Platelet factor 4 limits Th17 differentiation and cardiac allograft rejection

Journal of Clinical Investigation

Volumn 124, Issue 2, 2014, Pages 543-552

  Shi, Guanfang ^a   Field, David J ^a   Ko, Kyung Ae ^a   Ture, Sara ^a   Srivastava, Kalyan ^a   Levy, Scott ^a   Kowalska, M Anna ^b   Poncz, Mortimer ^b,c   Fowell, Deborah J ^a   Morrell, Craig N ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; BLOOD PLATELETS; BONE MARROW CELLS; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; GRAFT REJECTION; HEART TRANSPLANTATION; HOMEOSTASIS; HUMANS; INTERLEUKIN-17; JURKAT CELLS; MICE; MICE, TRANSGENIC; PLATELET FACTOR 4; RECOMBINANT PROTEINS; TH17 CELLS; TIME FACTORS; TRANSGENES;

EID: 84893845552     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI71858     Document Type: Article

References (71)

1. Boilard E, et al. Platelets amplify inflammation in arthritis via collagen-dependent microparticle production. Science. 2010;327(5965):580-583.
2. Gawaz M, Favaloro EJ. Platelets, inflammation and cardiovascular diseases. New concepts and therapeutic implications. Semin Thromb Hemost. 2010;36(2):129-130.
3. Gawaz M, Langer H, May AE. Platelets in inflammation and atherogenesis. J Clin Invest. 2005; 115(12):3378-3384.
4. Smyth SS, et al. Platelet functions beyond hemostasis. J Thromb Haemost. 2009;7(11):1759-1766.
5. Ombrello C, Block RC, Morrell CN. Our expanding view of platelet functions and its clinical implications. J Cardiovasc Transl Res. 2010;3(5):538-546.
6. Baldwin WM, Baldwin WM 3rd, Kuo HH, Morrell CN. Platelets: versatile modifiers of innate and adaptive immune responses to transplants. Curr Opin Organ Transplant. 2010;16(1):41-46.
7. Morrell CN, et al. In vivo platelet-endothelial cell interactions in response to major histocompatibility complex alloantibody. Circ Res. 2008;102(7):777-785.
8. Shi G, Morrell CN. Platelets as initiators and mediators of inflammation at the vessel wall. Thromb Res. 2010;127(5):387-390.
9. Weyrich A, Cipollone F, Mezzetti A, Zimmerman G. Platelets in atherothrombosis: new and evolving roles. Curr Pharm Des. 2007;13(16):1685-1691.
10. Massberg S, et al. Platelets secrete stromal cellderived factor 1alpha and recruit bone marrowderived progenitor cells to arterial thrombi in vivo. J Exp Med. 2006;203(5):1221-1233.
11. Gawaz M. Role of platelets in coronary thrombosis and reperfusion of ischemic myocardium. Cardiovasc Res. 2004;61(3):498-511.
12. Langer H, et al. Adherent platelets recruit and induce differentiation of murine embryonic endothelial progenitor cells to mature endothelial cells in vitro. Circ Res. 2006;98(2):e2-e10.
13. Huo Y, et al. Circulating activated platelets exacerbate atherosclerosis in mice deficient in apolipoprotein E. Nat Med. 2003;9(1):61-67.
14. von Hundelshausen P, et al. RANTES deposition by platelets triggers monocyte arrest on inflamed and atherosclerotic endothelium. Circulation. 2001;103(13):1772-1777.
15. Bustos M, Saadi S, Platt JL. Platelet-mediated activation of endothelial cells: implications for the pathogenesis of transplant rejection. Transplantation. 2001;72(3):509-515.
16. Kirk AD, Morrell CN, Baldwin WM. Platelets influence vascularized organ transplants from start to finish. Am J Transplant. 2009;9(1):14-22.
17. Porter KA. Morphological aspects of renal homograft rejection. Br Med Bull. 1965;21:171-175.
18. Fenech A, Nicholls A, Smith FW. Indium (111In)-labelled platelets in the diagnosis of renal transplant rejection: preliminary findings. Br J Radiol. 1981;54(640):325-327.
19. Oluwole S, et al. Use of indium-111-labeled cells in measurement of cellular dynamics of experimental cardiac allograft rejection. Transplantation. 1981;31(1):51-55.
20. Xu H, Zhang X, Mannon RB, Kirk AD. Plateletderived or soluble CD154 induces vascularized allograft rejection independent of cell-bound CD154. J Clin Invest. 2006;116(3):769-774.
21. Swaim AF, Field DJ, Fox-Talbot K, Baldwin WM, Baldwin WM 3rd, Morrell CN. Platelets contribute to allograft rejection through glutamate receptor signaling. J Immunol. 2010;185(11):6999-7006.
22. Fischereder M. Chemokines and chemokine receptors in renal transplantation-from bench to bedside. Acta Physiol Hung. 2007;94(1-2):67-81.
23. Schnickel GT, Hsieh GR, Garcia C, Shefizadeh A, Fishbein MC, Ardehali A. Role of CXCR3 and CCR5 in allograft rejection. Transplant Proc. 2006; 38(10):3221-3224.
24. Hoffmann U, et al. Expression of the chemokine receptor CXCR3 in human renal allografts-a prospective study. Nephrol Dial Transplant. 2006;21(5):1373-1381.
25. Baltus T, von Hundelshausen P, Mause SF, Buhre W, Rossaint R, Weber C. Differential and additive effects of platelet-derived chemokines on monocyte arrest on inflamed endothelium under flow conditions. J Leukoc Biol. 2005;78(2):435-441.
26. von Hundelshausen P, Petersen F, Brandt E. Platelet-derived chemokines in vascular biology. Thromb Haemost. 2007;97(5):704-713.
27. Luther SA, Cyster JG. Chemokines as regulators of T cell differentiation. Nat Immunol. 2001;2(2):102-107.
28. Sachais BS, Higazi AA, Cines DB, Poncz M, Kowalska MA. Interactions of platelet factor 4 with the vessel wall. Semin Thromb Hemost. 2004;30(3):351-358.
29. Lambert MP, Rauova L, Bailey M, Sola-Visner MC, Kowalska MA, Poncz M. Platelet factor 4 is a negative autocrine in vivo regulator of megakaryopoiesis: clinical and therapeutic implications. Blood. 2007;110(4):1153-1160.
30. Amiral J, Marfaing-Koka A, Poncz M, Meyer D. The biological basis of immune heparin-induced thrombocytopenia. Platelets. 1998;9(2):77-91.
31. Arepally GM, et al. Characterization of a murine monoclonal antibody that mimics heparininduced thrombocytopenia antibodies. Blood. 2000; 95(5):1533-1540.
32. Ziporen L, et al. Defining an antigenic epitope on platelet factor 4 associated with heparin-induced thrombocytopenia. Blood. 1998;92(9):3250-3259.
33. Eslin DE, et al. Transgenic mice studies demonstrate a role for platelet factor 4 in thrombosis: dissociation between anticoagulant and antithrombotic effect of heparin. Blood. 2004;104(10):3173-3180.
34. Koenen RR, et al. Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice. Nat Med. 2009;15(1):97-103.
35. Sachais BS, Turrentine T, Dawicki McKenna JM, Rux AH, Rader D, Kowalska MA. Elimination of platelet factor 4 (PF4) from platelets reduces atherosclerosis in C57Bl/6 and apoE-/-mice. Thromb Haemost. 2007;98(5):1108- 1113.
36. Aziz KA, Cawley JC, Zuzel M. Platelets prime PMN via released PF4: mechanism of priming and synergy with GM-CSF. Br J Haematol. 1995;91(4):846-853.
37. Engstad CS, Lia K, Rekdal O, Olsen JO, Osterud B. A novel biological effect of platelet factor 4 (PF4): enhancement of LPS-induced tissue factor activity in monocytes. J Leukoc Biol. 1995;58(5):575-581.
38. Srivastava K, et al. Platelet factor 4 mediates inflammation in experimental cerebral malaria. Cell Host Microbe. 2008;4(2):179-187.
39. Liu CY, Battaglia M, Lee SH, Sun QH, Aster RH, Visentin GP. Platelet factor 4 differentially modulates CD4+CD25+ (regulatory) versus CD4+CD25- (nonregulatory) T cells. J Immunol. 2005;174(5):2680-2686.
40. Afzali B, Lombardi G, Lechler RI, Lord GM. The role of T helper 17 (Th17) and regulatory T cells (Treg) in human organ transplantation and autoimmune disease. Clin Exp Immunol. 2007;148(1):32-46.
41. Gocke AR, et al. T-bet regulates the fate of Th1 and Th17 lymphocytes in autoimmunity. J Immunol. 2007;178(3):1341-1348.
42. Pappu R, Ramirez-Carrozzi V, Ota N, Ouyang W, Hu Y. The IL-17 family cytokines in immunity and disease. J Clin Immunol. 2010;30(2):185-195.
43. Bettelli E, Korn T, Oukka M, Kuchroo VK. Induction and effector functions of T(H)17 cells. Nature. 2008;453(7198):1051-1057.
44. Loverre A, et al. T helper 1, 2 and 17 cell subsets in renal transplant patients with delayed graft function. Transpl Int. 2011;24(3):233-242.
45. Shilling RA, Wilkes DS. Role of Th17 cells and IL-17 in lung transplant rejection. Semin Immunopathol. 2011;33(2):129-134.
46. Yuan X, et al. A novel role of CD4 Th17 cells in mediating cardiac allograft rejection and vasculopathy. J Exp Med. 2008;205(13):3133-3144.
47. Shi G, et al. Platelet factor 4 mediates vascular smooth muscle cell injury responses. Blood. 2013; 121(21):4417-4427.
48. Nagano H, Mitchell RN, Taylor MK, Hasegawa S, Tilney NL, Libby P. Interferon-gamma deficiency prevents coronary arteriosclerosis but not myocardial rejection in transplanted mouse hearts. J Clin Invest. 1997;100(3):550-557.
49. Hasegawa T, Visovatti SH, Hyman MC, Hayasaki T, Pinsky DJ. Heterotopic vascularized murine cardiac transplantation to study graft arteriopathy. Nat Protoc. 2007;2(3):471-480.
50. Gramzinski RA, Doolan DL, Sedegah M, Davis HL, Krieg AM, Hoffman SL. Interleukin-12-and α interferon-dependent protection against malaria conferred by CpG oligodeoxynucleotide in mice. Infect Immun. 2001;69(3):1643-1649.
51. Amante FH, Good MF. Prolonged Th1-like response generated by a Plasmodium yoelii-specific T cell clone allows complete clearance of infection in reconstituted mice. Parasite Immunol. 1997;19(3):111-126.
52. Ishida H, et al. Development of experimental cerebral malaria is independent of IL-23 and IL-17. Biochem Biophys Res Commun. 2010;402(4):790-795.
53. Mucida D, et al. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science. 2007;317(5835):256-260.
54. Whitson RH, Whitson RH Jr, Wong WL, Itakura K. Platelet factor 4 selectively inhibits binding of TGF-β1 to the type I TGF-β1 receptor. J Cell Biochem. 1991;47(1):31-42.
55. Gurney AL, Carver-Moore K, de Sauvage FJ, Moore MW. Thrombocytopenia in c-mpl-deficient mice. Science. 1994;265(5177):1445-1447.
56. Maier M, et al. Platelet factor 4 is highly upregulated in dendritic cells after severe trauma. Mol Med. 2009;15(11-12):384-391.
57. Schaffner A, Rhyn P, Schoedon G, Schaer DJ. Regulated expression of platelet factor 4 in human monocytes-role of PARs as a quantitatively important monocyte activation pathway. J Leukoc Biol. 2005;78(1):202-209.
58. Lasagni L, et al. An alternatively spliced variant of CXCR3 mediates the inhibition of endothelial cell growth induced by IP-10, Mig, and I-TAC, and acts as functional receptor for platelet factor 4. J Exp Med. 2003;197(11):1537- 1549.
59. Mueller A, et al. CXCL4-induced migration of activated T lymphocytes is mediated by the chemokine receptor CXCR3. J Leukoc Biol. 2008;83(4):875-882.
60. Rocha AM, et al. The levels of IL-17A and of the cytokines involved in Th17 cell commitment are increased in patients with chronic immune thrombocytopenia. Haematologica. 2011;96(10):1560-1564.
61. John ML, Scharrer I. Autoimmune disorders in patients with idiopathic thrombotic thrombocytopenic purpura. Hamostaseologie. 2012; 32(suppl 1):S86-S89.
62. Sachais BS, et al. Platelet factor 4 binds to lowdensity lipoprotein receptors and disrupts the endocytic machinery, resulting in retention of lowdensity lipoprotein on the cell surface. Blood. 2002; 99(10):3613-3622.
63. Aidoudi S, Bikfalvi A. Interaction of PF4 (CXCL4) with the vasculature: a role in atherosclerosis and angiogenesis. Thromb Haemost. 2010;104(5):941-948.
64. Chacko MK, Mathew T, Sugathan P, Nair LV. Heparin in psoriasis. Indian J Dermatol Venereol Leprol. 1998;64(6):273-274.
65. Calaminus SD, et al. Lineage tracing of Pf4-Cre marks hematopoietic stem cells and their progeny. PLoS One. 2012;7(12):e51361.
66. Maione F, Cicala C, Liverani E, Mascolo N, Perretti M, D'Acquisto F. IL-17A increases ADP-induced platelet aggregation. Biochem Biophys Res Commun. 2011;408(4):658-662.
67. Zhang S, et al. IL-17A facilitates platelet function through the ERK2 signaling pathway in patients with acute coronary syndrome. PLoS One. 2012; 7(7):e40641.
68. Ivanov II, et al. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe. 2008;4(4):337-349.
69. Ivanov II, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009; 139(3):485-498.
70. Morrell CN, Sun H, Swaim AM, Baldwin WM. Platelets an inflammatory force in transplantation. Am J Transplant. 2007;7(11):2447-2454.
71. Wasowska BA, Qian Z, Behrens E, Cangello D, Sanfilippo F, Baldwin WM. Inhibition of acute cardiac allograft rejection in immunoglobulin-deficient mice. Transplant Proc. 1999;31(1-2):136.