Mast cells: Important players in the orchestrated pathogenesis of abdominal aortic aneurysms

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 4, 2011, Pages 734-740

  Swedenborg, Jesper ^a,b   Mäyränpää, Mikko I ^c,d,e   Kovanen, Petri T ^c,d  

^a KAROLINSKA INSTITUTE   (Sweden)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c WIHURI RESEARCH INSTITUTE   (Finland)

^d UNIVERSITY OF HELSINKI   (Finland)

^e HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

Author keywords

aneurysms; angiogenesis; angiotensin II; apoptosis; immune system; macrophages; mast cells; proteolytic enzymes

Indexed keywords

ANTIHISTAMINIC AGENT; CARBOXYPEPTIDASE; CATHEPSIN G; CHEMOKINE; CHYMASE; CYTOKINE; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; HEPARIN; HISTAMINE; ICOSANOID; LEUKOTRIENE RECEPTOR BLOCKING AGENT; METALLOPROTEINASE; PROTEINASE; STABILIZING AGENT; TRYPTASE;

ABDOMINAL AORTA ANEURYSM; APOPTOSIS; ARTICLE; ATHEROSCLEROSIS; CYTOKINE RELEASE; DRUG EFFICACY; HUMAN; IMMUNITY; INFLAMMATION; MAST CELL; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SMOOTH MUSCLE FIBER; SYNTHESIS;

ANIMALS; AORTIC ANEURYSM, ABDOMINAL; APOPTOSIS; CATHEPSINS; DISEASE PROGRESSION; HUMANS; MAST CELLS; MATRIX METALLOPROTEINASES; MYOCYTES, SMOOTH MUSCLE; NEOVASCULARIZATION, PATHOLOGIC; RENIN-ANGIOTENSIN SYSTEM;

EID: 79953766381     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.110.213157     Document Type: Article

References (76)

1. Thompson RW. Basic science of abdominal aortic aneurysms: emerging therapeutic strategies for an unresolved clinical problem. Curr Opin Cardiol. 1996;11:504-518. (Pubitemid 26320991)
2. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med. 2005;352:1685-1695.
3. Laine P, Kaartinen M, Penttila A, Panula P, Paavonen T, Kovanen PT. Association between myocardial infarction and the mast cells in the adventitia of the infarct-related coronary artery. Circulation. 1999;99: 361-369. (Pubitemid 29051261)
4. Kovanen PT. Mast cells: multipotent local effector cells in atherothrombosis. Immunol Rev. 2007;217:105-122. (Pubitemid 46718148)
5. Tsuruda T, Kato J, Hatakeyama K, Kojima K, Yano M, Yano Y, Nakamura K, Nakamura-Uchiyama F, Matsushima Y, Imamura T, Onitsuka T, Asada Y, Nawa Y, Eto T, Kitamura K. Adventitial mast cells contribute to pathogenesis in the progression of abdominal aortic aneurysm. Circ Res. 2008;102:1368-1377.
6. Galli SJ, Gordon JR, Wershil BK. Cytokine production by mast cells and basophils. Curr Opin Immunol. 1991;3:865-872.
7. Kaartinen M, Penttila A, Kovanen PT. Mast cells of two types differing in neutral protease composition in the human aortic intima. Demonstration of tryptase- and tryptase/chymase-containing mast cells in normal intimas, fatty streaks, and the shoulder region of atheromas. Arterioscler Thromb. 1994;14:966-972.
8. Lindstedt KA, Mayranpaa MI, Kovanen PT. Mast cells in vulnerable atherosclerotic plaques-a view to a kill. J Cell Mol Med. 2007;11: 739-758. (Pubitemid 47313293)
9. Krishnaswamy G, Ajitawi O, Chi DS. The human mast cell: an overview. Methods Mol Biol. 2006;315:13-34.
10. Mayranpaa MI, Trosien JA, Fontaine V, Folkesson M, Kazi M, Eriksson P, Swedenborg J, Hedin U. Mast cells associate with neovessels in the media and adventitia of abdominal aortic aneurysms. J Vasc Surg. 2009; 50:388-395.
11. Sun J, Sukhova GK, Yang M, Wolters PJ, MacFarlane LA, Libby P, Sun C, Zhang Y, Liu J, Ennis TL, Knispel R, Xiong W, Thompson RW, Baxter BT, Shi GP. Mast cells modulate the pathogenesis of elastaseinduced abdominal aortic aneurysms in mice. J Clin Invest. 2007;117: 3359-3368. (Pubitemid 350096992)
12. Xiong W, Mactaggart J, Knispel R, Worth J, Persidsky Y, Baxter BT. Blocking tumor necrosis factor {alpha} attenuates aneurysm formation in a murine model. J Immunol. 2009;183:2741-2746.
13. Inoue N, Muramatsu M, Jin D, Takai S, Hayashi T, Katayama H, Kitaura Y, Tamai H, Miyazaki M. Effects of chymase inhibitor on angiotensin II-induced abdominal aortic aneurysm development in apolipoprotein E-deficient mice. Atherosclerosis. 2009;204:359-364.
14. Tsunemi K, Takai S, Nishimoto M, Jin D, Sakaguchi M, Muramatsu M, Yuda A, Sasaki S, Miyazaki M. A specific chymase inhibitor, 2-(5- formylamino-6-oxo-2- phenyl-1,6-dihydropyrimidine-1-yl)-N-[[3,4- dioxo- 1-phenyl-7-(2-pyridyloxy)]-2- heptyl]acetamide (NK3201), suppresses development of abdominal aortic aneurysm in hamsters. J Pharmacol Exp Ther. 2004;309:879-883. (Pubitemid 38669674)
15. Furubayashi K, Takai S, Jin D, Muramatsu M, Ibaraki T, Nishimoto M, Fukumoto H, Katsumata T, Miyazaki M. The significance of chymase in the progression of abdominal aortic aneurysms in dogs. Hypertens Res. 2007;30:349-357. (Pubitemid 46779983)
16. Yoshimura K, Aoki H, Ikeda Y, Fujii K, Akiyama N, Furutani A, Hoshii Y, Tanaka N, Ricci R, Ishihara T, Esato K, Hamano K, Matsuzaki M. Regression of abdominal aortic aneurysm by inhibition of c-Jun N-terminal kinase. Nat Med. 2005;11:1330-1338. (Pubitemid 41752914)
17. Wang LD, Wang M, Todisco A, Grand E, del Valle J. The human histamine H(2) receptor regulates c-jun and c-fos in a differential manner. Am J Physiol Cell Physiol. 2000;278:C1246-C1255. (Pubitemid 30432409)
18. Sun J, Zhang J, Lindholt JS, Sukhova GK, Liu J, He A, Abrink M, Pejler G, Stevens RL, Thompson RW, Ennis TL, Gurish MF, Libby P, Shi GP. Critical role of mast cell chymase in mouse abdominal aortic aneurysm formation. Circulation. 2009;120:973-982.
19. Thompson RW, Geraghty PJ, Lee JK. Abdominal aortic aneurysms: basic mechanisms and clinical implications. Curr Probl Surg. 2002;39: 110-230.
20. Fontaine V, Jacob MP, Houard X, Rossignol P, Plissonnier D, Angles-Cano E, Michel JB. Involvement of the mural thrombus as a site of protease release and activation in human aortic aneurysms. Am J Pathol. 2002;161:1701-1710. (Pubitemid 35265529)
21. Abisi S, Burnand KG, Waltham M, Humphries J, Taylor PR, Smith A. Cysteine protease activity in the wall of abdominal aortic aneurysms. J Vasc Surg. 2007;46:1260-1266. (Pubitemid 350267073)
22. Fontaine V, Touat Z, Mtairag el M, Vranckx R, Louedec L, Houard X, Andreassian B, Sebbag U, Palombi T, Jacob MP, Meilhac O, Michel JB. Role of leukocyte elastase in preventing cellular re-colonization of the mural thrombus. Am J Pathol. 2004;164:2077-2087. (Pubitemid 38669355)
23. Hans SS, Jareunpoon O, Balasubramaniam M, Zelenock GB. Size and location of thrombus in intact and ruptured abdominal aortic aneurysms. J Vasc Surg. 2005;41:584-588. (Pubitemid 40637655)
24. Sakalihasan N, Delvenne P, Nusgens BV, Limet R, Lapiere CM. Activated forms of MMP2 and MMP9 in abdominal aortic aneurysms. J Vasc Surg. 1996;24:127-133. (Pubitemid 26271963)
25. Gruber BL, Marchese MJ, Suzuki K, Schwartz LB, Okada Y, Nagase H, Ramamurthy NS. Synovial procollagenase activation by human mast cell tryptase dependence upon matrix metalloproteinase 3 activation. J Clin Invest. 1989;84:1657-1662. (Pubitemid 19272256)
26. Saarinen J, Kalkkinen N, Welgus HG, Kovanen PT. Activation of human interstitial procollagenase through direct cleavage of the Leu83-Thr84 bond by mast cell chymase. J Biol Chem. 1994;269:18134-18140.
27. Okada Y, Nakanishi I. Activation of matrix metalloproteinase 3 (stromelysin) and matrix metalloproteinase 2 ('gelatinase') by human neutrophil elastase and cathepsin G. FEBS Lett. 1989;249:353-356. (Pubitemid 19143491)
28. Saunders WB, Bayless KJ, Davis GE. MMP-1 activation by serine proteases and MMP-10 induces human capillary tubular network collapse and regression in 3D collagen matrices. J Cell Sci. 2005;118:2325-2340. (Pubitemid 40872853)
29. Furubayashi K, Takai S, Jin D, Miyazaki M, Katsumata T, Inagaki S, Kimura M, Tanaka K, Nishimoto M, Fukumoto H. Chymase activates promatrix metalloproteinase-9 in human abdominal aortic aneurysm. Clin Chim Acta. 2008;388:214-216. (Pubitemid 350266567)
30. Tchougounova E, Lundequist A, Fajardo I, Winberg JO, Abrink M, Pejler G. A key role for mast cell chymase in the activation of pro-matrix metalloprotease-9 and pro-matrix metalloprotease-2. J Biol Chem. 2005; 280:9291-9296. (Pubitemid 40409621)
31. Baram D, Vaday GG, Salamon P, Drucker I, Hershkoviz R, Mekori YA. Human mast cells release metalloproteinase-9 on contact with activated T cells: juxtacrine regulation by TNF-alpha. J Immunol. 2001;167: 4008-4016. (Pubitemid 32910846)
32. Alam R, Forsythe PA, Lett-Brown MA, Grant JA. Cellular origin of histamine-releasing factor produced by peripheral blood mononuclear cells. J Immunol. 1989;142:3951-3956. (Pubitemid 19164427)
33. Gordon JR, Galli SJ. Mast cells as a source of both preformed and immunologically inducible TNF-alpha/cachectin. Nature. 1990;346: 274-276.
34. Juvonen J, Surcel HM, Satta J, Teppo AM, Bloigu A, Syrjala H, Airaksinen J, Leinonen M, Saikku P, Juvonen T. Elevated circulating levels of inflammatory cytokines in patients with abdominal aortic aneurysm. Arterioscler Thromb Vasc Biol. 1997;17:2843-2847. (Pubitemid 28016030)
35. Saren P, Welgus HG, Kovanen PT. TNF-alpha and IL-1beta selectively induce expression of 92-kDa gelatinase by human macrophages. J Immunol. 1996;157:4159-4165. (Pubitemid 126449330)
36. Lutgens SP, Cleutjens KB, Daemen MJ, Heeneman S. Cathepsin cysteine proteases in cardiovascular disease. FASEB J. 2007;21:3029-3041. (Pubitemid 47565524)
37. Abdul-Hussien H, Soekhoe RG, Weber E, von der Thusen JH, Kleemann R, Mulder A, van Bockel JH, Hanemaaijer R, Lindeman JH. Collagen degradation in the abdominal aneurysm: a conspiracy of matrix metalloproteinase and cysteine collagenases. Am J Pathol. 2007;170:809-817. (Pubitemid 47339351)
38. Lindholt JS, Erlandsen EJ, Henneberg EW. Cystatin C deficiency is associated with the progression of small abdominal aortic aneurysms. Br J Surg. 2001;88:1472-1475. (Pubitemid 32989466)
39. 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. (Pubitemid 29536290)
40. Kaschina E, Scholz H, Steckelings UM, Sommerfeld M, Kemnitz UR, Artuc M, Schmidt S, Unger T. Transition from atherosclerosis to aortic aneurysm in humans coincides with an increased expression of RAS components. Atherosclerosis. 2009;205:396-403.
41. Holmes DR, Liao S, Parks WC, Thompson RW. Medial neovascularization in abdominal aortic aneurysms: a histopathologic marker of aneurysmal degeneration with pathophysiologic implications. J Vasc Surg. 1995;21:761-771.
42. Vorp DA, Federspiel WJ, Webster MW. Does laminated intraluminal thrombus within abdominal aortic aneurysm cause anoxia of the aortic wall? J Vasc Surg. 1996;23:540-541. (Pubitemid 26081301)
43. Kazi M, Thyberg J, Religa P, Roy J, Eriksson P, Hedin U, Swedenborg J. Influence of intraluminal thrombus on structural and cellular composition of abdominal aortic aneurysm wall. J Vasc Surg. 2003;38: 1283-1292. (Pubitemid 37517657)
44. Choke E, Thompson MM, Dawson J, Wilson WR, Sayed S, Loftus IM, Cockerill GW. Abdominal aortic aneurysm rupture is associated with increased medial neovascularization and overexpression of proangiogenic cytokines. Arterioscler Thromb Vasc Biol. 2006;26:2077-2082. (Pubitemid 44253791)
45. Choke E, Cockerill GW, Dawson J, Chung YL, Griffiths J, Wilson RW, Loftus IM, Thompson MM. Hypoxia at the site of abdominal aortic aneurysm rupture is not associated with increased lactate. Ann N Y Acad Sci. 2006;1085:306-310. (Pubitemid 47091977)
46. Norrby K. Mast cells and angiogenesis. APMIS. 2002;110:355-371.
47. Liu J, Divoux A, Sun J, Zhang J, Clement K, Glickman JN, Sukhova GK, Wolters PJ, Du J, Gorgun CZ, Doria A, Libby P, Blumberg RS, Kahn BB, Hotamisligil GS, Shi GP. Genetic deficiency and pharmacological stabilization of mast cells reduce diet-induced obesity and diabetes in mice. Nat Med. 2009;15:940-945.
48. Miwa K, Nakashima H, Aoki M, Miyake T, Kawasaki T, Iwai M, Oishi M, Kataoka K, Ohgi S, Ogihara T, Kaneda Y, Morishita R. Inhibition of ets, an essential transcription factor for angiogenesis, to prevent the development of abdominal aortic aneurysm in a rat model. Gene Ther. 2005;12:1109-1118. (Pubitemid 41030616)
49. Miyake T, Aoki M, Nakashima H, Kawasaki T, Oishi M, Kataoka K, Tanemoto K, Ogihara T, Kaneda Y, Morishita R. Prevention of abdominal aortic aneurysms by simultaneous inhibition of NFkappaB and ets using chimeric decoy oligonucleotides in a rabbit model. Gene Ther. 2006;13:695-704.
50. Daugherty A, Manning MW, Cassis LA. Angiotensin II promotes atherosclerotic lesions and aneurysms in apolipoprotein E-deficient mice. J Clin Invest. 2000;105:1605-1612. (Pubitemid 30390311)
51. Wang YX, Martin-McNulty B, Freay AD, Sukovich DA, Halks-Miller M, Li WW, Vergona R, Sullivan ME, Morser J, Dole WP, Deng GG. Angiotensin II increases urokinase-type plasminogen activator expression and induces aneurysm in the abdominal aorta of apolipoprotein E-deficient mice. Am J Pathol. 2001;159:1455-1464. (Pubitemid 32947975)
52. Schieffer B, Schieffer E, Hilfiker-Kleiner D, Hilfiker A, Kovanen PT, Kaartinen M, Nussberger J, Harringer W, Drexler H. Expression of angiotensin II and interleukin 6 in human coronary atherosclerotic plaques: potential implications for inflammation and plaque instability. Circulation. 2000;101:1372-1378. (Pubitemid 30169857)
53. Miyazaki M, Takai S, Jin D, Muramatsu M. Pathological roles of angiotensin II produced by mast cell chymase and the effects of chymase inhibition in animal models. Pharmacol Ther. 2006;112:668-676. (Pubitemid 44573489)
54. Owen CA, Campbell EJ. Angiotensin II generation at the cell surface of activated neutrophils: novel cathepsin G-mediated catalytic activity that is resistant to inhibition. J Immunol. 1998;160:1436-1443. (Pubitemid 28093445)
55. Veerappan A, Reid AC, Estephan R, O'Connor N, Thadani-Mulero M, Salazar-Rodriguez M, Levi R, Silver RB. Mast cell renin and a local renin-angiotensin system in the airway: role in bronchoconstriction. Proc Natl Acad Sci USA. 2008;105:1315-1320. (Pubitemid 351397050)
56. Liao S, Miralles M, Kelley BJ, Curci JA, Borhani M, Thompson RW. Suppression of experimental abdominal aortic aneurysms in the rat by treatment with angiotensin-converting enzyme inhibitors. J Vasc Surg. 2001;33:1057-1064. (Pubitemid 33586351)
57. Nishimoto M, Takai S, Fukumoto H, Tsunemi K, Yuda A, Sawada Y, Yamada M, Jin D, Sakaguchi M, Nishimoto Y, Sasaki S, Miyazaki M. Increased local angiotensin II formation in aneurysmal aorta. Life Sci. 2002;71:2195-2205.
58. Cassis LA, Rateri DL, Lu H, Daugherty A. Bone marrow transplantation reveals that recipient AT1a receptors are required to initiate angiotensin II-induced atherosclerosis and aneurysms. Arterioscler Thromb Vasc Biol. 2007;27:380-386. (Pubitemid 46143055)
59. Hackam DG, Thiruchelvam D, Redelmeier DA. Angiotensin-converting enzyme inhibitors and aortic rupture: a population-based case-control study. Lancet. 2006;368:659-665. (Pubitemid 44226485)
60. Sweeting MJ, Thompson SG, Brown LC, Greenhalgh RM, Powell JT. Use of angiotensin converting enzyme inhibitors is associated with increased growth rate of abdominal aortic aneurysms. J Vasc Surg. 2010;52:1-4.
61. Imig JD. ACE inhibition and bradykinin-mediated renal vascular responses: EDHF involvement. Hypertension. 2004;43:533-535. (Pubitemid 38282423)
62. Merino VF, Todiras M, Mori MA, Sales VM, Fonseca RG, Saul V, Tenner K, Bader M, Pesquero JB. Predisposition to atherosclerosis and aortic aneurysms in mice deficient in kinin B1 receptor and apolipoprotein E. J Mol Med. 2009;87:953-963.
63. Kaschina E, Stoll M, Sommerfeld M, Steckelings UM, Kreutz R, Unger T. Genetic kininogen deficiency contributes to aortic aneurysm formation but not to atherosclerosis. Physiol Genomics. 2004;19:41-49. (Pubitemid 40039912)
64. Arribas SM, Hinek A, Gonzalez MC. Elastic fibres and vascular structure in hypertension. Pharmacol Ther. 2006;111:771-791. (Pubitemid 44118433)
65. Michel JB. Anoikis in the cardiovascular system: known and unknown extracellular mediators. Arterioscler Thromb Vasc Biol. 2003;23: 2146-2154.
66. Leskinen MJ, Heikkila HM, Speer MY, Hakala JK, Laine M, Kovanen PT, Lindstedt KA. Mast cell chymase induces smooth muscle cell apoptosis by disrupting NF-kappaB-mediated survival signaling. Exp Cell Res. 2006;312:1289-1298.
67. Chamberlain CM, Ang LS, Boivin WA, Cooper DM, Williams SJ, Zhao H, Hendel A, Folkesson M, Swedenborg J, Allard MF, McManus BM, Granville DJ. Perforin-independent extracellular granzyme B activity contributes to abdominal aortic aneurysm. Am J Pathol. 2010;176: 1038-1049.
68. Pardo J, Wallich R, Ebnet K, Iden S, Zentgraf H, Martin P, Ekiciler A, Prins A, Mullbacher A, Huber M, Simon MM. Granzyme B is expressed in mouse mast cells in vivo and in vitro and causes delayed cell death independent of perforin. Cell Death Differ. 2007;14:1768-1779. (Pubitemid 47423644)
69. Wang Y, Shiota N, Leskinen MJ, Lindstedt KA, Kovanen PT. Mast cell chymase inhibits smooth muscle cell growth and collagen expression in vitro: transforming growth factor-beta1-dependent and -independent effects. Arterioscler Thromb Vasc Biol. 2001;21:1928-1933. (Pubitemid 34219743)
70. Mortality results for randomised controlled trial of early elective surgery or ultrasonographic surveillance for small abdominal aortic aneurysms. The UK Small Aneurysm Trial Participants. Lancet. 1998;352: 1649-1655.
71. Lederle FA, Wilson SE, Johnson GR, Reinke DB, Littooy FN, Acher CW, Ballard DJ, Messina LM, Gordon IL, Chute EP, Krupski WC, Busuttil SJ, Barone GW, Sparks S, Graham LM, Rapp JH, Makaroun MS, Moneta GL, Cambria RA, Makhoul RG, Eton D, Ansel HJ, Freischlag JA, Bandyk D. Immediate repair compared with surveillance of small abdominal aortic aneurysms. N Engl J Med. 2002;346:1437-1444. (Pubitemid 34755711)
72. Baxter BT, Terrin MC, Dalman RL. Medical management of small abdominal aortic aneurysms. Circulation. 2008;117:1883-1889. (Pubitemid 351507477)
73. Cowden JM, Riley JP, Ma JY, Thurmond RL, Dunford PJ. Histamine H4 receptor antagonism diminishes existing airway inflammation and dysfunction via modulation of Th2 cytokines. Respir Res. 2010;11:86.
74. Thurmond RL, Gelfand EW, Dunford PJ. The role of histamine H1 and H4 receptors in allergic inflammation: the search for new antihistamines. Nat Rev Drug Discov. 2008;7:41-53.
75. Boyce JA. Mast cells and eicosanoid mediators: a system of reciprocal paracrine and autocrine regulation. Immunol Rev. 2007;217:168-185. (Pubitemid 46718145)
76. Di Gennaro A, Wagsater D, Mayranpaa M, Gabrielsen A, Swedenborg J, Hamsten A, Samuelsson B, Eriksson P, Haeggstrom J. Increased expression of leukotriene C4 synthase and predominant formation of cysteinyl-leukotrienes in human abdominal aortic aneurysm. Proc Natl Acad Sci USA. 2010;107:21093-21097.