Molecular architecture and domain arrangement of the placental malaria protein VAR2CSA suggests a model for carbohydrate binding

Bewley, Maria C.; Gautam, Lovely; Jagadeeshaprasad, Mashanipalya G.; Gowda, D. Channe; Flanagan, John M.

doi:10.1074/jbc.ra120.014676

Molecular architecture and domain arrangement of the placental malaria protein VAR2CSA suggests a model for carbohydrate binding

Journal Article · Mon Nov 30 23:00:00 EST 2020 · Journal of Biological Chemistry

DOI:https://doi.org/10.1074/jbc.ra120.014676· OSTI ID:1765255

Bewley, Maria C. ^[1]; Gautam, Lovely ^[1]; ^[1]; ^[1]; Flanagan, John M. ^[1]

Pennsylvania State Univ. College of Medicine, Hershey, PA (United States)

VAR2CSA is the placental-malaria–specific member of the antigenically variant Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) family. It is expressed on the surface of Plasmodium falciparum-infected host red blood cells and binds to specific chondroitin-4-sulfate chains of the placental proteoglycan receptor. The functional ~310 kDa ectodomain of VAR2CSA is a multidomain protein that requires a minimum 12-mer chondroitin-4-sulfate molecule for specific, high affinity receptor binding. However, it is not known how the individual domains are organized and interact to create the receptor-binding surface, limiting efforts to exploit its potential as an effective vaccine or drug target. Using small angle X-ray scattering and single particle reconstruction from negative-stained electron micrographs of the ectodomain and multidomain constructs, we have determined the structural architecture of VAR2CSA. The relative locations of the domains creates two distinct pores that can each accommodate the 12-mer of chondroitin-4-sulfate, suggesting a model for receptor binding. This model has important implications for understanding cytoadherence of infected red blood cells and potentially provides a starting point for developing novel strategies to prevent and/or treat placental malaria.

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)

OSTI ID:: 1765255

Alternate ID(s):: OSTI ID: 1760513

Journal Information:: Journal of Biological Chemistry, Journal Name: Journal of Biological Chemistry Journal Issue: 52 Vol. 295; ISSN 0021-9258

Publisher:: American Society for Biochemistry and Molecular BiologyCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (77)

UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
Chondroitin 4-sulfate: The structure of a sulfated glycosaminoglycan Winter, W. T.; Arnott, Struther; Isaac, D. H. Journal of Molecular Biology, Vol. 125, Issue 1 https://doi.org/10.1016/0022-2836(78)90251-6	journal	October 1978
Malaria infection of the placenta in The Gambia, West Africa; its incidence and relationship to stillbirth, birthweight and placental weight McGregor, Ian A.; Wilson, M. E.; Billewicz, W. Z. Transactions of the Royal Society of Tropical Medicine and Hygiene, Vol. 77, Issue 2 https://doi.org/10.1016/0035-9203(83)90081-0	journal	January 1983
Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes Baruch, Dror I.; Pasloske, Britten L.; Singh, Hardeep B. Cell, Vol. 82, Issue 1 https://doi.org/10.1016/0092-8674(95)90054-3	journal	July 1995
The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of plasmodium falciparum-infected erythrocytes Su, Xin-zhuan; Heatwole, Virginia M.; Wertheimer, Samuel P. Cell, Vol. 82, Issue 1 https://doi.org/10.1016/0092-8674(95)90055-1	journal	July 1995
Switches in expression of plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes Smith, Joseph D.; Chitnis, Chetan E.; Craig, Alistar G. Cell, Vol. 82, Issue 1 https://doi.org/10.1016/0092-8674(95)90056-X	journal	July 1995
Membrane modifications in erythrocytes parasitized by Plasmodium falciparum Deitsch, Kirk W.; Wellems, Thomas E. Molecular and Biochemical Parasitology, Vol. 76, Issue 1-2 https://doi.org/10.1016/0166-6851(95)02575-8	journal	February 1996
Chondroitin sulfate proteoglycans of bovine cornea: structural characterization and assessment for the adherence of Plasmodium falciparum-infected erythrocytes Achur, Rajeshwara N.; Muthusamy, Arivalagan; Madhunapantula, Subbarao V. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1701, Issue 1-2 https://doi.org/10.1016/j.bbapap.2004.06.007	journal	September 2004
Structural Conservation Despite Huge Sequence Diversity Allows EPCR Binding by the PfEMP1 Family Implicated in Severe Childhood Malaria Lau, Clinton K. Y.; Turner, Louise; Jespersen, Jakob S. Cell Host & Microbe, Vol. 17, Issue 1 https://doi.org/10.1016/j.chom.2014.11.007	journal	January 2015
Structural Comparison of Two CSPG-Binding DBL Domains from the VAR2CSA Protein Important in Malaria during Pregnancy Khunrae, Pongsak; Philip, Judith M. D.; Bull, Duncan R. Journal of Molecular Biology, Vol. 393, Issue 1 https://doi.org/10.1016/j.jmb.2009.08.027	journal	October 2009
Structural and Immunological Correlations between the Variable Blocks of the VAR2CSA Domain DBL6ε from Two Plasmodium falciparum Parasite Lines Gangnard, Stéphane; Badaut, Cyril; Ramboarina, Stéphanie Journal of Molecular Biology, Vol. 425, Issue 10 https://doi.org/10.1016/j.jmb.2013.02.014	journal	May 2013
Visualizing density maps with UCSF Chimera Goddard, Thomas D.; Huang, Conrad C.; Ferrin, Thomas E. Journal of Structural Biology, Vol. 157, Issue 1 https://doi.org/10.1016/j.jsb.2006.06.010	journal	January 2007
NADPH oxidase activator p67phox behaves in solution as a multidomain protein with semi-flexible linkers Durand, Dominique; Vivès, Corinne; Cannella, Dominique Journal of Structural Biology, Vol. 169, Issue 1 https://doi.org/10.1016/j.jsb.2009.08.009	journal	January 2010
UCSF Chimera, MODELLER, and IMP: An integrated modeling system Yang, Zheng; Lasker, Keren; Schneidman-Duhovny, Dina Journal of Structural Biology, Vol. 179, Issue 3 https://doi.org/10.1016/j.jsb.2011.09.006	journal	September 2012
Scipion: A software framework toward integration, reproducibility and validation in 3D electron microscopy de la Rosa-Trevín, J. M.; Quintana, A.; del Cano, L. Journal of Structural Biology, Vol. 195, Issue 1 https://doi.org/10.1016/j.jsb.2016.04.010	journal	July 2016
A family affair: var genes, PfEMP1 binding, and malaria disease Kraemer, Susan M.; Smith, Joseph D. Current Opinion in Microbiology, Vol. 9, Issue 4 https://doi.org/10.1016/j.mib.2006.06.006	journal	August 2006
The role of PfEMP1 adhesion domain classification in Plasmodium falciparum pathogenesis research Smith, Joseph D. Molecular and Biochemical Parasitology, Vol. 195, Issue 2 https://doi.org/10.1016/j.molbiopara.2014.07.006	journal	July 2014
Malaria in Children Cohee, Lauren M.; Laufer, Miriam K. Pediatric Clinics of North America, Vol. 64, Issue 4 https://doi.org/10.1016/j.pcl.2017.03.004	journal	August 2017
The Sick Placenta—The Role of Malaria Brabin, B. Placenta, Vol. 25, Issue 5 https://doi.org/10.1016/j.placenta.2003.10.019	journal	May 2004
Variant surface antigens, virulence genes and the pathogenesis of malaria Deitsch, Kirk W.; Hviid, Lars Trends in Parasitology, Vol. 20, Issue 12 https://doi.org/10.1016/j.pt.2004.09.002	journal	December 2004
Designing a VAR2CSA-based vaccine to prevent placental malaria Fried, Michal; Duffy, Patrick E. Vaccine, Vol. 33, Issue 52 https://doi.org/10.1016/j.vaccine.2015.10.011	journal	December 2015
Large-Scale Identification of Phosphorylation Sites for Profiling Protein Kinase Selectivity Imamura, Haruna; Sugiyama, Naoyuki; Wakabayashi, Masaki Journal of Proteome Research, Vol. 13, Issue 7 https://doi.org/10.1021/pr500319y	journal	June 2014
Identification of Phosphorylation Sites within the Signaling Adaptor APPL1 by Mass Spectrometry Gant-Branum, Randi L.; Broussard, Joshua A.; Mahsut, Ablatt Journal of Proteome Research, Vol. 9, Issue 3 https://doi.org/10.1021/pr901043e	journal	March 2010
Maternal antibodies block malaria Fried, Michal; Nosten, François; Brockman, Alan Nature, Vol. 395, Issue 6705 https://doi.org/10.1038/27570	journal	October 1998
The pathogenic basis of malaria Miller, Louis H.; Baruch, Dror I.; Marsh, Kevin Nature, Vol. 415, Issue 6872 https://doi.org/10.1038/415673a	journal	February 2002
Genome sequence of the human malaria parasite Plasmodium falciparum Gardner, Malcolm J.; Hall, Neil; Fung, Eula Nature, Vol. 419, Issue 6906 https://doi.org/10.1038/nature01097	journal	October 2002
Severe malaria is associated with parasite binding to endothelial protein C receptor Turner, Louise; Lavstsen, Thomas; Berger, Sanne S. Nature, Vol. 498, Issue 7455 https://doi.org/10.1038/nature12216	journal	June 2013
The structural basis for CD36 binding by the malaria parasite Hsieh, Fu-Lien; Turner, Louise; Bolla, Jani Reddy Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12837	journal	September 2016
In-gel digestion for mass spectrometric characterization of proteins and proteomes Shevchenko, Andrej; Tomas, Henrik; Havli, Jan Nature Protocols, Vol. 1, Issue 6 https://doi.org/10.1038/nprot.2006.468	journal	December 2006
Structure of the DBL3x domain of pregnancy-associated malaria protein VAR2CSA complexed with chondroitin sulfate A Singh, Kavita; Gittis, Apostolos G.; Nguyen, Phuc Nature Structural & Molecular Biology, Vol. 15, Issue 9 https://doi.org/10.1038/nsmb.1479	journal	August 2008
Consensus Bayesian assessment of protein molecular mass from solution X-ray scattering data Hajizadeh, Nelly R.; Franke, Daniel; Jeffries, Cy M. Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-25355-2	journal	May 2018
Global genetic diversity of var2csa in Plasmodium falciparum with implications for malaria in pregnancy and vaccine development Benavente, Ernest Diez; Oresegun, Damilola R.; de Sessions, Paola Florez Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-33767-3	journal	October 2018
Single-molecule imaging and quantification of the immune-variant adhesin VAR2CSA on knobs of Plasmodium falciparum-infected erythrocytes Sanchez, Cecilia P.; Karathanasis, Christos; Sanchez, Rodrigo Communications Biology, Vol. 2, Issue 1 https://doi.org/10.1038/s42003-019-0429-z	journal	May 2019
Placental malaria vaccine candidate antigen VAR2CSA displays atypical domain architecture in some Plasmodium falciparum strains Doritchamou, Justin Y. A.; Morrison, Robert; Renn, Jonathan P. Communications Biology, Vol. 2, Issue 1 https://doi.org/10.1038/s42003-019-0704-z	journal	December 2019
Mechanisms underlying mutually exclusive expression of virulence genes by malaria parasites Dzikowski, Ron; Li, Felomena; Amulic, Borko EMBO reports, Vol. 8, Issue 10 https://doi.org/10.1038/sj.embor.7401063	journal	August 2007
Structure of the DBL3X-DBL4ε region of the VAR2CSA placental malaria vaccine candidate: insight into DBL domain interactions Gangnard, Stéphane; Lewit-Bentley, Anita; Dechavanne, Sébastien Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep14868	journal	October 2015
A Structure-free Method for Quantifying Conformational Flexibility in proteins Burger, Virginia M.; Arenas, Daniel J.; Stultz, Collin M. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep29040	journal	June 2016
Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria: Single var gene upregulation in CSA-adhering P. falciparum Salanti, Ali; Staalsoe, Trine; Lavstsen, Thomas Molecular Microbiology, Vol. 49, Issue 1 https://doi.org/10.1046/j.1365-2958.2003.03570.x	journal	May 2003
Full-length extracellular region of the var2CSA variant of PfEMP1 is required for specific, high-affinity binding to CSA Srivastava, A.; Gangnard, S.; Round, A. Proceedings of the National Academy of Sciences, Vol. 107, Issue 11 https://doi.org/10.1073/pnas.1000951107	journal	March 2010
Severe adult malaria is associated with specific PfEMP1 adhesion types and high parasite biomass Bernabeu, Maria; Danziger, Samuel A.; Avril, Marion Proceedings of the National Academy of Sciences, Vol. 113, Issue 23 https://doi.org/10.1073/pnas.1524294113	journal	May 2016
Structural insights into diverse modes of ICAM-1 binding by Plasmodium falciparum -infected erythrocytes Lennartz, Frank; Smith, Cameron; Craig, Alister G. Proceedings of the National Academy of Sciences, Vol. 116, Issue 40 https://doi.org/10.1073/pnas.1911900116	journal	September 2019
Plasmodium falciparum erythrocyte membrane protein 1 is a parasitized erythrocyte receptor for adherence to CD36, thrombospondin, and intercellular adhesion molecule 1. Baruch, D. I.; Gormely, J. A.; Ma, C. Proceedings of the National Academy of Sciences, Vol. 93, Issue 8 https://doi.org/10.1073/pnas.93.8.3497	journal	April 1996
The Structure of a Chondroitin Sulfate-binding Domain Important in Placental Malaria* Higgins, Matthew K. Journal of Biological Chemistry, Vol. 283, Issue 32 https://doi.org/10.1074/jbc.C800086200	journal	August 2008
Characterization of Proteoglycans of Human Placenta and Identification of Unique Chondroitin Sulfate Proteoglycans of the Intervillous Spaces That Mediate the Adherence ofPlasmodium falciparum-infected Erythrocytes to the Placenta Achur, Rajeshwara N.; Valiyaveettil, Manojkumar; Alkhalil, Abdulnaser Journal of Biological Chemistry, Vol. 275, Issue 51 https://doi.org/10.1074/jbc.M006398200	journal	December 2000
Structural Requirements for the Adherence ofPlasmodium falciparum-infected Erythrocytes to Chondroitin Sulfate Proteoglycans of Human Placenta Alkhalil, Abdulnaser; Achur, Rajeshwara N.; Valiyaveettil, Manojkumar Journal of Biological Chemistry, Vol. 275, Issue 51 https://doi.org/10.1074/jbc.M006399200	journal	December 2000
The Chondroitin Sulfate A-binding Site of the VAR2CSA Protein Involves Multiple N-terminal Domains Dahlbäck, Madeleine; Jørgensen, Lars M.; Nielsen, Morten A. Journal of Biological Chemistry, Vol. 286, Issue 18 https://doi.org/10.1074/jbc.M110.191510	journal	May 2011
Structural and Functional Insight into How the Plasmodium falciparum VAR2CSA Protein Mediates Binding to Chondroitin Sulfate A in Placental Malaria Clausen, Thomas M.; Christoffersen, Stig; Dahlbäck, Madeleine Journal of Biological Chemistry, Vol. 287, Issue 28 https://doi.org/10.1074/jbc.M112.348839	journal	July 2012
The Low Sulfated Chondroitin Sulfate Proteoglycans of Human Placenta Have Sulfate Group-clustered Domains That Can Efficiently Bind Plasmodium falciparum-infected Erythrocytes Achur, Rajeshwara N.; Valiyaveettil, Manojkumar; Gowda, D. Channe Journal of Biological Chemistry, Vol. 278, Issue 13 https://doi.org/10.1074/jbc.M211015200	journal	March 2003
Phosphoprotein Secretome of Tumor Cells as a Source of Candidates for Breast Cancer Biomarkers in Plasma Zawadzka, Anna M.; Schilling, Birgit; Cusack, Michael P. Molecular & Cellular Proteomics, Vol. 13, Issue 4 https://doi.org/10.1074/mcp.M113.035485	journal	April 2014
Evidence for the Involvement of VAR2CSA in Pregnancy-associated Malaria Salanti, Ali; Dahlbäck, Madeleine; Turner, Louise Journal of Experimental Medicine, Vol. 200, Issue 9 https://doi.org/10.1084/jem.20041579	journal	November 2004
The Impact of Placental Malaria on Gestational Age and Birth Weight Menendez, C.; Ordi, J.; Ismail, M. R. The Journal of Infectious Diseases, Vol. 181, Issue 5 https://doi.org/10.1086/315449	journal	May 2000
CHROMIXS: automatic and interactive analysis of chromatography-coupled small-angle X-ray scattering data Panjkovich, Alejandro; Svergun, Dmitri I. Bioinformatics, Vol. 34, Issue 11 https://doi.org/10.1093/bioinformatics/btx846	journal	December 2017
Parasites Causing Cerebral Falciparum Malaria Bind Multiple Endothelial Receptors and Express EPCR and ICAM-1-Binding PfEMP1 Tuikue Ndam, Nicaise; Moussiliou, Azizath; Lavstsen, Thomas The Journal of Infectious Diseases, Vol. 215, Issue 12 https://doi.org/10.1093/infdis/jix230	journal	June 2017
The PRIDE database and related tools and resources in 2019: improving support for quantification data Perez-Riverol, Yasset; Csordas, Attila; Bai, Jingwen Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky1106	journal	November 2018
Blood groups and malaria: fresh insights into pathogenesis and identification of targets for intervention Rowe, J. Alexandra; Opi, D. Herbert; Williams, Thomas N. Current Opinion in Hematology, Vol. 16, Issue 6 https://doi.org/10.1097/MOH.0b013e3283313de0	journal	January 2009
Malaria during Pregnancy Fried, Michal; Duffy, Patrick E. Cold Spring Harbor Perspectives in Medicine, Vol. 7, Issue 6 https://doi.org/10.1101/cshperspect.a025551	journal	February 2017
Ambiguity assessment of small-angle scattering curves from monodisperse systems Petoukhov, Maxim V.; Svergun, Dmitri I. Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 5 https://doi.org/10.1107/S1399004715002576	journal	April 2015
ATSAS 2.8 : a comprehensive data analysis suite for small-angle scattering from macromolecular solutions Franke, D.; Petoukhov, M. V.; Konarev, P. V. Journal of Applied Crystallography, Vol. 50, Issue 4 https://doi.org/10.1107/S1600576717007786	journal	June 2017
Malaria's deadly grip: cytoadhesion of Plasmodium falciparum -infected erythrocytes: Plasmodium falciparum cytoadhesion and var genes Smith, Joseph D.; Rowe, J. Alexandra; Higgins, Matthew K. Cellular Microbiology, Vol. 15, Issue 12 https://doi.org/10.1111/cmi.12183	journal	September 2013
Variable switching rates of malaria virulence genes are associated with chromosomal position: Switching rates of malaria virulence genes Frank, Matthias; Dzikowski, Ron; Amulic, Borko Molecular Microbiology, Vol. 64, Issue 6 https://doi.org/10.1111/j.1365-2958.2007.05736.x	journal	June 2007
Monitoring maternal and newborn health outcomes globally: a brief history of key events and initiatives Moller, Ann‐Beth; Patten, Jane H.; Hanson, Claudia Tropical Medicine & International Health, Vol. 24, Issue 12 https://doi.org/10.1111/tmi.13313	journal	November 2019
Principles that Govern the Folding of Protein Chains Anfinsen, C. B. Science, Vol. 181, Issue 4096 https://doi.org/10.1126/science.181.4096.223	journal	July 1973
Molecular Aspects of Severe Malaria Chen, Qijun; Schlichtherle, Martha; Wahlgren, Mats Clinical Microbiology Reviews, Vol. 13, Issue 3 https://doi.org/10.1128/CMR.13.3.439	journal	July 2000
Fresh Isolates from Children with Severe Plasmodium falciparum Malaria Bind to Multiple Receptors Heddini, Andreas; Pettersson, Fredrik; Kai, Oscar Infection and Immunity, Vol. 69, Issue 9 https://doi.org/10.1128/IAI.69.9.5849-5856.2001	journal	September 2001
Chondroitin Sulfate Proteoglycan Expression and Binding of Plasmodium falciparum-Infected Erythrocytes in the Human Placenta during Pregnancy Agbor-Enoh, Sean T.; Achur, Rajeshwara N.; Valiyaveettil, Manojkumar Infection and Immunity, Vol. 71, Issue 5 https://doi.org/10.1128/IAI.71.5.2455-2461.2003	journal	May 2003
Interaction between Endothelial Protein C Receptor and Intercellular Adhesion Molecule 1 to Mediate Binding of Plasmodium falciparum -Infected Erythrocytes to Endothelial Cells Avril, Marion; Bernabeu, Maria; Benjamin, Maxwell mBio, Vol. 7, Issue 4 https://doi.org/10.1128/mBio.00615-16	journal	July 2016
Malaria, the red Cell, and the Endothelium Pasloske, Ph. D., Brittan L.; Howard, Ph. D., Russell J. Annual Review of Medicine, Vol. 45, Issue 1 https://doi.org/10.1146/annurev.med.45.1.283	journal	February 1994
Intercellular adhesion molecule-1 and CD36 synergize to mediate adherence of Plasmodium falciparum-infected erythrocytes to cultured human microvascular endothelial cells. McCormick, C. J.; Craig, A.; Roberts, D. Journal of Clinical Investigation, Vol. 100, Issue 10 https://doi.org/10.1172/JCI119794	journal	November 1997
Phosphorylation of the VAR2CSA extracellular region is associated with enhanced adhesive properties to the placental receptor CSA Dorin-Semblat, Dominique; Tétard, Marilou; Claës, Aurélie PLOS Biology, Vol. 17, Issue 6 https://doi.org/10.1371/journal.pbio.3000308	journal	June 2019
Plasmodium falciparum Erythrocyte Membrane Protein 1 Diversity in Seven Genomes – Divide and Conquer Rask, Thomas S.; Hansen, Daniel A.; Theander, Thor G. PLoS Computational Biology, Vol. 6, Issue 9 https://doi.org/10.1371/journal.pcbi.1000933	journal	September 2010
Antibodies to a Full-Length VAR2CSA Immunogen Are Broadly Strain-Transcendent but Do Not Cross-Inhibit Different Placental-Type Parasite Isolates Avril, Marion; Hathaway, Marianne J.; Srivastava, Anand PLoS ONE, Vol. 6, Issue 2 https://doi.org/10.1371/journal.pone.0016622	journal	February 2011
Var2CSA Minimal CSA Binding Region Is Located within the N-Terminal Region Srivastava, Anand; Gangnard, Stéphane; Dechavanne, Sébastien PLoS ONE, Vol. 6, Issue 5 https://doi.org/10.1371/journal.pone.0020270	journal	May 2011
The Antibody Response of Pregnant Cameroonian Women to VAR2CSA ID1-ID2a, a Small Recombinant Protein Containing the CSA-Binding Site Babakhanyan, Anna; Leke, Rose G. F.; Salanti, Ali PLoS ONE, Vol. 9, Issue 2 https://doi.org/10.1371/journal.pone.0088173	journal	February 2014
Differential PfEMP1 Expression Is Associated with Cerebral Malaria Pathology Tembo, Dumizulu L.; Nyoni, Benjamin; Murikoli, Rekah V. PLoS Pathogens, Vol. 10, Issue 12 https://doi.org/10.1371/journal.ppat.1004537	journal	December 2014
A Coarse-Grained Molecular Model for Glycosaminoglycans: Application to Chondroitin, Chondroitin Sulfate, and Hyaluronic Acid Bathe, Mark; Rutledge, Gregory C.; Grodzinsky, Alan J. Biophysical Journal, Vol. 88, Issue 6 https://doi.org/10.1529/biophysj.104.058800	journal	June 2005
Placental Monocyte Infiltrates in Response to Plasmodium Falciparum Malaria Infection and Their Association with Adverse Pregnancy Outcomes Molyneux, Malcolm E.; Lema, Valentino M.; Pollina, Elena The American Journal of Tropical Medicine and Hygiene, Vol. 68, Issue 1 https://doi.org/10.4269/ajtmh.2003.68.1.0680115	journal	January 2003
New tools for automated high-resolution cryo-EM structure determination in RELION-3 Zivanov, Jasenko; Nakane, Takanori; Forsberg, Björn O. eLife, Vol. 7 https://doi.org/10.7554/eLife.42166	journal	November 2018

Cited By (1)

Progress and Insights Toward an Effective Placental Malaria Vaccine Gamain, Benoît; Chêne, Arnaud; Viebig, Nicola K. Frontiers in Immunology, Vol. 12 https://doi.org/10.3389/fimmu.2021.634508	journal	February 2021

Similar Records

Overproduction, purification and crystallization of a chondroitin sulfate A-binding DBL domain from a Plasmodium falciparum var2csa-encoded PfEMP1 protein

Journal Article · Fri Feb 29 23:00:00 EST 2008 · Acta Crystallographica. Section F · OSTI ID:22360490

The distinct proteome of placental malaria parasites.

Journal Article · Sat Sep 01 00:00:00 EDT 2007 · Molecular and Biochemical Parasitology, 155(1):57-65 · OSTI ID:977340

Structure of the DBL3x domain of pregnancy-associated malaria protein VAR2CSA complexed with chondroitin sulfate A

Journal Article · Fri Sep 19 00:00:00 EDT 2008 · Nat. Struct. Mol. Biol. · OSTI ID:1006835

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES

Molecular architecture and domain arrangement of the placental malaria protein VAR2CSA suggests a model for carbohydrate binding

Citation Formats

References (77)

Cited By (1)

Similar Records

Related Subjects