Lysosomal cysteine proteases in atherosclerosis

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 24, Issue 8, 2004, Pages 1359-1366

  Liu, Jian ^a   Sukhova, Galina K ^b   Sun, Jiu Song ^a   Xu, Wei Hua ^a   Libby, Peter ^b   Shi, Guo Ping ^b  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Atherosclerosis; Cathepsins; Cystatin; Cysteine proteases; Cytokines

Indexed keywords

ALOXISTATIN; CATHEPSIN B; CATHEPSIN H; CATHEPSIN K; CATHEPSIN L; CATHEPSIN S; COLLAGEN; CYSTATIN C; CYSTEINE PROTEINASE; CYSTEINE PROTEINASE INHIBITOR; CYTOKINE; ELASTIN; TISSUE EXTRACT;

ATHEROGENESIS; ATHEROSCLEROSIS; CELL CULTURE; CELL INFILTRATION; CELL INVASION; DISEASE COURSE; ELASTOLYSIS; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; HEART INFARCTION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LEUKOCYTE; MACROPHAGE; MONOCYTE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SECRETION; SHORT SURVEY; SMOOTH MUSCLE FIBER; STROKE; THROMBOSIS;

ANIMALS; APOLIPOPROTEINS E; ARTERIOSCLEROSIS; CELL ADHESION; CHEMOTAXIS, LEUKOCYTE; CYSTATINS; CYSTEINE ENDOPEPTIDASES; CYSTEINE PROTEINASE INHIBITORS; CYTOKINES; DISEASE PROGRESSION; ENDOTHELIUM, VASCULAR; ENZYME INDUCTION; EXTRACELLULAR MATRIX PROTEINS; HUMANS; LEUKOCYTES; LYSOSOMES; MACROPHAGES; MICE; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; RECEPTORS, LDL; THROMBOEMBOLISM;

EID: 4043106252     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.0000134530.27208.41     Document Type: Short Survey

References (83)

1. Libby P, Lee RT. Matrix matters. Circulation. 2000;102:1874-1876.
2. Parks WC. Who are the proteolytic culprits in vascular disease. J Clin Invest. 1999;104:1167-1168.
3. Weber AJ, De Bandt M. Angiogenesis: general mechanisms and implications for rheumatoid arthritis. Joint Bone Spine. 2000;67:366-383.
4. Ohtani H. Stromal reaction in cancer tissue: pathophysiologic significance of the expression of matrix-degrading enzymes in relation to matrix turnover and immune/inflammatory reactions. Pathol Int. 1998; 48:1-9.
5. Halloran BG. Pathogenesis of aneurysms. Semin Vasc Surg. 1995;8: 85-92.
6. MacSweenety STR. Pathogenesis of abdominal aortic aneurysm. Br J Surg. 1994;81:935-941.
7. Libby P. Molecular bases of the acute coronary syndromes. Circulation. 1995;91:2844-2850.
8. Libby P. Changing concepts of atherogenesis. J Intern Med. 2000;247: 349-358.
9. Galis ZS, Muszynski M, Sukhova GK, Simon-Morrissey E, Unemori EN, Lark MW, Amento E, Libby P. Cytokine-stimulated human vascular smooth muscle cells synthesize a complement of enzymes required for extracellular matrix digestion. Circ Res. 1994;75:181-189.
10. Newby AC, Southgate KM, Davies M. Extracellular matrix degrading metalloproteinases in the pathogenesis of atherosclerosis. Basic Res Cardiol Suppl. 1994;89:59-70.
11. Henney AM, Wakeley PR, Davies MJ, Foster K, Hembry R, Murphy G, Humphries S. Localization of stromelysin gene expression in atherosclerotic plaques by in situ hybridization. Proc Natl Acad Sci U S A. 1991;88:8154-8158.
12. Galis ZS, Sukhova GK, Lark MW, Libby P. Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques. J Clin Invest. 1994;94: 2493-2530.
13. Halpert I, Sires UI, Roby JD, Potter-Perigo S, Wight TN, Shapiro SD, Welgus HG, Wickline SA, Parks WC. Matrilysin is expressed by lipid-laden macrophages at sites of potential rupture in atherosclerotic lesions and localizes to areas of versican deposition, a proteoglycan substrate for the enzyme. Proc Natl Acad Sci U S A. 1996;93:9748-9753.
14. Woessner JF Jr. Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J. 1991;5:2145-2154.
15. Suzuki K, Enghild JJ, Morodomi T, Salvesen G, Nagase H. Mechanisms of activation of tissue procollagenase by matrix metalloproteinase 3 (stromelysin). Biochemistry. 1990;29:10261-10270.
16. Weisman HF, Bulkley BH. Pathophysiology of atherosclerotic heart disease. Cardiol Clin. 1984;2:555-569.
17. Bendeck MP, Irvin C, Reidy MA. Inhibition of matrix metalloproteinase activity inhibits smooth muscle cell migration but not neointimal thickening after arterial injury. Circ Res. 1996;78:38-43.
18. Ye S, Watts GF, Mandalia S, Humphries SE, Henney AM. Preliminary report: genetic variation in the human stromelysin promoter is associated with progression of coronary atherosclerosis. Br Heart J. 1995;73: 209-215.
19. George SJ, Baker AH, Angelini GD, Newby AC. Gene transfer of tissue inhibitor of metalloproteinase-2 inhibits metalloproteinase activity and neointima formation in human saphenous veins. Gene Ther. 1998;5: 1552-1560.
20. Lemaitre V, O'Byrne TK, Borczuk AC, Okada Y, Tall AR, D'Armiento J. ApoE knockout mice expressing human matrix metalloproteinase-1 in macrophages have less advanced atherosclerosis. J Clin Invest. 2001;107: 1227-1234.
21. Steins MB, Padro T, Li CX, Mesters RM, Ostermann H, Hammel D, Scheld HH, Berdel WE, Kienast J. Overexpression of tissue-type plasminogen activator in atherosclerotic human coronary arteries. Atherosclerosis. 1999;145:173-180.
22. Kienast J, Padro T, Steins M, Li CX, Schmid KW, Hammel D, Scheld HH, van de Loo JC. Relation of urokinase-type plasminogen activator expression to presence and severity of atherosclerotic lesions in human coronary arteries. Thromb Haemost. 1998;79:579-586.
23. Carmeliet P, Moons L, Lijnen R, Baes M, Lemaitre V, Tipping P, Drew A, Eeckhout Y, Shapiro S, Lupu F, Collen D. Urokinase-generated plasmin activates matrix metalloproteinases during aneurysm formation. Nat Genet. 1997;17:439-444.
24. Falkenberg M, Tom C, DeYoung MB, Wen S, Linnemann R, Dichek DA. Increased expression of urokinase during atherosclerotic lesion development causes arterial constriction and lumen loss, and accelerates lesion growth. Proc Natl Acad Sci U S A. 2002;99:10665-10670.
25. Xiao Q, Danton MJ, Witte DP, Kowala MC, Valentine MT, Bugge TH, Degen JL. Plasminogen deficiency accelerates vessel wall disease in mice predisposed to atherosclerosis. Proc Natl Acad Sci U S A. 1997;94: 10335-10340.
26. Dollery CM, Owen CA, Sukhova GK, Krettek A, Shapiro SD, Libby P. Neutrophil elastase in human atherosclerotic plaques: production by macrophages. Circulation. 2003;107:2829-2836.
27. Okumura Y, Sato H, Seiki M, Kido H. Proteolytic activation of the precursor of membrane type 1 matrix metalloproteinase by human plasmin: a possible cell surface activator. FEBS Lett. 1997;402:181-184.
28. Baramova EN, Bajou K, Remacle A, L'Hoir C, Krell HW, Weidle UH, Noel A, Foidart JM. Involvement of PA/plasmin system in the processing of pro-MMP-2 activation. FEBS Lett. 1997;405:157-162.
29. Chapman HA, Riese RJ, Shi GP. Emerging roles for cysteine proteases in human biology. Annu Rev Physiol. 1997;59:63-88.
30. Li Z, Yasuda Y, Li W, Bogyo M, Katz N, Gordon RE, Fields GB, Bromme D. Regulation of collagenase activities of human cathepsins by glycosaminoglycans. J Biol Chem. 2004;279:5470-5479.
31. Gelb BD, Shi GP, Chapman HA, Desnick RJ. Pyknodysostosis, a lysosomal disease caused by cathepsin K deficiency. Science. 1996;273: 1236-1238.
32. Saftig P, Hunziker E, Wehmeyer O, Jones S, Boyde A, Rommerskirch W, Moritz JD, Schu P, von Figura K. Impaired osteoclastic bone resorption leads to osteopetrosis in cathepsin-K-deficient mice. Proc Natl Acad Sci U S A. 1998;95:13453-13458.
33. Sukhova GK, Shi GP, Simon DI, Chapman HA, Libby P. Expression of the elastolytic cathepsins S and K in human atheroma and regulation of their production in smooth muscle cells. J Clin Invest. 1998;102: 576-583.
34. Shah PK, Falk E, Badimon JJ, Fernandez-Ortiz A, Mailhac A, Villareal-Levy G, Fallon JT, Regnstrom J, Fuster V. Human monocyte-derived macrophages induce collagen breakdown in fibrous caps of atherosclerotic plaques: potential role of matrix-degrading metalloproteinases and implications for plaque rupture. Circulation. 1995;92: 1565-1569.
35. Shi GP, Sukhova GK, Kuzuya M, Ye Q, Du J, Zhang Y, Pan JH, Lu ML, Cheng XW, Iguchi A, Perrey S, Lee AM, Chapman HA, Libby P. Deficiency of the cysteine protease cathepsin S impairs microvessel growth. Circ Res. 2003;92:493-500.
36. Jormsjo S, Wuttge DM, Sirsjo A, Whatling C, Hamsten A, Stemme S, Eriksson P. Differential expression of cysteine and aspartic proteases during progression of atherosclerosis in apolipoprotein E-deficient mice. Am J Pathol. 2002;161:939-945.
37. Shi GP, Sukhova GK, Grubb A, Ducharme A, Rhode LH, Lee RT, Ridker PM, Libby P, Chapman HA. Cystatin C deficiency in human atherosclerosis and aortic aneurysms. J Clin Invest. 1999;104:1191-1197.
38. Fabunmi RP, Sukhova GK, Sugiyama S, Libby P. Expression of tissue inhibitor of metalloproteinases-3 in human atheroma and regulation in lesion-associated cells: a potential protective mechanism in plaque stability. Circ Res. 1998;83:270-278.
39. Fabunmi RP, Baker AH, Murray EJ, Booth RF, Newby AC. Divergent regulation by growth factors and cytokines of 95 kDa and 72 kDa gelatinases and tissue inhibitors or metalloproteinases-1, -2, and -3 in rabbit aortic smooth muscle cells. Biochem J. 1996;315:335-342.
40. Ishibashi S, Goldstein JL, Brown MS, Herz J, Burns DK. Massive xanthomatosis and atherosclerosis in cholesterol-fed low density lipoprotein receptor-negative mice. J Clin Invest. 1994;93:1885-1893.
41. Shi GP, Chapman HA, Bhairi SM, DeLeeuw C, Reddy VY, Weiss SJ. Molecular cloning of human cathepsin O, a novel endoproteinase and homologue of rabbit OC2. FEBS Lett. 1995;357:129-134.
42. Reddy VY, Zhang QY, Weiss SJ. Pericellular mobilization of the tissue-destructive cysteine proteases, cathepsin B, L, and S, by human monocyte-derived macrophages. Proc Natl Acad Sci U S A. 1995;92:3849-3853.
43. Punturieri A, Filippov S, Allen E, Caras I, Murray R, Reddy V, Weiss SJ. Regulation of elastinolytic cysteine proteinase activity in normal and cathepsin K-deficient human macrophages. J Exp Med. 2000;192:789-799.
44. Grainger DJ, Kemp PR, Metcalfe JC, Liu AC, Lawn RM, Williams NR, Grace AA, Schofield PM, Chauhan A. The serum concentration of active transforming growth factor-β is severely depressed in advanced atherosclerosis. Nat Med. 1995;1:74-79.
45. Nishimura Y, Kawabata T, Yano S, Kato K. Inhibition of intracellular sorting and processing of lysosomal cathepsins H and L at reduced temperature in primary cultures of rat hepatocytes. Arch Biochem Biophys. 1990;283:458-463.
46. Kuliawat R, Klumperman J, Ludwig T, Arvan P. Differential sorting of lysosomal enzymes out of the regulated secretory pathway in pancreatic beta-cells. J Cell Biol. 1997;137:595-608.
47. Ahn K, Yeyeodu S, Collette J, Madden V, Arthur J, Li L, Erickson AH. An alternate targeting pathway for procathepsin L in mouse fibroblasts. Traffic. 2002;3:147-159.
48. Jackson RC, Blobel G. Post-translational cleavage of presecretory proteins with an extract of rough microsomes from dog pancreas containing signal peptidase activity. Proc Natl Acad Sci U S A. 1977;74:5598-5602.
49. Bromme D, Okamoto K, Wang BB, Biroc S. Human cathepsin O2, a matrix protein-degrading cysteine protease expressed in osteoclasts: functional expression of human cathepsin O2 in Spodoptera frugiperda and characterization of the enzyme. J Biol Chem. 1996;271:2126-2132.
50. Shi GP, Munger JS, Meara JP, Rich DH, Chapman HA. Molecular cloning and expression of human alveolar macrophage cathepsin S, an elastinolytic cysteine protease. J Biol Chem. 1992;267:7258-7262.
51. Sukhova GK, Zhang Y, Pan JH, Wada Y, Yamamoto T, Naito M, Kodama T, Tsimikas S, Witztum JL, Lu ML, Sakara Y, Chin MT, Libby P, Shi GP. Deficiency of cathepsin S reduces atherosclerosis in LDL receptor-deficient mice. J Clin invest. 2003;111:897-906.
52. Gu L, Okada Y, Clinton SK, Gerard C, Sukhova GK, Libby P, Rollins BJ. Absence of monocyte chemoattractant protein-1 reduces atherosclerosis in low density lipoprotein receptor-deficient mice. Mol Cell. 1998;2:275-281.
53. Inoue S, Egashira K, Ni W, Kitamoto S, Usui M, Otani K, Ishibashi M, Hiasa K, Nishida K, Takeshita A. Anti-monocyte chemoattractant protein-1 gene therapy limits progression and destabilization of established atherosclerosis in apolipoprotein E-knockout mice. Circulation. 2002;106:2700-2706.
54. Dansky HM, Barlow CB, Lominska C, Sikes JL, Kao C, Weinsaft J, Cybulsky MI, Smith JD. Adhesion of monocytes to arterial endothelium and initiation of atherosclerosis are critically dependent on vascular cell adhesion molecule-1 gene dosage. Arterioscler Thromb Vasc Biol. 2001;21:1662-1667.
55. Hummel V, Kallmann BA, Wagner S, Fuller T, Bayas A, Tonn JC, Benveniste EN, Toyka KV, Rieckmann P. Production of MMPs in human cerebral endothelial cells and their role in shedding adhesion molecules. J Neuropathol Exp Neurol. 2001;60:320-327.
56. Riese RJ, Shi GP, Villadangos J, Stetson D, Driessen C, Lennon-Dumenil AM, Chu CL, Naumov Y, Behar SM, Ploegh H, Locksley R, Chapman HA. Regulation of CD1 function and NK1.1(+) T cell selection and maturation by cathepsin S. Immunity. 2001;15:909-919.
57. Leca G, Mansur SE, Bensussan A. Expression of VCAM-1 (CD106) by a subset of TCR γδ-bearing lymphocyte clones: involvement of a metalloprotease in the specific hydrolytic release of the soluble isoform. J Immunol. 1995;154:1069-1077.
58. Kowalski J, Okopien B, Madej A, Makowiecka K, Zielinski M, Kalina Z, Herman ZS. Levels of sICAM-1, sVCAM-1 and MCP-1 in patients with hyperlipoproteinemia IIa and -IIb. Int J Clin Pharmacol Ther. 2001;39:48-52.
59. Wang G, Woo CW, Sung FL, Siow YL, O K. Increased monocyte adhesion to aortic endothelium in rats with hyperhomocysteinemia: role of chemokine and adhesion molecules. Artenoscler Thromb Vasc Biol. 2002;22:1777-1783.
60. Kittelberger R, Davis PF, Stehbens WE. Distribution of type IV collagen, laminin, nidogen and fibronectin in the haemodynamically stressed vascular wall. Histol Histopathol. 1990;5:161-167.
61. Navaratnam V. Organisation and reorganisation of blood vessels in embryonic development. Eye. 1991;5:147-150.
62. Del Maestro RF, Vaithilingam IS, McDonald W. Degradation of collagen type IV by C6 astrocytoma cells. J Neurooncol. 1995;24:75-81.
63. Libby P, Schönbeck U. Drilling for oxygen: angiogenesis involves proteolysis of the extracellular matrix. Circ Res. 2001;89:195-197.
64. Bromme D, Bonneau PR, Lachance P, Wiederanders B, Kirschke H, Peters C, Thomas DY, Storer AC, Vernet T. Functional expression of human cathepsin S in Saccharomyces cerevisiae: purification and characterization of the recombinant enzyme. J Biol Chem. 1993;268:4832-4838.
65. Dehrmann FM, Coetzer TH, Pike RN, Dennison C. Mature cathepsin L is substantially active in the ionic milieu of the extracellular medium. Arch Biochem Biophys. 1995;324:93-98.
66. Garnero P, Borel O, Byrjalsen I, Ferreras M, Drake FH, McQueney MS, Foged NT, Delmas PD, Delaisse JM. The collagenolytic activity of cathepsin K is unique among mammalian proteinases. J Biol Chem. 1998;273: 32347-32352.
67. Ishidoh K, Kominami E. Procathepsin L degrades extracellular matrix proteins in the presence of glycosaminoglycans in vitro. Biochem Biophys Res Commun. 1995;217:624-631.
68. Ooyama T, Fukuda K, Oda H, Nakamura H, Hikita Y. Substratum-bound elastin peptide inhibits aortic smooth muscle cell migration in vitro. Arteriosclerosis. 1987;7:593-598.
69. Karnik SK, Brooke BS, Bayes-Genis A, Sorensen L, Wythe JD, Schwartz RS, Keating MT, Li DY. A critical role for elastin signaling in vascular morphogenesis and disease. Development. 2003;130:411-423.
70. Vancompernolle K, Van Herreweghe F, Pynaert G, Van de Craen M, De Vos K, Totty N, Sterling A, Fiers W, Vandenabeele P, Grooten J. Atractyloside-induced release of cathepsin B, a protease with caspase-processing activity. FEBS Lett. 1998;438:150-158.
71. Ishisaka R, Utsumi T, Kanno T, Arita K, Katunuma N, Akiyama J, Utsumi K. Participation of a cathepsin L-type protease in the activation of caspase-3. Cell Struct Funct. 1999;24:465-470.
72. Guicciardi ME, Deussing J, Miyoshi H, Bronk SF, Svingen PA, Peters C, Kaufmann SH, Gores GJ. Cathepsin B contributes to TNF-α-mediated hepatocyte apoptosis by promoting mitochondrial release of cytochrome C. J Clin Invest. 2000;106:1127-1137.
73. Li W, Dalen H, Eaton JW, Yuan XM. Apoptotic death of inflammatory cells in human atheroma. Arterioscler Thromb Vasc Biol. 2001;21:1124-1130.
74. Li W, Yuan XM, Olsson AG, Brunk UT. Uptake of oxidized LDL by macrophages results in partial lysosomal enzyme inactivation and relocation. Arterioscler Thromb Vasc Biol. 1998;18:177-184.
75. Shi GP, Villadangos JA, Dranoff G, Small C, Gu L, Haley KJ, Riese R, Ploegh HL, Chapman HA. Cathepsin S required for normal MHC class II peptide loading and germinal center development Immunity. 1999;10:197-206.
76. Nakagawa T, Roth W, Wong P, Nelson A, Farr A, Deussing J, Villadangos JA, Ploegh H, Peters C, Rudensky AY. Cathepsin L: critical role in Ii degradation and CD4 T cell selection in the thymus. Science. 1998;280: 450-453.
77. Hansson G, Libby P, Schoenbeck U, Yan Z-Q. Innate and adaptive immunity in the pathogenesis of atherosclerosis. Circ Res. 2002;91:281-291.
78. Zhang Y, Cliff WJ, Schoefl GI, Higgins G. Immunohistochemical study of intimal microvessels in coronary atherosclerosis. Am J Pathol. 1993;143: 164-172.
79. Sukhova GK, Schonbeck U, Rabkin E, Schoen FJ, Poole AR, Billinghurst RC, Libby P. Evidence for increased collagenolysis by interstitial collagenases-1 and -3 in vulnerable human atheromatous plaques. Circulation. 1999; 99:2503-2509.
80. Chen J, Tung CH, Mahmood U, Ntziachristos V, Gyurko R, Fishman MC, Huang PL, Weissleder R. In vivo imaging of proteolytic activity in atherosclerosis. Circulation. 2002;105:2766-2771.
81. Liuzzo JP, Petanceska SS, Moscatelli D, Devi LA. Inflammatory mediators regulate cathepsin S in macrophages and microglia: a role in attenuating heparan sulfate interactions. Mol Med. 1999;5:320-333.
82. Day SM, Reeve JL, Mundada L, Pan JH, Shi GP, Fay W. Cathepsin S-deficient mice display a prothrombotic phenotype. Circulation. 2002;106:195.
83. Villadangos JA, Bryant RA, Deussing J, Driessen C, Lennon-Dumenil AM, Riese RJ, Roth W, Saftig P, Shi GP, Chapman HA, Peters C, Ploegh HL. Proteases involved in MHC class II antigen presentation. Immunol Rev. 1999;172:109-120.