Reciprocal interactions between mitral valve endothelial and interstitial cells reduce endothelial-to-mesenchymal transition and myofibroblastic activation

Journal of Molecular and Cellular Cardiology

Volumn 80, Issue , 2015, Pages 175-185

  Shapero, Kayle ^a,b   Wylie Sears, Jill ^a   Levine, Robert A ^c   Mayer, John E ^a   Bischoff, Joyce ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b Boston University   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Endothelial cells; Endothelial to mesenchymal transition; Mitral valve; Valve interstitial cells

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CHONDROMODULIN 1; COLLAGEN TYPE 1; GELATINASE A; PEPTIDES AND PROTEINS; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; BIOLOGICAL MARKER;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CELL INTERACTION; CELL TRANSFORMATION; CELLULAR SECRETION; COCULTURE; CONTROLLED STUDY; ENDOTHELIAL MESENCHYMAL TRANSITION; HEART MUSCLE CONTRACTILITY; IN VITRO STUDY; LEUKOCYTE ADHERENCE; MESENCHYME CELL; MITRAL VALVE; MITRAL VALVE ENDOTHELIUM CELL; MITRAL VALVE INTERSTITIAL CELL; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHEEP; WESTERN BLOTTING; ANIMAL; CELL COMMUNICATION; CELL CULTURE; CELL TRANSDIFFERENTIATION; CYTOLOGY; DRUG EFFECTS; ENDOTHELIUM CELL; IMMUNOPHENOTYPING; METABOLISM; PHENOTYPE;

ANIMALS; BIOMARKERS; CELL COMMUNICATION; CELL TRANSDIFFERENTIATION; CELLS, CULTURED; COCULTURE TECHNIQUES; ENDOTHELIAL CELLS; IMMUNOPHENOTYPING; MITRAL VALVE; MYOFIBROBLASTS; PHENOTYPE; SHEEP; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84923010640     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2015.01.006     Document Type: Article

References (56)

1. Grande-Allen KJ, Barber JE, Klatka KM, Houghtaling PL, Vesely I, Moravec CS, et al. Mitral valve stiffening in end-stage heart failure: evidence of an organic contribution to functional mitral regurgitation. J Thorac Cardiovasc Surg 2005;130:783-90.
2. Grande-Allen KJ, Borowski AG, Troughton RW, Houghtaling PL, Dipaola NR, Moravec CS, et al. Apparently normal mitral valves in patients with heart failure demonstrate biochemical and structural derangements: an extracellular matrix and echocardiographic study. J Am Coll Cardiol 2005;45:54-61.
3. Dal-Bianco JP, Aikawa E, Bischoff J, Guerrero JL, Handschumacher MD, Sullivan S, et al. Active adaptation of the tethered mitral valve: insights into a compensatory mechanism for functional mitral regurgitation. Circulation 2009;120: 334-42.
4. Aikawa E, Whittaker P, Farber M, Mendelson K, Padera RF, Aikawa M, et al. Human semilunar cardiac valve remodeling by activated cells from fetus to adult: implications for postnatal adaptation, pathology, and tissue engineering. Circulation 2006; 113:1344-52.
5. Liu AC, Joag VR, Gotlieb AI. The emerging role of valve interstitial cell phenotypes in regulating heart valve pathobiology. Am J Pathol 2007;171:1407-18.
6. Flanagan TC, Black A, O'Brien M, Smith TJ, Pandit AS. Reference models for mitral valve tissue engineering based on valve cell phenotype and extracellular matrix analysis. Cells Tissues Organs 2006;183:12-23.
7. Hinton RB, Yutzey KE. Heart valve structure and function in development and disease. Annu Rev Physiol 2011;73:29-46.
8. Bischoff J, Aikawa E. Progenitor cells confer plasticity to cardiac valve endothelium. J Cardiovasc Transl Res 2011;4:710-9.
9. Wylie-Sears J, Aikawa E, Levine RA, Yang JH, Bischoff J. Mitral valve endothelial cells with osteogenic differentiation potential. Arterioscler Thromb Vasc Biol 2011;31: 598-607.
10. Paranya G, Vineberg S, Dvorin E, Kaushal S, Roth SJ, Rabkin E, et al. Aortic valve endothelial cells undergo transforming growth factor-beta-mediated and nontransforming growth factor-beta-mediated transdifferentiation in vitro. Am J Pathol 2001;159:1335-43.
11. Paruchuri S, Yang JH, Aikawa E, Melero-Martin JM, Khan ZA, Loukogeorgakis S, et al. Human pulmonary valve progenitor cells exhibit endothelial/mesenchymal plasticity in response to vascular endothelial growth factor-A and transforming growth factor-beta2. Circ Res 2006;99:861-9.
12. Lincoln J, Yutzey KE. Molecular and developmental mechanisms of congenital heart valve disease. Birth Defects Res A Clin Mol Teratol 2011;91:526-34.
13. Yoshioka M, Yuasa S, Matsumura K, Kimura K, Shiomi T, Kimura N, et al. Chondromodulin-I maintains cardiac valvular function by preventing angiogenesis. Nat Med 2006;12:1151-9.
14. Rabkin-Aikawa E, Farber M, Aikawa M, Schoen FJ. Dynamic and reversible changes of interstitial cell phenotype during remodeling of cardiac valves. J Heart Valve Dis 2004;13:841-7.
15. Stephens EH, Timek TA, Daughters GT, Kuo JJ, Patton AM, Baggett LS, et al. Significant changes in mitral valve leaflet matrix composition and turnover with tachycardiainduced cardiomyopathy. Circulation 2009;120:S112-9.
16. Dvorin EL, Jacobson J, Roth SJ, Bischoff J. Human pulmonary valve endothelial cells express functional adhesion molecules for leukocytes. J Heart Valve Dis 2003;12: 617-24.
17. Jang GH, Park IS, Yang JH, Bischoff J, Lee YM. Differential functions of genes regulated by VEGF-NFATc1 signaling pathway in themigration of pulmonary valve endothelial cells. FEBS Lett 2010;584:141-6.
18. Balachandran K, Sucosky P, Yoganathan AP. Hemodynamics and mechanobiology of aortic valve inflammation and calcification. Int J Inflamm 2011;2011:263870.
19. Mahler GJ, Farrar EJ, Butcher JT. Inflammatory cytokines promote mesenchymal transformation in embryonic and adult valve endothelial cells. Arterioscler Thromb Vasc Biol 2013;33:121-30.
20. Quinlan AM, Billiar KL. Investigating the role of substrate stiffness in the persistence of valvular interstitial cell activation. J Biomed Mater Res A 2012;100:2474-82.
21. Duan B, Hockaday LA, Kapetanovic E, Kang KH, Butcher JT. Stiffness and Adhesivity Control Aortic Valve Interstitial Cell Behavior within Hyaluronic Acid Based Hydrogels. Acta Biomater 2013.
22. Walker GA, Masters KS, Shah DN, Anseth KS, Leinwand LA. Valvular myofibroblast activation by transforming growth factor-beta: implications for pathological extracellular matrix remodeling in heart valve disease. Circ Res 2004;95:253-60.
23. Geirsson A, Singh M, Ali R, Abbas H, Li W, Sanchez JA, et al. Modulation of transforming growth factor-beta signaling and extracellular matrix production in myxomatous mitral valves by angiotensin II receptor blockers. Circulation 2012; 126:S189-97.
24. Hakuno D, Kimura N, Yoshioka M, Mukai M, Kimura T, Okada Y, et al. Periostin advances atherosclerotic and rheumatic cardiac valve degeneration by inducing angiogenesis and MMP production in humans and rodents. J Clin Invest 2010;120: 2292-306.
25. Chester AH. Endothelin-1 and the aortic valve. Curr Vasc Pharmacol 2005;3:353-7.
26. Chester AH, Misfeld M, Yacoub MH. Receptor-mediated contraction of aortic valve leaflets. J Heart Valve Dis 2000;9:250-4 [discussion 4-5].
27. Cushing MC, Mariner PD, Liao JT, Sims EA, Anseth KS. Fibroblast growth factor represses Smad-mediated myofibroblast activation in aortic valvular interstitial cells. FASEB J 2008;22:1769-77.
28. Miyamoto S, Iwamoto R, Furuya A, Takahashi K, Sasaki Y, Ando H, et al. A novel antihuman HB-EGF monoclonal antibody with multiple antitumor mechanisms against ovarian cancer cells. Clin Cancer Res 2011;17:6733-41.
29. Moustakas A, Pardali K, Gaal A, Heldin CH. Mechanisms of TGF-beta signaling in regulation of cell growth and differentiation. Immunol Lett 2002;82:85-91.
30. Bajaj P, Tang X, Saif TA, Bashir R. Stiffness of the substrate influences the phenotype of embryonic chicken cardiac myocytes. J Biomed Mater Res A 2010;95:1261-9.
31. Butcher JT, Nerem RM. Valvular endothelial cells regulate the phenotype of interstitial cells in co-culture: effects of steady shear stress. Tissue Eng 2006;12:905-15.
32. Ku CH, Johnson PH, Batten P, Sarathchandra P, Chambers RC, Taylor PM, et al. Collagen synthesis by mesenchymal stem cells and aortic valve interstitial cells in response to mechanical stretch. Cardiovasc Res 2006;71:548-56.
33. Waxman AS, Kornreich BG, Gould RA, Moise NS, Butcher JT. Interactions between TGFbeta1 and cyclic strain in modulation ofmyofibroblastic differentiation of canine mitral valve interstitial cells in 3D culture. J Vet Cardiol 2012;14:211-21.
34. El-Hamamsy I, Balachandran K, Yacoub MH, Stevens LM, Sarathchandra P, Taylor PM, et al. Endothelium-dependent regulation of the mechanical properties of aortic valve cusps. J Am Coll Cardiol 2009;53:1448-55.
35. Lupu F, SimionescuM. Organization of the intercellular junctions in the endothelium of cardiac valves. J Submicrosc Cytol 1985;17:119-32.
36. Bosse K, Hans CP, Zhao N, Koenig SN, Huang N, Guggilam A, et al. Endothelial nitric oxide signaling regulates Notch1 in aortic valve disease. J Mol Cell Cardiol 2013;60: 27-35.
37. Richards J, El-Hamamsy I, Chen S, Sarang Z, Sarathchandra P, YacoubMH, et al. Sidespecific endothelial-dependent regulation of aortic valve calcification: interplay of hemodynamics and nitric oxide signaling. Am J Pathol 2013;182:1922-31.
38. El Accaoui RN, Gould ST, Hajj GP, Chu Y, Davis MK, Kraft DC, et al. Aortic Valve Sclerosis in Mice Deficient in Endothelial Nitric Oxide Synthase. Am J Physiol Heart Circ Physiol 2014.
39. Kaushal S, Amiel GE, Guleserian KJ, Shapira OM, Perry T, Sutherland FW, et al. Functional small-diameter neovessels created using endothelial progenitor cells expanded ex vivo. Nat Med 2001;7:1035-40.
40. Melero-Martin JM, De Obaldia ME, Kang SY, Khan ZA, Yuan L, Oettgen P, et al. Engineering robust and functional vascular networks in vivo with human adult and cord blood-derived progenitor cells. Circ Res 2008;103:194-202.
41. Bucala R, Spiegel LA, Chesney J, Hogan M, Cerami A. Circulating fibrocytes define a new leukocyte subpopulation that mediates tissue repair. Mol Med 1994;1:71-81.
42. Wylie-Sears J, Levine RA, Bischoff J. Losartan inhibits endothelial-to-mesenchymal transformation in mitral valve endothelial cells by blocking transforming growth factor-beta-induced phosphorylation of ERK. Biochem Biophys Res Commun 2014.
43. Wu B, Wang Y, Lui W, Langworthy M, Tompkins KL, Hatzopoulos AK, et al. Nfatc1 coordinates valve endocardial cell lineage development required for heart valve formation. Circ Res 2011;109:183-92.
44. Wu B, Baldwin HS, Zhou B. Nfatc1 directs the endocardial progenitor cells to make heart valve primordium. Trends Cardiovasc Med 2013;23:294-300.
45. Cheng SL, Shao JS, Behrmann A, Krchma K, Towler DA. Dkk1 and MSX2-Wnt7b signaling reciprocally regulate the endothelial-mesenchymal transition in aortic endothelial cells. Arterioscler Thromb Vasc Biol 2013;33:1679-89.
46. Zeidan A, Sward K, Nordstrom I, Ekblad E, Zhang JC, Parmacek MS, et al. Ablation of SM22alpha decreases contractility and actin contents of mouse vascular smooth muscle. FEBS Lett 2004;562:141-6.
47. Chen JH, Yip CY, Sone ED, Simmons CA. Identification and characterization of aortic valve mesenchymal progenitor cells with robust osteogenic calcification potential. Am J Pathol 2009;174:1109-19.
48. Mahler GJ, Frendl CM, Cao Q, Butcher JT. Effects of shear stress pattern and magnitude on mesenchymal transformation and invasion of aortic valve endothelial cells. Biotechnol Bioeng 2014.
49. Mitamura T, Higashiyama S, Taniguchi N, Klagsbrun M, Mekada E. Diphtheria toxin binds to the epidermal growth factor (EGF)-like domain of human heparin-binding EGF-like growth factor/diphtheria toxin receptor and inhibits specifically its mitogenic activity. J Biol Chem 1995;270:1015-9.
50. Yamazaki S, Iwamoto R, Saeki K, Asakura M, Takashima S, Yamazaki A, et al. Mice with defects in HB-EGF ectodomain shedding show severe developmental abnormalities. J Cell Biol 2003;163:469-75.
51. Chen PY, Qin L, Barnes C, Charisse K, Yi T, Zhang X, et al. FGF regulates TGF-beta signaling and endothelial-to-mesenchymal transition via control of let-7 miRNA expression. Cell Rep 2012;2:1684-96.
52. Gould ST, Matherly EE, Smith JN, Heistad DD, Anseth KS. The role of valvular endothelial cell paracrine signaling and matrix elasticity on valvular interstitial cell activation. Biomaterials 2014;35:3596-606.
53. Stephens EH, Durst CA, West JL, Grande-Allen KJ. Mitral valvular interstitial cell responses to substrate stiffness depend on age and anatomic region. Acta Biomater 2011;7:75-82.
54. Akhurst RJ, Lehnert SA, Faissner A, Duffie E. TGF beta in murine morphogenetic processes: the early embryo and cardiogenesis. Development 1990;108:645-56.
55. Gatherer D, Ten Dijke P, Baird DT, Akhurst RJ. Expression of TGF-beta isoforms during first trimester human embryogenesis. Development 1990;110:445-60.
56. Molin DG, Bartram U, Van der Heiden K, Van Iperen L, Speer CP, Hierck BP, et al. Expression patterns of Tgfbeta1-3 associate withmyocardialisation of the outflow tract and the development of the epicardium and the fibrous heart skeleton. Dev Dyn 2003;227:431-44.