Platelet recruitment to the inflamed glomerulus occurs via an αIIbβ3/GPVI-dependent pathway

American Journal of Pathology

Volumn 177, Issue 3, 2010, Pages 1131-1142

  Devi, Sapna ^a   Kuligowski, Michael P ^a,d   Kwan, Rain Y Q ^a,d   Westein, Erik ^c   Jackson, Shaun P ^c   Kitching, A Richard ^a,b   Hickey, Michael J ^a  

^a MONASH UNIVERSITY   (Australia)

^b MONASH MEDICAL CENTRE   (Australia)

^c MONASH UNIVERSITY   (Australia)

^d CENTENARY INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA2BBETA3 INTEGRIN; FIBRINOGEN; GLOMERULUS BASEMENT MEMBRANE ANTIBODY; GLYCOPROTEIN VI; INTEGRIN; INTERCELLULAR ADHESION MOLECULE 1; PADGEM PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOACCUMULATION; BONE MARROW; CHIMERA; ENDOTHELIUM CELL; GLOMERULONEPHRITIS; GLOMERULUS; GLOMERULUS CAPILLARY; IMMUNE COMPLEX DEPOSITION; INFLAMMATION; LEUKOCYTE; MALE; MICROSCOPY; MOUSE; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; THROMBOCYTE;

EID: 77956510719     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.091143     Document Type: Article

References (68)

1. Springer TA: Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 1994, 76:301-314
2. Jung U, Ley K: Regulation of E-selectin. P-selectin, and intercellular adhesion molecule 1 expression in mouse cremaster muscle vasculature. Microcirculation 1997, 4:311-319
3. Ley K, Gaehtgens P: Endothelial, not hemodynamic, differences are responsible for preferential leukocyte rolling in rat mesenteric venules. Circ Res 1991, 69:1034-1041
4. Kuligowski MP, Kitching AR, Hickey MJ: Leukocyte recruitment to the inflamed glomerulus: a critical role for platelet-derived P-selectin in the absence of rolling. J Immunol 2006, 176:6991-6999
5. Mizgerd JP, Meek BB, Kutkoski GJ, Bullard DC, Beaudet AL, Doerschuk CM: Selectins and neutrophil traffic: margination and Streptococcus pneumoniae-induced emigration in murine lungs. J Exp Med 1996, 184:639-645
6. Wong J, Johnston B, Lee SS, Bullard DC, Smith CW, Beaudet AL, Kubes P: A minimal role for selectins in the recruitment of leukocytes into the inflamed liver microvasculature. J Clin Invest 1997, 99:2782-2790 (Pubitemid 27259826)
7. Holdsworth SR, Tipping PG: Leukocytes in glomerular injury. Semin Immunopathol 2007, 29:355-374
8. Ikezumi Y, Kanno K, Karasawa T, Han GD, Ito Y, Koike H, Toyabe S, Uchiyama M, Shimizu F, Kawachi H: The role of lymphocytes in the experimental progressive glomerulonephritis. Kidney Int 2004, 66:1036-1048 (Pubitemid 39121008)
9. Zachem CR, Alpers CE, Way W, Shankland SJ, Couser WG, Johnson RJ: A role for P-selectin in neutrophil and platelet infiltration in immune complex glomerulonephritis. J Am Soc Nephrol 1997, 8:1838-1844 (Pubitemid 28185441)
10. Barnes JL: Platelets in glomerular disease. Nephron 1997, 77:378-393
11. Zoja C, Remuzzi G: Role of platelets in progressive glomerular diseases. Pediatr Nephrol 1995, 9:495-502
12. Cameron JS: Platelets in glomerular disease. Annu Rev Med 1984, 35:175-180
13. Ideura T, Ogasawara M, Tomura S, Ida T, Chida Y, Kuriyama R, Takeuchi J, Motomiya T, Yamazaki H: Effect of thrombocytopenia on the onset of immune complex glomerulonephritis. Nephron 1992, 60:49-55
14. Johnson RJ, Alpers CE, Pritzl P, Schulze M, Baker P, Pruchno C, Couser WG: Platelets mediate neutrophil-dependent immune complex nephritis in the rat. J Clin Invest 1988, 82:1225-1235
15. Simon DI, Chen Z, Xu H, Li CQ, Dong J, McIntire LV, Ballantye CM, Zhang Li, Furman MI, Berndt MC. and Lopez JA: Platelet Glycoprotein Ib-alpha is a Counterreceptor for the Leukocyte Integrin Mac-1 (CD11b/CD18). J Exp Med 2000, 192:193-204 (Pubitemid 30470302)
16. Romo GM, Dong JF, Schade AJ, Gardiner EE, Kansas GS, Li CQ, McIntire LV, Berndt MC, Lopez JA: The glycoprotein Ib-IX-V complex is a platelet counterreceptor for P-selectin. J Exp Med 1999, 190:803-814
17. Nieswandt B, Brakebusch C, Bergmeier W, Schulte V, Bouvard D, Mokhtari-Nejad R, Lindhout T, Heemskerk JW, Zirngibl H, Fassler R: Glycoprotein VI but not alpha2beta1 integrin is essential for platelet interaction with collagen. EMBO J 2001, 20:2120-2130 (Pubitemid 32410582)
18. Zarbock A, Polanowska-Grabowska RK, Ley K: Platelet-neutrophil- interactions: linking hemostasis and inflammation. Blood Rev 2007, 21:99-111
19. Andrews RK, Shen Y, Gardiner EE, Berndt MC: Platelet adhesion receptors and (patho)physiological thrombus formation. Histol Histopathol 2001, 16:969-980 (Pubitemid 32700407)
20. Massberg S, Enders G, Matos FC, Tomic LI, Leiderer R, Eisenmenger S, Messmer K, Krombach F: Fibrinogen deposition at the postischemic vessel wall promotes platelet adhesion during ischemia-reperfusion in vivo. Blood 1999, 94:3829-3838
21. Savage B, Saldivar E, Ruggeri ZM: Initiation of platelet adhesion by arrest onto fibrinogen or translocation on von Willebrand factor. Cell 1996, 84:289-297 (Pubitemid 26040846)
22. Massberg S, Gawaz M, Gruner S, Schulte V, Konrad I, Zohlnhofer D, Heinzmann U, Nieswandt B: A crucial role of glycoprotein VI for platelet recruitment to the injured arterial wall in vivo. J Exp Med 2003, 197:41-49 (Pubitemid 36110256)
23. Ishikawa M, Cooper D, Arumugam TV, Zhang JH, Nanda A, Granger DN: Platelet-leukocyte-endothelial cell interactions after middle cerebral artery occlusion and reperfusion. J Cereb Blood Flow Metab 2004, 24:907-915 (Pubitemid 39045408)
24. Cooper D, Chitman KD, Williams MC, and Granger DN: Time-depenedent platelet-vessel wall interactions induced by intestinal ischaemia-reperfusion. Am J Physiol Gastrointest Liver Physiol 2003, 284:G1027-G1033 (Pubitemid 36597346)
25. Massberg S, Enders G, Leiderer R, Eisenmenger S, Vestweber D, Krombach F, Messmer K: Platelet-endothelial cell interactions during ischemia/reperfusion: the role of P-selectin. Blood 1998, 92:507-515 (Pubitemid 28323713)
26. Frenette PS, Johnson RC, Hynes RO and Wagner DD: Platelets roll on stimulated endothelium in vivo: An interaction mediated by endothelial P-selectin. Proc Natl Acad Sci USA 1995, 92:7450-7454
27. Rosenkranz AR, Mendrick DL, Cotran RS, Mayadas TN: P-selectin deficiency exacerbates experimental glomerulonephritis: a protective role for endothelial P-selectin in inflammation. J Clin Invest 1999, 103:649-659
28. McEver RP, Beckstead JH, Moore KL, Marshall-Carlson L, Bainton DF: GMP-140, a platelet alpha-granule membrane protein, is also synthesized by vascular endothelial cells and is localized in Weibel-Palade bodies. J Clin Invest 1989, 84:92-99 (Pubitemid 19170099)
29. Carvalho-Tavares J, Hickey MJ, Hutchison J, Michaud J, Sutcliffe IT, Kubes P: A role for platelets and endothelial selectins in tumor necrosis factor-alpha-induced leukocyte recruitment in the brain microvasculature. Circ Res 2000, 87:1141-1148
30. Asaduzzaman M, Lavasani S, Rahman M, Zhang S, Braun OO, Jeppsson B, Thorlacius H: Platelets support pulmonary recruitment of neutrophils in abdominal sepsis. Crit Care Med 2009, 37:1389-1396
31. Huo Y, Schober A, Forlow SB, Smith DF, Hyman MC, Jung S, Littman DR, Weber C, Ley K: Circulating activated platelets exacerbate atherosclerosis in mice deficient in apolipoprotein E. Nat Med 2003, 9:61-67 (Pubitemid 36098261)
32. Fernandes LS, Conde ID, Wayne Smith C, Kansas GS, Snapp KR, Bennet N, Ballantyne C, McIntire LV, O'Brian Smith E, Klem JA, Mathew S, Frangogiannis N, Turner NA, Maresh KJ, Kleiman NS: Platelet-monocyte complex formation: effect of blocking PSGL-1 alone, and in combination with alphaIIbbeta3 and alphaMbeta2, in coronary stenting. Thromb Res 2003, 111:171-177 (Pubitemid 37532856)
33. Zarbock A, Singbartl K, Ley K: Complete reversal of acid-induced acute lung injury by blocking of platelet-neutrophil aggregation. J Clin Invest 2006, 116:3211-3219 (Pubitemid 44878635)
34. Nieswandt B, Bergmeier W, Schulte V, Rackebrandt K, Gessner JE, Zirngibl H: Expression and function of the mouse collagen receptor glycoprotein VI is strictly dependent on its association with the FcR-gamma chain. J Biol Chem 2000, 275:23998-24002 (Pubitemid 30624690)
35. Maxwell MJ, Yuan Y, Anderson KE, Hibbs ML, Salem HH, Jackson SP: SHIP1 and Lyn Kinase Negatively Regulate Integrin alpha IIb beta 3 signaling in platelets. J Biol Chem 2004, 279:32196-32204
36. Choudhri TF, Hoh BL, Zerwes HG, Prestigiacomo CJ, Kim SC, Connolly ES Jr, Kottirsch G, Pinsky DJ: Reduced microvascular thrombosis and improved outcome in acute murine stroke by inhibiting GP IIb/IIIa receptor-mediated platelet aggregation. J Clin Invest 1998, 102:1301-1310 (Pubitemid 28467558)
37. Andrews RK, Kroll MH, Ward CM, Rose JW, Scarborough RM, Smith AI, Lopez JA, Berndt MC: Binding of a novel 50-kilodalton alboaggregin from Trimeresurus albolabris and related viper venom proteins to the platelet membrane glycoprotein Ib-IX-V complex. Effect on platelet aggregation and glycoprotein Ib-mediated platelet activation, Biochemistry 1996, 35:12629-12639
38. Sun D, McNicol A, James AA, Peng Z: Expression of functional recombinant mosquito salivary apyrase: a potential therapeutic platelet aggregation inhibitor. Platelets 2006, 17:178-184 (Pubitemid 43791630)
39. Nesbitt WS, Westein E, Tovar-Lopez FJ, Tolouei E, Mitchell A, Fu J, Carberry J, Fouras A, Jackson SP: A shear gradient-dependent platelet aggregation mechanism drives thrombus formation. Nat Med 2009, 15:665-673
40. Kuligowski MP, Kwan RY, Lo C, Wong C, James WG, Bourges D, Ooi JD, Abeynaike LD, Hall P, Kitching AR, Hickey MJ: Antimyeloperoxidase antibodies rapidly induce alpha-4-integrin-dependent glomerular neutrophil adhesion. Blood 2009, 113:6485-6494
41. Ruth AJ, Kitching AR, Semple TJ, Tipping PG, Holdsworth SR: Intrinsic renal cell expression of CD40 directs Th1 effectors inducing experimental crescentic glomerulonephritis. J Am Soc Nephrol 2003, 14:2813-2822
42. Tailor A, Granger DN: Hypercholesterolemia promotes P-selectin-dependent platelet-endothelial cell adhesion in postcapillary venules. Arterioscler Thromb Vasc Biol 2003, 23:675-680 (Pubitemid 36438083)
43. Larson MK, Watson SP: Regulation of proplatelet formation and platelet release by integrin alpha IIb beta3. Blood 2006, 108:1509-1514
44. Kuhn K, Ryan GB, Hein SJ, Galaske RG, Karnovsky MJ: An ultrastructural study of the mechanisms of proteinuria in rat nephrotoxic nephritis. Lab Invest 1977, 36:375-387 (Pubitemid 8097891)
45. Kottirsch G, Zerwes HG, Cook NS, and Tapparelli, C: Beta- amino acid derivatives as orally active non-peptide fibrinogen receptor antagonists. Bioorg Med Chem Lett 1997, 727-732 (Pubitemid 27121188)
46. Alevriadou BR, Moake JL, Turner NA, Ruggeri ZM, Folie BJ, Phillips MD, Schreiber AB, Hrinda ME, McIntire LV: Real-time analysis of shear-dependent thrombus formation and its blockade by inhibitors of von Willebrand factor binding to platelets. Blood 1993, 81:1263-1276
47. Chen H, Locke D, Liu Y, Liu C, Kahn ML: The platelet receptor GPVI mediates both adhesion and signaling responses to collagen in a receptor density-dependent fashion. J Biol Chem 2002, 277:3011-3019 (Pubitemid 34953338)
48. Moroi M, Jung SM, Shinmyozu K, Tomiyama Y, Ordinas A, Diaz-Ricart M: Analysis of platelet adhesion to a collagen-coated surface under flow conditions: the involvement of glycoprotein VI in the platelet adhesion. Blood 1996, 88:2081-2092 (Pubitemid 26307910)
49. Ruggeri ZM, Mendolicchio GL: Adhesion mechanisms in platelet function. Circ Res 2007, 100:1673-1685
50. Hill PA, Lan HY, Nikolic-Paterson DJ, Atkins RC: The ICAM-1/LFA-1 interaction in glomerular leukocytic accumulation in anti-GBM glomerulonephritis. Kidney Int 1994, 45:700-708
51. Coxon A, Cullere X, Knight S, Sethi S, Wakelin MW, Stavrakis G, Luscinskas FW, Mayadas TN: Fc gamma RIII mediates neutrophil recruitment to immune complexes. a mechanism for neutrophil accumulation in immune-mediated inflammation. Immunity 2001, 14:693-704 (Pubitemid 32592417)
52. Tang T, Rosenkranz A, Assmann KJ, Goodman MJ, Gutierrez-Ramos JC, Carroll MC, Cotran RS, Mayadas TN: A role for Mac-1 (CDIIb/CD18) in immune complex-stimulated neutrophil function in vivo: mac-1 deficiency abrogates sustained Fcgamma receptor-dependent neutrophil adhesion and complement-dependent proteinuria in acute glomerulonephritis. J Exp Med 1997, 186:1853-1863 (Pubitemid 27524595)
53. Huang XR, Tipping PG, Apostolopoulos J, Oettinger C, D'Souza M, Milton G, Holdsworth SR: Mechanisms of T cell-induced glomerular injury in anti-glomerular basement membrane (GBM) glomerulonephritis in rats. Clin Exp Immunol 1997, 109:134-142 (Pubitemid 27293895)
54. Jackson SP: The growing complexity of platelet aggregation. Blood 2007, 109:5087-5095
55. Wagner DD, Burger PC: Platelets in inflammation and thrombosis. Arterioscler Thromb Vasc Biol 2003, 23:2131-2137
56. Khandoga A, Biberthaler P, Enders G, Axmann S, Hutter J, Messmer K, Krombach F: Platelet adhesion mediated by fibrinogen-intercelllular adhesion molecule-1 binding induces tissue injury in the postischemic liver in vivo. Transplantation 2002, 74:681-688
57. Bombeli T, Schwartz BR, Harlan JM: Adhesion of activated platelets to endothelial cells: evidence for a GPIIbIIIa-dependent bridging mechanism and novel roles for endothelial intercellular adhesion molecule 1 (ICAM-1), alphavbeta3 integrin, and GPIbalpha. J Exp Med 1998, 187:329-339 (Pubitemid 28080062)
58. Boutaud A, Borza DB, Bondar O, Gunwar S, Netzer KO, Singh N, Ninomiya Y, Sado Y, Noelken ME, Hudson BG: Type IV collagen of the glomerular basement membrane. Evidence that the chain specificity of network assembly is encoded by the noncollagenous NC1 domains. J Biol Chem 2000, 275:30716-30724
59. Miyatake N, Shikata K, Sugimoto H, Kushiro M, Shikata Y, Ogawa S, Hayashi Y, Miyasaka, M. and Makino H: Intercellular adhesion molecule 1 mediates mononuclear cell infiltration into rat glomeruli after renal ablation. Nephron 1998, 79:91-98 (Pubitemid 28204044)
60. Wada J, Shikata K, Makino H, Morioka S, Hirata K, Ota K, Tamatani T, Miyasaka M, Horiuchi T, Noji S, Nishikawa K, Myokai F, Taniguchi S, Kanwar Y, Ota Z: The critical role of intercellular adhesion molecule-1 in Masugi nephritis in rats. Nephron 1996, 73:264-272 (Pubitemid 26159346)
61. Xu H, Gonzalo JA, St Pierre, Y, Williams IR, Kupper TS, Cotran RS, Springer TA, Gutierrez-Ramos JC: Leukocytosis and resistance to septic shock in intercellular adhesion molecule 1-deficient mice. J Exp Med 1994, 180:95-109 (Pubitemid 24181059)
62. Sligh JJ, Ballantyne C, Rich S, Hawkins HK, Smith CW, Bradley A, Beaudet AL: Inflammatory and immune responses are impaired in mice deficient in intercellular adhesion molecule 1. Proc Natl Acad Sci USA 1993, 90:8529-8533 (Pubitemid 23277702)
63. Takai T, Li M, Sylvestre D, Clynes R, Ravetch JV: FcR gamma chain deletion results in pleiotrophic effector cell defects. Cell 1994, 76:519-529 (Pubitemid 24064172)
64. Kato Y, Hori S, Fujita N, Tsuruo T: A novel anti-platelet monoclonal antibody induces mouse platelet aggregation through an Fc receptor-independent mechanism. Biochem Biophys Res Commun 1998, 242:250-255 (Pubitemid 28412413)
65. Nieswandt B, Watson SP: Platelet-collagen interaction: is GPVI the central receptor? Blood 2003, 102:449-461
66. Ma YQ, Qin J, Plow EF: Platelet integrin alpha(IIb)beta(3): activation mechanisms. J Thromb Haemost 2007, 5:1345-1352
67. Andrews RK, Gardiner EE, Shen Y, Berndt MC: Platelet interactions in thrombosis. IUBMB Life 2004, 56:13-18
68. Suzuki-Inoue K, Inoue O, Frampton J, Watson SP: Murine GPVI stimulates weak integrin activation in PLCgamma2-/- platelets: involvement of PLCgamma1 and PI3-kinase. Blood 2003, 102:1367-1373 (Pubitemid 36988045)