Perforin and Granzyme B Have Separate and Distinct Roles during Atherosclerotic Plaque Development in Apolipoprotein E Knockout Mice

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Hiebert, Paul R ^a,b   Boivin, Wendy A ^a,b   Zhao, Hongyan ^a   McManus, Bruce M ^a,b   Granville, David J ^a,b  

^a ST PAUL S HOSPITAL   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN E; DECORIN; GRANZYME B; PERFORIN; PROTEOGLYCAN; COLLAGEN; DCN PROTEIN, MOUSE; GRANZYME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROTIC PLAQUE; BIOAVAILABILITY; CONTROLLED STUDY; EXTRACELLULAR MATRIX; IMMUNOREACTIVITY; LIPID BLOOD LEVEL; LIPID DIET; MOUSE; NONHUMAN; PATHOGENESIS; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; T LYMPHOCYTE; TISSUE LEVEL; ANIMAL; GENE INACTIVATION; GENETICS; KNOCKOUT MOUSE; LIPID METABOLISM; METABOLISM; PATHOLOGY; PHYSIOLOGY; THORACIC AORTA;

ANIMALS; AORTA, THORACIC; APOLIPOPROTEINS E; COLLAGEN; DECORIN; DIET, HIGH-FAT; GENE KNOCKOUT TECHNIQUES; GRANZYMES; LIPID METABOLISM; MICE, KNOCKOUT; PERFORIN; PLAQUE, ATHEROSCLEROTIC;

EID: 84886249315     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0078939     Document Type: Article

References (58)

1. Boivin WA, Cooper DM, Hiebert PR, Granville DJ, (2009) Intracellular versus extracellular granzyme B in immunity and disease: challenging the dogma. Lab Invest 89: 1195-1220. doi:10.1038/labinvest.2009.91. PubMed: 19770840.
2. Barry M, Bleackley RC, (2002) Cytotoxic T lymphocytes: all roads lead to death. Nat Rev Immunol 2: 401-409. PubMed: 12093006.
3. Smyth MJ, Trapani JA, (1995) Granzymes: exogenous proteinases that induce target cell apoptosis. Immunol Today 16: 202-206. doi:10.1016/0167-5699(95)80122-7. PubMed: 7734049.
4. Horiuchi K, Saito S, Sasaki R, Tomatsu T, Toyama Y, (2003) Expression of granzyme B in human articular chondrocytes. J Rheumatol 30: 1799-1810. PubMed: 12913938.
5. Hernandez-Pigeon H, Jean C, Charruyer A, Haure MJ, Baudouin C, et al. (2007) UVA induces granzyme B in human keratinocytes through MIF: implication in extracellular matrix remodeling. J Biol Chem 282: 8157-8164. doi:10.1074/jbc.M607436200. PubMed: 17224449.
6. Hernandez-Pigeon H, Jean C, Charruyer A, Haure MJ, Titeux M, et al. (2006) Human keratinocytes acquire cellular cytotoxicity under UV-B irradiation. Implication of granzyme B and perforin. J Biol Chem 281: 13525-13532. doi:10.1074/jbc.M512694200. PubMed: 16524880.
7. Strik MC, de Koning PJ, Kleijmeer MJ, Bladergroen BA, Wolbink AM, et al. (2007) Human mast cells produce and release the cytotoxic lymphocyte associated protease granzyme B upon activation. Mol Immunol 44: 3462-3472. doi:10.1016/j.molimm.2007.03.024. PubMed: 17485116.
8. Kim WJ, Kim H, Suk K, Lee WH, (2007) Macrophages express granzyme B in the lesion areas of atherosclerosis and rheumatoid arthritis. Immunol Lett 111: 57-65. doi:10.1016/j.imlet.2007.05.004. PubMed: 17604848.
9. Wagner C, Iking-Konert C, Denefleh B, Stegmaier S, Hug F, et al. (2004) Granzyme B and perforin: constitutive expression in human polymorphonuclear neutrophils. Blood 103: 1099-1104. PubMed: 14512315.
10. Tschopp CM, Spiegl N, Didichenko S, Lutmann W, Julius P, et al. (2006) Granzyme B, a novel mediator of allergic inflammation: its induction and release in blood basophils and human asthma. Blood 108: 2290-2299. doi:10.1182/blood-2006-03-010348. PubMed: 16794249.
11. Rissoan MC, Duhen T, Bridon JM, Bendriss-Vermare N, Péronne C, et al. (2002) Subtractive hybridization reveals the expression of immunoglobulin-like transcript 7, Eph-B1, granzyme B, and 3 novel transcripts in human plasmacytoid dendritic cells. Blood 100: 3295-3303. doi:10.1182/blood-2002-02-0638. PubMed: 12384430.
12. Namekawa T, Wagner UG, Goronzy JJ, Weyand CM, (1998) Functional subsets of CD4 T cells in rheumatoid synovitis. Arthritis Rheum 41: 2108-2116. doi:10.1002/1529-0131(199812)41:12. PubMed: 9870867.
13. Grossman WJ, Verbsky JW, Tollefsen BL, Kemper C, Atkinson JP, et al. (2004) Differential expression of granzymes A and B in human cytotoxic lymphocyte subsets and T regulatory cells. Blood 104: 2840-2848. doi:10.1182/blood-2004-03-0859. PubMed: 15238416.
14. Vernooy JH, Möller GM, van Suylen RJ, van Spijk MP, Cloots RH, et al. (2007) Increased granzyme A expression in type II pneumocytes of patients with severe chronic obstructive pulmonary disease. Am J Respir Crit Care Med 175: 464-472. doi:10.1164/rccm.200602-169OC. PubMed: 17138956.
15. Pardo J, Wallich R, Ebnet K, Iden S, Zentgraf H, et al. (2007) Granzyme B is expressed in mouse mast cells in vivo and in vitro and causes delayed cell death independent of perforin. Cell Death Differ 14: 1768-1779. doi:10.1038/sj.cdd.4402183. PubMed: 17599099.
16. Skjelland M, Michelsen AE, Krohg-Sørensen K, Tennøe B, Dahl A, et al. (2007) Plasma levels of granzyme B are increased in patients with lipid-rich carotid plaques as determined by echogenicity. Atherosclerosis 195: e142-e146. doi:10.1016/j.atherosclerosis.2007.05.001. PubMed: 17568588.
17. Bratke K, Böttcher B, Leeder K, Schmidt S, Küpper M, et al. (2004) Increase in granzyme B+ lymphocytes and soluble granzyme B in bronchoalveolar lavage of allergen challenged patients with atopic asthma. Clin Exp Immunol 136: 542-548. doi:10.1111/j.1365-2249.2004.02468.x. PubMed: 15147358.
18. Tremblay GM, Wolbink AM, Cormier Y, Hack CE, (2000) Granzyme activity in the inflamed lung is not controlled by endogenous serine proteinase inhibitors. J Immunol 165: 3966-3969. PubMed: 11034405.
19. Tak PP, Spaeny-Dekking L, Kraan MC, Breedveld FC, Froelich CJ, et al. (1999) The levels of soluble granzyme A and B are elevated in plasma and synovial fluid of patients with rheumatoid arthritis (RA). Clin Exp Immunol 116: 366-370. doi:10.1046/j.1365-2249.1999.00881.x. PubMed: 10337032.
20. Malmeström C, Lycke J, Haghighi S, Andersen O, Carlsson L, et al. (2008) Relapses in multiple sclerosis are associated with increased CD8+ T-cell mediated cytotoxicity in CSF. J Neuroimmunol 196: 159-165. doi:10.1016/j.jneuroim.2008.03.001. PubMed: 18396337.
21. Takahashi Y, Mine J, Kubota Y, Yamazaki E, Fujiwara T, (2009) A substantial number of Rasmussen syndrome patients have increased IgG, CD4(+) T cells, TNFalpha, and Granzyme B in CSF. Epilepsia.
22. Buzza MS, Zamurs L, Sun J, Bird CH, Smith AI, et al. (2005) Extracellular matrix remodeling by human granzyme B via cleavage of vitronectin, fibronectin, and laminin. J Biol Chem 280: 23549-23558. doi:10.1074/jbc.M412001200. PubMed: 15843372.
23. Chamberlain CM, Ang LS, Boivin WA, Cooper DM, Williams SJ, et al. (2010) Perforin-independent extracellular granzyme B activity contributes to abdominal aortic aneurysm. Am J Pathol 176: 1038-1049. doi:10.2353/ajpath.2010.090700. PubMed: 20035050.
24. Boivin WA, Shackleford M, Vanden Hoek A, Zhao H, Hackett TL, et al. (2012) Granzyme B Cleaves Decorin, Biglycan and Soluble Betaglycan, Releasing Active Transforming Growth Factor-beta1. PLOS ONE 7: e33163. doi:10.1371/journal.pone.0033163. PubMed: 22479366.
25. Hiebert PR, Boivin WA, Abraham T, Pazooki S, Zhao H, et al. (2011) Granzyme B contributes to extracellular matrix remodeling and skin aging in apolipoprotein E knockout mice. Exp Gerontol 46: 489-499. doi:10.1016/j.exger.2011.02.004. PubMed: 21316440.
26. Choy JC, Hung VH, Hunter AL, Cheung PK, Motyka B, et al. (2004) Granzyme B induces smooth muscle cell apoptosis in the absence of perforin: involvement of extracellular matrix degradation. Arterioscler Thromb Vasc Biol 24: 2245-2250. doi:10.1161/01.ATV.0000147162.51930.b7. PubMed: 15472125.
27. Froelich CJ, Zhang X, Turbov J, Hudig D, Winkler U, et al. (1993) Human granzyme B degrades aggrecan proteoglycan in matrix synthesized by chondrocytes. J Immunol 151: 7161-7171. PubMed: 8258716.
28. Ang LS, Boivin WA, Williams SJ, Zhao H, Abraham T, et al. (2011) Serpina3n attenuates granzyme B-mediated decorin cleavage and rupture in a murine model of aortic aneurysm. Cell Death. Drosophila Inf Serv 2: e209.
29. Hendel A, Granville DJ, (2013) Granzyme B Cleavage of Fibronectin Disrupts Endothelial Cell Adhesion, Migration and Capillary Tube Formation. Matrix Biol 31(1):: 14-22. PubMed: 23228447.
30. Halvorsen B, Otterdal K, Dahl TB, Skjelland M, Gullestad L, et al. (2008) Atherosclerotic plaque stability--what determines the fate of a plaque? Prog Cardiovasc Dis 51: 183-194. doi:10.1016/j.pcad.2008.09.001. PubMed: 19026853.
31. Tuttolomondo A, Di Raimondo D, Pecoraro R, Arnao V, Pinto A, et al. (2012) Atherosclerosis as an inflammatory disease. Curr Pharm Des 18: 4266-4288. doi:10.2174/138161212802481237. PubMed: 22390643.
32. Kyaw T, Winship A, Tay C, Kanellakis P, Hosseini H, et al. (2013) Cytotoxic and proinflammatory CD8+ T lymphocytes promote development of vulnerable atherosclerotic plaques in apoE-deficient mice. Circulation 127: 1028-1039. doi:10.1161/CIRCULATIONAHA.112.001347. PubMed: 23395974.
33. Hendel A, Cooper D, Abraham T, Zhao H, Allard MF, et al. (2012) Proteinase inhibitor 9 is reduced in human atherosclerotic lesion development. Cardiovasc Pathol 21: 28-38. doi:10.1016/j.carpath.2010.12.002. PubMed: 21296596.
34. Choy JC, McDonald PC, Suarez AC, Hung VH, Wilson JE, et al. (2003) Granzyme B in atherosclerosis and transplant vascular disease: association with cell death and atherosclerotic disease severity. Mod Pathol 16: 460-470. doi:10.1097/01.MP.0000067424.12280.BC. PubMed: 12748253.
35. Kondo H, Hojo Y, Tsuru R, Nishimura Y, Shimizu H, et al. (2009) Elevation of plasma granzyme B levels after acute myocardial infarction. Circ J 73: 503-507. doi:10.1253/circj.CJ-08-0668. PubMed: 19145036.
36. Simon MM, Prester M, Nerz G, Kramer MD, Fruth U, (1988) Release of biologically active fragments from human plasma-fibronectin by murine T cell-specific proteinase 1 (TSP-1). Biol Chem Hoppe Seyler 369 (Suppl):: 107-112. PubMed: 3060134.
37. Hirayasu H, Yoshikawa Y, Tsuzuki S, Fushiki T, (2008) A lymphocyte serine protease granzyme A causes detachment of a small-intestinal epithelial cell line (IEC-6). Biosci Biotechnol Biochem 72: 2294-2302. doi:10.1271/bbb.80140. PubMed: 18776688.
38. Simon MM, Kramer MD, Prester M, Gay S, (1991) Mouse T-cell associated serine proteinase 1 degrades collagen type IV: a structural basis for the migration of lymphocytes through vascular basement membranes. Immunology 73: 117-119. PubMed: 2045125.
39. Irmler M, Hertig S, MacDonald HR, Sadoul R, Becherer JD, et al. (1995) Granzyme A is an interleukin 1 beta-converting enzyme. J Exp Med 181: 1917-1922. doi:10.1084/jem.181.5.1917. PubMed: 7722467.
40. Sower LE, Klimpel GR, Hanna W, Froelich CJ, (1996) Extracellular activities of human granzymes. I. Granzyme A induces IL6 and IL8 production in fibroblast and epithelial cell lines. Cell Immunol 171: 159-163. doi:10.1006/cimm.1996.0187.
41. Metkar SS, Menaa C, Pardo J, Wang B, Wallich R, et al. (2008) Human and mouse granzyme A induce a proinflammatory cytokine response. Immunity 29: 720-733. doi:10.1016/j.immuni.2008.08.014. PubMed: 18951048.
42. Yoshikawa Y, Hirayasu H, Tsuzuki S, Fushiki T, (2010) Granzyme A and thrombin differentially promote the release of interleukin-8 from alveolar epithelial A549 cells. Cytotechnology 62: 325-332. doi:10.1007/s10616-010-9275-z. PubMed: 20424914.
43. Chamberlain CM, Granville DJ, (2007) The role of Granzyme B in atheromatous diseases. Can J Physiol Pharmacol 85: 89-95. doi:10.1139/y06-090. PubMed: 17487248.
44. Hendel A, Hiebert PR, Boivin WA, Williams SJ, Granville DJ, (2010) Granzymes in age-related cardiovascular and pulmonary diseases. Cell Death Differ 17: 596-606. doi:10.1038/cdd.2010.5. PubMed: 20139894.
45. Boivin WA, Shackleford M, Vanden Hoek A, Zhao H, Hackett TL, et al. (2012) Granzyme B cleaves decorin, biglycan and soluble betaglycan, releasing active transforming growth factor-beta1. PLOS ONE 7: e33163. doi:10.1371/journal.pone.0033163. PubMed: 22479366.
46. Danielson KG, Baribault H, Holmes DF, Graham H, Kadler KE, et al. (1997) Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J Cell Biol 136: 729-743. doi:10.1083/jcb.136.3.729. PubMed: 9024701.
47. Al Haj Zen A, Caligiuri G, Sainz J, Lemitre M, Demerens C, et al. (2006) Decorin overexpression reduces atherosclerosis development in apolipoprotein E-deficient mice. Atherosclerosis 187: 31-39. doi:10.1016/j.atherosclerosis.2005.08.023. PubMed: 16183063.
48. Cooper DM, Pechkovsky DV, Hackett TL, Knight DA, Granville DJ, (2011) Granzyme K activates protease-activated receptor-1. PLOS ONE 6: e21484. doi:10.1371/journal.pone.0021484. PubMed: 21760880.
49. Joeckel LT, Wallich R, Martin P, Sanchez-Martinez D, Weber FC, et al. (2011) Mouse granzyme K has pro-inflammatory potential. Cell Death Differ 18: 1112-1119. doi:10.1038/cdd.2011.5. PubMed: 21311565.
50. Anthony DA, Andrews DM, Chow M, Watt SV, House C, et al. (2010) A role for granzyme M in TLR4-driven inflammation and endotoxicosis. J Immunol 185: 1794-1803. doi:10.4049/jimmunol.1000430. PubMed: 20585036.
51. Afonina IS, Tynan GA, Logue SE, Cullen SP, Bots M, et al. (2011) Granzyme B-dependent proteolysis acts as a switch to enhance the proinflammatory activity of IL-1alpha. Mol Cell 44: 265-278. doi:10.1016/j.molcel.2011.07.037. PubMed: 22017873.
52. Omoto Y, Yamanaka K, Tokime K, Kitano S, Kakeda M, et al. (2010) Granzyme B is a novel interleukin-18 converting enzyme. J Dermatol Sci 59: 129-135. doi:10.1016/j.jdermsci.2010.05.004. PubMed: 20621450.
53. Viswanathan K, Bot I, Liu L, Dai E, Turner PC, et al. (2012) Viral cross-class serpin inhibits vascular inflammation and T lymphocyte fratricide; a study in rodent models in vivo and human cell lines in vitro. PLOS ONE 7: e44694. doi:10.1371/journal.pone.0044694. PubMed: 23049756.
54. Schiller NK, Boisvert WA, Curtiss LK, (2002) Inflammation in atherosclerosis: lesion formation in LDL receptor-deficient mice with perforin and Lyst(beige) mutations. Arterioscler Thromb Vasc Biol 22: 1341-1346. doi:10.1161/01.ATV.0000024082.46387.38. PubMed: 12171798.
55. Getz GS, Reardon CA, (2012) Animal models of atherosclerosis. Arterioscler Thromb Vasc Biol 32: 1104-1115. doi:10.1161/ATVBAHA.111.237693. PubMed: 22383700.
56. Tangirala RK, Rubin EM, Palinski W, (1995) Quantitation of atherosclerosis in murine models: correlation between lesions in the aortic origin and in the entire aorta, and differences in the extent of lesions between sexes in LDL receptor-deficient and apolipoprotein E-deficient mice. J Lipid Res 36: 2320-2328. PubMed: 8656070.
57. Merat S, Fruebis J, Sutphin M, Silvestre M, Reaven PD, (2000) Effect of aging on aortic expression of the vascular cell adhesion molecule-1 and atherosclerosis in murine models of atherosclerosis. J Gerontol A Biol Sci Med Sci 55: B85-B94. doi:10.1093/gerona/55.2.B85. PubMed: 10737683.
58. Dai E, Liu LY, Wang H, McIvor D, Sun YM, et al. (2010) Inhibition of chemokine-glycosaminoglycan interactions in donor tissue reduces mouse allograft vasculopathy and transplant rejection. PLOS ONE 5: e10510. doi:10.1371/journal.pone.0010510. PubMed: 20463901.