CD39: Interface between vascular thrombosis and inflammation

Current Atherosclerosis Reports

Volumn 16, Issue 7, 2014, Pages

  Kanthi, Yogendra M ^a   Sutton, Nadia R ^a   Pinsky, David J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Adenosine; ADP; Atherosclerosis; ATP; CD39; Ectonucleotidase; ENTPD1; Leokocyte self regulation; Leokocyte trafficking; Myocardial ischemia; Phosphodiesterases 3; Pulmonary hypertension; Purinergic signaling; Stroke; Thrombosis; Vascular inflammation

Indexed keywords

CD39 ANTIGEN; APYRASE; LEUKOCYTE ANTIGEN;

ANTIGEN EXPRESSION; ANTIGEN FUNCTION; ANTIGEN STRUCTURE; ARTICLE; ATHEROSCLEROSIS; DEGRANULATION; DENDRITIC CELL; HUMAN; LEUKOCYTE ACTIVATION; LEUKOCYTE MIGRATION; LYMPHOCYTE; MACROPHAGE; MONOCYTE; NEUTROPHIL; NONHUMAN; OCCLUSIVE CEREBROVASCULAR DISEASE; PROTEIN TARGETING; REPERFUSION INJURY; SIGNAL TRANSDUCTION; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOSIS; VASCULITIS; CEREBROVASCULAR ACCIDENT; HEART MUSCLE ISCHEMIA; IMMUNOLOGY; INFLAMMATION; METABOLISM; PHYSIOLOGY; PULMONARY HYPERTENSION; VASCULAR ENDOTHELIUM;

ANTIGENS, CD; APYRASE; ATHEROSCLEROSIS; ENDOTHELIUM, VASCULAR; HUMANS; HYPERTENSION, PULMONARY; INFLAMMATION; MYOCARDIAL ISCHEMIA; MYOCARDIAL REPERFUSION INJURY; SIGNAL TRANSDUCTION; STROKE; THROMBOSIS; VASCULITIS;

EID: 84901244450     PISSN: 15233804     EISSN: 15346242     Source Type: Journal    
DOI: 10.1007/s11883-014-0425-1     Document Type: Article

References (56)

1. Schenk U, Westendorf AM, Radaelli E, Casati A, Ferro M, Fumagalli M, et al. Purinergic control of T cell activation by ATP released through pannexin-1 hemichannels. Sci Signal. 2008;1(39): ra6. doi:10.1126/scisignal.1160583.
2. Kukulski F, Levesque SA, Sevigny J. Impact of ectoenzymes on p2 and p1 receptor signaling. Adv Pharmacol. 2011;61:263-99. doi: 10.1016/B978-0-12- 385526-8.00009-6.
3. Deaglio S, Robson SC. Ectonucleotidases as regulators of purinergic signaling in thrombosis, inflammation, and immunity. Adv Pharmacol. 2011;61:301-32. doi:10.1016/B978-0-12-385526-8.00010-2.
4. Bonner F, Borg N, Burghoff S, Schrader J. Resident cardiac immune cells and expression of the ectonucleotidase enzymes CD39 and CD73 after ischemic injury. PLoS One. 2012;7(4):e34730. doi: 10.1371/journal.pone.0034730.
5. Maliszewski CR, Delespesse GJ, Schoenborn MA, Armitage RJ, Fanslow WC, Nakajima T, et al. The CD39 lymphoid cell activation antigen. Molecular cloning and structural characterization. J Immunol. 1994;153(8):3574-83. (Pubitemid 24313861)
6. Pulte ED, Broekman MJ, Olson KE, Drosopoulos JH, Kizer JR, Islam N, et al. CD39/NTPDase-1 activity and expression in normal leukocytes. Thromb Res. 2007;121(3):309-17. doi:10.1016/j.thromres.2007.04.008.
7. Behdad A, Sun X, Khalpey Z, Enjyoji K, Wink M, Wu Y, et al. Vascular smooth muscle cell expression of ectonucleotidase CD39 (ENTPD1) is required for neointimal formation in mice. Purinergic Signal. 2009;5(3):335-42. doi:10.1007/s11302-009-9158-y.
8. Smith TM, Kirley TL. Cloning, sequencing, and expression of a human brain ecto-apyrase related to both the ecto-ATPases and CD39 ecto-apyrases1. Biochim Biophys Acta. 1998;1386(1):65-78. (Pubitemid 29333218)
9. Koziak K, Kaczmarek E, Kittel A, Sevigny J, Blusztajn JK, Schulte Am Esch 2nd J, et al. Palmitoylation targets CD39/endothelial ATP diphosphohydrolase to caveolae. J Biol Chem. 2000;275(3):2057-62. (Pubitemid 30060833)
10. •• Baek AE, Kanthi Y, Sutton NR, Liao H, Pinsky DJ. Regulation of ecto-apyrase CD39 (ENTPD1) expression by phosphodiesterase III (PDE3). FASEB J. 2013;27(11):4419-28. doi:10.1096/fj.13-234625. This is an important study demonstrating pharmacologic modulation ofCD39 expression with existing drugs approved by the US Food and Drug Administration. Use of the PDE3 inhibitor family of pharmaceuticals represents a novel approach to harness CD39 expression.
11. Papanikolaou A, Papafotika A, Murphy C, Papamarcaki T, Tsolas O, Drab M, et al. Cholesterol-dependent lipid assemblies regulate the activity of the ecto-nucleotidase CD39. J Biol Chem. 2005;280(28):26406-14. doi:10.1074/jbc. M413927200. (Pubitemid 41022237)
12. Strohmeier GR, Lencer WI, Patapoff TW, Thompson LF, Carlson SL, Moe SJ, et al. Surface expression, polarization, and functional significance of CD73 in human intestinal epithelia. J Clin Invest. 1997;99(11):2588-601. doi:10.1172/JCI119447. (Pubitemid 27259805)
13. Liao H, Hyman MC, Baek AE, Fukase K, Pinsky DJ. cAMP/CREB-mediated transcriptional regulat ion of ectonucleoside triphosphate diphosphohydrolase 1 (CD39) expression. J Biol Chem. 2010;285(19):14791-805. doi:10.1074/jbc.M110. 116905.
14. Pluskota E, Ma Y, Bledzka KM, Bialkowska K, Soloviev DA, Szpak D, et al. Kindlin-2 regulates hemostasis by controlling endothelial cell-surface expression of ADP/AMP catabolic enzymes via a clathrin-dependentmechanism. Blood. 2013;122(14):2491-9. doi:10.1182/blood-2013-04-497669.
15. •• Chalmin F, Mignot G, Bruchard M, Chevriaux A, Vegran F, Hichami A, et al. Stat3 and Gfi-1 transcription factors control Th17 cell immunosuppressive activity via the regulation of ectonucleotidase expression. Immunity. 2012;36(3):362-73. doi:10.1016/j.immuni.2011.12.019. This is an important study that implicates CD39 in the mechanism of immune modulation by T helper 17 cells. It further identifies direct and indirect transcriptional signals that regulate CD39 expression under cellular stress.
16. Hot A, Lavocat F, Lenief V, Miossec P. Simvastatin inhibits the proinflammatory and pro-thrombotic effects of IL-17 and TNF-alpha on endothelial cells. Ann Rheum Dis. 2013;72(5):754-60. doi:10.1136/annrheumdis-2012-201887.
17. Robson SC, Kaczmarek E, Siegel JB, Candinas D, Koziak K, Millan M, et al. Loss of ATP diphosphohydrolase activity with endothelial cell activation. J Exp Med. 1997;185(1):153-63. (Pubitemid 27039449)
18. Eltzschig HK, Kohler D, Eckle T, Kong T, Robson SC, Colgan SP. Central role of Sp1-regulated CD39 in hypoxia/ischemia protection. Blood. 2009;113(1):224-32. doi:10.1182/blood-2008-06-165746.
19. Ogawa S, Clauss M, Kuwabara K, Shreeniwas R, Butura C, Koga S, et al. Hypoxia induces endothelial cell synthesis of membrane-associated proteins. Proc Natl Acad Sci U S A. 1991;88(21):9897-901. (Pubitemid 21915742)
20. Manalo DJ, Rowan A, Lavoie T, Natarajan L, Kelly BD, Ye SQ, et al. Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood. 2005;105(2):659-69. doi: 10.1182/blood-2004-07-2958. (Pubitemid 40070750)
21. Banz Y, Beldi G, Wu Y, Atkinson B, Usheva A, Robson SC. CD39 is incorporated into plasma microparticles where it maintains functional properties and impacts endothelial activation. Br J Haematol. 2008;142(4):627-37. doi:10.1111/j.1365-2141.2008.07230.x. (Pubitemid 352020213)
22. • Visovatti SH, Hyman MC, Bouis D, Neubig R, McLaughlin VV, Pinsky DJ. Increased CD39 nucleotidase activity on microparticles from patients with idiopathic pulmonary arterial hypertension. PLoS One. 2012;7(7):e40829. doi:10.1371/journal.pone.0040829. This is an important study that demonstrates a potential role for CD39 in pulmonary arterial hypertension, a devastating disease with poor prognosis and limited therapeutics.
23. Hyman MC, Petrovic-Djergovic D, Visovatti SH, Liao H, Yanamadala S, Bouis D, et al. Self-regulation of inflammatory cell trafficking in mice by the leukocyte surface apyrase CD39. J Clin Invest. 2009;119(5):1136-49. doi:10.1172/JCI36433.
24. Enjyoji K, Sevigny J, Lin Y, Frenette PS, Christie PD, Esch 2nd JS, et al. Targeted disruption of cd39/ATP diphosphohydrolase results in disordered hemostasis and thromboregulation. Nat Med. 1999;5(9):1010-7. doi:10.1038/12447. (Pubitemid 29439571)
25. Huttinger ZM, Milks MW, Nickoli MS, Aurand WL, Long LC, Wheeler DG, et al. Ectonucleotide triphosphate diphosphohydrolase-1 (CD39) mediates resistance to occlusive arterial thrombus formation after vascular injury in mice. Am J Pathol. 2012;181(1):322-33. doi:10.1016/j.ajpath.2012.03.024.
26. Pinsky DJ, Broekman MJ, Peschon JJ, Stocking KL, Fujita T, Ramasamy R, et al. Elucidation of the thromboregulatory role of CD39/ectoapyrase in the ischemic brain. J Clin Invest. 2002;109(8):1031-40. doi:10.1172/JCI10649. (Pubitemid 34408578)
27. Wheeler DG, Joseph ME, Mahamud SD, Aurand WL, Mohler PJ, Pompili VJ, et al. Transgenic swine: expression of human CD39 protects against myocardial injury. J Mol Cell Cardiol. 2012;52(5):958-61. doi:10.1016/j.yjmcc.2012.01.002.
28. Cai M, Huttinger ZM, He H, Zhang W, Li F, Goodman LA, et al. Transgenic over expression of ectonucleotide triphosphate diphosphohydrolase-1 protects against murinemyocardial ischemic injury. J Mol Cell Cardiol. 2011;51(6):927-35. doi:10.1016/j.yjmcc.2011.09.003.
29. Dwyer KM, Robson SC, Nandurkar HH, Campbell DJ, Gock H, Murray-Segal LJ, et al. Thromboregulatory manifestations in human CD39 transgenic mice and the implications for thrombotic disease and transplantation. J Clin Invest. 2004;113(10):1440-6. doi:10.1172/JCI19560. (Pubitemid 39071699)
30. McRae JL, Russell PA, Chia JS, Dwyer KM. Overexpression of CD39 protects in a mouse model of preeclampsia. Nephrology. 2013;18(5):351-5. doi:10.1111/nep.12058.
31. Crikis S, Lu B, Murray-Segal LM, Selan C, Robson SC, D'Apice AJ, et al. Transgenic overexpression of CD39 protects against renal ischemia-reperfusion and transplant vascular injury. Am J Transplant. 2010;10(12):2586-95. doi:10.1111/j.1600-6143.2010.03257.x.
32. Hatakeyama K, Hao H, Imamura T, Ishikawa T, Shibata Y, Fujimura Y, et al. Relation of CD39 to plaque instability and thrombus formation in directional atherectomy specimens from patients with stable and unstable angina pectoris. Am J Cardiol. 2005;95(5):632-5. doi:10.1016/j.amjcard.2004.11.012. (Pubitemid 40255256)
33. Kaneider NC, Egger P, Dunzendorfer S, Noris P, Balduini CL, Gritti D, et al. Reversal of thrombin-induced deactivation of CD39/ATPDase in endothelial cells by HMG-CoA reductase inhibition: effects on Rho-GTPase and adenosine nucleotide metabolism. Arterioscler Thromb Vasc Biol. 2002;22(6):894-900. (Pubitemid 34655214)
34. Kohler D, Eckle T, Faigle M, Grenz A, Mittelbronn M, Laucher S, et al. CD39/ectonucleoside triphosphate diphosphohydrolase 1 provides myocardial protection during cardiac ischemia/reperfusion injury. Circulation. 2007;116(16):1784-94. doi:10.1161/CIRCULATIONAHA.107.690180. (Pubitemid 350287103)
35. Yoshida O, Kimura S, Jackson EK, Robson SC, Geller DA, Murase N, et al. CD39 expression by hepatic myeloid dendritic cells attenuates inflammation in liver transplant ischemia-reperfusion injury in mice. Hepatology. 2013;58(6):2163-75. doi:10.1002/hep.26593.
36. Chen Y, Corriden R, Inoue Y, Yip L, Hashiguchi N, Zinkernagel A, et al. ATP release guides neutrophil chemotaxis via P2Y2 and A3 receptors. Science. 2006;314(5806):1792-5. doi:10.1126/science.1132559. (Pubitemid 44969094)
37. Eltzschig HK, Thompson LF, Karhausen J, Cotta RJ, Ibla JC, Robson SC, et al. Endogenous adenosine produced during hypoxia attenuates neutrophil accumulation: coordination by extracellular nucleotide metabolism. Blood. 2004;104(13):3986-92. (Pubitemid 39620148)
38. Reutershan J, Vollmer I, Stark S, Wagner R, Ngamsri KC, Eltzschig HK. Adenosine and inflammation: CD39 and CD73 are critical mediators in LPS-induced PMN trafficking into the lungs. FASEB J. 2009;23(2):473-82. doi:10.1096/fj.08- 119701.
39. Corriden R, Chen Y, Inoue Y, Beldi G, Robson SC, Insel PA, et al. Ecto-nucleoside triphosphate diphosphohydrolase 1 (E-NTPDase1/ CD39) regulates neutrophil chemotaxis by hydrolyzing released ATP to adenosine. J Biol Chem. 2008;283(42):28480-6. doi:10.1074/jbc.M800039200.
40. Kukulski F, Bahrami F, Ben Yebdri F, Lecka J, Martin-Satue M, Levesque SA, et al. NTPDase1 controls IL-8 production by human neutrophils. J Immunol. 2011;187(2):644-53. doi:10.4049/jimmunol.1002680.
41. Shah D, Romero F, Stafstrom W, Duong M, Summer R. Extracellular ATP mediates the late phase of neutrophil recruitment to the lung in murine models of acute lung injury. Am J Physiol Lung Cell Mol Physiol. 2014;306(2):L152-61. doi:10.1152/ajplung.00229.2013.
42. Zanin RF, Braganhol E, Bergamin LS, Campesato LF, Filho AZ, Moreira JC, et al. Differential macrophage activation alters the expression profile of NTPDase and ecto-5′-nucleotidase. PLoS One. 2012;7(2):e31205. doi:10.1371/journal.pone.0031205.
43. Csoka B, Selmeczy Z, Koscso B, Nemeth ZH, Pacher P, Murray PJ, et al. Adenosine promotes alternative macrophage activation via A2A and A2B receptors. FASEB J. 2012;26(1):376-86. doi:10.1096/fj.11-190934.
44. Hotchkiss RS, Coopersmith CM, McDunn JE, Ferguson TA. The sepsis seesaw: tilting toward immunosuppression. Nat Med. 2009;15(5):496-7. doi:10.1038/nm0509-496.
45. Cohen HB, Briggs KT, Marino JP, Ravid K, Robson SC, Mosser DM. TLR stimulation initiates a CD39-based autoregulatory mechanism that limits macrophage inflammatory responses. Blood. 2013;122(11):1935-45. doi:10.1182/blood-2013-04-496216.
46. Levesque SA, Kukulski F, Enjyoji K, Robson SC, Sevigny J. NTPDase1 governs P2X7-dependent functions in murine macrophages. Eur J Immunol. 2010;40(5):1473-85. doi:10.1002/eji.200939741.
47. Borsellino G, Kleinewietfeld M, DiMitri D, Sternjak A, Diamantini A, Giometto R, et al. Expression of ectonucleotidase CD39 by Foxp3+ Treg cells: hydrolysis of extracellular ATP and immune suppression. Blood. 2007;110(4):1225-32. doi:10.1182/blood-2006-12-064527. (Pubitemid 47281420)
48. Deaglio S, Dwyer KM, Gao W, Friedman D, Usheva A, Erat A, et al. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J Exp Med. 2007;204(6):1257-65. doi:10.1084/jem.20062512. (Pubitemid 46919862)
49. Dwyer KM, Hanidziar D, Putheti P, Hill PA, Pommey S, McRae JL, et al. Expression of CD39 by human peripheral blood CD4+ CD25+ T cells denotes a regulatory memory phenotype. Am J Transplant. 2010;10(11):2410-20. doi:10.1111/j.1600-6143.2010.03291.x.
50. Zhou Q, Yan J, Putheti P, Wu Y, Sun X, Toxavidis V, et al. Isolated CD39 expression on CD4+ T cells denotes both regulatory and memory populations. Am J Transplant. 2009;9(10):2303-11. doi: 10.1111/j.1600-6143.2009.02777.x.
51. Moncrieffe H, Nistala K, Kamhieh Y, Evans J, Eddaoudi A, Eaton S, et al. High expression of the ectonucleotidase CD39 on T cells from the inflamed site identifies two distinct populations, one regulatory and one memory T cell population. J Immunol. 2010;185(1):134-43. doi:10.4049/jimmunol.0803474.
52. Thiolat A, Semerano L, Pers YM, Biton J, Lemeiter D, Portales P, et al. Interleukin-6 receptor blockade enhances CD39+ regulatory T cell development in rheumatoid arthritis and in experimental arthritis. Arthritis Rheumatol. 2014;66(2):273-83. doi:10.1002/art.38246.
53. Kansas GS, Wood GS, Tedder TF. Expression, distribution, and biochemistry of human CD39. Role in activation-associated homotypic adhesion of lymphocytes. J Immunol. 1991;146(7):2235-44.
54. la Sala A, Ferrari D, Corinti S, Cavani A, Di Virgilio F, Girolomoni G. Extracellular ATP induces a distorted maturation of dendritic cells and inhibits their capacity to initiate Th1 responses. J Immunol. 2001;166(3):1611-7. (Pubitemid 32114641)
55. Idzko M, Dichmann S, Ferrari D, Di Virgilio F, la Sala A, Girolomoni G, et al. Nucleotides induce chemotaxis and actin polymerization in immature but not mature human dendritic cells via activation of pertussis toxin-sensitive P2y receptors. Blood. 2002;100(3):925-32. (Pubitemid 34832619)
56. Mizumoto N, Kumamoto T, Robson SC, Sevigny J, Matsue H, Enjyoji K, et al. CD39 is the dominant Langerhans cell-associated ecto-NTPDase: modulatory roles in inflammation and immune responsiveness. Nat Med. 2002;8(4):358-65. doi:10.1038/nm0402-358. (Pubitemid 34407030)