Neutrophil-derived matrix metalloproteinase 9 triggers acute aortic dissection

Circulation

Volumn 126, Issue 25, 2012, Pages 3070-3080

  Kurihara, Tomohiro ^a   Shimizu Hirota, Ryoko ^a   Shimoda, Masayuki ^a   Adachi, Takeshi ^b   Shimizu, Hideyuki ^a   Weiss, Stephen J ^c   Itoh, Hiroshi ^a   Hori, Shingo ^a   Aikawa, Naoki ^a   Okada, Yasunori ^a  

^a KEIO UNIVERSITY   (Japan)

^b NATIONAL DEFENSE MEDICAL COLLEGE   (Japan)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

acute aortic dissection; angiotensin II; leukocytes; MMP9

Indexed keywords

ANGIOTENSIN II; DIFFERENTIATION ANTIGEN; ENZYME INHIBITOR; GELATINASE B;

ACUTE AORTIC DISSECTION; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA ANEURYSM; AORTA DISSECTION; AORTA INTIMA; ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; HUMAN; IMMUNOLOCALIZATION; MAJOR CLINICAL STUDY; MALE; MAMMARY ARTERY; MORBIDITY; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ACUTE DISEASE; AGED; ANEURYSM, DISSECTING; ANGIOTENSIN II; ANIMALS; AORTIC ANEURYSM; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MALE; MATRIX METALLOPROTEINASE 9; MICE; MIDDLE AGED; NEUTROPHIL INFILTRATION; NEUTROPHILS;

EID: 84871304112     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.112.097097     Document Type: Article

References (51)

1. Golledge J, Eagle KA. Acute aortic dissection. Lancet. 2008;372: 55-66.
2. Pretre R, Von Segesser LK. Aortic dissection. Lancet. 1997;349: 1461-1464.
3. Schlatmann TJ, Becker AE. Histologic changes in the normal aging aorta: implications for dissecting aortic aneurysm. Am J Cardiol. 1977;39: 13-20.
4. Carlson RG, Lillehei CW, Edwards JE. Cystic medial necrosis of the ascending aorta in relation to age and hypertension. Am J Cardiol. 1970;25:411-415.
5. Eldadah ZA, Brenn T, Furthmayr H, Dietz HC. Expression of a mutant human fibrillin allele upon a normal human or murine genetic background recapitulates a Marfan cellular phenotype. J Clin Invest. 1995;95: 874-880.
6. Maki JM, Rasanen J, Tikkanen H, Sormunen R, Makikallio K, Kivirikko KI, Soininen R. Inactivation of the lysyl oxidase gene Lox leads to aortic aneurysms, cardiovascular dysfunction, and perinatal death in mice. Circulation. 2002;106:2503-2509.
7. Kumar D, Trent MB, Boor PJ. Allylamine and beta-aminopropionitrile induced aortic medial necrosis: mechanisms of synergism. Toxicology. 1998;125:107-115.
8. Page RC, Benditt EP. Molecular diseases of connective and vascular tissues: 3. The aldehyde content of normal and lathyritic soluble collagen. Lab Invest. 1968;18:124-130.
9. 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: 2493-2503.
10. Newby AC. Metalloproteinases and vulnerable atherosclerotic plaques. Trends Cardiovasc Med. 2007;17:253-258.
11. Katsuda S, Okada Y, Imai K, Nakanishi I. Matrix metalloproteinase-9 (92-kd gelatinase/type IV collagenase equals gelatinase B) can degrade arterial elastin. Am J Pathol. 1994;145:1208-1218.
12. Gough PJ, Gomez IG, Wille PT, Raines EW. Macrophage expression of active MMP-9 induces acute plaque disruption in apoE-deficient mice. J Clin Invest. 2006;116:59-69.
13. Loftus IM, Naylor AR, Goodall S, Crowther M, Jones L, Bell PR, Thompson MM. Increased matrix metalloproteinase-9 activity in unstable carotid plaques: a potential role in acute plaque disruption. Stroke. 2000; 31:40-47.
14. Wilson WR, Anderton M, Schwalbe EC, Jones JL, Furness PN, Bell PR, Thompson MM. Matrix metalloproteinase-8 and-9 are increased at the site of abdominal aortic aneurysm rupture. Circulation. 2006;113: 438-445.
15. Nagashima H, Uto K, Sakomura Y, Aoka Y, Sakuta A, Aomi S, Hagiwara N, Kawana M, Kasanuki H. An angiotensin-converting enzyme inhibitor, not an angiotensin II type-1 receptor blocker, prevents beta-aminopropionitrile monofumarate-induced aortic dissection in rats. J Vasc Surg. 2002;36: 818-823.
16. Shimizu-Hirota R, Sasamura H, Kuroda M, Kobayashi E, Hayashi M, Saruta T. Extracellular matrix glycoprotein biglycan enhances vascular smooth muscle cell proliferation and migration. Circ Res. 2004;94: 1067-1074.
17. Hariya A, Takazawa K, Yamamoto T, Amano A. ONO-4817, a novel matrix metalloproteinase inhibitor, attenuates allograft vasculopathy in a rat cardiac transplant. J Heart Lung Transplant. 2004;23: 1163-1169.
18. Shirahane K, Yamaguchi K, Koga K, Watanabe M, Kuroki S, Tanaka M. Hepatic ischemia/reperfusion injury is prevented by a novel matrix metalloproteinase inhibitor, ONO-4817. Surgery. 2006;139:653-664.
19. Yamada A, Uegaki A, Nakamura T, Ogawa K. ONO-4817, an orally active matrix metalloproteinase inhibitor, prevents lipopolysaccharide-induced proteoglycan release from the joint cartilage in guinea pigs. Inflamm Res. 2000;49:144-146.
20. Nozawa H, Chiu C, Hanahan D. Infiltrating neutrophils mediate the initial angiogenic switch in a mouse model of multistage carcinogenesis. Proc Natl Acad Sci USA. 2006;103:12493-12498.
21. 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.
22. Abu Nabah YN, Losada M, Estelles R, Mateo T, Company C, Piqueras L, Lopez-Gines C, Sarau H, Cortijo J, Morcillo EJ, Jose PJ, Sanz MJ. CXCR2 blockade impairs angiotensin II-induced CC chemokine synthesis and mononuclear leukocyte infiltration. Arterioscler Thromb Vasc Biol. 2007;27:2370-2376.
23. Arndt PG, Young SK, Poch KR, Nick JA, Falk S, Schrier RW, Worthen GS. Systemic inhibition of the angiotensin-converting enzyme limits lipopolysaccharide-induced lung neutrophil recruitment through both bradykinin and angiotensin II-regulated pathways. J Immunol. 2006;177: 7233-7241.
24. Guo RW, Yang LX, Wang H, Liu B, Wang L. Angiotensin II induces matrix metalloproteinase-9 expression via a nuclear factor-kappaB-dependent pathway in vascular smooth muscle cells. Regul Pept. 2008; 147:37-44.
25. Szocs K, Lassegue B, Sorescu D, Hilenski LL, Valppu L, Couse TL, Wilcox JN, Quinn MT, Lambeth JD, Griendling KK. Upregulation of Nox-based NAD(P)H oxidases in restenosis after carotid injury. Arterioscler Thromb Vasc Biol. 2002;22:21-27.
26. Mauro A, Buscemi M, Gerbino A. Immunohistochemical and transcrip-tional expression of matrix metalloproteinases in full-term human umbilical cord and human umbilical vein endothelial cells. J Mol Histol. 2010;41:367-377.
27. Bruel A, Ortoft G, Oxlund H. Inhibition of cross-links in collagen is associated with reduced stiffness of the aorta in young rats. Atherosclerosis. 1998;140:135-145.
28. Schlatmann TJ, Becker AE. Pathogenesis of dissecting aneurysm of aorta: comparative histopathologic study of significance of medial changes. Am J Cardiol. 1977;39:21-26.
29. Gaetani P, Tartara F, Grazioli V, Tancioni F, Infuso L, Rodriguez y Baena R. Collagen cross-linkage, elastolytic and collagenolytic activities in cerebral aneurysms: a preliminary investigation. Life Sci. 1998;63: 285-292.
30. Tang PC, Coady MA, Lovoulos C, Dardik A, Aslan M, Elefteriades JA, Tellides G. Hyperplastic cellular remodeling of the media in ascending thoracic aortic aneurysms. Circulation. 2005;112:1098-1105.
31. Chung AW, Au Yeung K, Sandor GG, Judge DP, Dietz HC, van Breemen C. Loss of elastic fiber integrity and reduction of vascular smooth muscle contraction resulting from the upregulated activities of matrix metalloproteinase-2 and-9 in the thoracic aortic aneurysm in Marfan syndrome. Circ Res. 2007;101:512-522.
32. Chung AW, Yang HH, Radomski MW, van Breemen C. Long-term doxycycline is more effective than atenolol to prevent thoracic aortic aneurysm in Marfan syndrome through the inhibition of matrix metalloproteinase-2 and-9. Circ Res. 2008;102:e73-e85.
33. McMillan WD, Pearce WH. Increased plasma levels of metalloproteinase-9 are associated with abdominal aortic aneurysms. J Vasc Surg. 1999;29: 122-127; discussion 127-129.
34. Borregaard N, Sehested M, Nielsen BS, Sengelov H, Kjeldsen L. Biosynthesis of granule proteins in normal human bone marrow cells: gela-tinase is a marker of terminal neutrophil differentiation. Blood. 1995;85: 812-817.
35. Okada Y, Gonoji Y, Naka K, Tomita K, Nakanishi I, Iwata K, Yamashita K, Hayakawa T. Matrix metalloproteinase 9 (92-kDa gelatinase/type IV collagenase) from HT 1080 human fibrosarcoma cells: purification and activation of the precursor and enzymic properties. J Biol Chem. 1992; 267:21712-21719.
36. Parks WC, Wilson CL, Lopez-Boado YS. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat Rev Immunol. 2004;4:617-629.
37. Schonbeck U, Mach F, Libby P. Generation of biologically active IL-1 beta by matrix metalloproteinases: a novel caspase-1-independent pathway of IL-1 beta processing. J Immunol. 1998;161:3340-3346.
38. Van den Steen PE, Proost P, Wuyts A, Van Damme J, Opdenakker G. Neutrophil gelatinase B potentiates interleukin-8 tenfold by ami-noterminal processing, whereas it degrades CTAP-III, PF-4, and GRO-alpha and leaves RANTES and MCP-2 intact. Blood. 2000;96: 2673-2681.
39. Lanone S, Zheng T, Zhu Z, Liu W, Lee CG, Ma B, Chen Q, Homer RJ, Wang J, Rabach LA, Rabach ME, Shipley JM, Shapiro SD, Senior RM, Elias JA. Overlapping and enzyme-specific contributions of matrix metalloproteinases-9 and-12 in IL-13-induced inflammation and remodeling. J Clin Invest. 2002;110:463-474.
40. Lindeman JH, Abdul-Hussien H, van Bockel JH, Wolterbeek R, Kleemann R. Clinical trial of doxycycline for matrix metalloproteinase-9 inhibition in patients with an abdominal aneurysm: doxycycline selectively depletes aortic wall neutrophils and cytotoxic T cells. Circulation. 2009;119:2209-2216.
41. Albaiceta GM, Gutierrez-Fernandez A, Parra D, Astudillo A, Garcia-Prieto E, Taboada F, Fueyo A. Lack of matrix metalloproteinase-9 worsens ventilator-induced lung injury. Am J Physiol Lung Cell Mol Physiol. 2008;294:L535-L543.
42. Keck T, Balcom JH, Fernandez-del Castillo C, Antoniu BA, Warshaw AL. Matrix metalloproteinase-9 promotes neutrophil migration and alveolar capillary leakage in pancreatitis-associated lung injury in the rat. Gastroenterology. 2002;122:188-201.
43. Sabeh F, Shimizu-Hirota R, Weiss SJ. Protease-dependent versus-independent cancer cell invasion programs: three-dimensional amoeboid movement revisited. J Cell Biol. 2009;185:11-19.
44. Habashi JP, Judge DP, Holm TM, Cohn RD, Loeys BL, Cooper TK, Myers L, Klein EC, Liu G, Calvi C, Podowski M, Neptune ER, Halushka MK, Bedja D, Gabrielson K, Rifkin DB, Carta L, Ramirez F, Huso DL, Dietz HC. Losartan, an AT1 antagonist, prevents aortic aneurysm in a mouse model of Marfan syndrome. Science. 2006;312:117-121.
45. Yu Q, Stamenkovic I. Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev. 2000;14:163-176.
46. Saraff K, Babamusta F, Cassis LA, Daugherty A. Aortic dissection precedes formation of aneurysms and atherosclerosis in angiotensin II-infused, apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2003;23:1621-1626.
47. Brooke BS, Habashi JP, Judge DP, Patel N, Loeys B, Dietz HC, III. Angiotensin II blockade and aortic-root dilation in Marfan's syndrome. N Engl J Med. 2008;358:2787-2795.
48. El Bekay R, Alvarez M, Monteseirin J, Alba G, Chacon P, Vega A, Martin-Nieto J, Jimenez J, Pintado E, Bedoya FJ, Sobrino F. Oxidative stress is a critical mediator of the angiotensin II signal in human neu-trophils: involvement of mitogen-activated protein kinase, calcineurin, and the transcription factor NF-kappaB. Blood. 2003;102:662-671.
49. Weiss SJ, Peppin G, Ortiz X, Ragsdale C, Test ST. Oxidative autoacti-vation of latent collagenase by human neutrophils. Science. 1985;227: 747-749.
50. Eggebrecht H, Naber CK, Bruch C, Kroger K, von Birgelen C, Schmermund A, Wichert M, Bartel T, Mann K, Erbel R. Value of plasma fibrin D-dimers for detection of acute aortic dissection. J Am Coll Cardiol. 2004;44:804-809.
51. Weber T, Hogler S, Auer J, Berent R, Lassnig E, Kvas E, Eber B. D-dimer in acute aortic dissection. Chest. 2003;123:1375-1378.