Cardiovascular Pathology
Volume 21, Issue 1 , Pages 28-38 , January 2012

Proteinase inhibitor 9 is reduced in human atherosclerotic lesion development

Received 30 July 2010 ,Revised 2 December 2010 ,Accepted 12 December 2010.

References 

  1. Libby P. Coronary artery injury and the biology of atherosclerosis: inflammation, thrombosis, and stabilization. Am J Cardiol. 2000;86(8B):3J–8Jdiscussion 8J–9J
  2. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med. 2005;352(16):1685–1695
  3. Bjorkerud S, Bjorkerud B. Apoptosis is abundant in human atherosclerotic lesions, especially in inflammatory cells (macrophages and T cells), and may contribute to the accumulation of gruel and plaque instability. Am J Pathol. 1996;149(2):367–380
  4. Kockx MM, Herman AG. Apoptosis in atherosclerosis: beneficial or detrimental?. Cardiovasc Res. 2000;45(3):736–746
  5. Choy JC, McDonald PC, Suarez AC, Hung VH, Wilson JE, McManus BM, et al. Granzyme B in atherosclerosis and transplant vascular disease: association with cell death and atherosclerotic disease severity. Mod Pathol. 2003;16(5):460–470
  6. Chamberlain CM, Granville DJ. The role of granzyme B in atheromatous diseases. Can J Physiol Pharmacol. 2007;85(1):89–95
  7. Hendel A, Hiebert PR, Boivin WA, Williams SJ, Granville DJ. Granzymes in age-related cardiovascular and pulmonary diseases. Cell Death Differ. 2010;17(4):596–606
  8. Voskoboinik I, Smyth MJ, Trapani JA. Perforin-mediated target-cell death and immune homeostasis. Nat Rev Immunol. 2006;6(12):940–952
  9. Choy JC, Hung VH, Hunter AL, Cheung PK, Motyka B, Goping IS, et al. Granzyme B induces smooth muscle cell apoptosis in the absence of perforin: involvement of extracellular matrix degradation. Arterioscler Thromb Vasc Biol. 2004;24(12):2245–2250
  10. Buzza MS, Zamurs L, Sun J, Bird CH, Smith AI, Trapani JA, et al. Extracellular matrix remodeling by human granzyme B via cleavage of vitronectin, fibronectin, and laminin. J Biol Chem. 2005;280(25):23549–23558
  11. Froelich CJ, Zhang X, Turbov J, Hudig D, Winkler U, Hanna WL, et al. degrades aggrecan proteoglycan in matrix synthesized by chondrocytes. J Immunol. 1993;151(12):7161–7171
  12. Boivin WA, Cooper DM, Hiebert PR, Granville DJ. Intracellular versus extracellular granzyme B in immunity and disease: challenging the dogma. Lab Invest. 2009;89(11):1195–1220
  13. Chamberlain CM, Ang LS, Boivin WA, Cooper DM, Williams SJ, Zhao H, et al. Perforin-independent extracellular granzyme B activity contributes to abdominal aortic aneurysm. Am J Pathol. 2010;176(2):1038–1049
  14. Kondo H, Hojo Y, Tsuru R, Nishimura Y, Shimizu H, Takahashi N, et al. Elevation of plasma granzyme B levels after acute myocardial infarction. Circ J. 2009;73(3):503–507
  15. Skjelland M, Michelsen AE, Krohg-Sorensen K, Tennoe B, Dahl A, Bakke S, et al. Plasma levels of granzyme B are increased in patients with lipid-rich carotid plaques as determined by echogenicity. Atherosclerosis. 2007;195(2):e142–e146
  16. Tsuru R, Kondo H, Hojo Y, Gama M, Mizuno O, Katsuki T, et al. Increased granzyme B production from peripheral blood mononuclear cells in patients with acute coronary syndrome. Heart. 2008;94(3):305–310
  17. Sun J, Bird CH, Sutton V, McDonald L, Coughlin PB, De Jong TA, et al. A cytosolic granzyme B inhibitor related to the viral apoptotic regulator cytokine response modifier A is present in cytotoxic lymphocytes. J Biol Chem. 1996;271(44):27802–27809
  18. Kaiserman D, Bird PI. Control of granzymes by serpins. Cell Death Differ. 2010;17(4):586–595
  19. Bladergroen BA, Strik MC, Bovenschen N, van Berkum O, Scheffer GL, Meijer CJ, et al. The granzyme B inhibitor, protease inhibitor 9, is mainly expressed by dendritic cells and at immune-privileged sites. J Immunol. 2001;166(5):3218–3225
  20. Buzza MS, Hirst CE, Bird CH, Hosking P, McKendrick J, Bird PI. The granzyme B. inhibitor, PI-9, is present in endothelial and mesothelial cells, suggesting that it protects bystander cells during immune responses. Cell Immunol. 2001;210(1):21–29
  21. Young JL, Sukhova GK, Foster D, Kisiel W, Libby P, Schonbeck U. The serpin proteinase inhibitor 9 is an endogenous inhibitor of interleukin 1beta-converting enzyme (caspase-1) activity in human vascular smooth muscle cells. J Exp Med. 2000;191(9):1535–1544
  22. Lin H, Wilson JE, Roberts CR, Horley KJ, Winters GL, Costanzo MR, et al. Biglycan, decorin, and versican protein expression patterns in coronary arteriopathy of human cardiac allograft: distinctness as compared to native atherosclerosis. J Heart Lung Transplant. 1996;15(12):1233–1247
  23. Virmani R, Kolodgie FD, Burke AP, Farb A, Schwartz SM. Lessons from sudden coronary death: a comprehensive morphological classification scheme for atherosclerotic lesions. Arterioscler Thromb Vasc Biol. 2000;20(5):1262–1275
  24. Rowshani AT, Florquin S, Bemelman F, Kummer JA, Hack CE, Ten Berge IJ. Hyperexpression of the granzyme B inhibitor PI-9 in human renal allografts: a potential mechanism for stable renal function in patients with subclinical rejection. Kidney Int. 2004;66(4):1417–1422
  25. Classen CF, Ushmorov A, Bird P, Debatin KM. The granzyme B inhibitor PI-9 is differentially expressed in all main subtypes of pediatric acute lymphoblastic leukemias. Haematologica. 2004;89(11):1314–1321
  26. Marchant D, Dou Y, Luo H, Garmaroudi FS, McDonough JE, Si X, et al. Bosentan enhances viral load via endothelin-1 receptor type-A-mediated p38 mitogen-activated protein kinase activation while improving cardiac function during coxsackievirus-induced myocarditis. Circ Res. 2009;104(6):813–821
  27. Abraham T, Carthy J, McManus B. Collagen matrix remodeling in 3-dimensional cellular space resolved using second harmonic generation and multiphoton excitation fluorescence. J Struct Biol. 2010;169(1):36–44
  28. Campbell GR, Campbell JH. The phenotypes of smooth muscle expressed in human atheroma. Ann N Y Acad Sci. 1990;598:143–158
  29. Davies MJ, Richardson PD, Woolf N, Katz DR, Mann J. Risk of thrombosis in human atherosclerotic plaques: role of extracellular lipid, macrophage, and smooth muscle cell content. Br Heart J. 1993;69(5):377–381
  30. Burke AP, Farb A, Malcom GT, Liang YH, Smialek J, Virmani R. Coronary risk factors and plaque morphology in men with coronary disease who died suddenly. N Engl J Med. 1997;336(18):1276–1282
  31. Gown AM, Willingham MC. Improved detection of apoptotic cells in archival paraffin sections: immunohistochemistry using antibodies to cleaved caspase 3. J Histochem Cytochem. 2002;50(4):449–454
  32. Atkinson EA, Barry M, Darmon AJ, Shostak I, Turner PC, Moyer RW, et al. Cytotoxic T lymphocyte-assisted suicide. Caspase 3 activation is primarily the result of the direct action of granzyme B. J Biol Chem. 1998;273(33):21261–21266
  33. Medema JP, de Jong J, Peltenburg LT, Verdegaal EM, Gorter A, Bres SA, et al. Blockade of the granzyme B/perforin pathway through overexpression of the serine protease inhibitor PI-9/SPI-6 constitutes a mechanism for immune escape by tumors. Proc Natl Acad Sci U S A. 2001;98(20):11515–11520
  34. Bladergroen BA, Meijer CJ, ten Berge RL, Hack CE, Muris JJ, Dukers DF, et al. Expression of the granzyme B inhibitor, protease inhibitor 9, by tumor cells in patients with non-Hodgkin and Hodgkin lymphoma: a novel protective mechanism for tumor cells to circumvent the immune system?. Blood. 2002;99(1):232–237
  35. ten Berge RL, Meijer CJ, Dukers DF, Kummer JA, Bladergroen BA, Vos W, et al. Expression levels of apoptosis-related proteins predict clinical outcome in anaplastic large cell lymphoma. Blood. 2002;99(12):4540–4546
  36. Hao H, Gabbiani G, Bochaton-Piallat ML. Arterial smooth muscle cell heterogeneity: implications for atherosclerosis and restenosis development. Arterioscler Thromb Vasc Biol. 2003;23(9):1510–1520
  37. Ross R. Atherosclerosis-an inflammatory disease. N Engl J Med. 1999;340(2):115–126
  38. Gittenberger-de Groot AC, DeRuiter MC, Bergwerff M, Poelmann RE. Smooth muscle cell origin and its relation to heterogeneity in development and disease. Arterioscler Thromb Vasc Biol. 1999;19(7):1589–1594
  39. Zalewski A, Shi Y, Johnson AG. Diverse origin of intimal cells: smooth muscle cells, myofibroblasts, fibroblasts, and beyond?. Circ Res. 2002;91(8):652–655
  40. Li WG, Miller FJ, Brown MR, Chatterjee P, Aylsworth GR, Shao J, et al. Enhanced H(2)O(2)-induced cytotoxicity in “epithelioid” smooth muscle cells: implications for neointimal regression. Arterioscler Thromb Vasc Biol. 2000;20(6):1473–1479
  41. Orlandi A, Francesconi A, Cocchia D, Corsini A, Spagnoli LG. Phenotypic heterogeneity influences apoptotic susceptibility to retinoic acid and cis-platinum of rat arterial smooth muscle cells in vitro: Implications for the evolution of experimental intimal thickening. Arterioscler Thromb Vasc Biol. 2001;21(7):1118–1123
  42. Chan SW, Hegyi L, Scott S, Cary NR, Weissberg PL, Bennett MR. Sensitivity to Fas-mediated apoptosis is determined below receptor level in human vascular smooth muscle cells. Circ Res. 2000;86(10):1038–1046
  43. Clarke M, Bennett M. The emerging role of vascular smooth muscle cell apoptosis in atherosclerosis and plaque stability. Am J Nephrol. 2006;26(6):531–535
  44. Clarke MC, Figg N, Maguire JJ, Davenport AP, Goddard M, Littlewood TD, et al. Apoptosis of vascular smooth muscle cells induces features of plaque vulnerability in atherosclerosis. Nat Med. 2006;12(9):1075–1080
  45. Clarke MC, Littlewood TD, Figg N, Maguire JJ, Davenport AP, Goddard M, et al. Chronic apoptosis of vascular smooth muscle cells accelerates atherosclerosis and promotes calcification and medial degeneration. Circ Res. 2008;102(12):1529–1538
  46. Littlewood TD, Bennett MR. Apoptotic cell death in atherosclerosis. Curr Opin Lipidol. 2003;14(5):469–475
  47. Stout-Delgado HW, Getachew Y, Rogers TE, Miller BC, Thiele DL. The role of serpinb9/serine protease inhibitor 6 in preventing granzyme B-dependent hepatotoxicity. Hepatology. 2007;46(5):1530–1540
  48. Hirst CE, Buzza MS, Bird CH, Warren HS, Cameron PU, Zhang M, et al. The intracellular granzyme B inhibitor, proteinase inhibitor 9, is up-regulated during accessory cell maturation and effector cell degranulation, and its overexpression enhances CTL potency. J Immunol. 2003;170(2):805–815
  49. Medema JP, Schuurhuis DH, Rea D, van Tongeren J, de Jong J, Bres SA, et al. Expression of the serpin serine protease inhibitor 6 protects dendritic cells from cytotoxic T lymphocyte-induced apoptosis: differential modulation by T helper type 1 and type 2 cells. J Exp Med. 2001;194(5):657–667

 This research was funded in part from grants from the Heart and Stroke Foundation of British Columbia and Yukon (HSFBCY) (DJG) and the Canadian Institutes for Health Research (CIHR) (MFA, DJG). Funding sources: AH is grateful for the support from a CIHR Canada Graduate Scholarship Master's Award and the Vanier Canada Graduate Scholarship. DC is funded by the HSFBCY, CIHR/IMPACT, and NSERC Fellowship.

PII: S1054-8807(10)00198-5

doi: 10.1016/j.carpath.2010.12.002

Cardiovascular Pathology
Volume 21, Issue 1 , Pages 28-38 , January 2012