CD36 Recruits α5β1 Integrin to Promote Cytoadherence of P. falciparum-Infected Erythrocytes

PLoS Pathogens

Volumn 9, Issue 8, 2013, Pages

  Davis, Shevaun P ^a   Lee, Kristine ^a   Gillrie, Mark R ^a   Roa, Lina ^a   Amrein, Matthias ^a   Ho, May ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CD36 ANTIGEN; INTERCELLULAR ADHESION MOLECULE 1; PADGEM PROTEIN; SMALL INTERFERING RNA; VERY LATE ACTIVATION ANTIGEN 5; CALCIUM; MULTIPROTEIN COMPLEX; PROTEIN TYROSINE KINASE;

ARTICLE; ATOMIC FORCE MICROSCOPY; CELL ADHESION; CONFOCAL MICROSCOPY; DISEASE COURSE; ERYTHROCYTE; FLOW CYTOMETRY; GAIN OF FUNCTION MUTATION; HUMAN; IMMUNOFLUORESCENCE MICROSCOPY; LOSS OF FUNCTION MUTATION; MICROCIRCULATION; MICROVASCULAR ENDOTHELIAL CELL; NONHUMAN; OUTCOME ASSESSMENT; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHEAR STRESS; CELL CULTURE; CLINICAL TRIAL; FEMALE; GENETICS; MALARIA FALCIPARUM; MALE; METABOLISM; MULTICENTER STUDY; PARASITOLOGY; PATHOLOGY; PHOSPHORYLATION; PLASMODIUM FALCIPARUM; VASCULAR ENDOTHELIUM;

ANTIGENS, CD36; CALCIUM; CELL ADHESION; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; ERYTHROCYTES; FEMALE; HUMANS; INTEGRIN ALPHA5BETA1; MALARIA, FALCIPARUM; MALE; MULTIPROTEIN COMPLEXES; PHOSPHORYLATION; PLASMODIUM FALCIPARUM; SRC-FAMILY KINASES;

EID: 84883394005     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003590     Document Type: Article

References (50)

1. Ley K, Laudanna C, Cybulsky MI, Nourshargh S, (2007) Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 7: 678-689.
2. Legate KR, Wickström SA, Fässler R, (2009) Genetic and cell biological analysis of integrin outside-in signaling. Genes Dev 23: 397-418.
3. Yipp BG, Anand S, Schollaardt T, Patel KD, Looareesuwan S, et al. (2000) Synergism of multiple adhesion molecules in mediating cytoadherence of Plasmodium falciparum-infected erythrocytes to microvascular endothelial cells under flow. Blood 96: 2292-2298.
4. Yipp BG, Hickey MJ, Andonegui G, Murray AG, Looareesuwan S, et al. (2007) Differential roles of CD36, ICAM-1, and P-selectin in Plasmodium falciparum cytoadherence in vivo. Microcirculation 14: 593-602.
5. Yipp BG, Robbins SM, Resek ME, Baruch DI, Looareesuwan S, et al. (2003) Src-family kinase signaling modulates the adhesion of Plasmodium falciparum on human microvascular endothelium under flow. Blood 101: 2850-2857.
6. Davis SP, Amrein M, Gillrie MR, Lee K, Muruve DA, et al. (2012) Plasmodium falciparum-induced CD36 clustering rapidly strengthens cytoadherence via p130CAS-mediated actin cytoskeletal rearrangement. FASEB J 26: 1119-1130.
7. Jenkins N, Wu Y, Chakravorty SJ, Kai O, Marsh K, et al. (2007) Plasmodium falciparum ICAM-1-based cytoadherence-related signalling in human endothelial cells. J Infect Dis 196: 321-327.
8. Ochola LB, Siddondo BR, Ocholla H, Nkya S, Kimani EN, et al. (2011) Specific receptor usage in Plasmodium falciparum cytoadherence is associated with disease outcome. PLoS One 6: e14741.
9. Janes JH, Wang CP, Levin-Edens E, Vigan-Womas I, Guillotte MP, et al. (2011) Investigating the host binding signature on the Plasmodium falciparum PfEMP1 protein family. PLoS Pathogen 7: e1002032.
10. Bengtsson A, Joergensen L, Rask TS, Olsen RW, Andersen MA, et al. (2013) A novel domain cassette identifies Plasmodium falciparum PfEMP1 proteins binding ICAM-1 and is a target of cross-reactive, adhesion-inhibitory antibodies. J Immunol 190: 240-249.
11. Knowles DM 2nd, Tolidjian B, Marboe C, D'Agati V, Grimes M, et al. (1984) Monoclonal anti-human monocyte antibodies OKM1 and OKM5 possess distinctive tissue distributions including differential reactivity with vascular endothelium. J Immunol 132: 2170-2173.
12. Turner GD, Morrison H, Jones M, Davis TM, Looareesuwan S, 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.
13. Fonager J, Pasini EM, Braks JA, Klop O, Ramesar J, et al. (2012) Reduced CD36-dependent tissue sequestration of Plasmodium-infected erythrocytes is detrimental to malaria parasite growth in vivo. J Exp Med 209: 93-107.
14. McMorran BJ, Wieczorski L, Drysdale KE, Chan JA, Huang HM, et al. (2012) Platelet factor 4 and Duffy antigen required for platelet killing of Plasmodium falciparum. Science 338: 1348-1351.
15. Love MS, Millholland MG, Mishra S, Kulkarni S, Freeman KB, et al. (2012) Platelet Factor 4 activity against P. falciparum and its translation to nonpeptidic mimics as antimalarials. Cell Host Microbe 12: 815-823.
16. Bamberger ME, Harris ME, McDonald DR, Husemann J, Landreth GE, (2003) A cell surface receptor complex for fibrillar beta-amyloid mediates microglial activation. J Neurosci 23: 2665-2674.
17. Koenigsknecht J, Landreth G, (2004) Microglial phagocytosis of fibrillar beta-amyloid through a beta1 integrin-dependent mechanism. J Neurosci 24: 9838-9846.
18. Stewart CR, Stuart LM, Wilkinson K, van Gils JM, Deng J, et al. (2010) CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat Immunol 11: 155-161.
19. Smith JD, Gamain B, Baruch DI, Kyes S, (2001) Decoding the language of var genes and Plasmodium falciparum sequestration. Trends Parasitol 17: 538-545.
20. Porter JC, Hogg N, (1998) Integrins take partners: cross-talk between integrins and other membrane receptors. Trends Cell Biol 8: 390-396.
21. Thorne RF, Marshall JF, Shafren DR, Gibson PG, Hart IR, et al. (2000) The integrins alpha3beta1 and alpha6beta1 physically and functionally associate with CD36 in human melanoma cells. Requirement for the extracellular domain OF CD36. J Biol Chem 275: 35264-35275.
22. Baruch DI, Pasloske B, Singh HB, Xiahui Bi, Ma XC, et al. (1995) Cloning the P. falciparum gene encoding PfEMPl, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell 82: 77-87.
23. Su XZ, Heatwole VM, Wertheimer SP, Guinet F, Herrfeldt JA, et al. (1995) The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell 82: 89-100.
24. 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.
25. Roberts DD, Sherwood JA, Spitalnik SL, Panton LJ, Howard RJ, et al. (1985) Thrombospondin binds falciparum malaria parasitized erythrocytes and may mediate cytoadherence. Nature 318: 64-66.
26. Siano JP, Grady KK, Millet P, Wick TM, (1998) Short report: Plasmodium falciparum: cytoadherence to alpha(v)beta3 on human microvascular endothelial cells. Am J Trop Med Hyg 59: 77-79.
27. Urban BC, Willcox N, Roberts DJ, (2001) A role for CD36 in the regulation of dendritic cell function. Proc Natl Acad Sci USA 98: 8750-8755.
28. Goodman SL, Picard M, (2012) Integrins as therapeutic targets. Trends Pharmacol Sci 33: 405-412.
29. Xu Y, Swerlick RA, Sepp N, Bosse D, Ades EW, et al. (1994) Characterization of expression and modulation of cell adhesion molecules on an immortalized human dermal microvascular endothelial cell line (HMEC-1). J Invest Dermatol 102: 833-837.
30. Ruoslahti E, (1996) RGD and other recognition sequences for integrins. Ann Rev Cell Dev Biol 12: 697-715.
31. Kazerounian S, Duquette M, Reyes MA, Lawler JT, Song K, et al. (2011) Priming of the vascular endothelial growth factor signaling pathway by thrombospondin-1, CD36, and spleen tyrosine kinase. Blood 117: 4658-4666.
32. Chakravorty SJ, Hughes KR, Craig AG, (2008) Host response to cytoadherence in Plasmodium falciparum. Biochem Soc Trans 36: 221-228.
33. Rowe, J A, Claessens A., Corrigan, R A., and Arman M. (2009) Adhesion of Plasmodium falciparum-infected erythrocytes to human cells: molecular mechanisms and therapeutic implications. Expert Rev Mol Med. 11, e16.
34. Kessler H, Diefenbach B, Finsinger D, Geyer A, Gurrath M, et al. (1995) Design of superactive and selective integrin receptor antagonists containing the RGD sequence. Letters in Peptide Science 2: 155-160.
35. Kwiatkowski D, Hill AV, Sambou I, Twumasi P, Castracana J, et al. (1990) TNF concentration in fatal cerebral, non-fatal cerebral, and uncomplicated Plasmodium falciparum malaria. Lancet 336: 1201-1204.
36. Day NP, Hien TT, Schollaardt T, Loc PP, Chuong LV, et al. (1999) The prognostic and pathophysiologic role of pro- and anti-inflammatory cytokines in severe malaria. J Infect Dis 180: 1288-1297.
37. Arroya AG, Garcia-Pardo A, Sanchez-Madrid F, (1993) A high affinity conformational state on VLA integrin heterodimers induced by an anti-β1 chain monoclonal antibody. J Biol Chem 268: 9863-9868.
38. Roca-Cusachs P, Gauthier NC, Del Rio A, Sheetz MP, (2009) Clustering of α5β1 integrins determines adhesion strength whereas αvβ3 and talin enable mechanotransduction. Proc Natl Acad Sci USA 106: 16245-16250.
39. Baruch DI, Ma XC, Singh HB, Bi X, Pasloske BL, et al. (1997) Identification of a region of PfEMP1 that mediates adherence of Plasmodium falciparum infected erythrocytes to CD36: conserved function with variant sequence. Blood 90: 3766-3775.
40. Kucik DF, Dustin ML, Miller JM, Brown EJ, (1996) Adhesion-activating phorbol ester increases the mobility of leukocyte integrin LFA-1 in cultured lymphocytes. J Clin Invest 97: 2139-2144.
41. Yu T, Wu X, Gupta KB, Kucik DF, (2010) Affinity, lateral mobility, and clustering contribute independently to beta 2-integrin-mediated adhesion. Am J Physiol Cell Physiol 299: C399-410.
42. White NJ, Turner GD, Day NP, Dondorp AM, (2013) Lethal malaria: Marchiafava and Bignami were right. J Infect Dis doi: 10.1093/infdis/jit116 [epub ahead of print].
43. Miao WM, Vasile E, Lane WS, Lawler J, (2001) CD36 associates with CD9 and integrins on human blood platelets. Blood 97: 1689-1696.
44. Takagi J, Strokovich K, Springer TA, Walz T, (2003) Structure of integrin a5b1 in complex with fibronectin. EMBO J 22: 4607-4615.
45. Mould AP, Askari JA, Aota S, Yamada KM, Irie A, et al. (1997) Defining the topology of integrin α5β1-fibronectin interactions using inhibitory anti-α5 and anti-β1 monoclonal antibodies. J Biol Chem 272: 17283-17292.
46. Li F, Redick SD, Erickson HP, Moy VT, (2003) Force measurements of the alpha5beta1 integrin-fibronectin interaction. Biophys J 84: 1252-1262.
47. Sabri S, Soler M, Foa C, Pierres A, Benoliel A, et al. (2000) Glycocalyx modulation is a physiological means of regulating cell adhesion. J Cell Sci 113: 1589-1600.
48. Boettiger D, (2012) Mechanical control of integrin-mediated adhesion and signaling. Curr Opin Cell Biol 24: 592-599.
49. Zhi H, Rauova L, Hayes V, Gao C, Boylan B, (2013) Cooperative integrin/ITAM signaling in platelets enhances thrombus formation in vitro and in vivo. Blood 121 (10):: 1858-67.
50. Eda S, Sherman IW, (2002) Cytoadherence of malaria-infected red blood cells involves exposure of phosphatidylserine. Cell Physiol Biochem 12: 373-384.