Interaction between endothelial protein C receptor and intercellular adhesion molecule 1 to mediate binding of plasmodium falciparum-infected erythrocytes to endothelial cells

mBio

Volumn 7, Issue 4, 2016, Pages

  Avril, Marion ^a   Bernabeu, Maria ^a   Benjamin, Maxwell ^a   Brazier, Andrew Jay ^a   Smith, Joseph D ^a,b  

^a SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD36 ANTIGEN; ENDOTHELIAL PROTEIN C RECEPTOR; INTERCELLULAR ADHESION MOLECULE 1; TUMOR NECROSIS FACTOR; CELL SURFACE RECEPTOR; ERYTHROCYTE MEMBRANE PROTEIN 1, PLASMODIUM FALCIPARUM; LEUKOCYTE ANTIGEN; PROCR PROTEIN, HUMAN; PROTOZOAL PROTEIN;

ARTICLE; CEREBRAL MALARIA; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME INHIBITION; ERYTHROCYTE; HUMAN; HUMAN CELL; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; CELL ADHESION; CELL CULTURE; METABOLISM; PARASITOLOGY; PHYSIOLOGY;

ANTIGENS, CD; CELL ADHESION; CELLS, CULTURED; ENDOTHELIAL CELLS; ERYTHROCYTES; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; PROTEIN INTERACTION MAPPING; PROTOZOAN PROTEINS; RECEPTORS, CELL SURFACE;

EID: 84986540204     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00615-16     Document Type: Article

References (36)

1. MacPherson GG, Warrell MJ, White NJ, Looareesuwan S, Warrell DA. 1985. Human cerebral malaria. A quantitative ultrastructural analysis of parasitized erythrocyte sequestration. Am J Pathol 119:385-401.
2. Taylor TE, Fu WJ, Carr RA, Whitten RO, Mueller JS, Fosiko NG, Lewallen S, Liomba NG, Molyneux ME, Mueller JG. 2004. Differentiat-ing the pathologies of cerebral malaria by postmortem parasite counts. Nat Med 10:143-145. http://dx.doi.org/10.1038/nm986.
3. Rowe JA, Claessens A, Corrigan RA, Arman M. 2009. Adhesion of Plasmodium falciparum-infected erythrocytes to human cells: molecular mechanisms and therapeutic implications. Expert Rev Mol Med 11:e16. http://dx.doi.org/10.1017/S1462399409001082.
4. Mosnier LO, Zlokovic BV, Griffin JH. 2007. The cytoprotective protein C pathway. Blood 109:3161-3172. http://dx.doi.org/10.1182/blood-2006-09-003004.
5. Turner L, Lavstsen T, Berger SS, Wang CW, Petersen JE, Avril M, Brazier AJ, Freeth J, Jespersen JS, Nielsen MA, Magistrado P, Lusingu J, Smith JD, Higgins MK, Theander TG. 2013. Severe malaria is associated with parasite binding to endothelial protein C receptor. Nature 498: 502-505. http://dx.doi.org/10.1038/nature12216.
6. Avril M, Tripathi AK, Brazier AJ, Andisi C, Janes JH, Soma VL, Sullivan DJ, Jr., Bull PC, Stins MF, Smith JD. 2012. A restricted subset of var genes mediates adherence of Plasmodium falciparum-infected erythrocytes to brain endothelial cells. Proc Natl Acad Sci U S A 109: E1782-E1790. http://dx.doi.org/10.1073/pnas.1120534109.
7. Claessens A, Adams Y, Ghumra A, Lindergard G, Buchan CC, Andisi C, Bull PC, Mok S, Gupta AP, Wang CW, Turner L, Arman M, Raza A, Bozdech Z, Rowe JA. 2012. A subset of group A-like var genes encodes the malaria parasite ligands for binding to human brain endothelial cells. Proc Natl Acad Sci U S A 109:E1772-E1781. http://dx.doi.org/10.1073/pnas.1120461109.
8. Bertin GI, Lavstsen T, Guillonneau F, Doritchamou J, Wang CW, Jespersen JS, Ezimegnon S, Fievet N, Alao MJ, Lalya F, Massougbodji A, Ndam NT, Theander TG, Deloron P. 2013. Expression of the domain cassette 8 Plasmodium falciparum erythrocyte membrane protein 1 is associated with cerebral malaria in Benin. PLoS One 8:e68368. http://dx.doi.org/10.1371/journal.pone.0068368.
9. Lavstsen T, Turner L, Saguti F, Magistrado P, Rask TS, Jespersen JS, Wang CW, Berger SS, Baraka V, Marquard AM, Seguin-Orlando A, Willerslev E, Gilbert MT, Lusingu J, Theander TG. 2012. Plasmodium falciparum erythrocyte membrane protein 1 domain cassettes 8 and 13 are associated with severe malaria in children. Proc Natl Acad Sci U S A 109: E1791-E1800. http://dx.doi.org/10.1073/pnas.1120455109.
10. Bernabeu M, Danziger SA, Avril M, Vaz M, Babar PH, Brazier AJ, Herricks T, Maki JN, Pereira L, Mascarenhas A, Gomes E, Chery L, Aitchison JD, Rathod PK, Smith JD. 2016. Severe adult malaria is associated with specific PfEMP1 adhesion types and high parasite biomass. Proc Natl Acad Sci U S A 113:E3270-E3279. http://dx.doi.org/10.1073/pnas.1524294113.
11. Turner GD, Morrison H, Jones M, Davis TM, Looareesuwan S, Buley ID, Gatter KC, Newbold CI, Pukritayakamee S, Nagachinta B, et al. 1994. An immunohistochemical study of the pathology of fatal malaria. Evidence for widespread endothelial activation and a potential role for intercellular adhesion molecule-1 in cerebral sequestration. Am J Pathol 145:1057-1069.
12. Silamut K, Phu NH, Whitty C, Turner GD, Louwrier K, Mai NT, Simpson JA, Hien TT, White NJ. 1999. A quantitative analysis of the microvascular sequestration of malaria parasites in the human brain. Am J Pathol 155:395-410. http://dx.doi.org/10.1016/S0002-9440(10)65136-X.
13. Kraemer SM, Smith JD. 2006. A family affair: var genes, PfEMP1 binding, and malaria disease. Curr Opin Microbiol 9:374-380. http://dx.doi.org/10.1016/j.mib.2006.06.006.
14. Lavstsen T, Salanti A, Jensen AT, Arnot DE, Theander TG. 2003. Sub-grouping of Plasmodium falciparum 3D7 var genes based on sequence analysis of coding and non-coding regions. Malar J 2:27. http://dx.doi.org/10.1186/1475-2875-2-27.
15. Rask TS, Hansen DA, Theander TG, Gorm Pedersen A, Lavstsen T. 2010. Plasmodium falciparum erythrocyte membrane protein 1 diversity in seven genomes—divide and conquer. PLoS Comput Biol 6:e1000933. http://dx.doi.org/10.1371/journal.pcbi.1000933.
16. Smith JD, Subramanian G, Gamain B, Baruch DI, Miller LH. 2000. Classification of adhesive domains in the Plasmodium falciparum erythrocyte membrane protein 1 family. Mol Biochem Parasitol 110:293-310. http://dx.doi.org/10.1016/S0166-6851(00)00279-6.
17. Smith JD, Rowe JA, Higgins MK, Lavstsen T. 2013. Malaria’s deadly grip: cytoadhesion of Plasmodium falciparum-infected erythrocytes. Cell Microbiol 15:1976-1983. http://dx.doi.org/10.1111/cmi.12183.
18. Lau CK, Turner L, Jespersen JS, Lowe ED, Petersen B, Wang CW, Petersen JE, Lusingu J, Theander TG, Lavstsen T, Higgins MK. 2015. Structural conservation despite huge sequence diversity allows EPCR binding by the PfEMP1 family implicated in severe childhood malaria. Cell Host Microbe 17:118-129. http://dx.doi.org/10.1016/j.chom.2014.11.007.
19. Robinson BA, Welch TL, Smith JD. 2003. Widespread functional specialization of Plasmodium falciparum erythrocyte membrane protein 1 family members to bind CD36 analysed across a parasite genome. Mol Microbiol 47:1265-1278. http://dx.doi.org/10.1046/j.1365-2958.2003.03378.x.
20. Howell DP, Levin EA, Springer AL, Kraemer SM, Phippard DJ, Schief WR, Smith JD. 2008. Mapping a common interaction site used by Plasmodium falciparum Duffy binding-like domains to bind diverse host receptors. Mol Microbiol 67:78-87. http://dx.doi.org/10.1111/j.1365-2958.2007.06019.x.
21. Bengtsson A, Joergensen L, Rask TS, Olsen RW, Andersen MA, Turner L, Theander TG, Hviid L, Higgins MK, Craig A, Brown A, Jensen AT. 2013. A novel domain cassette identifies Plasmodium falciparum PfEMP1 proteins binding ICAM-1 and is a target of cross-reactive, adhesioninhibitory antibodies. J Immunol 190:240-249. http://dx.doi.org/10.4049/jimmunol.1202578.
22. Oleinikov AV, Amos E, Frye IT, Rossnagle E, Mutabingwa TK, Fried M, Duffy PE. 2009. High throughput functional assays of the variant antigen PfEMP1 reveal a single domain in the 3D7 Plasmodium falciparum genome that binds ICAM1 with high affinity and is targeted by naturally acquired neutralizing antibodies. PLoS Pathog 5:e1000386. http://dx.doi.org/10.1371/journal.ppat.1000386.
23. Avril M, Brazier AJ, Melcher M, Sampath S, Smith JD. 2013. DC8 and DC13 var genes associated with severe malaria bind avidly to diverse endothelial cells. PLoS Pathog 9:e1003430. http://dx.doi.org/10.1371/journal.ppat.1003430.
24. Avril M, Cartwright MM, Hathaway MJ, Hommel M, Elliott SR, Williamson K, Narum DL, Duffy PE, Fried M, Beeson JG, Smith JD. 2010. Immunization with VAR2CSA-DBL5 recombinant protein elicits broadly cross-reactive antibodies to placental Plasmodium falciparum-infected erythrocytes. Infect Immun 78:2248-2256. http://dx.doi.org/10.1128/IAI.00410-09.
25. Janes JH, Wang CP, Levin-Edens E, Vigan-Womas I, Guillotte M, Melcher M, Mercereau-Puijalon O, Smith JD. 2011. Investigating the host binding signature on the Plasmodium falciparum PfEMP1 protein family. PLoS Pathog 7:e1002032. http://dx.doi.org/10.1371/journal.ppat.1002032.
26. McCormick CJ, Craig A, Roberts D, Newbold CI, Berendt AR. 1997. Intercellular adhesion molecule-1 and CD36 synergize to mediate adherence of Plasmodium falciparum-infected erythrocytes to cultured human microvascular endothelial cells. J Clin Invest 100:2521-2529. http://dx.doi.org/10.1172/JCI119794.
27. Fukudome K, Esmon CT. 1994. Identification, cloning, and regulation of a novel endothelial cell protein C/activated protein C receptor. J Biol Chem 269:26486-26491.
28. Newbold C, Warn P, Black G, Berendt A, Craig A, Snow B, Msobo M, Peshu N, Marsh K. 1997. Receptor-specific adhesion and clinical disease in Plasmodium falciparum. Am J Trop Med Hyg 57:389-398.
29. Ochola LB, Siddondo BR, Ocholla H, Nkya S, Kimani EN, Williams TN, Makale JO, Liljander A, Urban BC, Bull PC, Szestak T, Marsh K, Craig AG. 2011. Specific receptor usage in Plasmodium falciparum cytoadherence is associated with disease outcome. PLoS One 6:e14741. http://dx.doi.org/10.1371/journal.pone.0014741.
30. Rogerson SJ, Tembenu R, Dobaño C, Plitt S, Taylor TE, Molyneux ME. 1999. Cytoadherence characteristics of Plasmodium falciparum-infected erythrocytes from Malawian children with severe and uncomplicated malaria. Am J Trop Med Hyg 61:467-472.
31. Ho M, Hickey MJ, Murray AG, Andonegui G, Kubes P. 2000. Visualization of Plasmodium falciparum-endothelium interactions in human microvasculature: mimicry of leukocyte recruitment. J Exp Med 192: 1205-1211. http://dx.doi.org/10.1084/jem.192.8.1205.
32. Carlson J, Helmby H, Hill AV, Brewster D, Greenwood BM, Wahlgren M. 1990. Human cerebral malaria: association with erythrocyte rosetting and lack of anti-rosetting antibodies. Lancet 336:1457-1460. http://dx.doi.org/10.1016/0140-6736(90)93174-N.
33. Ghumra A, Semblat JP, Ataide R, Kifude C, Adams Y, Claessens A, Anong DN, Bull PC, Fennell C, Arman M, Amambua-Ngwa A, Walther M, Conway DJ, Kassambara L, Doumbo OK, Raza A, Rowe JA. 2012. Induction of strain-transcending antibodies against group A PfEMP1 surface antigens from virulent malaria parasites. PLoS Pathog 8:e1002665. http://dx.doi.org/10.1371/journal.ppat.1002665.
34. Gillrie MR, Avril M, Brazier AJ, Davis SP, Stins MF, Smith JD, Ho M. 2015. Diverse functional outcomes of Plasmodium falciparum ligation of EPCR: potential implications for malarial pathogenesis. Cell Microbiol 17:1883-1899. http://dx.doi.org/10.1111/cmi.12479.
35. Ockenhouse CF, Betageri R, Springer TA, Staunton DE. 1992. Plasmodium falciparum-infected erythrocytes bind ICAM-1 at a site distinct from LFA-1, Mac-1, and human rhinovirus. Cell 68:63-69. http://dx.doi.org/10.1016/0092-8674(92)90206-R.
36. Sampath S, Brazier AJ, Avril M, Bernabeu M, Vigdorovich V, Mascarenhas A, Gomes E, Sather DN, Esmon CT, Smith JD. 2015. Plasmodium falciparum adhesion domains linked to severe malaria differ in blockade of endothelial protein C receptor. Cell Microbiol 17:1868-1882. http://dx.doi.org/10.1111/cmi.12478.