Cadherin-11 expression patterns in heart valves associate with key functions during embryonic cushion formation, valve maturation and calcification

Cells Tissues Organs

Volumn 198, Issue 4, 2014, Pages 300-310

  Zhou, Jingjing ^a   Bowen, Caitlin ^a   Lu, Gloria ^a   Knapp Iii, Calvin ^a   Recknagel, Andrew ^a   Norris, Russell A ^b   Butcher, Jonathan T ^a  

^a School of Operations Research and Industrial Engineering   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Cadherin; Calcific aortic valve disease; Heart valve development

Indexed keywords

APOLIPOPROTEIN E; CADHERIN; CADHERIN 11; CD31 ANTIGEN; UNCLASSIFIED DRUG; MESSENGER RNA; OSTEOBLAST CADHERIN;

ANIMAL CELL; AORTA VALVE; AORTA VALVE DISEASE; ARTICLE; CALCIFICATION; CELL ACTIVATION; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO DEVELOPMENT; EMBRYONIC STRUCTURES; ENDOCARDIAL CUSHION; HEART DEVELOPMENT; HEART VALVE; HIS BUNDLE; HUMAN; HUMAN CELL; INTERSTITIUM; MESENCHYME CELL; MITRAL VALVE; MOUSE; MYOFIBROBLAST; NONHUMAN; OSTEOBLAST; OUTFLOW TRACT; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY SPECIFICITY; CELL MIGRATION; CHICK EMBRYO; EMBRYO; ENDOTHELIUM CELL; LIMB BUD; SOMITE; VALVULAR HEART DISEASE; WILD TYPE; ANIMAL; AORTA VALVE STENOSIS; BIOSYNTHESIS; C57BL MOUSE; CALCINOSIS; CELL MOTION; CYTOLOGY; EMBRYOLOGY; GENE EXPRESSION; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

MURINAE; MUS;

ANIMALS; AORTIC VALVE; AORTIC VALVE STENOSIS; CADHERINS; CALCINOSIS; CELL DIFFERENTIATION; CELL MOVEMENT; CHICK EMBRYO; GENE EXPRESSION; HEART VALVES; HUMANS; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 84896716937     PISSN: 14226405     EISSN: 14226421     Source Type: Journal    
DOI: 10.1159/000356762     Document Type: Article

References (58)

1. Butcher, J.T., R.R. Markwald (2007) Valvulogenesis: the moving target. Philos Trans R Soc Lond B Biol Sci 362: 1489-1503. (Pubitemid 47195036)
2. Butcher, J.T., R.M. Nerem (2004) Porcine aortic valve interstitial cells in three-dimensional culture: comparison of phenotype with aortic smooth muscle cells. J Heart Valve Dis 13: 478-485, discussion 485-476.
3. Butcher, J.T., S. Tressel, T. Johnson, D. Turner, G. Sorescu, H. Jo, R.M. Nerem (2006) Transcriptional profiles of valvular and vascular endothelial cells reveal phenotypic differences. Arterioscler Thromb Vasc Biol 26: 69-77. (Pubitemid 43732230)
4. Camenisch, T.D., A.P. Spicer, T. Brehm-Gibson, J. Biesterfeldt, M.L. Augustine, A. Calabro Jr, S. Kubalak, S.E. Klewer, J.A. McDonald (2000) Disruption of hyaluronan synthase-2 abrogates normal cardiac morphogenesis and hyaluronan-mediated transformation of epithelium to mesenchyme. J Clin Invest 106: 349-360. (Pubitemid 30655635)
5. Chakraborty, S., J. Cheek, B. Sakthivel, B.J. Aronow, K.E. Yutzey (2008) Shared gene expression profiles in developing heart valves and osteoblast progenitor cells. Physiol Genomics 35: 75-85.
6. Chang, S.K., Z. Gu, M.B. Brenner (2010) Fibroblast-like synoviocytes in inflammatory arthritis pathology: the emerging role of cadherin-11. Immunol Rev 233: 256-266.
7. Chang, S.K., E.H. Noss, M. Chen, Z. Gu, K. Townsend, R. Grenha, L. Leon, S.Y. Lee, D.M. Lee, M.B. Brenner (2011) Cadherin-11 regulates fibroblast inflammation. Proc Natl Acad Sci USA 108: 8402-8407.
8. Chen, J.H., C.Y. Yip, E.D. Sone, C.A. Simmons (2009) Identification and characterization of aortic valve mesenchymal progenitor cells with robust osteogenic calcification potential. Am J Pathol 174: 1109-1119.
9. de Lange, F.J., A.F. Moorman, R.H. Anderson, J. Manner, A.T. Soufan, C. de Gier-de Vries, M.D. Schneider, S. Webb, M.J. van den Hoff, V.M. Christoffels (2004) Lineage and morphogenetic analysis of the cardiac valves. Circ Res 95: 645-654. (Pubitemid 39274380)
10. Di Benedetto, A., M. Watkins, S. Grimston, V. Salazar, C. Donsante, G. Mbalaviele, G.L. Radice, R. Civitelli (2010) N-cadherin and cadherin 11 modulate postnatal bone growth and osteoblast differentiation by distinct mechanisms. J Cell Sci 123: 2640-2648.
11. Feltes, C.M., A. Kudo, O. Blaschuk, S.W. Byers (2002) An alternatively spliced cadherin-11 enhances human breast cancer cell invasion. Cancer Res 62: 6688-6697. (Pubitemid 35364139)
12. Friedlander, D.R., R.M. Mege, B.A. Cunningham, G.M. Edelman (1989) Cell sorting-out is modulated by both the specificity and amount of different cell adhesion molecules (CAMs) expressed on cell surfaces. Proc Natl Acad Sci USA 86: 7043-7047. (Pubitemid 19240863)
13. Guerraty, M.A., G.R. Grant, J.W. Karanian, O.A. Chiesa, W.F. Pritchard, P.F. Davies (2010) Hypercholesterolemia induces side-specific phenotypic changes and peroxisome proliferator-activated receptor-γ pathway activation in swine aortic valve endothelium. Arterioscler Thromb Vasc Biol 30: 225-231.
14. Henderson, D.J., A.J. Copp (1998) Versican expression is associated with chamber specification, septation, and valvulogenesis in the developing mouse heart. Circ Res 83: 523-532. (Pubitemid 28411054)
15. Hjortnaes, J., J. Butcher, J.L. Figueiredo, M. Riccio, R.H. Kohler, K.M. Kozloff, R. Weissleder, E. Aikawa (2010) Arterial and aortic valve calcification inversely correlates with osteoporotic bone remodelling: a role for inflammation. Eur Heart J 31: 1975-1984.
16. Horiuchi, K., N. Amizuka, S. Takeshita, H. Takamatsu, M. Katsuura, H. Ozawa, Y. Toyama, L.F. Bonewald, A. Kudo (1999) Identification and characterization of a novel protein, periostin, with restricted expression to periosteum and periodontal ligament and increased expression by transforming growth factor β. J Bone Miner Res 14: 1239-1249. (Pubitemid 29314070)
17. Hutcheson, J.D., J. Chen, M.K. Sewell-Loftin, L.M. Ryzhova, C.I. Fisher, Y.R. Su, W.D. Merryman (2013) Cadherin-11 regulates cell-cell tension necessary for calcific nodule formation by valvular myofibroblasts. Arterioscler Thromb Vasc Biol 33: 114-120.
18. Kaden, J.J., C.E. Dempfle, R. Grobholz, C.S. Fischer, D.C. Vocke, R. Kilic, A. Sarikoc, R. Pinol, S. Hagl, S. Lang, M. Brueckmann, M. Borggrefe (2005) Inflammatory regulation of extracellular matrix remodeling in calcific aortic valve stenosis. Cardiovasc Pathol 14: 80-87. (Pubitemid 40381303)
19. Kashima, T., J. Kawaguchi, S. Takeshita, M. Kuroda, M. Takanashi, H. Horiuchi, T. Imamura, Y. Ishikawa, T. Ishida, S. Mori, R. Machinami, A. Kudo (1999) Anomalous cadherin expression in osteosarcoma: possible relationships to metastasis and morphogenesis. Am J Pathol 155: 1549-1555.
20. Kawaguchi, J., Y. Azuma, K. Hoshi, I. Kii, S. Takeshita, T. Ohta, H. Ozawa, M. Takeichi, O. Chisaka, A. Kudo (2001) Targeted disruption of cadherin-11 leads to a reduction in bone density in calvaria and long bone metaphyses. J Bone Miner Res 16: 1265-1271. (Pubitemid 32574655)
21. Kern, C.B., A. Wessels, J. McGarity, L.J. Dixon, E. Alston, W.S. Argraves, D. Geeting, C.M. Nelson, D.R. Menick, S.S. Apte (2010) Reduced versican cleavage due to Adamts9 haploinsufficiency is associated with cardiac and aortic anomalies. Matrix Biol 29: 304-316.
22. Kii, I., N. Amizuka, J. Shimomura, Y. Saga, A. Kudo (2004) Cell-cell interaction mediated by cadherin-11 directly regulates the differentiation of mesenchymal cells into the cells of the osteo-lineage and the chondro-lineage. J Bone Miner Res 19: 1840-1849. (Pubitemid 41103436)
23. Kimura, Y., H. Matsunami, T. Inoue, K. Shimamura, N. Uchida, T. Ueno, T. Miyazaki, M. Takeichi (1995) Cadherin-11 expressed in association with mesenchymal morphogenesis in the head, somite, and limb bud of early mouse embryos. Dev Biol 169: 347-358.
24. Kruithof, B.P.T., S.A. Krawitz, V. Gaussin (2007) Atrioventricular valve development during late embryonic and postnatal stages involves condensation and extracellular matrix remodeling. Dev Biol 302: 208-217. (Pubitemid 46099040)
25. Lee, C.H., B.M. Gumbiner (1995) Disruption of gastrulation movements in Xenopus by a dominant-negative mutant for C-cadherin. Dev Biol 171: 363-373.
26. Lee, D.M., H.P. Kiener, S.K. Agarwal, E.H. Noss, G.F.M. Watts, O. Chisaka, M. Takeichi, M.B. Brenner (2007) Cadherin-11 in synovial lining formation and pathology in arthritis. Science 315: 1006-1010. (Pubitemid 46281192)
27. Levine, E., C.H. Lee, C. Kintner, B.M. Gumbiner (1994) Selective disruption of E-cadherin function in early Xenopus embryos by a dominant negative mutant. Development 120: 901-909. (Pubitemid 24111554)
28. Liu, A.C., V.R. Joag, A.I. Gotlieb (2007) The emerging role of valve interstitial cell phenotypes in regulating heart valve pathobiology. Am J Pathol 171: 1407-1418. (Pubitemid 350158303)
29. Lloyd-Jones, D., R. Adams, M. Carnethon, G. De Simone, T.B. Ferguson, K. Flegal, E. Ford, K. Furie, A. Go, K. Greenlund, N. Haase, S. Hailpern, M. Ho, V. Howard, B. Kissela, S. Kittner, D. Lackland, L. Lisabeth, A. Marelli, M. Mc-Dermott, J. Meigs, D. Mozaffarian, G. Nichol, C. O'Donnell, V. Roger, W. Rosamond, R. Sacco, P. Sorlie, R. Stafford, J. Steinberger, T. Thom, S. Wasserthiel-Smoller, N. Wong, J. Wylie-Rosett, Y. Hong (2009) Heart disease and stroke statistics-2009 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 119: e21-e181.
30. Mahler, G.J., E.J. Farrar, J.T. Butcher (2013) Inflammatory cytokines promote mesenchymal transformation in embryonic and adult valve endothelial cells. Arterioscler Thromb Vasc Biol 33: 121-130.
31. Markwald, R.R., T.P. Fitzharris, F.J. Manasek (1977) Structural development of endocardial cushions. Am J Anat 148: 85-119. (Pubitemid 8034351)
32. Markwald, R.R., T.P. Fitzharris, W.N. Smith (1975) Sturctural analysis of endocardial cytodifferentiation. Dev Biol 42: 160-180.
33. Mjaatvedt, C.H., H. Yamamura, A.A. Capehart, D. Turner, R.R. Markwald (1998) The Cspg2 gene, disrupted in the hdf mutant, is required for right cardiac chamber and endocardial cushion formation. Dev Biol 202: 56-66. (Pubitemid 28467247)
34. Mohler, E.R. 3rd, M.K. Chawla, A.W. Chang, N. Vyavahare, R.J. Levy, L. Graham, F.H. Gannon (1999) Identification and characterization of calcifying valve cells from human and canine aortic valves. J Heart Valve Dis 8: 254-260. (Pubitemid 29274326)
35. Muller, A.M., C. Cronen, L.I. Kupferwasser, H. Oelert, K.M. Muller, C.J. Kirkpatrick (2000) Expression of endothelial cell adhesion molecules on heart valves: up-regulation in degeneration as well as acute endocarditis. J Pathol 191: 54-60. (Pubitemid 30235649)
36. Nagafuchi, A., Y. Shirayoshi, K. Okazaki, K. Yasuda, M. Takeichi (1987) Transformation of cell adhesion properties by exogenously introduced E-cadherin cDNA. Nature 329: 341-343. (Pubitemid 17125410)
37. Nakashima, Y., A.S. Plump, E.W. Raines, J.L. Bres low, R. Ross (1994) ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler Thromb 14: 133-140.
38. Niessen, C.M., D. Leckband, A.S. Yap (2011) Tissue organization by cadherin adhesion molecules: dynamic molecular and cellular mechanisms of morphogenetic regulation. Physiol Rev 91: 691-731.
39. Okazaki, M., S. Takeshita, S. Kawai, R. Kikuno, A. Tsujimura, A. Kudo, E. Amann (1994) Molecular cloning and characterization of OBcadherin, a new member of cadherin family expressed in osteoblasts. J biol Chem 269: 12092-12098. (Pubitemid 24196706)
40. Osman, L., M.H. Yacoub, N. Latif, M. Amrani, A.H. Chester (2006) Role of human valve interstitial cells in valve calcification and their response to atorvastatin. Circulation 114(1 suppl): I-547-I-552. (Pubitemid 44297206)
41. Paranya, G., S. Vineberg, E. Dvorin, S. Kaushal, S.J. Roth, E. Rabkin, F.J. Schoen, J. Bischoff (2001) Aortic valve endothelial cells undergo transforming growth factor-β-mediated and non-transforming growth factor-β-mediated transdifferentiation in vitro. Am J Pathol 159: 1335-1343. (Pubitemid 32947963)
42. Person, A.D., S.E. Klewer, R.B. Runyan (2005) Cell biology of cardiac cushion development. Int Rev Cytol 243: 287-335. (Pubitemid 41557302)
43. Pishvaian, M.J., C.M. Feltes, P. Thompson, M.J. Bussemakers, J.A. Schalken, S.W. Byers (1999) Cadherin-11 is expressed in invasive breast cancer cell lines. Cancer Res 59: 947-952. (Pubitemid 29086753)
44. Pittet, P., K. Lee, A.J. Kulik, J.J. Meister, B. Hinz (2008) Fibrogenic fibroblasts increase intercellular adhesion strength by reinforcing individual OB-cadherin bonds. J Cell Sci 121: 877-886. (Pubitemid 351578123)
45. Plump, A.S., J.D. Smith, T. Hayek, K. Aalto-Setala, A. Walsh, J.G. Verstuyft, E.M. Rubin, J.L. Breslow (1992) Severe hypercholesterolemia and atherosclerosis in apolipoprotein Edeficient mice created by homologous recombination in ES cells. Cell 71: 343-353.
46. Ramsdell, A.F., R.R. Markwald (1997) Induction of endocardial cushion tissue in the avian heart is regulated, in part, by TGFβ-3-mediated autocrine signaling. Dev Biol 188: 64-74. (Pubitemid 27360087)
47. Reddick, R.L., S.H. Zhang, N. Maeda (1994) Atherosclerosis in mice lacking apo E: evaluation of lesional development and progression. Arterioscler Thromb Vasc Biol 14: 141-147.
48. Richards, J., I. El-Hamamsy, S. Chen, Z. Sarang, P. Sarathchandra, M.H. Yacoub, A.H. Chester, J.T. Butcher (2013) Side-specific endothelial-dependent regulation of aortic valve calcification: interplay of hemodynamics and nitric oxide signaling. Am J Pathol 182: 1922-1931.
49. Schneider, D.J., M. Wu, T.T. Le, S.H. Cho, M.B. Brenner, M.R. Blackburn, S.K. Agarwal (2012) Cadherin-11 contributes to pulmonary fibrosis: potential role in TGF-β production and epithelial to mesenchymal transition. FASEB J 26: 503-512.
50. Shelton, E.L., K.E. Yutzey (2008) Twist1 function in endocardial cushion cell proliferation, migration, and differentiation during heart valve development. Dev Biol 317: 282-295.
51. Shibata, T., A. Ochiai, M. Gotoh, R. Machinami, S. Hirohashi (1996) Simultaneous expression of cadherin-11 in signet-ring cell carcinoma and stromal cells of diffuse-type gastric cancer. Cancer Lett 99: 147-153. (Pubitemid 26034628)
52. Takakura, N., T. Watanabe, S. Suenobu, Y. Yamada, T. Noda, Y. Ito, M. Satake, T. Suda (2000) A role for hematopoietic stem cells in promoting angiogenesis. Cell 102: 199-209.
53. Tomita, K., A. van Bokhoven, G.J. van Leenders, E.T. Ruijter, C.F. Jansen, M.J. Bussemakers, J.A. Schalken (2000) Cadherin switching in human prostate cancer progression. Cancer Res 60: 3650-3654. (Pubitemid 30482189)
54. Valencia, X., J.M. Higgins, H.P. Kiener, D.M. Lee, T.A. Podrebarac, C.C. Dascher, G.F. Watts, E. Mizoguchi, B. Simmons, D.D. Patel, A.K. Bhan, M.B. Brenner (2004) Cadherin-11 provides specific cellular adhesion between fibroblast-like synoviocytes. J Exp Med 200: 1673-1679. (Pubitemid 40094191)
55. Visconti, R.P., Y. Ebihara, A.C. LaRue, P.A. Fleming, T.C. McQuinn, M. Masuya, H. Minamiguchi, R.R. Markwald, M. Ogawa, C.J. Drake (2006) An in vivo analysis of hematopoietic stem cell potential: hematopoietic origin of cardiac valve interstitial cells. Circ Res 98: 690-696.
56. Yagi, T., M. Takeichi (2000) Cadherin superfamily genes: functions, genomic organization, and neurologic diversity. Genes Dev 14: 1169-1180. (Pubitemid 30327498)
57. Yip, C.Y., J.H. Chen, R. Zhao, C.A. Simmons (2009) Calcification by valve interstitial cells is regulated by the stiffness of the extracellular matrix. Arterioscler Thromb Vasc Biol 29: 936-942.
58. Zhang, Y., L. Cao, B.L. Yang, B.B. Yang (1998) The G3 domain of versican enhances cell proliferation via epidermial growth factor-like motifs. J Biol Chem 273: 21342-21351 (Pubitemid 28385428)