Local tenomodulin absence, angiogenesis, and matrix metalloproteinase activation are associated with the rupture of the chordae tendineae cordis

Circulation

Volumn 118, Issue 17, 2008, Pages 1737-1747

  Kimura, Naritaka ^a   Shukunami, Chisa ^b   Hakuno, Daihiko ^a   Yoshioka, Masatoyo ^a   Miura, Shigenori ^b   Docheva, Denitsa ^c   Kimura, Tokuhiro ^a   Okada, Yasunori ^a   Matsumura, Goki ^d   Shin'oka, Toshiharu ^d   Yozu, Ryohei ^a   Kobayashi, Junjiro ^e   Ishibashi Ueda, Hatsue ^e   Hiraki, Yuji ^b   Fukuda, Keiichi ^a,f  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^d TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

^e NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

^f NONE   (Japan)

Author keywords

Angiogenesis; Chordae tendineae cordis; Metalloproteinases; Tenomodulin; Valves

Indexed keywords

ANGIOGENESIS INHIBITOR; ELASTIN; MATRIX METALLOPROTEINASE; SMALL INTERFERING RNA; TENOMODULIN; UNCLASSIFIED DRUG; VASCULOTROPIN; MEMBRANE PROTEIN; TNMD PROTEIN, MOUSE;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOPSY; CELL CULTURE; CELL INFILTRATION; CELL MOTILITY; CHORDA TENDINEA CORDIS RUPTURE; CHORDA TENDINEA RUPTURE; CONTROLLED STUDY; DOG; ENDOTHELIUM CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INFLAMMATORY CELL; LEYDIG CELL; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RODENT; SUBENDOTHELIUM; TRICUSPID VALVE DISEASE; AGED; ANIMAL; CHORDA TENDINEA; COMPARATIVE STUDY; ENZYME ACTIVATION; ENZYMOLOGY; FEMALE; GENETICS; HUMAN; INJURY; INSTITUTE FOR CANCER RESEARCH MOUSE; MALE; METABOLISM; MIDDLE AGED; NEOVASCULARIZATION (PATHOLOGY); PATHOPHYSIOLOGY; PHYSIOLOGY; RABBIT; RUPTURE; SWINE; VALVULAR HEART DISEASE; VASCULAR ENDOTHELIUM;

AGED; AGED, 80 AND OVER; ANIMALS; CELLS, CULTURED; CHORDAE TENDINEAE; DOGS; ELASTIN; ENDOTHELIUM, VASCULAR; ENZYME ACTIVATION; FEMALE; HEART VALVE DISEASES; HUMANS; MALE; MATRIX METALLOPROTEINASES; MEMBRANE PROTEINS; MICE; MICE, INBRED ICR; MIDDLE AGED; NEOVASCULARIZATION, PATHOLOGIC; RABBITS; RUPTURE; SWINE;

EID: 55449091806     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.108.780031     Document Type: Article

References (37)

1. Millington-Sanders C, Meir A, Lawrence L, Stolinski C. Structure of chordae tenidineae in the left ventricle of the human heart. J Anat. 1998;192:573-581.
2. Soini Y, Salo T, Satta J. Angiogenesis is involved in the pathogenesis of nonrheumatic aortic valve stenosis. Hum Pathol. 2003;34:756-763.
3. Yamauchi R, Tanaka M, Kume N, Minami M, Kawamoto T, Togi K, Shimaoka T, Takahashi S, Yamaguchi J, Nishina T, Kitaichi M, Komeda M, Manabe T, Yonehara S, Kita T. Upregulation of SR-PSOX/CXCL16 and recruitment of CD8+ T cells in cardiac valves during inflammatory valvular heart disease. Arterioscler Thromb Vasc Biol. 2004;24:282-287.
4. Mohler ER III, Gannon F, Reynolds C, Zimmerman R, Keane MG, Kaplan FS. Bone formation and inflammation in cardiac valves. Circulation. 2001;103:1522-1528.
5. Hiraki Y, Inoue H, Iyama K, Kamizono A, Ochiai M, Shukunami C, Iijima S, Suzuki F, Kondo J. Identification of chondromodulin I as a novel endothelial cell growth inhibitor: purification and its localization in the avascular zone of epiphyseal cartilage. J Biol Chem. 1997;272:32419-32426.
6. Hiraki Y, Kono T, Sato M, Shukunami C, Kondo J. Inhibition of DNA synthesis and tube morphogenesis of cultured vascular endothelial cells by chondromodulin-I. FEBS Lett. 1997;415:321-324.
7. Nakamichi Y, Shukunami C, Yamada T, Aihara K, Kawano H, Sato T, Nishizaki Y, Yamamoto Y, Shindo M, Yoshimura K, Nakamura T, Takahashi N, Kawaguchi H, Hiraki Y, Kato S. Chondromodulin I is a bone remodeling factor. Mol Cell Biol. 2003;23:636-644.
8. Yamana K, Wada H, Takahashi Y, Sato H, Kasahara Y, Kiyoki M. Molecular cloning and characterization of CHM1L, a novel membrane molecule similar to chondromodulin-I. Biochem Biophys Res Commun. 2001;280:1101-1106.
9. Yoshioka M, Yuasa S, Matsumura K, Kimura K, Shiomi T, Kimura N, Shukunami C, Okada Y, Mukai M, Shin H, Yozu R, Sata M, Ogawa S, Hiraki Y, Fukuda K. Chondromodulin-I maintains cardiac valvular function by preventing angiogenesis. Nat Med. 2006;12:1151-1159.
10. Chimal-Monroy J, Rodriguez-Leon J, Montera JA, Ganan Y, Macias D, Merino R, Hurle JM. Analysis of the molecular cascade responsible for mesodermal limb chondrogenesis: Sox genes and BMP signaling. Dev Biol. 2003;257:292-301.
11. Lincoln J, Alfieri CM, Yutzey KE. Development of heart valve leaflets and supporting apparatus in chicken and mouse embryos. Dev Dyn. 2004;230:239-250.
12. Chiquet M, Fambrough DM. Chick myotendinous antigen: a monoclonal antibody as a marker for tendon and muscle morphogenesis. J Cell Biol. 1984;98:1926-1936.
13. Schweitzer R, Chyung JH, Murtaugh LC, Brent AE, Rosen V, Olson EN, Lassar A, Tabin CJ. Analysis of the tendon cell fate using Scleraxis, a specific marker for tendons and ligaments. Development. 2001;128:3855-3866.
14. Lincoln J, Alfieri CM, Yutzey KE. BMP and FGF regulatory pathways control cell lineage diversification of heart valve precursor cells. Dev Biol. 2006;292:292-302.
15. Zhao B, Etter L, Hinton RB Jr, Benson DW. BMP and FGF regulatory pathways in semilunar valve precursor cells. Dev Dyn. 2007;236:971-980.
16. Shukunami C, Oshima Y, Hiraki Y. Molecular cloning of tenomodulin, a novel chondromodulin-I related gene. Biochem Biophys Res Commun. 2001;280:1323-1327.
17. Oshima Y, Shukunami C, Honda J, Nishida K, Tashiro F, Miyazaki J, Hiraki Y, Tano Y. Expression and localization of tenomodulin, a transmembrane type chondromodulin-I-related angiogenesis inhibitor, in mouse eyes. Invest Ophthalmol Vis Sci. 2003;44:1814-1823.
18. Shukunami C, Oshima Y, Hiraki Y. Chondromodulin-I and tenomodulin: a new class of tissue-specific angiogenesis inhibitors found in hypovascular connective tissues. Biochem Biophys Res Commun. 2005;333:299-307.
19. Shukunami C, Takimoto A, Oro M, Hiraki Y. Scleraxis positively regulates the expression of tenomodulin, a differentiation marker of tenocytes. Dev Biol. 2006;298:234-247.
20. Hiraki Y, Shukunami C. Angiogenesis inhibitors localized in hypovascular mesenchymal tissues: chondromodulin-I and tenomodulin. Connect Tissue Res. 2005;46:3-11.
21. Docheva D, Hunziker EB, Fassler R, Brandau O. Tenomodulin is necessary for tenocyte proliferation and tendon maturation. Mol Cell Biol. 2005;25:699-705.
22. Oshima Y, Sato K, Tashiro F, Miyazaki J, Nishida K, Hiraki Y, Tano Y, Shukunami C. Anti-angiogenic action of the C-terminal domain of tenomodulin that shares homology with chondromodulin-I. J Cell Sci. 2004;117:2731-2744.
23. Funaki H, Sawaguchi S, Yaoeda K, Koyama Y, Yaoita E, Funaki S, Shirakashi M, Oshima Y, Shukunami C, Hiraki Y, Abe H, Yamamoto T. Expression and localization of angiogenic inhibitory factor, chondromodulin-I, in adult rat eye. Invest Ophthalmol Vis Sci. 2001;42:1193-1200.
24. Fujimoto N, Iwata K. Use of EIA to measure MMPs and TIMPs. Methods Mol Biol. 2001;151:347-358.
25. Zacks S, Rosenthal A, Granton B, Havenith M, Opas M, Gotlieb AI. Characterization of Cobblestone mitral valve interstitial cells. Arch Pathol Lab Med. 1991;115:774-779.
26. Pufe T, Petersen W, Kurz B, Tsokos M, Tillmann B, Mentlein R. Mechanical factors influence the expression of endostatin - an inhibitor of angiogenesis - in tendons. J Orthop Res. 2003;21:610-616.
27. Chalajour F, Treede H, Ebrahimnejad A, Lauke H, Reichenspurner H, Ergun S. Angiogenic activation of valvular endothelial cells in aortic valve stenosis. Exp Cell Res. 2004;298:455-464.
28. Freed LA, Acierno JS Jr, Dai D, Leyne M, Marshall JE, Nesta F, Levine RA, Slaugenhaupt SA. A locus for autosomal dominant mitral valve prolapse on chromosome 11p15.4. Am J Hum Genet. 2003;72:1551-1559.
29. Sedransk KL, Grande-Allen KJ, Vesely I. Failure mechanics of mitral valve chordae tendineae. J Heart Valve Dis. 2002;11:644-650.
30. Rodriguez F, Langer F, Hairington KB, Tibayan FA, Zasio MK, Cheng A, Liang D, Daughters GT, Covell JW, Criscione JC, Ingels NB, Miller DC. Importance of mitral valve second-order chordae for left ventricular geometry, wall thickening mechanics, and global systolic function. Circulation. 2004;110:11115-11122.
31. Lin TH, Su HM, Voon WC, Lai HM, Yen HW, Lai WT, Sheu SH. Association between hypertension and primary mitral chordae tendinae rupture. Am J Hypertens. 2006;19:75-79.
32. Jozsa LG, Kannus P. Human Tendons: Anatomy, Physiology, and Pathology. Champaign, Ill: Human Kinetics; 1997.
33. Movin T, Gad A, Reinholt FP, Rolf C. Tendon pathology in long-standing achillodynia: biopsy findings in 40 patients. Acta Orthop Scand. 1997;68:170-175.
34. Kannus P, Jozsa L. Histopathological changes preceding spontaneous rupture of a tendon: controlled study of 891 patients. J Bone Joint Surg Am. 1991;73:1507-1525.
35. Pufe T, Petersen W, Tillmann B, Mentlein R. The angiogenic peptide vascular endothelial growth factor is expressed in foetal and ruptured tendons. Virchows Arch. 2001;439:579-585.
36. Pufe T, Petersen WJ, Mentlein R, Tillmann BN. The role of vasculature and angiogenesis for the pathogenesis of degenerative tendons disease. Scand J Med Sci Sports. 2005;15:211-222.
37. Tallon C, Maffulli N, Ewen SW. Ruptured Achilles tendons are significantly more degenerated than tendinopathic tendons. Med Sci Sports Exerc. 2001;33:1983-1990.