Login Register Cart 0
Generic placeholder image

Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Mini-Review Article

Variable Surface Antigens of Plasmodium falciparum: Protein Families with Divergent Roles

Author(s): Jasweer Kaur, Prakash Chandra Mishra and Rachna Hora*

Volume 31, Issue 6, 2024

Published on: 21 June, 2024

Page: [409 - 423] Pages: 15

DOI: 10.2174/0109298665298567240530170924

Abstract

Malaria caused by Plasmodium falciparum (Pf) is an illness that contributes significantly to the global health burden. Pf makes significant alterations to the host cell to meet its metabolic demands and escape the immune response of the host. These include the export of a large number of parasite proteins to the infected Red Blood Cells (iRBC). Variable Surface Antigens (VSAs), which are highly polymorphic protein families with important roles in immune evasion, form an important component of the exported proteins. A total of five protein families constitute the VSAs, viz. PfEMP1 (Pf erythrocyte membrane protein 1), RIFIN (repetitive interspersed family), STEVOR (sub-telomeric open reading frame), SURFIN (surface-associated interspersed gene family), and PfMC-2TM (Pf Maurer’s cleft two transmembrane). With orthologues present in various simian-infecting species, VSAs take up a variety of domain topologies and organizational structures while exhibiting differential expressions throughout the parasite life cycle. Their expression varies across clinical isolates and laboratory strains, which suggests their crucial role in host cell survival and defense. Members of VSAs are reported to contribute significantly to disease pathogenesis through immune evasion processes like cytoadherence, iRBC sequestration in the host vasculature, rosetting, reduced erythrocyte deformability, and direct immunosuppression. In this study, we have gathered information on various aspects of VSAs, like their orthologues, domain architecture, surface topology, functions and interactions, and three-dimensional structures, while emphasizing discoveries in the field. Considering the vast repertoire of Plasmodial VSAs with new emergent functions, a lot remains unknown about these families and, hence, malaria biology.

Next »
Graphical Abstract

[1]
World malaria report 2023. Available from: https://www.who.int/teams/global-malaria-programme/reports/world-malaria-report-2023
[2]
White, N.J.; Ho, M. The Pathophysiology of Malaria.In: Advances in Parasitology; Baker, J.R.; Muller, R., Eds.; Academic Press, 1992, Vol. 31, pp. 83-173.
[http://dx.doi.org/10.1016/S0065-308X(08)60021-4]
[3]
CDC, Malaria, Biology. 2020. Available from: https://www.cdc.gov/malaria/about/biology/index.html
[4]
Marti, M.; Good, R.T.; Rug, M.; Knuepfer, E.; Cowman, A.F. Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science, 2004, 306(5703), 1930-1933.
[http://dx.doi.org/10.1126/science.1102452] [PMID: 15591202]
[5]
Hiller, N.L.; Bhattacharjee, S.; Van Ooij, C.; Liolios, K.; Harrison, T.; Lopez-Estraño, C.; Haldar, K. A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science, 2004, 306(5703), 1934-1937.
[http://dx.doi.org/10.1126/science.1102737] [PMID: 15591203]
[6]
Maier, A.G.; Rug, M.; O’Neill, M.T.; Brown, M.; Chakravorty, S.; Szestak, T.; Chesson, J.; Wu, Y.; Hughes, K.; Coppel, R.L.; Newbold, C.; Beeson, J.G.; Craig, A.; Crabb, B.S.; Cowman, A.F. Exported proteins required for virulence and rigidity of Plasmodium falciparum-infected human erythrocytes. Cell, 2008, 134(1), 48-61.
[http://dx.doi.org/10.1016/j.cell.2008.04.051] [PMID: 18614010]
[7]
Mundwiler-Pachlatko, E.; Beck, H.P. Maurer’s clefts, the enigma of Plasmodium falciparum. Proc. Natl. Acad. Sci. USA, 2013, 110(50), 19987-19994.
[http://dx.doi.org/10.1073/pnas.1309247110] [PMID: 24284172]
[8]
Petersen, W.; Külzer, S.; Engels, S.; Zhang, Q.; Ingmundson, A.; Rug, M.; Maier, A.G.; Przyborski, J.M. J-dot targeting of an exported HSP40 in Plasmodium falciparum-infected erythrocytes. Int. J. Parasitol., 2016, 46(8), 519-525.
[http://dx.doi.org/10.1016/j.ijpara.2016.03.005] [PMID: 27063072]
[9]
Kriek, N.; Tilley, L.; Horrocks, P.; Pinches, R.; Elford, B.C.; Ferguson, D.J.P.; Lingelbach, K.; Newbold, C.I. Characterization of the pathway for transport of the cytoadherence-mediating protein, PfEMP1, to the host cell surface in malaria parasite-infected erythrocytes. Mol. Microbiol., 2003, 50(4), 1215-1227.
[http://dx.doi.org/10.1046/j.1365-2958.2003.03784.x] [PMID: 14622410]
[10]
Leech, J.H.; Barnwell, J.W.; Miller, L.H.; Howard, R.J. Identification of a strain-specific malarial antigen exposed on the surface of Plasmodium falciparum-infected erythrocytes. J. Exp. Med., 1984, 159(6), 1567-1575.
[http://dx.doi.org/10.1084/jem.159.6.1567] [PMID: 6374009]
[11]
Fernandez, V.; Hommel, M.; Chen, Q.; Hagblom, P.; Wahlgren, M. Small, clonally variant antigens expressed on the surface of the Plasmodium falciparum-infected erythrocyte are encoded by the rif gene family and are the target of human immune responses. J. Exp. Med., 1999, 190(10), 1393-1404.
[http://dx.doi.org/10.1084/jem.190.10.1393] [PMID: 10562315]
[12]
Kyes, S.A.; Rowe, J.A.; Kriek, N.; Newbold, C.I. Rifins: A second family of clonally variant proteins expressed on the surface of red cells infected with Plasmodium falciparum. Proc. Natl. Acad. Sci. USA, 1999, 96(16), 9333-9338.
[http://dx.doi.org/10.1073/pnas.96.16.9333] [PMID: 10430943]
[13]
Blythe, J.E.; Yam, X.Y.; Kuss, C.; Bozdech, Z.; Holder, A.A.; Marsh, K.; Langhorne, J.; Preiser, P.R. Plasmodium falciparum STEVOR proteins are highly expressed in patient isolates and located in the surface membranes of infected red blood cells and the apical tips of merozoites. Infect. Immun., 2008, 76(7), 3329-3336.
[http://dx.doi.org/10.1128/IAI.01460-07] [PMID: 18474651]
[14]
Kaviratne, M.; Khan, S.M.; Jarra, W.; Preiser, P.R. Small variant STEVOR antigen is uniquely located within Maurer’s clefts in Plasmodium falciparum-infected red blood cells. Eukaryot. Cell, 2002, 1(6), 926-935.
[http://dx.doi.org/10.1128/EC.1.6.926-935.2002] [PMID: 12477793]
[15]
Niang, M.; Yan Yam, X.; Preiser, P.R. The Plasmodium falciparum STEVOR multigene family mediates antigenic variation of the infected erythrocyte. PLoS Pathog., 2009, 5(2), e1000307.
[http://dx.doi.org/10.1371/journal.ppat.1000307] [PMID: 19229319]
[16]
Winter, G.; Kawai, S.; Haeggström, M.; Kaneko, O.; von Euler, A.; Kawazu, S.; Palm, D.; Fernandez, V.; Wahlgren, M. SURFIN is a polymorphic antigen expressed on Plasmodium falciparum merozoites and infected erythrocytes. J. Exp. Med., 2005, 201(11), 1853-1863.
[http://dx.doi.org/10.1084/jem.20041392] [PMID: 15939796]
[17]
Lavazec, C.; Sanyal, S.; Templeton, T.J. Hypervariability within the Rifin, Stevor and Pfmc-2TM superfamilies in Plasmodium falciparum. Nucleic Acids Res., 2006, 34(22), 6696-6707.
[http://dx.doi.org/10.1093/nar/gkl942] [PMID: 17148488]
[18]
Sam-Yellowe, T.Y.; Florens, L.; Johnson, J.R.; Wang, T.; Drazba, J.A.; Le Roch, K.G.; Zhou, Y.; Batalov, S.; Carucci, D.J.; Winzeler, E.A.; Yates, J.R., III A Plasmodium gene family encoding Maurer’s cleft membrane proteins: structural properties and expression profiling. Genome Res., 2004, 14(6), 1052-1059.
[http://dx.doi.org/10.1101/gr.2126104] [PMID: 15140830]
[19]
Wahlgren, M.; Goel, S.; Akhouri, R.R. Variant surface antigens of Plasmodium falciparum and their roles in severe malaria. Nat. Rev. Microbiol., 2017, 15(8), 479-491.
[http://dx.doi.org/10.1038/nrmicro.2017.47] [PMID: 28603279]
[20]
Howitt, C.A.; Wilinski, D.; Llinás, M.; Templeton, T.J.; Dzikowski, R.; Deitsch, K.W. Clonally variant gene families in Plasmodium falciparum share a common activation factor. Mol. Microbiol., 2009, 73(6), 1171-1185.
[http://dx.doi.org/10.1111/j.1365-2958.2009.06846.x] [PMID: 19708920]
[21]
Guizetti, J.; Scherf, A. Silence, activate, poise and switch! Mechanisms of antigenic variation inPlasmodium falciparum. Cell. Microbiol., 2013, 15(5), 718-726.
[http://dx.doi.org/10.1111/cmi.12115] [PMID: 23351305]
[22]
Nash, G.B.; Cooke, B.M.; Carlson, J.; Wahlgren, M. Rheological properties of rosettes formed by red blood cells parasitized by Plasmodium falciparum. Br. J. Haematol., 1992, 82(4), 757-763.
[http://dx.doi.org/10.1111/j.1365-2141.1992.tb06955.x] [PMID: 1482664]
[23]
Thiagarajan, P.; Parker, C.J.; Prchal, J.T. How Do Red Blood Cells Die? Front. Physiol., 2021, 12, 655393.
[http://dx.doi.org/10.3389/fphys.2021.655393] [PMID: 33790808]
[24]
Lee, W.C.; Russell, B.; Rénia, L. Sticking for a cause: The falciparum malaria parasites cytoadherence paradigm. Front. Immunol., 2019, 10, 1444.
[http://dx.doi.org/10.3389/fimmu.2019.01444] [PMID: 31316507]
[25]
Kaul, D.K.; Roth, E.F.J., Jr; Nagel, R.L.; Howard, R.J.; Handunnetti, S.M. Rosetting of Plasmodium falciparum-infected red blood cells with uninfected red blood cells enhances microvascular obstruction under flow conditions. Blood, 1991, 78(3), 812-819.
[http://dx.doi.org/10.1182/blood.V78.3.812.812] [PMID: 1859893]
[26]
Treutiger, C.J.; Carlson, J.; Greenwood, B.M.; Wahlgren, M.; Jepson, A.; Helmby, H.; Kwiatkowski, D.; Hedlund, I.; Twumasi, P. Rosette formation in Plasmodium falciparum isolates and anti-rosette activity of sera from Gambians with cerebral or uncomplicated malaria. Am. J. Trop. Med. Hyg., 1992, 46(5), 503-510.
[http://dx.doi.org/10.4269/ajtmh.1992.46.503] [PMID: 1599043]
[27]
Rowe, J.A.; Raza, A.; Obiero, J.; Marsh, K. Short report: Positive correlation between rosetting and parasitemia in Plasmodium falciparum clinical isolates. Am. J. Trop. Med. Hyg., 2002, 66(5), 458-460.
[http://dx.doi.org/10.4269/ajtmh.2002.66.458] [PMID: 12201576]
[28]
Carlson, J.; Nash, G.B.; Gabutti, V.; al-Yaman, F.; Wahlgren, M. Natural protection against severe Plasmodium falciparum malaria due to impaired rosette formation. Blood, 1994, 84(11), 3909-3914.
[http://dx.doi.org/10.1182/blood.V84.11.3909.bloodjournal84113909] [PMID: 7949147]
[29]
Rowe, A.; Obeiro, J.; Newbold, C.I.; Marsh, K. Plasmodium falciparum rosetting is associated with malaria severity in Kenya. Infect. Immun., 1995, 63(6), 2323-2326.
[http://dx.doi.org/10.1128/iai.63.6.2323-2326.1995] [PMID: 7768616]
[30]
Doumbo, O.K.; Plowe, C.V.; Lyke, K.E.; Raza, A.; Tempest, L.J.; Rowe, J.A.; Koné, A.K.; Thera, M.A. High levels of Plasmodium falciparum rosetting in all clinical forms of severe malaria in African children. Am. J. Trop. Med. Hyg., 2009, 81(6), 987-993.
[http://dx.doi.org/10.4269/ajtmh.2009.09-0406] [PMID: 19996426]
[31]
Carlson, J.; Helmby, H.; Wahlgren, M.; Carlson, J.; Helmby, H.; Wahlgren, M.; Hill, A.; Brewster, D.; Greenwood, B.M. Human cerebral malaria: association with erythrocyte rosetting and lack of anti-rosetting antibodies. Lancet, 1990, 336(8729), 1457-1460.
[http://dx.doi.org/10.1016/0140-6736(90)93174-N] [PMID: 1979090]
[32]
Al-Yaman, F.; Genton, B.; Mokela, D.; Raiko, A.; Kati, S.; Rogerson, S.; Reeder, J.; Alpers, M. Human cerebral malaria: lack of significant association between erythrocyte resetting and disease severity. Trans. R. Soc. Trop. Med. Hyg., 1995, 89(1), 55-58.
[http://dx.doi.org/10.1016/0035-9203(95)90658-4] [PMID: 7747308]
[33]
Rogerson, S.J.; Beck, H.P.; Al-Yaman, F.; Currie, B.; Alpers, M.P.; Brown, G.V. Disruption of erythrocyte rosettes and agglutination of erythrocytes infected with Plasmodium falciparum by the sera of Papua New Guineans. Trans. R. Soc. Trop. Med. Hyg., 1996, 90(1), 80-84.
[http://dx.doi.org/10.1016/S0035-9203(96)90487-3] [PMID: 8730319]
[34]
Rogerson, S.J.; Plitt, S.; Taylor, T.E.; Dobaño, C.; Tembenu, R.; Molyneux, M.E. Cytoadherence characteristics of Plasmodium falciparum-infected erythrocytes from Malawian children with severe and uncomplicated malaria. Am. J. Trop. Med. Hyg., 1999, 61(3), 467-472.
[http://dx.doi.org/10.4269/ajtmh.1999.61.467] [PMID: 10497992]
[35]
Angkasekwinai, P.; Looareesuwan, S.; Chaiyaroj, S.C. Lack of significant association between rosette formation and parasitized erythrocyte adherence to purified CD36. Southeast Asian J. Trop. Med. Public Health, 1998, 29(1), 41-45.
[PMID: 9740266]
[36]
Sherman, I.W.; Eda, S.; Winograd, E. Cytoadherence and sequestration in Plasmodium falciparum: defining the ties that bind. Microbes Infect., 2003, 5(10), 897-909.
[http://dx.doi.org/10.1016/S1286-4579(03)00162-X] [PMID: 12919858]
[37]
McHugh, E.; Carmo, O.M.S.; Blanch, A.; Looker, O.; Liu, B.; Tiash, S.; Andrew, D.; Batinovic, S.; Low, A.J.Y.; Cho, H.J.; McMillan, P.; Tilley, L.; Dixon, M.W.A. Role of Plasmodium falciparum protein GEXP07 in Maurer’s cleft morphology, knob architecture, and P. falciparum EMP1 trafficking. MBio, 2020, 11(2), e03320-19.
[http://dx.doi.org/10.1128/mBio.03320-19] [PMID: 32184257]
[38]
Lee, W.C.; Russell, B.; Lee, B.; Chu, C.S.; Phyo, A.P.; Sriprawat, K.; Lau, Y.L.; Nosten, F.; Rénia, L. Plasmodium falciparum rosetting protects schizonts against artemisinin. EBioMedicine, 2021, 73, 103680.
[http://dx.doi.org/10.1016/j.ebiom.2021.103680] [PMID: 34749300]
[39]
Lee, W.C.; Russell, B.; Lau, Y.L.; Nosten, F.; Rénia, L. Rosetting responses of Plasmodium-infected erythrocytes to antimalarials. Am. J. Trop. Med. Hyg., 2022, 106(6), 1670-1674.
[http://dx.doi.org/10.4269/ajtmh.21-1229] [PMID: 35405642]
[40]
Yam, X.Y.; Niang, M.; Madnani, K.G.; Preiser, P.R. Three is a crowd – New insights into rosetting in Plasmodium falciparum. Trends Parasitol., 2017, 33(4), 309-320.
[http://dx.doi.org/10.1016/j.pt.2016.12.012] [PMID: 28109696]
[41]
Urban, B.C.; Willcox, N.; Roberts, D.J. A role for CD36 in the regulation of dendritic cell function. Proc. Natl. Acad. Sci. USA, 2001, 98(15), 8750-8755.
[http://dx.doi.org/10.1073/pnas.151028698] [PMID: 11447263]
[42]
D’Ombrain, M.C.; Voss, T.S.; Maier, A.G.; Pearce, J.A.; Hansen, D.S.; Cowman, A.F.; Schofield, L. Plasmodium falciparum erythrocyte membrane protein-1 specifically suppresses early production of host interferon-gamma. Cell Host Microbe, 2007, 2(2), 130-138.
[http://dx.doi.org/10.1016/j.chom.2007.06.012] [PMID: 18005727]
[43]
Ji, C.; Shen, H.; Su, C.; Li, Y.; Chen, S.; Sharp, T.H.; Xiao, J. Plasmodium falciparum has evolved multiple mechanisms to hijack human immunoglobulin M. Nat. Commun., 2023, 14(1), 2650.
[http://dx.doi.org/10.1038/s41467-023-38320-z] [PMID: 37156765]
[44]
Harrison, T.E.; Mørch, A.M.; Felce, J.H.; Sakoguchi, A.; Reid, A.J.; Arase, H.; Dustin, M.L.; Higgins, M.K. Structural basis for RIFIN-mediated activation of LILRB1 in malaria. Nature, 2020, 587(7833), 309-312.
[http://dx.doi.org/10.1038/s41586-020-2530-3] [PMID: 32650338]
[45]
Chen, Y.; Xu, K.; Piccoli, L.; Foglierini, M.; Tan, J.; Jin, W.; Gorman, J.; Tsybovsky, Y.; Zhang, B.; Traore, B.; Silacci-Fregni, C.; Daubenberger, C.; Crompton, P.D.; Geiger, R.; Sallusto, F.; Kwong, P.D.; Lanzavecchia, A. Structural basis of malaria RIFIN binding by LILRB1-containing antibodies. Nature, 2021, 592(7855), 639-643.
[http://dx.doi.org/10.1038/s41586-021-03378-6] [PMID: 33790470]
[46]
Sakoguchi, A.; Saito, F.; Hirayasu, K.; Shida, K.; Matsuoka, S.; Itagaki, S.; Nakai, W.; Kohyama, M.; Suenaga, T.; Iwanaga, S.; Horii, T.; Arase, H. Plasmodium falciparum RIFIN is a novel ligand for inhibitory immune receptor LILRB2. Biochem. Biophys. Res. Commun., 2021, 548, 167-173.
[http://dx.doi.org/10.1016/j.bbrc.2021.02.033] [PMID: 33647792]
[47]
Pasternak, N.D.; Dzikowski, R. PfEMP1: An antigen that plays a key role in the pathogenicity and immune evasion of the malaria parasite Plasmodium falciparum. Int. J. Biochem. Cell Biol., 2009, 41(7), 1463-1466.
[http://dx.doi.org/10.1016/j.biocel.2008.12.012] [PMID: 19150410]
[48]
Baruch, D.I.; Pasloske, B.L.; Singh, H.B.; Bi, X.; Ma, X.C.; Feldman, M.; Taraschi, T.F.; Howard, R.J. Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell, 1995, 82(1), 77-87.
[http://dx.doi.org/10.1016/0092-8674(95)90054-3] [PMID: 7541722]
[49]
Smith, J.D.; Chitnis, C.E.; Craig, A.G.; Roberts, D.J.; Hudson-Taylor, D.E.; Peterson, D.S.; Pinches, R.; Newbold, C.I.; Miller, L.H. Switches in expression of Plasmodium falciparum var. genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell, 1995, 82(1), 101-110.
[http://dx.doi.org/10.1016/0092-8674(95)90056-X] [PMID: 7606775]
[50]
zhuan, S.X.; Heatwole , V.M.; Wertheimer, S.P. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell., 1995, 82(1), 89-100.
[http://dx.doi.org/10.1016/0092-8674(95)90055-1]
[51]
Gardner, M.J.; Hall, N.; Fung, E.; White, O.; Berriman, M.; Hyman, R.W.; Carlton, J.M.; Pain, A.; Nelson, K.E.; Bowman, S.; Paulsen, I.T.; James, K.; Eisen, J.A.; Rutherford, K.; Salzberg, S.L.; Craig, A.; Kyes, S.; Chan, M.S.; Nene, V.; Shallom, S.J.; Suh, B.; Peterson, J.; Angiuoli, S.; Pertea, M.; Allen, J.; Selengut, J.; Haft, D.; Mather, M.W.; Vaidya, A.B.; Martin, D.M.A.; Fairlamb, A.H.; Fraunholz, M.J.; Roos, D.S.; Ralph, S.A.; McFadden, G.I.; Cummings, L.M.; Subramanian, G.M.; Mungall, C.; Venter, J.C.; Carucci, D.J.; Hoffman, S.L.; Newbold, C.; Davis, R.W.; Fraser, C.M.; Barrell, B. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature, 2002, 419(6906), 498-511.
[http://dx.doi.org/10.1038/nature01097] [PMID: 12368864]
[52]
Smith, J.D.; Gamain, B.; Baruch, D.I.; Kyes, S. Decoding the language of var genes and Plasmodium falciparum sequestration. Trends Parasitol., 2001, 17(11), 538-545.
[http://dx.doi.org/10.1016/S1471-4922(01)02079-7] [PMID: 11872399]
[53]
Kirchgatter, K.; Mosbach, R.; del Portillo, H.A. Plasmodium falciparum: DBL-1 var sequence analysis in field isolates from central Brazil. Exp. Parasitol., 2000, 95(2), 154-157.
[http://dx.doi.org/10.1006/expr.2000.4520] [PMID: 10910718]
[54]
Kyes, S.; Pinches, R.; Newbold, C. A simple RNA analysis method shows var and rif multigene family expression patterns in Plasmodium falciparum. Mol. Biochem. Parasitol., 2000, 105(2), 311-315.
[http://dx.doi.org/10.1016/S0166-6851(99)00193-0] [PMID: 10693754]
[55]
Quadt, K.A.; Barfod, L.; Andersen, D.; Bruun, J.; Gyan, B.; Hassenkam, T.; Ofori, M.F.; Hviid, L. The density of knobs on Plasmodium falciparum-infected erythrocytes depends on developmental age and varies among isolates. PLoS One, 2012, 7(9), e45658.
[http://dx.doi.org/10.1371/journal.pone.0045658] [PMID: 23029166]
[56]
Cheng, Q.; Cloonan, N.; Fischer, K.; Thompson, J.; Waine, G.; Lanzer, M.; Saul, A. stevor and rif are Plasmodium falciparum multicopy gene families which potentially encode variant antigens. Mol. Biochem. Parasitol., 1998, 97(1-2), 161-176.
[http://dx.doi.org/10.1016/S0166-6851(98)00144-3] [PMID: 9879895]
[57]
Scherf, A.; Lopez-Rubio, J.J.; Rivière, L. Antigenic variation in Plasmodium falciparum. Annu. Rev. Microbiol., 2008, 62(1), 445-470.
[http://dx.doi.org/10.1146/annurev.micro.61.080706.093134] [PMID: 18785843]
[58]
Hodder, A.N.; Czabotar, P.E.; Uboldi, A.D.; Clarke, O.B.; Lin, C.S.; Healer, J.; Smith, B.J.; Cowman, A.F. Insights into Duffy binding-like domains through the crystal structure and function of the merozoite surface protein MSPDBL2 from Plasmodium falciparum. J. Biol. Chem., 2012, 287(39), 32922-32939.
[http://dx.doi.org/10.1074/jbc.M112.350504] [PMID: 22843685]
[59]
Hsieh, F.L.; Turner, L.; Bolla, J.R.; Robinson, C.V.; Lavstsen, T.; Higgins, M.K. The structural basis for CD36 binding by the malaria parasite. Nat. Commun., 2016, 7(1), 12837.
[http://dx.doi.org/10.1038/ncomms12837] [PMID: 27667267]
[60]
Clausen, T.M.; Christoffersen, S.; Dahlbäck, M.; Langkilde, A.E.; Jensen, K.E.; Resende, M.; Agerbæk, M.Ø.; Andersen, D.; Berisha, B.; Ditlev, S.B.; Pinto, V.V.; Nielsen, M.A.; Theander, T.G.; Larsen, S.; Salanti, A. Structural and functional insight into how the Plasmodium falciparum VAR2CSA protein mediates binding to chondroitin sulfate A in placental malaria. J. Biol. Chem., 2012, 287(28), 23332-23345.
[http://dx.doi.org/10.1074/jbc.M112.348839] [PMID: 22570492]
[61]
Hadjilaou, A.; Brandi, J.; Riehn, M.; Friese, M.A.; Jacobs, T. Pathogenetic mechanisms and treatment targets in cerebral malaria. Nat. Rev. Neurol., 2023, 19(11), 688-709.
[http://dx.doi.org/10.1038/s41582-023-00881-4] [PMID: 37857843]
[62]
Bouwens, E.A.M.; Tamayo, I.; Turner, L.; Wang, C.W.; Stins, M.; Theander, T.G.; Petersen, J.E.V.; Hermida, J.; Mosnier, L.O.; Lavstsen, T. Protein C system defects inflicted by the malaria parasite protein PfEMP1 can be overcome by a soluble EPCR variant. Thromb. Haemost., 2015, 114(11), 1038-1048.
[http://dx.doi.org/10.1160/TH15-01-0018] [PMID: 26155776]
[63]
Krych-Goldberg, M.; Moulds, J.M.; Atkinson, J.P. Human complement receptor type 1 (CR1) binds to a major malarial adhesin. Trends Mol. Med., 2002, 8(11), 531-537.
[http://dx.doi.org/10.1016/S1471-4914(02)02419-X] [PMID: 12421687]
[64]
Barragan, A.; Kremsner, P.G.; Wahlgren, M.; Carlson, J. Blood group A antigen is a coreceptor in Plasmodium falciparum rosetting. Infect. Immun., 2000, 68(5), 2971-2975.
[http://dx.doi.org/10.1128/IAI.68.5.2971-2975.2000] [PMID: 10768996]
[65]
Angeletti, D.; Sandalova, T.; Wahlgren, M.; Achour, A. Binding of subdomains 1/2 of PfEMP1-DBL1α to heparan sulfate or heparin mediates Plasmodium falciparum rosetting. PLoS One, 2015, 10(3), e0118898.
[http://dx.doi.org/10.1371/journal.pone.0118898] [PMID: 25742651]
[66]
Hora, R.; Bridges, D.J.; Craig, A.; Sharma, A. Erythrocytic casein kinase II regulates cytoadherence of Plasmodium falciparum-infected red blood cells. J. Biol. Chem., 2009, 284(10), 6260-6269.
[http://dx.doi.org/10.1074/jbc.M809756200] [PMID: 19131328]
[67]
Kumar, V.; Kaur, J.; Singh, A.P.; Singh, V.; Bisht, A.; Panda, J.J.; Mishra, P.C.; Hora, R. PHIST c protein family members localize to different subcellular organelles and bind Plasmodium falciparum major virulence factor PfEMP-1. FEBS J., 2018, 285(2), 294-312.
[http://dx.doi.org/10.1111/febs.14340] [PMID: 29155505]
[68]
Oberli, , A.; Slater, L.M.; Cutts, E.; Brand, F. A Plasmodium falciparum PHIST protein binds the virulence factor PfEMP1 and comigrates to knobs on the host cell surface FASEB J., 28(10), 4420-4433.
[69]
Tolia, N.H.; Enemark, E.J.; Sim, B.K.L.; Joshua-Tor, L. Structural basis for the EBA-175 erythrocyte invasion pathway of the malaria parasite Plasmodium falciparum. Cell, 2005, 122(2), 183-193.
[http://dx.doi.org/10.1016/j.cell.2005.05.033] [PMID: 16051144]
[70]
Singh, S.K.; Hora, R.; Belrhali, H.; Chitnis, C.E.; Sharma, A. Structural basis for Duffy recognition by the malaria parasite Duffy-binding-like domain. Nature, 2006, 439(7077), 741-744.
[http://dx.doi.org/10.1038/nature04443] [PMID: 16372020]
[71]
Burley, S.K.; Berman, H.M.; Duarte, J.M.; Feng, Z.; Flatt, J.W.; Hudson, B.P.; Lowe, R.; Peisach, E.; Piehl, D.W.; Rose, Y.; Sali, A.; Sekharan, M.; Shao, C.; Vallat, B.; Voigt, M.; Westbrook, J.D.; Young, J.Y.; Zardecki, C. Protein Data Bank: A Comprehensive Review of 3D Structure Holdings and Worldwide Utilization by Researchers, Educators, and Students. Biomolecules, 2022, 12(10), 1425.
[http://dx.doi.org/10.3390/biom12101425] [PMID: 36291635]
[72]
Wang, K.; Dagil, R.; Lavstsen, T.; Misra, S.K.; Spliid, C.B.; Wang, Y.; Gustavsson, T.; Sandoval, D.R.; Vidal-Calvo, E.E.; Choudhary, S.; Agerbaek, M.Ø.; Lindorff-Larsen, K.; Nielsen, M.A.; Theander, T.G.; Sharp, J.S.; Clausen, T.M.; Gourdon, P.; Salanti, A. Cryo-EM reveals the architecture of placental malaria VAR2CSA and provides molecular insight into chondroitin sulfate binding. Nat. Commun., 2021, 12(1), 2956.
[http://dx.doi.org/10.1038/s41467-021-23254-1] [PMID: 34011972]
[73]
Wang, W.; Wang, Z.; Yang, X.; Gao, Y.; Zhang, X.; Cao, L.; Dai, A.; Sun, J.; Sun, L.; Jiang, L.; Chen, Z.; Wang, L. The molecular mechanism of cytoadherence to placental or tumor cells through VAR2CSA from Plasmodium falciparum. Cell Discov., 2021, 7(1), 94.
[http://dx.doi.org/10.1038/s41421-021-00324-8] [PMID: 34663782]
[74]
Raghavan, S.S.R.; Dagil, R.; Lopez-Perez, M.; Conrad, J.; Bassi, M.R.; Quintana, M.P.; Choudhary, S.; Gustavsson, T.; Wang, Y.; Gourdon, P.; Ofori, M.F.; Christensen, S.B.; Minja, D.T.R.; Schmiegelow, C.; Nielsen, M.A.; Barfod, L.; Hviid, L.; Salanti, A.; Lavstsen, T.; Wang, K. Cryo-EM reveals the conformational epitope of human monoclonal antibody PAM1.4 broadly reacting with polymorphic malarial protein VAR2CSA. PLoS Pathog., 2022, 18(11), e1010924.
[http://dx.doi.org/10.1371/journal.ppat.1010924] [PMID: 36383559]
[75]
Mayer, C.; Slater, L.; Erat, M.C.; Konrat, R.; Vakonakis, I. Structural analysis of the Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) intracellular domain reveals a conserved interaction epitope. J. Biol. Chem., 2012, 287(10), 7182-7189.
[http://dx.doi.org/10.1074/jbc.M111.330779] [PMID: 22249178]
[76]
Joannin, N.; Abhiman, S.; Sonnhammer, E.L.; Wahlgren, M. Sub-grouping and sub-functionalization of the RIFIN multi-copy protein family. BMC Genomics, 2008, 9(1), 19.
[http://dx.doi.org/10.1186/1471-2164-9-19] [PMID: 18197962]
[77]
Kaur, J.; Hora, R. ‘2TM proteins’: an antigenically diverse superfamily with variable functions and export pathways. PeerJ, 2018, 6, e4757.
[http://dx.doi.org/10.7717/peerj.4757] [PMID: 29770278]
[78]
Petter, M.; Haeggström, M.; Khattab, A.; Fernandez, V.; Klinkert, M.Q.; Wahlgren, M. Variant proteins of the Plasmodium falciparum RIFIN family show distinct subcellular localization and developmental expression patterns. Mol. Biochem. Parasitol., 2007, 156(1), 51-61.
[http://dx.doi.org/10.1016/j.molbiopara.2007.07.011] [PMID: 17719658]
[79]
Florens, L.; Washburn, M.P.; Raine, J.D.; Anthony, R.M.; Grainger, M.; Haynes, J.D.; Moch, J.K.; Muster, N.; Sacci, J.B.; Tabb, D.L.; Witney, A.A.; Wolters, D.; Wu, Y.; Gardner, M.J.; Holder, A.A.; Sinden, R.E.; Yates, J.R.; Carucci, D.J. A proteomic view of the Plasmodium falciparum life cycle. Nature, 2002, 419(6906), 520-526.
[http://dx.doi.org/10.1038/nature01107] [PMID: 12368866]
[80]
Goel, S.; Palmkvist, M.; Moll, K.; Joannin, N.; Lara, P.; R Akhouri, R.; Moradi, N.; Öjemalm, K.; Westman, M.; Angeletti, D.; Kjellin, H.; Lehtiö, J.; Blixt, O.; Ideström, L.; Gahmberg, C.G.; Storry, J.R.; Hult, A.K.; Olsson, M.L.; von Heijne, G.; Nilsson, I.; Wahlgren, M. RIFINs are adhesins implicated in severe Plasmodium falciparum malaria. Nat. Med., 2015, 21(4), 314-317.
[http://dx.doi.org/10.1038/nm.3812] [PMID: 25751816]
[81]
Colonna, M.; Navarro, F.; Bellón, T.; Llano, M.; García, P.; Samaridis, J.; Angman, L.; Cella, M.; López-Botet, M. A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and myelomonocytic cells. J. Exp. Med., 1997, 186(11), 1809-1818.
[http://dx.doi.org/10.1084/jem.186.11.1809] [PMID: 9382880]
[82]
Shiroishi, M.; Kuroki, K.; Rasubala, L.; Tsumoto, K.; Kumagai, I.; Kurimoto, E.; Kato, K.; Kohda, D.; Maenaka, K. Structural basis for recognition of the nonclassical MHC molecule HLA-G by the leukocyte Ig-like receptor B2 (LILRB2/ LIR2/ILT4/CD85d). Proc. Natl. Acad. Sci. USA, 2006, 103(44), 16412-16417.
[http://dx.doi.org/10.1073/pnas.0605228103] [PMID: 17056715]
[83]
Prod’homme, V; Griffin, C; Aicheler, RJ The human cytomegalovirus MHC class I homolog UL18 inhibits LIR-1+ but activates LIR-1- NK cells. J. Immunol., 2007, 178(7), 4473-4481.
[http://dx.doi.org/10.4049/jimmunol.178.7.4473]
[84]
Chan, K.R.; Ong, E.Z.; Tan, H.C.; Zhang, S.L.X.; Zhang, Q.; Tang, K.F.; Kaliaperumal, N.; Lim, A.P.C.; Hibberd, M.L.; Chan, S.H.; Connolly, J.E.; Krishnan, M.N.; Lok, S.M.; Hanson, B.J.; Lin, C.N.; Ooi, E.E. Leukocyte immunoglobulin-like receptor B1 is critical for antibody-dependent dengue. Proc. Natl. Acad. Sci. USA, 2014, 111(7), 2722-2727.
[http://dx.doi.org/10.1073/pnas.1317454111] [PMID: 24550301]
[85]
Bashirova, A.A.; Martin-Gayo, E.; Jones, D.C.; Qi, Y.; Apps, R.; Gao, X.; Burke, P.S.; Taylor, C.J.; Rogich, J.; Wolinsky, S.; Bream, J.H.; Duggal, P.; Hussain, S.; Martinson, J.; Weintrob, A.; Kirk, G.D.; Fellay, J.; Buchbinder, S.P.; Goedert, J.J.; Deeks, S.G.; Pereyra, F.; Trowsdale, J.; Lichterfeld, M.; Telenti, A.; Walker, B.D.; Allen, R.L.; Carrington, M.; Yu, X.G. LILRB2 interaction with HLA class I correlates with control of HIV-1 infection. PLoS Genet., 2014, 10(3), e1004196.
[http://dx.doi.org/10.1371/journal.pgen.1004196] [PMID: 24603468]
[86]
Chen, H.M.; van der Touw, W.; Wang, Y.S.; Kang, K.; Mai, S.; Zhang, J.; Alsina-Beauchamp, D.; Duty, J.A.; Mungamuri, S.K.; Zhang, B.; Moran, T.; Flavell, R.; Aaronson, S.; Hu, H.M.; Arase, H.; Ramanathan, S.; Flores, R.; Pan, P.Y.; Chen, S.H. Blocking immunoinhibitory receptor LILRB2 reprograms tumor-associated myeloid cells and promotes antitumor immunity. J. Clin. Invest., 2018, 128(12), 5647-5662.
[http://dx.doi.org/10.1172/JCI97570] [PMID: 30352428]
[87]
Saito, F.; Hirayasu, K.; Satoh, T.; Wang, C.W.; Lusingu, J.; Arimori, T.; Shida, K.; Palacpac, N.M.Q.; Itagaki, S.; Iwanaga, S.; Takashima, E.; Tsuboi, T.; Kohyama, M.; Suenaga, T.; Colonna, M.; Takagi, J.; Lavstsen, T.; Horii, T.; Arase, H. Immune evasion of Plasmodium falciparum by RIFIN via inhibitory receptors. Nature, 2017, 552(7683), 101-105.
[http://dx.doi.org/10.1038/nature24994] [PMID: 29186116]
[88]
Lebbink, R.J.; de Ruiter, T.; Adelmeijer, J.; Brenkman, A.B.; van Helvoort, J.M.; Koch, M.; Farndale, R.W.; Lisman, T.; Sonnenberg, A.; Lenting, P.J.; Meyaard, L. Collagens are functional, high affinity ligands for the inhibitory immune receptor LAIR-1. J. Exp. Med., 2006, 203(6), 1419-1425.
[http://dx.doi.org/10.1084/jem.20052554] [PMID: 16754721]
[89]
Son, M.; Santiago-Schwarz, F.; Al-Abed, Y.; Diamond, B. C1q limits dendritic cell differentiation and activation by engaging LAIR-1. Proc. Natl. Acad. Sci. USA, 2012, 109(46), E3160-E3167.
[http://dx.doi.org/10.1073/pnas.1212753109] [PMID: 23093673]
[90]
Olde Nordkamp, M.J.M.; Van Eijk, M.; Urbanus, R.T.; Bont, L.; Haagsman, H.P.; Meyaard, L. Leukocyte-associated Ig-like receptor-1 is a novel inhibitory receptor for surfactant protein D. J. Leukoc. Biol., 2014, 96(1), 105-111.
[http://dx.doi.org/10.1189/jlb.3AB0213-092RR] [PMID: 24585933]
[91]
Huang, H.; Li, T.; Ye, G.; Zhao, L.; Zhang, Z.; Mo, D.; Wang, Y.; Zhang, C.; Deng, H.; Li, G.; Liu, H. High expression of COL10A1 is associated with poor prognosis in colorectal cancer. OncoTargets Ther., 2018, 11, 1571-1581.
[http://dx.doi.org/10.2147/OTT.S160196] [PMID: 29593423]
[92]
Wu, Y-H.; Chang, T-H.; Huang, Y-F.; Huang, H-D.; Chou, C-Y. COL11A1 promotes tumor progression and predicts poor clinical outcome in ovarian cancer. Oncogene, 2014, 33(26), 3432-3440.
[http://dx.doi.org/10.1038/onc.2013.307] [PMID: 23934190]
[93]
Ke, Z.; He, W.; Lai, Y.; Guo, X.; Chen, S.; Li, S.; Wang, Y.; Wang, L. Overexpression of Collagen Triple Helix Repeat Containing 1 (CTHRC1) is associated with tumour aggressiveness and poor prognosis in human non-small cell lung cancer. Oncotarget, 2014, 5(19), 9410-9424.
[http://dx.doi.org/10.18632/oncotarget.2421] [PMID: 25238260]
[94]
Tan, J.; Pieper, K.; Piccoli, L.; Abdi, A.; Foglierini, M.; Geiger, R.; Maria Tully, C.; Jarrossay, D.; Maina Ndungu, F.; Wambua, J.; Bejon, P.; Silacci Fregni, C.; Fernandez-Rodriguez, B.; Barbieri, S.; Bianchi, S.; Marsh, K.; Thathy, V.; Corti, D.; Sallusto, F.; Bull, P.; Lanzavecchia, A. A LAIR1 insertion generates broadly reactive antibodies against malaria variant antigens. Nature, 2016, 529(7584), 105-109.
[http://dx.doi.org/10.1038/nature16450] [PMID: 26700814]
[95]
Arora, G.; Hart, G.T.; Manzella-Lapeira, J.; Doritchamou, J.Y.A.; Narum, D.L.; Thomas, L.M.; Brzostowski, J.; Rajagopalan, S.; Doumbo, O.K.; Traore, B.; Miller, L.H.; Pierce, S.K.; Duffy, P.E.; Crompton, P.D.; Desai, S.A.; Long, E.O. NK cells inhibit Plasmodium falciparum growth in red blood cells via antibody-dependent cellular cytotoxicity. eLife, 2018, 7, e36806.
[http://dx.doi.org/10.7554/eLife.36806] [PMID: 29943728]
[96]
Chapman, T.L.; Heikema, A.P.; West, A.P., Jr; Bjorkman, P.J. Crystal structure and ligand binding properties of the D1D2 region of the inhibitory receptor LIR-1 (ILT2). Immunity, 2000, 13(5), 727-736.
[http://dx.doi.org/10.1016/S1074-7613(00)00071-6] [PMID: 11114384]
[97]
Hsieh, F.L.; Higgins, M.K. The structure of a LAIR1-containing human antibody reveals a novel mechanism of antigen recognition. eLife, 2017, 6, e27311.
[http://dx.doi.org/10.7554/eLife.27311] [PMID: 28527239]
[98]
Niang, M.; Bei, A.K.; Madnani, K.G.; Pelly, S.; Dankwa, S.; Kanjee, U.; Gunalan, K.; Amaladoss, A.; Yeo, K.P.; Bob, N.S.; Malleret, B.; Duraisingh, M.T.; Preiser, P.R. STEVOR is a Plasmodium falciparum erythrocyte binding protein that mediates merozoite invasion and rosetting. Cell Host Microbe, 2014, 16(1), 81-93.
[http://dx.doi.org/10.1016/j.chom.2014.06.004] [PMID: 25011110]
[99]
Naissant, B.; Dupuy, F.; Duffier, Y.; Lorthiois, A.; Duez, J.; Scholz, J.; Buffet, P.; Merckx, A.; Bachmann, A.; Lavazec, C. Plasmodium falciparum STEVOR phosphorylation regulates host erythrocyte deformability enabling malaria parasite transmission. Blood, 2016, 127(24), e42-e53.
[http://dx.doi.org/10.1182/blood-2016-01-690776] [PMID: 27136945]
[100]
Jumper, J.; Evans, R.; Pritzel, A. Highly accurate protein structure prediction with AlphaFold. Nature, 2021, 596, 583-589.
[101]
Mphande, F.A.; Ribacke, U.; Kaneko, O.; Kironde, F.; Winter, G.; Wahlgren, M. SURFIN4.1, a schizont-merozoite associated protein in the SURFIN family of Plasmodium falciparum. Malar. J., 2008, 7(1), 116.
[http://dx.doi.org/10.1186/1475-2875-7-116] [PMID: 18593471]
[102]
Kagaya, W.; Miyazaki, S.; Yahata, K.; Ohta, N.; Kaneko, O. The cytoplasmic region of Plasmodium falciparum SURFIN 4.2. Is required for transport from Maurer’s clefts to the red blood cell surface. Trop. Med. Health, 2015, 43(4), 265-272.
[http://dx.doi.org/10.2149/tmh.2015-38] [PMID: 26865830]
[103]
Chitama, B.Y.A.; Miyazaki, S.; Zhu, X.; Kagaya, W.; Yahata, K.; Kaneko, O. Multiple charged amino acids of Plasmodium falciparum SURFIN4.1 N-terminal region are important for efficient export to the red blood cell. Parasitol. Int., 2019, 71, 186-193.
[http://dx.doi.org/10.1016/j.parint.2019.04.019] [PMID: 31028841]
[104]
Miyazaki, S.; Chitama, B.Y.A.; Kagaya, W.; Lucky, A.B.; Zhu, X.; Yahata, K.; Morita, M.; Takashima, E.; Tsuboi, T.; Kaneko, O. Plasmodium falciparum SURFIN4.1 forms an intermediate complex with PTEX components and Pf113 during export to the red blood cell. Parasitol. Int., 2021, 83, 102358.
[http://dx.doi.org/10.1016/j.parint.2021.102358] [PMID: 33901679]
[105]
Quintana, M.P.; Ch’ng, J.H.; Zandian, A.; Imam, M.; Hultenby, K.; Theisen, M.; Nilsson, P.; Qundos, U.; Moll, K.; Chan, S.; Wahlgren, M. SURGE complex of Plasmodium falciparum in the rhoptry-neck (SURFIN4.2-RON4-GLURP) contributes to merozoite invasion. PLoS One, 2018, 13(8), e0201669.
[http://dx.doi.org/10.1371/journal.pone.0201669] [PMID: 30092030]
[106]
Chaianantakul, N.; Sungkapong, T.; Changpad, J.; Thongma, K.; Sim-ut, S.; Kaewthamasorn, M. Genetic polymorphism of the extracellular region in surface associated interspersed 1.1 gene of Plasmodium falciparum field isolates from Thailand. Malar. J., 2021, 20(1), 343.
[http://dx.doi.org/10.1186/s12936-021-03876-y] [PMID: 34399778]
[107]
Aurrecoechea, C.; Brestelli, J.; Brunk, B.P.; Dommer, J.; Fischer, S.; Gajria, B.; Gao, X.; Gingle, A.; Grant, G.; Harb, O.S.; Heiges, M.; Innamorato, F.; Iodice, J.; Kissinger, J.C.; Kraemer, E.; Li, W.; Miller, J.A.; Nayak, V.; Pennington, C.; Pinney, D.F.; Roos, D.S.; Ross, C.; Stoeckert, C.J., Jr; Treatman, C.; Wang, H. PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res., 2009, 37(Database), D539-D543.
[http://dx.doi.org/10.1093/nar/gkn814] [PMID: 18957442]
[108]
Yadavalli, R.; Peterson, J.W.; Drazba, J.A.; Sam-Yellowe, T.Y. Trafficking and association of Plasmodium falciparum MC-2TM with the Maurer’s Clefts. Pathogens, 2021, 10(4), 431.
[http://dx.doi.org/10.3390/pathogens10040431] [PMID: 33916455]
[109]
Lavazec, C.; Sanyal, S.; Templeton, T.J. Expression switching in the stevor and Pfmc-2TM superfamilies in Plasmodium falciparum. Mol. Microbiol., 2007, 64(6), 1621-1634.
[http://dx.doi.org/10.1111/j.1365-2958.2007.05767.x] [PMID: 17555442]
[110]
Bachmann, A.; Scholz, J.A.M.; Janßen, M.; Klinkert, M.Q.; Tannich, E.; Bruchhaus, I.; Petter, M. A comparative study of the localization and membrane topology of members of the RIFIN, STEVOR and PfMC-2TM protein families in Plasmodium falciparum-infected erythrocytes. Malar. J., 2015, 14(1), 274.
[http://dx.doi.org/10.1186/s12936-015-0784-2] [PMID: 26173856]
[111]
Tsarukyanova, I.; Drazba, J.A.; Fujioka, H.; Yadav, S.P.; Sam-Yellowe, T.Y. Proteins of the Plasmodium falciparum two transmembrane Maurer’s cleft protein family, PfMC-2TM, and the 130 kDa Maurer’s cleft protein define different domains of the infected erythrocyte intramembranous network. Parasitol. Res., 2009, 104(4), 875-891.
[http://dx.doi.org/10.1007/s00436-008-1270-3] [PMID: 19130087]
[112]
Bernabeu, M.; Danziger, S.A.; Avril, M.; Vaz, M.; Babar, P.H.; Brazier, A.J.; Herricks, T.; Maki, J.N.; Pereira, L.; Mascarenhas, A.; Gomes, E.; Chery, L.; Aitchison, J.D.; Rathod, P.K.; Smith, J.D. Severe adult malaria is associated with specific PfEMP1 adhesion types and high parasite biomass. Proc. Natl. Acad. Sci. USA, 2016, 113(23), E3270-E3279.
[http://dx.doi.org/10.1073/pnas.1524294113] [PMID: 27185931]
[113]
Janes, J.H.; Wang, C.P.; Levin-Edens, E.; Vigan-Womas, I.; Guillotte, M.; Melcher, M.; Mercereau-Puijalon, O.; Smith, J.D. Investigating the host binding signature on the Plasmodium falciparum PfEMP1 protein family. PLoS Pathog., 2011, 7(5), e1002032.
[http://dx.doi.org/10.1371/journal.ppat.1002032] [PMID: 21573138]
[114]
Chew, M.; Ye, W.; Omelianczyk, R.I.; Pasaje, C.F.; Hoo, R.; Chen, Q.; Niles, J.C.; Chen, J.; Preiser, P. Selective expression of variant surface antigens enables Plasmodium falciparum to evade immune clearance in vivo. Nat. Commun., 2022, 13(1), 4067.
[http://dx.doi.org/10.1038/s41467-022-31741-2] [PMID: 35831417]

Rights & Permissions Print Cite
© 2025 Bentham Science Publishers | Privacy Policy