MMP-2 Regulates Erk1/2 phosphorylation and aortic dilatation in marfan syndrome

Circulation Research

Volumn 110, Issue 12, 2012, Pages

  Xiong, Wanfen ^a   Meisinger, Trevor ^a   Knispel, Rebecca ^a   Worth, Jennifer M ^a   Baxter, B Timothy ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Aortic aneurysms; Doxycycline; Losartan; Marfan syndrome; Matrix metalloproteinases; Transforming growth factor

Indexed keywords

DOXYCYCLINE; FIBRILLIN 1; GELATIN; GELATINASE A; LOSARTAN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA; ARTERY DIAMETER; ARTERY DILATATION; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DOWNSTREAM PROCESSING; LIFESPAN; MARFAN SYNDROME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; VASODILATATION; WESTERN BLOTTING; ZYMOGRAPHY;

ANIMALS; AORTA, THORACIC; DISEASE PROGRESSION; DOXYCYCLINE; DRUG THERAPY, COMBINATION; LOSARTAN; MAP KINASE SIGNALING SYSTEM; MARFAN SYNDROME; MATRIX METALLOPROTEINASE 2; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PHOSPHORYLATION; TRANSFORMING GROWTH FACTOR BETA; VASODILATION;

EID: 84862281710     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.112.268268     Document Type: Article

References (49)

1. Dietz HC, Cutting GR, Pyeritz RE, Maslen CL, Sakai LY, Corson GM, Puffenberger EG, Hamosh A, Nanthakumar EJ, Curristin SM. Marfan syndrome caused by a recurrent de novo missense mutation in the fibrillin gene. Nature. 1991;352:337-339. (Pubitemid 21912353)
2. Dietz HC, Pyeritz RE. Mutations in the human gene for fibrillin-1 (fbn1) in the marfan syndrome and related disorders. Hum Mol Genet. 1995;4: 1799-1809.
3. Murdoch JL, Walker BA, Halpern BL, Kuzma JW, McKusick VA. Life expectancy and causes of death in the Marfan syndrome. N Engl J Med. 1972;286:804-808.
4. Ramirez F, Dietz HC. Marfan syndrome: From molecular pathogenesis to clinical treatment. Curr Opin Genet Dev. 2007;17:252-258. (Pubitemid 46843550)
5. Prokop EK, Palmer RF, Wheat MW Jr. Hydrodynamic forces in dissecting aneurysms. In-vitro studies in a tygon model and in dog aortas. Circ Res. 1970;27:121-127.
6. Engelfriet P, Mulder B. Is there benefit of beta-blocking agents in the treatment of patients with the Marfan syndrome? Int J Cardiol. 2007; 114:300-302. (Pubitemid 44855913)
7. Gersony DR, McClaughlin MA, Jin Z, Gersony WM. The effect of beta-blocker therapy on clinical outcome in patients with Marfan's syndrome: A meta-analysis. Inte J Cardiol. 2007;114:303-308. (Pubitemid 44855907)
8. Selamet Tierney ES, Feingold B, Printz BF, Park SC, Graham D, Kleinman CS, Mahnke CB, Timchak DM, Neches WH, Gersony WM. Beta-blocker therapy does not alter the rate of aortic root dilation in pediatric patients with Marfan syndrome. J Pediatr. 2007;150:77-82. (Pubitemid 44940887)
9. Neptune ER, Frischmeyer PA, Arking DE, Myers L, Bunton TE, Gayraud B, Ramirez F, Sakai LY, Dietz HC. Dysregulation of TGF-beta activation contributes to pathogenesis in Marfan syndrome. Nat Genet. 2003;33:407-411. (Pubitemid 36278859)
10. Ng CM, Cheng A, Myers LA, Martinez-Murillo F, Jie C, Bedja D, Gabrielson KL, Hausladen JM, Mecham RP, Judge DP, Dietz HC. TGFbeta-dependent pathogenesis of mitral valve prolapse in a mouse model of Marfan syndrome. J Clin Invest. 2004;114:1586-1592. (Pubitemid 40385549)
11. Habashi JP, Judge DP, Holm TM, et al. Losartan, an AT1 antagonist, prevents aortic aneurysm in a mouse model of Marfan syndrome. Science. 2006;312:117-121.
12. Judge DP, Biery NJ, Keene DR, Geubtner J, Myers L, Huso DL, Sakai LY, Dietz HC. Evidence for a critical contribution of haploinsufficiency in the complex pathogenesis of Marfan syndrome. J Clin Invest. 2004; 114:172-181. (Pubitemid 39071622)
13. Yang HH, Kim JM, Chum E, van Breemen C, Chung AW. Effectiveness of combination of losartan potassium and doxycycline versus single-drug treatments in the secondary prevention of thoracic aortic aneurysm in marfan syndrome. J Thoracic Cardiovasc Surg. 2010;140:305.e302-312.e302.
14. Holm TM, Habashi JP, Doyle JJ, et al. Noncanonical TGFbeta signaling contributes to aortic aneurysm progression in Marfan syndrome mice. Science. 2011;332:358-361.
15. Ge G, Greenspan DS. BMP1 controls TGFbeta1 activation via cleavage of latent TGFbeta-binding protein. J Cell Biol. 2006;175:111-120. (Pubitemid 44537203)
16. Ikonomidis JS, Jones JA, Barbour JR, Stroud RE, Clark LL, Kaplan BS, Zeeshan A, Bavaria JE, Gorman JH III, Spinale FG, Gorman RC. Expression of matrix metalloproteinases and endogenous inhibitors within ascending aortic aneurysms of patients with Marfan syndrome. Circulation. 2006;114:I365-I370. (Pubitemid 44297177)
17. Wang M, Zhao D, Spinetti G, Zhang J, Jiang LQ, Pintus G, Monticone R, Lakatta EG. Matrix metalloproteinase 2 activation of transforming growth factor-beta1 (TGF-beta1) and TGF-beta1-type II receptor signaling within the aged arterial wall. Arterioscler Thromb Vasc Biol. 2006;26:1503-1509. (Pubitemid 44288975)
18. Xiong W, Knispel RA, Dietz HC, Ramirez F, Baxter BT. Doxycycline delays aneurysm rupture in a mouse model of marfan syndrome. J Vasc Surg. 2008;47:166-172; discussion 172.
19. 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. (Pubitemid 351591557)
20. Xiong W, Knispel R, MacTaggart J, Greiner TC, Weiss SJ, Baxter BT. Membrane-type 1 matrix metalloproteinase regulates macrophagedependent elastolytic activity and aneurysm formation in vivo. J Biol Chem. 2009;284:1765-1771.
21. Kadar A, Bihari-Varga M, Csonka E. The synthesis, transport and excretion of connective tissue macromolecules by smooth muscle cells. Connect Tissue Res. 1981;8:175-180. (Pubitemid 11052752)
22. Habashi JP, Doyle JJ, Holm TM, Aziz H, Schoenhoff F, Bedja D, Chen Y, Modiri AN, Judge DP, Dietz HC. Angiotensin II type 2 receptor signaling attenuates aortic aneurysm in mice through ERK antagonism. Science. 2011;332:361-365.
23. Kato T, Kure T, Chang JH, Gabison EE, Itoh T, Itohara S, Azar DT. Diminished corneal angiogenesis in gelatinase A-deficient mice. FEBS Lett. 2001;508:187-190. (Pubitemid 33079244)
24. Prall AK, Longo GM, Mayhan WG, Waltke EA, Fleckten B, Thompson RW, Baxter BT. Doxycycline in patients with abdominal aortic aneurysms and in mice: Comparison of serum levels and effect on aneurysm growth in mice. J Vasc Surg. 2002;35:923-929.
25. Xiong W, MacTaggart J, Knispel R, Worth J, Persidsky Y, Baxter BT. Blocking TNF-alpha attenuates aneurysm formation in a murine model. J Immunol. 2009;183:2741-2746.
26. Longo GM, Xiong W, Greiner TC, Zhao Y, Fiotti N, Baxter BT. Matrix metalloproteinases 2 and 9 work in concert to produce aortic aneurysms. J Clin Invest. 2002;110:625-632. (Pubitemid 34988786)
27. Nataatmadja M, West M, West J, Summers K, Walker P, Nagata M, Watanabe T. Abnormal extracellular matrix protein transport associated with increased apoptosis of vascular smooth muscle cells in marfan syndrome and bicuspid aortic valve thoracic aortic aneurysm. Circulation. 2003;108(Suppl 1):II329-II334. (Pubitemid 37099977)
28. Segura AM, Luna RE, Horiba K, Stetler-Stevenson WG, McAllister HA Jr, Willerson JT, Ferrans VJ. Immunohistochemistry of matrix metalloproteinases and their inhibitors in thoracic aortic aneurysms and aortic valves of patients with Marfan's syndrome. Circulation. 1998;98: II331-II337; discussion II337-II338. (Pubitemid 28512208)
29. Pereira L, Lee SY, Gayraud B, Andrikopoulos K, Shapiro SD, Bunton T, Biery NJ, Dietz HC, Sakai LY, Ramirez F. Pathogenetic sequence for aneurysm revealed in mice underexpressing fibrillin-1. Proc Natl Acad Sci USA. 1999;96:3819-3823. (Pubitemid 29168994)
30. Kleiner DE, Stetler-Stevenson WG. Quantitative zymography: Detection of picogram quantities of gelatinases. Anal Biochem. 1994;218:325-329. (Pubitemid 24141631)
31. Campistol JM, Inigo P, Jimenez W, Lario S, Clesca PH, Oppenheimer F, Rivera F. Losartan decreases plasma levels of TGF-beta1 in transplant patients with chronic allograft nephropathy. Kidney Int. 1999;56:714-719. (Pubitemid 29353172)
32. Schwill S, Kallenbach K, Beller CJ, Karck M. An alternative surgical approach for the combined treatment of pectus excavatum and acute aortic dissection type-A in Marfan syndrome. Interact Cardiovasc Thorac Surg. 2011;12:526-528.
33. Loeys BL, Schwarze U, Holm T, et al. Aneurysm syndromes caused by mutations in the TGF-beta receptor. N Engl J Med. 2006;355:788-798. (Pubitemid 44285584)
34. Akutsu K, Morisaki H, Takeshita S, Sakamoto S, Tamori Y, Yoshimuta T, Yokoyama N, Nonogi H, Ogino H, Morisaki T. Phenotypic heterogeneity of Marfan-like connective tissue disorders associated with mutations in the transforming growth factor-beta receptor genes. Circ J. 2007;71:1305-1309. (Pubitemid 47195351)
35. Nataatmadja M, West J, West M. Overexpression of transforming growth factor-beta is associated with increased hyaluronan content and impairment of repair in Marfan syndrome aortic aneurysm. Circulation. 2006;114:I371-I377. (Pubitemid 44297178)
36. Booms P, Ney A, Barthel F, Moroy G, Counsell D, Gille C, Guo G, Pregla R, Mundlos S, Alix AJ, Robinson PN. A fibrillin-1-fragment containing the elastin-binding-protein GxxPG consensus sequence upregulates matrix metalloproteinase-1: Biochemical and computational analysis. J Mol Cell Cardiol. 2006;40:234-246. (Pubitemid 43152380)
37. Booms P, Pregla R, Ney A, Barthel F, Reinhardt DP, Pletschacher A, Mundlos S, Robinson PN. RGF-containing fibrillin-1 fragments upregulate matrix metalloproteinase expression in cell culture: A potential factor in the pathogenesis of the Marfan syndrome. Hum Genet. 2005;116:51-61. (Pubitemid 40057916)
38. Kim HS, Shang T, Chen Z, Pflugfelder SC, Li DQ. TGF-beta1 stimulates production of gelatinase (MMP-9), collagenases (MMP-1,-13) and stromelysins (MMP-3,-10,-11) by human corneal epithelial cells. Exp Eye Res. 2004;79:263-274. (Pubitemid 39119415)
39. Page-McCaw A, Ewald AJ, Werb Z. Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol. 2007;8:221-233.
40. Park JM, Kim A, Oh JH, Chung AS. Methylseleninic acid inhibits PMA-stimulated pro-MMP-2 activation mediated by MT1-mmp expression and further tumor invasion through suppression of NF-kappaB activation. Carcinogenesis. 2007;28:837-847. (Pubitemid 46530375)
41. Vidal A, Sabatini M, Rolland-Valognes G, Renard P, Madelmont JC, Mounetou E. Synthesis and in vitro evaluation of targeted tetracycline derivatives: Effects on inhibition of matrix metalloproteinases. Bioorg Med Chem. 2007;15:2368-2374. (Pubitemid 46240914)
42. Wang Y, Morlandt AB, Xu X, Carnes DL Jr, Chen Z, Steffensen B. Tetracycline at subcytotoxic levels inhibits matrix metalloproteinase-2 and-9 but does not remove the smear layer. J Periodontol. 2005;76:1129-1139. (Pubitemid 41065403)
43. Liu J, Xiong W, Baca-Regen L, Nagase H, Baxter BT. Mechanism of inhibition of matrix metalloproteinase-2 expression by doxycycline in human aortic smooth muscle cells. J Vasc Surg. 2003;38:1376-1383. (Pubitemid 37517672)
44. Carmeli E, Kodesh E, Nemcovsky C. Tetracycline therapy for muscle atrophy due to immobilization. J Musculoskelet Neuronal Interact. 2009; 9:81-88.
45. Franklin IJ, Harley SL, Greenhalgh RM, Powell JT. Uptake of tetracycline by aortic aneurysm wall and its effect on inflammation and proteolysis. Br J Surg. 1999;86:771-775. (Pubitemid 29271942)
46. Dietz HC, Loeys B, Carta L, Ramirez F. Recent progress towards a molecular understanding of Marfan syndrome. Am J Med Genet. 2005; 139C:4-9. (Pubitemid 41739241)
47. Boileau C, Jondeau G, Mizuguchi T, Matsumoto N. Molecular genetics of Marfan syndrome. Curr Opin Cardiol. 2005;20:194-200. (Pubitemid 40704876)
48. Kaartinen V, Warburton D. Fibrillin controls TGF-beta activation. Nat Genet. 2003;33:331-332.
49. Yu Q, Stamenkovic I. Cell surface-localized matrix metalloproteinase-9 proteolytically activates tgf-beta and promotes tumor invasion and angiogenesis. Genes Develop. 2000;14:163-176. (Pubitemid 30070982)