doi.org/10.1016/s0021-9258(17)41475-x	journal	January 1946
Production of Nicotinic acid Deficiency with 3-Acetylpyridine, the Ketone Analogue of Nicotinic acid Woolley, D. W. Journal of Biological Chemistry, Vol. 157, Issue 2 https://doi.org/10.1016/s0021-9258(18)51081-4	journal	February 1945
An Enzymatic Activity in the Yeast Sir2 Protein that Is Essential for Gene Silencing Tanny, Jason C.; Dowd, Gustave J.; Huang, Julie Cell, Vol. 99, Issue 7 https://doi.org/10.1016/s0092-8674(00)81671-2	journal	December 1999
Discoveries of Nicotinamide Riboside as a Nutrient and Conserved NRK Genes Establish a Preiss-Handler Independent Route to NAD+ in Fungi and Humans Bieganowski, Pawel; Brenner, Charles Cell, Vol. 117, Issue 4 https://doi.org/10.1016/s0092-8674(04)00416-7	journal	May 2004
A Streptomyces rimosus aphVIII gene coding for a new type phosphotransferase provides stable antibiotic resistance to Chlamydomonas reinhardtii Sizova, Irina; Fuhrmann, Markus; Hegemann, Peter Gene, Vol. 277, Issue 1-2 https://doi.org/10.1016/s0378-1119(01)00616-3	journal	October 2001
Increased dosage of a sir-2 gene extends lifespan in Caenorhabditis elegans Tissenbaum, Heidi A.; Guarente, Leonard Nature, Vol. 410, Issue 6825 https://doi.org/10.1038/35065638	journal	March 2001
The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans King, Nicole; Westbrook, M. Jody; Young, Susan L. Nature, Vol. 451, Issue 7180 https://doi.org/10.1038/nature06617	journal	February 2008
SIRT6 is a histone H3 lysine 9 deacetylase that modulates telomeric chromatin Michishita, Eriko; McCord, Ronald A.; Berber, Elisabeth Nature, Vol. 452, Issue 7186 https://doi.org/10.1038/nature06736	journal	March 2008
Centrosome misorientation reduces stem cell division during ageing Cheng, Jun; Türkel, Nezaket; Hemati, Nahid Nature, Vol. 456, Issue 7222 https://doi.org/10.1038/nature07386	journal	December 2008
Asymmetric centrosome inheritance maintains neural progenitors in the neocortex Wang, Xiaoqun; Tsai, Jin-Wu; Imai, Janice H. Nature, Vol. 461, Issue 7266 https://doi.org/10.1038/nature08435	journal	October 2009
NAD+-dependent deacetylation of H4 lysine 16 by class III HDACs Vaquero, A.; Sternglanz, R.; Reinberg, D. Oncogene, Vol. 26, Issue 37 https://doi.org/10.1038/sj.onc.1210617	journal	August 2007
Sir2 mediates longevity in the fly through a pathway related to calorie restriction Rogina, B.; Helfand, S. L. Proceedings of the National Academy of Sciences, Vol. 101, Issue 45 https://doi.org/10.1073/pnas.0404184101	journal	November 2004
Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features Derelle, E.; Ferraz, C.; Rombauts, S. Proceedings of the National Academy of Sciences, Vol. 103, Issue 31 https://doi.org/10.1073/pnas.0604795103	journal	July 2006
Metabolic regulation of SIRT1 transcription via a HIC1:CtBP corepressor complex Zhang, Qinghong; Wang, Su-Yan; Fleuriel, Capucine Proceedings of the National Academy of Sciences, Vol. 104, Issue 3 https://doi.org/10.1073/pnas.0610590104	journal	January 2007
The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation Palenik, B.; Grimwood, J.; Aerts, A. Proceedings of the National Academy of Sciences, Vol. 104, Issue 18 https://doi.org/10.1073/pnas.0611046104	journal	April 2007
Silencing of poly(ADP-ribose) polymerase in plants alters abiotic stress signal transduction Vanderauwera, S.; De Block, M.; Van de Steene, N. Proceedings of the National Academy of Sciences, Vol. 104, Issue 38 https://doi.org/10.1073/pnas.0706668104	journal	September 2007
Essential Bacillus subtilis genes Kobayashi, K.; Ehrlich, S. D.; Albertini, A. Proceedings of the National Academy of Sciences, Vol. 100, Issue 8 https://doi.org/10.1073/pnas.0730515100	journal	April 2003
PCR amplification of up to 35-kb DNA with high fidelity and high yield from lambda bacteriophage templates. Barnes, W. M. Proceedings of the National Academy of Sciences, Vol. 91, Issue 6 https://doi.org/10.1073/pnas.91.6.2216	journal	March 1994
Extension of Human Cell Lifespan by Nicotinamide Phosphoribosyltransferase* van der Veer, Eric; Ho, Cynthia; O'Neil, Caroline Journal of Biological Chemistry, Vol. 282, Issue 15 https://doi.org/10.1074/jbc.c700018200	journal	April 2007
Insights into the Structural Organization of the I1 Inner Arm Dynein from a Domain Analysis of the 1β Dynein Heavy Chain Perrone, Catherine A.; Myster, Steven H.; Bower, Raqual Molecular Biology of the Cell, Vol. 11, Issue 7 https://doi.org/10.1091/mbc.11.7.2297	journal	July 2000
The UNI3 Gene Is Required for Assembly of Basal Bodies of Chlamydomonas and Encodes δ-Tubulin, a New Member of the Tubulin Superfamily Dutcher, Susan K.; Trabuco, Emanuel C. Molecular Biology of the Cell, Vol. 9, Issue 6 https://doi.org/10.1091/mbc.9.6.1293	journal	June 1998
Clustal W and Clustal X version 2.0 Larkin, M. A.; Blackshields, G.; Brown, N. P. Bioinformatics, Vol. 23, Issue 21, p. 2947-2948 https://doi.org/10.1093/bioinformatics/btm404	journal	September 2007
Genetic interactions at the FLA10 locus: suppressors and synthetic phenotypes that affect the cell cycle and flagellar function in Chlamydomonas reinhardtii. Lux, F. G.; Dutcher, S. K. Genetics, Vol. 128, Issue 3 https://doi.org/10.1093/genetics/128.3.549	journal	July 1991
Localization of the nic-7, ac-29 and thi-10 genes within the mating-type locus of Chlamydomonas reinhardtii. Ferris, P. J. Genetics, Vol. 141, Issue 2 https://doi.org/10.1093/genetics/141.2.543	journal	October 1995
Linkage maps in Chlamydomonas Reinhardi Ebersold, W. T.; Levine, R. P.; Levine, E. E. Genetics, Vol. 47, Issue 5 https://doi.org/10.1093/genetics/47.5.531	journal	May 1962
GENETIC CONTROL OF NICOTINIC ACID METABOLISM IN CHLAMYDOMONAS EUGAMETOS Nakamura, Kazuo; Gowans, C. Shields Genetics, Vol. 51, Issue 6 https://doi.org/10.1093/genetics/51.6.931	journal	June 1965
Reappraisal of the Genetic Map of Chlamydomonas reinhardtii Dutcher, S. K.; Power, J.; Galloway, R. E. Journal of Heredity, Vol. 82, Issue 4 https://doi.org/10.1093/oxfordjournals.jhered.a111089	journal	July 1991
The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms Kaeberlein, M.; McVey, M.; Guarente, L. Genes & Development, Vol. 13, Issue 19 https://doi.org/10.1101/gad.13.19.2570	journal	October 1999
Early Steps in the Biosynthesis of NAD in Arabidopsis Start with Aspartate and Occur in the Plastid Katoh, Akira; Uenohara, Kazuya; Akita, Mitsuru Plant Physiology, Vol. 141, Issue 3 https://doi.org/10.1104/pp.106.081091	journal	May 2006
Down-Regulation of a SILENT INFORMATION REGULATOR2 -Related Histone Deacetylase Gene, OsSRT1, Induces DNA Fragmentation and Cell Death in Rice Huang, Limin; Sun, Qianwen; Qin, Fujun Plant Physiology, Vol. 144, Issue 3 https://doi.org/10.1104/pp.107.099473	journal	April 2007
The Arabidopsis onset of leaf death5 Mutation of Quinolinate Synthase Affects Nicotinamide Adenine Dinucleotide Biosynthesis and Causes Early Ageing Schippers, Jos H. M.; Nunes-Nesi, Adriano; Apetrei, Roxana The Plant Cell, Vol. 20, Issue 10 https://doi.org/10.1105/tpc.107.056341	journal	October 2008
Pond Scum Genomics: The Genomes of Chlamydomonas and Ostreococcus Peers, Graham; Niyogi, Krishna K. The Plant Cell, Vol. 20, Issue 3 https://doi.org/10.1105/tpc.107.056556	journal	March 2008
Regulation of Clock and NPAS2 DNA Binding by the Redox State of NAD Cofactors Rutter, J. Science, Vol. 293, Issue 5529 https://doi.org/10.1126/science.1060698	journal	July 2001
The Chlamydomonas Genome Reveals the Evolution of Key Animal and Plant Functions Merchant, S. S.; Prochnik, S. E.; Vallon, O. Science, Vol. 318, Issue 5848, p. 245-250 https://doi.org/10.1126/science.1143609	journal	October 2007
Green Evolution and Dynamic Adaptations Revealed by Genomes of the Marine Picoeukaryotes Micromonas Worden, A. Z.; Lee, J. -H.; Mock, T. Science, Vol. 324, Issue 5924 https://doi.org/10.1126/science.1167222	journal	April 2009
Aging, Chromatin, and Food Restriction--Connecting the Dots Campisi, Judith Science, Vol. 289, Issue 5487 https://doi.org/10.1126/science.289.5487.2062	journal	September 2000
Molecular Map of the Chlamydomonas reinhardtii Nuclear Genome Kathir, Pushpa; LaVoie, Matthew; Brazelton, William J. Eukaryotic Cell, Vol. 2, Issue 2 https://doi.org/10.1128/ec.2.2.362-379.2003	journal	April 2003
Linkage of Six Genes in Chlamydomonas reinhardtii and the Construction of Linkage Test Strains Smyth, Robert D.; Martinek, George W.; Ebersold, W. T. Journal of Bacteriology, Vol. 124, Issue 3 https://doi.org/10.1128/jb.124.3.1615-1617.1975	journal	January 1975
The Escherichia coli NadR Regulator Is Endowed with Nicotinamide Mononucleotide Adenylyltransferase Activity Raffaelli, Nadia; Lorenzi, Teresa; Mariani, P. Luigi Journal of Bacteriology, Vol. 181, Issue 17 https://doi.org/10.1128/jb.181.17.5509-5511.1999	journal	September 1999
Regulation of NAD Synthesis by the Trifunctional NadR Protein of Salmonella enterica Grose, Julianne H.; Bergthorsson, Ulfar; Roth, John R. Journal of Bacteriology, Vol. 187, Issue 8 https://doi.org/10.1128/jb.187.8.2774-2782.2005	journal	April 2005
The CRY1 Gene in Chlamydomonas reinhardtii: Structure and Use as a Dominant Selectable Marker for Nuclear Transformation Nelson, Julie A. E.; Savereide, Paul B.; Lefebvre, Paul A. Molecular and Cellular Biology, Vol. 14, Issue 6 https://doi.org/10.1128/mcb.14.6.4011-4019.1994	journal	June 1994
Nicotinamidase modulation of NAD+ biosynthesis and nicotinamide levels separately affect reproductive development and cell survival in C. elegans Vrablik, T. L.; Huang, L.; Lange, S. E. Development, Vol. 136, Issue 21 https://doi.org/10.1242/dev.028431	journal	October 2009
Involvement of SIRT7 in resumption of rDNA transcription at the exit from mitosis Grob, A.; Roussel, P.; Wright, J. E. Journal of Cell Science, Vol. 122, Issue 4 https://doi.org/10.1242/jcs.042382	journal	January 2009
Drosophila NMNAT Maintains Neural Integrity Independent of Its NAD Synthesis Activity Zhai, R. Grace; Cao, Yu; Hiesinger, P. Robin PLoS Biology, Vol. 4, Issue 12 https://doi.org/10.1371/journal.pbio.0040416	journal	November 2006
Gametogenesis in the Chlamydomonas reinhardtii minus Mating Type Is Controlled by Two Genes, MID and MTD1 Lin, Huawen; Goodenough, Ursula W. Genetics, Vol. 176, Issue 2 https://doi.org/10.1534/genetics.106.066167	journal	April 2007
Nicotinamide Phosphoribosyltransferase (Nampt): A Link Between NAD Biology, Metabolism, and Diseases Imai, Shin-ichiro Current Pharmaceutical Design, Vol. 15, Issue 1 https://doi.org/10.2174/138161209787185814	journal	January 2009
Molecular biology of pyridine nucleotide and nicotine biosynthesis Katoh, Akira Frontiers in Bioscience, Vol. 9, Issue 1-3 https://doi.org/10.2741/1350	journal	January 2004
Sirtuin/Sir2 phylogeny, evolutionary considerations and structural conservation Greiss, Sebastian; Gartner, Anton Molecules and Cells, Vol. 28, Issue 5 https://doi.org/10.1007/s10059-009-0169-x	journal	November 2009
Reversal by Tryptophane of the Biological Effects of 3-Acetylpyridine Woolley, D. W. Journal of Biological Chemistry, Vol. 162, Issue 1 https://doi.org/10.1016/S0021-9258(17)41475-X	journal	January 1946
Production of Nicotinic acid Deficiency with 3-Acetylpyridine, the Ketone Analogue of Nicotinic acid Woolley, D. W. Journal of Biological Chemistry, Vol. 157, Issue 2 https://doi.org/10.1016/S0021-9258(18)51081-4	journal	February 1945
An Enzymatic Activity in the Yeast Sir2 Protein that Is Essential for Gene Silencing Tanny, Jason C.; Dowd, Gustave J.; Huang, Julie Cell, Vol. 99, Issue 7 https://doi.org/10.1016/S0092-8674(00)81671-2	journal	December 1999
Negative Control of p53 by Sir2α Promotes Cell Survival under Stress Luo, Jianyuan; Nikolaev, Anatoly Y.; Imai, Shin-ichiro Cell, Vol. 107, Issue 2 https://doi.org/10.1016/S0092-8674(01)00524-4	journal	October 2001
Discoveries of Nicotinamide Riboside as a Nutrient and Conserved NRK Genes Establish a Preiss-Handler Independent Route to NAD+ in Fungi and Humans Bieganowski, Pawel; Brenner, Charles Cell, Vol. 117, Issue 4 https://doi.org/10.1016/S0092-8674(04)00416-7	journal	May 2004
A Streptomyces rimosus aphVIII gene coding for a new type phosphotransferase provides stable antibiotic resistance to Chlamydomonas reinhardtii Sizova, Irina; Fuhrmann, Markus; Hegemann, Peter Gene, Vol. 277, Issue 1-2 https://doi.org/10.1016/S0378-1119(01)00616-3	journal	October 2001
Nicotinamide Riboside Promotes Sir2 Silencing and Extends Lifespan via Nrk and Urh1/Pnp1/Meu1 Pathways to NAD+ Belenky, Peter; Racette, Frances G.; Bogan, Katrina L. Cell, Vol. 129, Issue 3 https://doi.org/10.1016/j.cell.2007.03.024	journal	May 2007
A Common Mechanism of Cellular Death Induced by Bactericidal Antibiotics Kohanski, Michael A.; Dwyer, Daniel J.; Hayete, Boris Cell, Vol. 130, Issue 5, p. 797-810 https://doi.org/10.1016/j.cell.2007.06.049	journal	September 2007
Nutrient-Sensitive Mitochondrial NAD+ Levels Dictate Cell Survival Yang, Hongying; Yang, Tianle; Baur, Joseph A. Cell, Vol. 130, Issue 6 https://doi.org/10.1016/j.cell.2007.07.035	journal	September 2007
SIRT1 Redistribution on Chromatin Promotes Genomic Stability but Alters Gene Expression during Aging Oberdoerffer, Philipp; Michan, Shaday; McVay, Michael Cell, Vol. 135, Issue 5 https://doi.org/10.1016/j.cell.2008.10.025	journal	November 2008
Glucose Restriction Extends Caenorhabditis elegans Life Span by Inducing Mitochondrial Respiration and Increasing Oxidative Stress Schulz, Tim J.; Zarse, Kim; Voigt, Anja Cell Metabolism, Vol. 6, Issue 4 https://doi.org/10.1016/j.cmet.2007.08.011	journal	October 2007
The Structure of a Eukaryotic Nicotinic Acid Phosphoribosyltransferase Reveals Structural Heterogeneity among Type II PRTases Chappie, Joshua S.; Cànaves, Jaume M.; Han, Gye Won Structure, Vol. 13, Issue 9 https://doi.org/10.1016/j.str.2005.05.016	journal	September 2005
Epigenetics and aging: the targets and the marks Fraga, Mario F.; Esteller, Manel Trends in Genetics, Vol. 23, Issue 8 https://doi.org/10.1016/j.tig.2007.05.008	journal	August 2007
NAD synthase NMNAT acts as a chaperone to protect against neurodegeneration Zhai, R. Grace; Zhang, Fan; Hiesinger, P. Robin Nature, Vol. 452, Issue 7189 https://doi.org/10.1038/nature06721	journal	March 2008
Extension of Human Cell Lifespan by Nicotinamide Phosphoribosyltransferase* van der Veer, Eric; Ho, Cynthia; O'Neil, Caroline Journal of Biological Chemistry, Vol. 282, Issue 15 https://doi.org/10.1074/jbc.C700018200	journal	April 2007
Structure of Human NMN Adenylyltransferase Garavaglia, Silvia; D'Angelo, Igor; Emanuelli, Monica Journal of Biological Chemistry, Vol. 277, Issue 10 https://doi.org/10.1074/jbc.M111589200	journal	March 2002
Crystal Structure of a Nicotinate Phosphoribosyltransferase from Thermoplasma acidophilum Shin, Dong Hae; Oganesyan, Natalia; Jancarik, Jaru Journal of Biological Chemistry, Vol. 280, Issue 18 https://doi.org/10.1074/jbc.M501622200	journal	May 2005
Nicotinamide Riboside and Nicotinic Acid Riboside Salvage in Fungi and Mammals Belenky, Peter; Christensen, Kathryn C.; Gazzaniga, Francesca Journal of Biological Chemistry, Vol. 284, Issue 1 https://doi.org/10.1074/jbc.M807976200	journal	January 2009
LC2, the Chlamydomonas Homologue of the t Complex-encoded Protein Tctex2, Is Essential for Outer Dynein Arm Assembly Pazour, Gregory J.; Koutoulis, Anthony; Benashski, Sharon E. Molecular Biology of the Cell, Vol. 10, Issue 10 https://doi.org/10.1091/mbc.10.10.3507	journal	October 1999
Transformation of chloroplast ribosomal RNA genes in Chlamydomonas: molecular and genetic characterization of integration events. Newman, S. M.; Boynton, J. E.; Gillham, N. W. Genetics, Vol. 126, Issue 4 https://doi.org/10.1093/genetics/126.4.875	journal	December 1990
Genetic Structure of the Mating-Type Locus of Chlamydomonas reinhardtii Ferris, Patrick J.; Armbrust, E. Virginia; Goodenough, Ursula W. Genetics, Vol. 160, Issue 1 https://doi.org/10.1093/genetics/160.1.181	journal	January 2002
Mammalian Sir2 homolog SIRT7 is an activator of RNA polymerase I transcription Ford, E. Genes & Development, Vol. 20, Issue 9 https://doi.org/10.1101/gad.1399706	journal	May 2006
A systematic forward genetic analysis identified components of the Chlamydomonas circadian system Matsuo, T.; Okamoto, K.; Onai, K. Genes & Development, Vol. 22, Issue 7 https://doi.org/10.1101/gad.1650408	journal	April 2008
Arabidopsis thaliana nicotinate/nicotinamide mononucleotide adenyltransferase (AtNMNAT) is required for pollen tube growth: AtNMNATis required for pollen tube growth Hashida, Shin-nosuke; Takahashi, Hideyuki; Kawai-Yamada, Maki The Plant Journal, Vol. 49, Issue 4 https://doi.org/10.1111/j.1365-313X.2006.02989.x	journal	January 2007
Stoichiometry and compartmentation of NADH metabolism in Saccharomyces cerevisiae Bakker, Barbara M.; Overkamp, Karin M.; van Maris, Antonius J. A. FEMS Microbiology Reviews, Vol. 25, Issue 1, p. 15-37 https://doi.org/10.1111/j.1574-6976.2001.tb00570.x	journal	January 2001
Calorie Restriction Promotes Mammalian Cell Survival by Inducing the SIRT1 Deacetylase Cohen, H. Y. Science, Vol. 305, Issue 5682 https://doi.org/10.1126/science.1099196	journal	July 2004
Circadian Control of the NAD+ Salvage Pathway by CLOCK-SIRT1 Nakahata, Y.; Sahar, S.; Astarita, G. Science, Vol. 324, Issue 5927 https://doi.org/10.1126/science.1170803	journal	March 2009
GENOMICS: Green Evolution, Green Revolution Archibald, J. M. Science, Vol. 324, Issue 5924 https://doi.org/10.1126/science.1172972	journal	April 2009
Requirement of NAD and SIR2 for Life-Span Extension by Calorie Restriction in Saccharomyces cerevisiae Lin, S. -J. Science, Vol. 289, Issue 5487 https://doi.org/10.1126/science.289.5487.2126	journal	September 2000
Molecular Map of the Chlamydomonas reinhardtii Nuclear Genome Kathir, Pushpa; LaVoie, Matthew; Brazelton, William J. Eukaryotic Cell, Vol. 2, Issue 2 https://doi.org/10.1128/EC.2.2.362-379.2003	journal	April 2003
Linkage of Six Genes in Chlamydomonas reinhardtii and the Construction of Linkage Test Strains Smyth, Robert D.; Martinek, George W.; Ebersold, W. T. Journal of Bacteriology, Vol. 124, Issue 3 https://doi.org/10.1128/JB.124.3.1615-1617.1975	journal	January 1975
The Escherichia coli NadR Regulator Is Endowed with Nicotinamide Mononucleotide Adenylyltransferase Activity Raffaelli, Nadia; Lorenzi, Teresa; Mariani, P. Luigi Journal of Bacteriology, Vol. 181, Issue 17 https://doi.org/10.1128/JB.181.17.5509-5511.1999	journal	September 1999
Regulation of NAD Synthesis by the Trifunctional NadR Protein of Salmonella enterica Grose, Julianne H.; Bergthorsson, Ulfar; Roth, John R. Journal of Bacteriology, Vol. 187, Issue 8 https://doi.org/10.1128/JB.187.8.2774-2782.2005	journal	April 2005
The CRY1 gene in Chlamydomonas reinhardtii: structure and use as a dominant selectable marker for nuclear transformation. Nelson, J. A.; Savereide, P. B.; Lefebvre, P. A. Molecular and Cellular Biology, Vol. 14, Issue 6 https://doi.org/10.1128/MCB.14.6.4011	journal	June 1994
Improving Gene-finding in Chlamydomonas reinhardtii:GreenGenie2 Kwan, Alan L.; Li, Linya; Kulp, David C. BMC Genomics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2164-10-210	journal	January 2009
Cell Size Checkpoint Control by the Retinoblastoma Tumor Suppressor Pathway Fang, Su-Chiung; Reyes, Chris de los; Umen, James G. PLoS Genetics, Vol. 2, Issue 10 https://doi.org/10.1371/journal.pgen.0020167	journal	October 2006
Retrograde Intraflagellar Transport Mutants Identify Complex A Proteins With Multiple Genetic Interactions in Chlamydomonas reinhardtii Iomini, Carlo; Li, Linya; Esparza, Jessica M. Genetics, Vol. 183, Issue 3 https://doi.org/10.1534/genetics.109.101915	journal	August 2009
Biochemical Mutants of Chlamydomonas reinhardi Eversole, Russel A. American Journal of Botany, Vol. 43, Issue 6 https://doi.org/10.2307/2439015	journal	June 1956
The Molecular Biology of Mammalian SIRT Proteins: SIRT2 Functions on Cell Cycle Regulation Inoue, Toshiaki; Hiratsuka, Masaharu; Osaki, Mitsuhiko Cell Cycle, Vol. 6, Issue 9 https://doi.org/10.4161/cc.6.9.4219	journal	May 2007

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A simple and inexpensive physical lysis method for DNA and RNA extraction from freshwater microalgae Yee, Willy; Abdul-Kadir, Ruzanna; Lee, Leng May 3 Biotech, Vol. 8, Issue 8 https://doi.org/10.1007/s13205-018-1381-1	journal	August 2018
Modular engineering to increase intracellular NAD(H/+) promotes rate of extracellular electron transfer of Shewanella oneidensis Li, Feng; Li, Yuan-Xiu; Cao, Ying-Xiu Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05995-8	journal	September 2018
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Horizontal Gene Transfer as an Indispensable Driver for Evolution of Neocallimastigomycota into a Distinct Gut-Dwelling Fungal Lineage Murphy, Chelsea L.; Youssef, Noha H.; Hanafy, Radwa A. Applied and Environmental Microbiology, Vol. 85, Issue 15 https://doi.org/10.1128/aem.00988-19	journal	May 2019
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