Molecular determinants of SR-B1-dependent Plasmodium sporozoite entry into hepatocytes.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
11 08 2020
11 08 2020
Historique:
received:
17
03
2020
accepted:
13
07
2020
entrez:
13
8
2020
pubmed:
13
8
2020
medline:
22
12
2020
Statut:
epublish
Résumé
Sporozoite forms of the Plasmodium parasite, the causative agent of malaria, are transmitted by mosquitoes and first infect the liver for an initial round of replication before parasite proliferation in the blood. The molecular mechanisms involved during sporozoite invasion of hepatocytes remain poorly understood. Two receptors of the Hepatitis C virus (HCV), the tetraspanin CD81 and the scavenger receptor class B type 1 (SR-B1), play an important role during the entry of Plasmodium sporozoites into hepatocytes. In contrast to HCV entry, which requires both CD81 and SR-B1 together with additional host factors, CD81 and SR-B1 operate independently during malaria liver infection. Sporozoites from human-infecting P. falciparum and P. vivax rely respectively on CD81 or SR-B1. Rodent-infecting P. berghei can use SR-B1 to infect host cells as an alternative pathway to CD81, providing a tractable model to investigate the role of SR-B1 during Plasmodium liver infection. Here we show that mouse SR-B1 is less functional as compared to human SR-B1 during P. berghei infection. We took advantage of this functional difference to investigate the structural determinants of SR-B1 required for infection. Using a structure-guided strategy and chimeric mouse/human SR-B1 constructs, we could map the functional region of human SR-B1 within apical loops, suggesting that this region of the protein may play a crucial role for interaction of sporozoite ligands with host cells and thus the very first step of Plasmodium infection.
Identifiants
pubmed: 32782257
doi: 10.1038/s41598-020-70468-2
pii: 10.1038/s41598-020-70468-2
pmc: PMC7419504
doi:
Substances chimiques
CD36 Antigens
0
Tetraspanin 28
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
13509Références
World Health Organization. World Malaria Report 2019. 1–232 (2019).
Rodrigues, C. D. et al. Host scavenger receptor SR-BI plays a dual role in the establishment of malaria parasite liver infection. Cell Host Microbe4, 271–282 (2008).
doi: 10.1016/j.chom.2008.07.012
Silvie, O. et al. Hepatocyte CD81 is required for Plasmodium falciparum and Plasmodium yoelii sporozoite infectivity. Nat. Med.9, 93–96 (2003).
doi: 10.1038/nm808
Manzoni, G. et al.Plasmodium P36 determines host cell receptor usage during sporozoite invasion. Elife6(e25903), 1–24 (2017).
Yalaoui, S. et al. Scavenger receptor BI boosts hepatocyte permissiveness to Plasmodium infection. Cell Host Microbe4, 283–292 (2008).
doi: 10.1016/j.chom.2008.07.013
Neculai, D. et al. Structure of LIMP-2 provides functional insights with implications for SR-BI and CD36. Nature504, 172–176 (2013).
doi: 10.1038/nature12684
Hsieh, F. L. et al. The structural basis for CD36 binding by the malaria parasite. Nat. Commun.7(12837), 1–11 (2016).
Acton, S. et al. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science271, 518–520 (1996).
doi: 10.1126/science.271.5248.518
Rhainds, D. et al. The role of human and mouse hepatic scavenger receptor class B type I (SR-BI) in the selective uptake of low-density lipoprotein-cholesteryl esters. Biochemistry42, 7527–7538 (2003).
doi: 10.1021/bi026949a
Huby, T. et al. Knockdown expression and hepatic deficiency reveal an atheroprotective role for SR-BI in liver and peripheral tissues. J. Clin. Invest.116, 2767–2776 (2006).
doi: 10.1172/JCI26893
Silvie, O. et al. Cholesterol contributes to the organization of tetraspanin-enriched microdomains and to CD81-dependent infection by malaria sporozoites. J. Cell Sci.119, 1992–2002 (2006).
doi: 10.1242/jcs.02911
Silvie, O., Franetich, J. F., Boucheix, C., Rubinstein, E. & Mazier, D. Alternative invasion pathways for Plasmodium berghei sporozoites. Int. J. Parasitol.37, 173–182 (2007).
doi: 10.1016/j.ijpara.2006.10.005
Mueller, A. K. et al.Plasmodium liver stage developmental arrest by depletion of a protein at the parasite-host interface. Proc. Natl. Acad. Sci. USA102, 3022–3027 (2005).
doi: 10.1073/pnas.0408442102
Silvie, O. et al. Expression of human CD81 differently affects host cell susceptibility to malaria sporozoites depending on the Plasmodium species. Cell. Microbiol.8, 1134–1146 (2006).
doi: 10.1111/j.1462-5822.2006.00697.x
Leung, L. L. K., Li, W. X., McGregor, J. L., Albrecht, G. & Howard, R. J. CD36 peptides enhance or inhibit CD36-thrombospondin binding. A two-step process of ligand-receptor interaction. J. Biol. Chem.267, 18244–18250 (1992).
pubmed: 1381367
Viñals, M., Xu, S., Vasile, E. & Krieger, M. Identification of the N-linked glycosylation sites on the high density lipoprotein (HLD) receptor SR-BI and assessment of their effects on HDL binding and selective lipid uptake. J. Biol. Chem.278, 5325–5332 (2003).
doi: 10.1074/jbc.M211073200
Zunke, F. et al. Characterization of the complex formed by β-glucocerebrosidase and the lysosomal integral membrane protein type-2. Proc. Natl. Acad. Sci. USA113, 3791–3796 (2016).
doi: 10.1073/pnas.1514005113
Yamayoshi, S. & Koike, S. Identification of a human SCARB2 region that is important for enterovirus 71 binding and infection. J. Virol.85, 4937–4946 (2011).
doi: 10.1128/JVI.02358-10
Chen, P. et al. Molecular determinants of enterovirus 71 viral entry: Cleft around GLN-172 on VP1 protein interacts with variable region on scavenge receptor B 2. J. Biol. Chem.287, 6406–6420 (2012).
doi: 10.1074/jbc.M111.301622
Yamayoshi, S. et al. Scavenger receptor B2 is a cellular receptor for enterovirus 71. Nat. Med.15, 798–801 (2009).
doi: 10.1038/nm.1992
Ockenhouse, C. F., Tandon, N. N., Magowan, C., Jamieson, G. A. & Chulay, J. D. Identification of a platelet membrane glycoprotein as a falciparum malaria sequestration receptor. Science243, 1469–1471 (1989).
doi: 10.1126/science.2467377
Oquendo, P., Hundt, E., Lawler, J. & Seed, B. CD36 directly mediates cytoadherence of Plasmodium falciparum parasitized erythrocytes. Cell58, 95–101 (1989).
doi: 10.1016/0092-8674(89)90406-6
Barnwell, J. W. et al. A human 88-kD membrane glycoprotein (CD36) functions in vitro as a receptor for a cytoadherence ligand on Plasmodium falciparum-infected erythrocytes. J. Clin. Invest.84, 765–772 (1989).
doi: 10.1172/JCI114234
Franke-Fayard, B. et al. Murine malaria parasite sequestration: CD36 is the major receptor, but cerebral pathology is unlinked to sequestration. Proc. Natl. Acad. Sci. USA102, 11468–11473 (2005).
doi: 10.1073/pnas.0503386102
Sinnis, P. & Febbraio, M. Plasmodium yoelii sporozoites infect CD36-deficient mice. Exp Parasitol100, 12–16 (2002).
doi: 10.1006/expr.2001.4676
Manzoni, G. et al. A rapid and robust selection procedure for generating drug-selectable marker-free recombinant malaria parasites. Sci. Rep.4(4760), 1–10 (2014).
Ramakrishnan, C. et al. Laboratory maintenance of rodent malaria parasites. Methods Mol. Biol.923, 51–72 (2013).
doi: 10.1007/978-1-62703-026-7_5
Rénia, L. et al. A malaria heat-shock-like determinant expressed on the infected hepatocyte surface is the target of antibody-dependent cell-mediated cytotoxic mechanisms by nonparenchymal liver cells. Eur. J. Immunol.20, 1445–1449 (1990).
doi: 10.1002/eji.1830200706
Söding, J., Biegert, A. & Lupas, A. N. The HHpred interactive server for protein homology detection and structure prediction. Nucl. Acids Res.33, W244–W248 (2005).
doi: 10.1093/nar/gki408
Schwede, T., Kopp, J., Guex, N. & Peitsch, M. C. SWISS-MODEL: an automated protein homology-modeling server. Nucl.Acids Res.31, 3381–3385 (2003).
doi: 10.1093/nar/gkg520
Heo, L., Park, H. & Seok, C. GalaxyRefine: protein structure refinement driven by side-chain repacking. Nucl. Acids Res.41, W384–W388 (2013).
doi: 10.1093/nar/gkt458
Krieger, E. et al. Improving physical realism, stereochemistry, and side-chain accuracy in homology modeling: four approaches that performed well in CASP8. Proteins: Structure, Function and Bioinformatics77, 114–122 (2009).
Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. Sect. D Biol. Crystallogr.66, 12–21 (2010).
doi: 10.1107/S0907444909042073
Wiederstein, M. & Sippl, M. J. ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucl. Acids Res.35, W407–W410 (2007).
doi: 10.1093/nar/gkm290
Baker, N. A., Sept, D., Joseph, S., Holst, M. J. & McCammon, J. A. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. USA98, 10037–10041 (2001).
doi: 10.1073/pnas.181342398
Dolinsky, T. J., Nielsen, J. E., McCammon, J. A. & Baker, N. A. PDB2PQR: an automated pipeline for the setup of Poisson–Boltzmann electrostatics calculations. Nucl. Acids Res.32, W665–W667 (2004).
doi: 10.1093/nar/gkh381
Pettersen, E. F. et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem.25, 1605–1612 (2004).
doi: 10.1002/jcc.20084
Thi, V. L. D. et al. Characterization of hepatitis C virus particle subpopulations reveals multiple usage of the scavenger receptor BI for entry steps. J. Biol. Chem.287, 31242–31257 (2012).
doi: 10.1074/jbc.M112.365924
Maillard, P. et al. The interaction of natural hepatitis C virus with human scavenger receptor SR-BI/Cla1 is mediated by ApoB-containing lipoproteins. FASEB J.20, 735–737 (2006).
doi: 10.1096/fj.05-4728fje