CD36 Recruits αβ Integrin to Promote Cytoadherence of -Infected Erythrocytes

English version České info

The adhesion of Plasmodium falciparum-infected erythrocytes (IRBC) to receptors on different host cells plays a divergent yet critical role in determining the progression and outcome of the infection. Based on our ex vivo studies with clinical parasite isolates from adult Thai patients, we have previously proposed a paradigm for IRBC cytoadherence under physiological shear stress that consists of a recruitment cascade mediated largely by P-selectin, ICAM-1 and CD36 on primary human dermal microvascular endothelium (HDMEC). In addition, we detected post-adhesion signaling events involving Src family kinases and the adaptor protein p130CAS in endothelial cells that lead to CD36 clustering and cytoskeletal rearrangement which enhance the magnitude of the adhesive strength, allowing adherent IRBC to withstand shear stress of up to 20 dynes/cm². In this study, we addressed whether CD36 supports IRBC adhesion as part of an assembly of membrane receptors. Using a combination of flow chamber assay, atomic force and confocal microscopy, we showed for the first time by loss- and gain-of function assays that in the resting state, the integrin α₅β₁ does not support adhesive interactions between IRBC and HDMEC. Upon IRBC adhesion to CD36, the integrin is recruited either passively as part of a molecular complex with CD36, or actively to the site of IRBC attachment through phosphorylation of Src family kinases, a process that is Ca²⁺-dependent. Clustering of β₁ integrin is associated with an increase in IRBC recruitment as well as in adhesive strength after attachment (∼40% in both cases). The adhesion of IRBC to a multimolecular complex on the surface of endothelial cells could be of critical importance in enabling adherent IRBC to withstand the high shear stress in the microcirculations. Targeting integrins may provide a novel approach to decrease IRBC cytoadherence to microvascular endothelium.

Vyšlo v časopise: CD36 Recruits αβ Integrin to Promote Cytoadherence of -Infected Erythrocytes. PLoS Pathog 9(8): e32767. doi:10.1371/journal.ppat.1003590
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003590

Souhrn

Zdroje

1. LeyK, LaudannaC, CybulskyMI, NoursharghS (2007) Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 7: 678–689.

2. LegateKR, WickströmSA, FässlerR (2009) Genetic and cell biological analysis of integrin outside-in signaling. Genes Dev 23: 397–418.

3. YippBG, AnandS, SchollaardtT, PatelKD, LooareesuwanS, 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. YippBG, HickeyMJ, AndoneguiG, MurrayAG, LooareesuwanS, et al. (2007) Differential roles of CD36, ICAM-1, and P-selectin in Plasmodium falciparum cytoadherence in vivo. Microcirculation 14: 593–602.

5. YippBG, RobbinsSM, ResekME, BaruchDI, LooareesuwanS, et al. (2003) Src-family kinase signaling modulates the adhesion of Plasmodium falciparum on human microvascular endothelium under flow. Blood 101: 2850–2857.

6. DavisSP, AmreinM, GillrieMR, LeeK, MuruveDA, et al. (2012) Plasmodium falciparum-induced CD36 clustering rapidly strengthens cytoadherence via p130CAS-mediated actin cytoskeletal rearrangement. FASEB J 26: 1119–1130.

7. JenkinsN, WuY, ChakravortySJ, KaiO, MarshK, et al. (2007) Plasmodium falciparum ICAM-1-based cytoadherence-related signalling in human endothelial cells. J Infect Dis 196: 321–327.

8. OcholaLB, SiddondoBR, OchollaH, NkyaS, KimaniEN, et al. (2011) Specific receptor usage in Plasmodium falciparum cytoadherence is associated with disease outcome. PLoS One 6: e14741.

9. JanesJH, WangCP, Levin-EdensE, Vigan-WomasI, GuillotteMP, et al. (2011) Investigating the host binding signature on the Plasmodium falciparum PfEMP1 protein family. PLoS Pathogen 7: e1002032.

10. BengtssonA, JoergensenL, RaskTS, OlsenRW, AndersenMA, 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. KnowlesDM2nd, TolidjianB, MarboeC, D'AgatiV, GrimesM, 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. TurnerGD, MorrisonH, JonesM, DavisTM, LooareesuwanS, 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. FonagerJ, PasiniEM, BraksJA, KlopO, RamesarJ, 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. McMorranBJ, WieczorskiL, DrysdaleKE, ChanJA, HuangHM, et al. (2012) Platelet factor 4 and Duffy antigen required for platelet killing of Plasmodium falciparum. Science 338: 1348–1351.

15. LoveMS, MillhollandMG, MishraS, KulkarniS, FreemanKB, 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. BambergerME, HarrisME, McDonaldDR, HusemannJ, LandrethGE (2003) A cell surface receptor complex for fibrillar beta-amyloid mediates microglial activation. J Neurosci 23: 2665–2674.

17. KoenigsknechtJ, LandrethG (2004) Microglial phagocytosis of fibrillar beta-amyloid through a beta1 integrin-dependent mechanism. J Neurosci 24: 9838–9846.

18. StewartCR, StuartLM, WilkinsonK, van GilsJM, DengJ, 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. SmithJD, GamainB, BaruchDI, KyesS (2001) Decoding the language of var genes and Plasmodium falciparum sequestration. Trends Parasitol 17: 538–545.

20. PorterJC, HoggN (1998) Integrins take partners: cross-talk between integrins and other membrane receptors. Trends Cell Biol 8: 390–396.

21. ThorneRF, MarshallJF, ShafrenDR, GibsonPG, HartIR, 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. BaruchDI, PasloskeB, SinghHB, XiahuiBi, MaXC, 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. SuXZ, HeatwoleVM, WertheimerSP, GuinetF, HerrfeldtJA, 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. RaskTS, HansenDA, TheanderTG, Gorm PedersenA, LavstsenT (2010) Plasmodium falciparum erythrocyte membrane protein 1 diversity in seven genomes-divide and conquer. PLoS Comput Biol 6: e1000933.

25. RobertsDD, SherwoodJA, SpitalnikSL, PantonLJ, HowardRJ, et al. (1985) Thrombospondin binds falciparum malaria parasitized erythrocytes and may mediate cytoadherence. Nature 318: 64–66.

26. SianoJP, GradyKK, MilletP, WickTM (1998) Short report: Plasmodium falciparum: cytoadherence to alpha(v)beta3 on human microvascular endothelial cells. Am J Trop Med Hyg 59: 77–79.

27. UrbanBC, WillcoxN, RobertsDJ (2001) A role for CD36 in the regulation of dendritic cell function. Proc Natl Acad Sci USA 98: 8750–8755.

28. GoodmanSL, PicardM (2012) Integrins as therapeutic targets. Trends Pharmacol Sci 33: 405–412.

29. XuY, SwerlickRA, SeppN, BosseD, AdesEW, 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. RuoslahtiE (1996) RGD and other recognition sequences for integrins. Ann Rev Cell Dev Biol 12: 697–715.

31. KazerounianS, DuquetteM, ReyesMA, LawlerJT, SongK, 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. ChakravortySJ, HughesKR, CraigAG (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. KesslerH, DiefenbachB, FinsingerD, GeyerA, GurrathM, et al. (1995) Design of superactive and selective integrin receptor antagonists containing the RGD sequence. Letters in Peptide Science 2: 155–160.

35. KwiatkowskiD, HillAV, SambouI, TwumasiP, CastracanaJ, et al. (1990) TNF concentration in fatal cerebral, non-fatal cerebral, and uncomplicated Plasmodium falciparum malaria. Lancet 336: 1201–1204.

36. DayNP, HienTT, SchollaardtT, LocPP, ChuongLV, et al. (1999) The prognostic and pathophysiologic role of pro- and anti-inflammatory cytokines in severe malaria. J Infect Dis 180: 1288–1297.

37. ArroyaAG, Garcia-PardoA, Sanchez-MadridF (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-CusachsP, GauthierNC, Del RioA, SheetzMP (2009) Clustering of α5β1 integrins determines adhesion strength whereas αvβ3 and talin enable mechanotransduction. Proc Natl Acad Sci USA 106: 16245–16250.

39. BaruchDI, MaXC, SinghHB, BiX, PasloskeBL, 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. KucikDF, DustinML, MillerJM, BrownEJ (1996) Adhesion-activating phorbol ester increases the mobility of leukocyte integrin LFA-1 in cultured lymphocytes. J Clin Invest 97: 2139–2144.

41. YuT, WuX, GuptaKB, KucikDF (2010) Affinity, lateral mobility, and clustering contribute independently to beta 2-integrin-mediated adhesion. Am J Physiol Cell Physiol 299: C399–410.

42. WhiteNJ, TurnerGD, DayNP, DondorpAM (2013) Lethal malaria: Marchiafava and Bignami were right. J Infect Dis doi: 10.1093/infdis/jit116 [epub ahead of print]

43. MiaoWM, VasileE, LaneWS, LawlerJ (2001) CD36 associates with CD9 and integrins on human blood platelets. Blood 97: 1689–1696.

44. TakagiJ, StrokovichK, SpringerTA, WalzT (2003) Structure of integrin a5b1 in complex with fibronectin. EMBO J 22: 4607–4615.

45. MouldAP, AskariJA, AotaS, YamadaKM, IrieA, 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. LiF, RedickSD, EricksonHP, MoyVT (2003) Force measurements of the alpha5beta1 integrin-fibronectin interaction. Biophys J 84: 1252–1262.

47. SabriS, SolerM, FoaC, PierresA, BenolielA, et al. (2000) Glycocalyx modulation is a physiological means of regulating cell adhesion. J Cell Sci 113: 1589–1600.

48. BoettigerD (2012) Mechanical control of integrin-mediated adhesion and signaling. Curr Opin Cell Biol 24: 592–599.

49. ZhiH, RauovaL, HayesV, GaoC, BoylanB (2013) Cooperative integrin/ITAM signaling in platelets enhances thrombus formation in vitro and in vivo. Blood 121(10): 1858–67.

50. EdaS, ShermanIW (2002) Cytoadherence of malaria-infected red blood cells involves exposure of phosphatidylserine. Cell Physiol Biochem 12: 373–384.