TGF-Β1 diminishes collagen production during long-term cyclic stretching of engineered connective tissue: Implication of decreased ERK signaling

Journal of Biomechanics

Volumn 44, Issue 5, 2011, Pages 848-855

  Syedain, Zeeshan H ^a,b   Tranquillo, Robert T ^a,b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b University of Minnesota   (United States)

Author keywords

Collagen deposition; Cyclic stretching; ERK; P38; TGF ; Tissue engineering; Tissue growth and remodeling

Indexed keywords

COLLAGEN DEPOSITION; CYCLIC STRETCHING; ERK; P38; TISSUE GROWTH AND REMODELING;

BIOMECHANICS; CELL CULTURE; COLLAGEN; GLYCOPROTEINS; MECHANICAL PROPERTIES; MUSCULOSKELETAL SYSTEM; PHOSPHORYLATION; RATING; SIGNALING; TENSILE STRENGTH; TENSILE TESTING; TISSUE;

TISSUE ENGINEERING;

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN; ELASTIN; MITOGEN ACTIVATED PROTEIN KINASE; SMAD2 PROTEIN; SMAD3 PROTEIN; SYNAPTOPHYSIN; TRANSFORMING GROWTH FACTOR BETA1;

ARTICLE; CONNECTIVE TISSUE; CONTROLLED STUDY; CORRELATION ANALYSIS; ELASTICITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; FIBROBLAST; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; STAINING; STRETCHING; TENSILE STRENGTH; TISSUE ENGINEERING; WESTERN BLOTTING;

AZO COMPOUNDS; COLLAGEN; CONNECTIVE TISSUE; ELASTICITY; ENZYME INHIBITORS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLASTS; HUMANS; INFANT, NEWBORN; P38 MITOGEN-ACTIVATED PROTEIN KINASES; SIGNAL TRANSDUCTION; SKIN; STRESS, MECHANICAL; TENSILE STRENGTH; TISSUE ENGINEERING; TRANSFORMING GROWTH FACTOR BETA1;

EID: 79952043058     PISSN: 00219290     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jbiomech.2010.12.007     Document Type: Article

References (41)

1. Balguid A., Rubbens M.P., Mol A., Bank R.A., Bogers A.J., van Kats J.P., de Mol B.A., Baaijens F.P., Bouten C.V. The role of collagen cross-links in biomechanical behavior of human aortic heart valve leaflets-relevance for tissue engineering. Tissue Eng. 2007, 13(7):1501-1511.
2. Bastiaansen-Jenniskens Y.M., Koevoet W., De Bart A.C., Zuurmond A.M., Bank R.A., Verhaar J.A., DeGroot J., van Osch G.J. TGFbeta affects collagen cross-linking independent of chondrocyte phenotype but strongly depending on physical environment. Tissue Eng. Part A 2008, 14(6):1059-1066.
3. Bilodeau K., Mantovani D. Bioreactors for tissue engineering: focus on mechanical constraints. A comparative review. Tissue Eng. 2006, 12(8):2367-2383.
4. Bujor A.M., Pannu J., Bu S., Smith E.A., Muise-Helmericks R.C., Trojanowska M. Akt blockade downregulates collagen and upregulates MMP1 in human dermal fibroblasts. J. Invest. Dermatol. 2008, 128(8):1906-1914.
5. Chambers R.C., Leoni P., Kaminski N., Laurent G.J., Heller R.A. Global expression profiling of fibroblast responses to transforming growth factor-beta1 reveals the induction of inhibitor of differentiation-1 and provides evidence of smooth muscle cell phenotypic switching. Am. J. Pathol. 2003, 162(2):533-546.
6. Clark R.A., Nielsen L.D., Welch M.P., McPherson J.M. Collagen matrices attenuate the collagen-synthetic response of cultured fibroblasts to TGF-beta. J. Cell Sci. 1995, 108(Pt 3):1251-1261.
7. Davidson J.M., LuValle P.A., Zoia O., Quaglino D., Giro M. Ascorbate differentially regulates elastin and collagen biosynthesis in vascular smooth muscle cells and skin fibroblasts by pretranslational mechanisms. J. Biol. Chem. 1997, 272(1):345-352.
8. Dayan D., Hiss Y., Hirshberg A., Bubis J.J., Wolman M. Are the polarization colors of picrosirius red-stained collagen determined only by the diameter of the fibers?. Histochemistry 1989, 93(1):27-29.
9. Grouf J.L., Throm A.M., Balestrini J.L., Bush K.A., Billiar K.L. Differential effects of EGF and TGF-beta1 on fibroblast activity in fibrin-based tissue equivalents. Tissue Eng. 2007, 13(4):799-807.
10. Gutierrez J.A., Perr H.A. Mechanical stretch modulates TGF-beta1 and alpha1(I) collagen expression in fetal human intestinal smooth muscle cells. Am. J. Physiol. 1999, 277(5 Pt 1):G1074-G1080.
11. Isenberg B.C., Tranquillo R.T. Long-term cyclic distention enhances the mechanical properties of collagen-based media-equivalents. Ann. Biomed. Eng. 2003, 31:937-949.
12. Isenberg B.C., Williams C., Tranquillo R.T. Small-diameter artificial arteries engineered in vitro. Circ. Res. 2006, 98(1):25-35.
13. Junqueira L.C., Montes G.S., Sanchez E.M. The influence of tissue section thickness on the study of collagen by the Picrosirius-polarization method. Histochemistry 1982, 74(1):153-156.
14. Kuang P.P., Goldstein R.H. Regulation of elastin gene transcription by proteasome dysfunction. Am. J. Physiol. Cell Physiol. 2005, 289(3):C766-C773.
15. Kuang P.P., Zhang X.H., Rich C.B., Foster J.A., Subramanian M., Goldstein R.H. Activation of elastin transcription by transforming growth factor-beta in human lung fibroblasts. Am. J. Physiol. Lung Cell Mol. Physiol. 2007, 292(4):L944-L952.
16. Kucich U., Rosenbloom J.C., Abrams W.R., Rosenbloom J. Transforming growth factor-beta stabilizes elastin mRNA by a pathway requiring active Smads, protein kinase C-delta, and p38. Am. J. Respir. Cell Mol. Biol. 2002, 26(2):183-188.
17. Lima E.G., Bian L., Ng K.W., Mauck R.L., Byers B.A., Tuan R.S., Ateshian G.A., Hung C.T. The beneficial effect of delayed compressive loading on tissue-engineered cartilage constructs cultured with TGF-beta3. Osteoarthritis Cartilage 2007, 15(9):1025-1033.
18. Lindahl G.E., Chambers R.C., Papakrivopoulou J., Dawson S.J., Jacobsen M.C., Bishop J.E., Laurent G.J. Activation of fibroblast procollagen alpha 1(I) transcription by mechanical strain is transforming growth factor-beta-dependent and involves increased binding of CCAAT-binding factor (CBF/NF-Y) at the proximal promoter. J. Biol. Chem. 2002, 277(8):6153-6161.
19. Long J.L., Tranquillo R.T. Elastic fiber production in cardiovascular tissue-equivalents. Matrix Biol. 2003, 22(4):339-350.
20. Massague J. How cells read TGF-beta signals. Nat. Rev. Mol. Cell Biol. 2000, 1(3):169-178.
21. Massague J., Seoane J., Wotton D. Smad transcription factors. Genes Dev. 2005, 19(23):2783-2810.
22. Merryman W.D., Lukoff H.D., Long R.A., Engelmayr G.C., Hopkins R.A., Sacks M.S. Synergistic effects of cyclic tension and transforming growth factor-beta1 on the aortic valve myofibroblast. Cardiovasc. Pathol. 2007, 16(5):268-276.
23. Moreau J.E., Bramono D.S., Horan R.L., Kaplan D.L., Altman G.H. Sequential biochemical and mechanical stimulation in the development of tissue-engineered ligaments. Tissue Eng. Part A 2008, 14(7):1161-1172.
24. Neidert M.R., Lee E.S., Oegema T.R., Tranquillo R.T. Enhanced fibrin remodeling in vitro with TGF-beta1, insulin and plasmin for improved tissue-equivalents. Biomaterials 2002, 23(17):3717-3731.
25. Pannu J., Nakerakanti S., Smith E., ten Dijke P., Trojanowska M. Transforming growth factor-beta receptor type I-dependent fibrogenic gene program is mediated via activation of Smad1 and ERK1/2 pathways. J. Biol. Chem. 2007, 282(14):10405-10413.
26. Papakrivopoulou J., Lindahl G.E., Bishop J.E., Laurent G.J. Differential roles of extracellular signal-regulated kinase 1/2 and p38MAPK in mechanical load-induced procollagen alpha1(I) gene expression in cardiac fibroblasts. Cardiovasc. Res. 2004, 61(4):736-744.
27. Poobalarahi F., Baicu C.F., Bradshaw A.D. Cardiac myofibroblasts differentiated in 3D culture exhibit distinct changes in collagen I production, processing, and matrix deposition. Am. J. Physiol. Heart Circ. Physiol. 2006, 291(6):H2924-H2932.
28. Robinson P.S., Johnson S.L., Evans M.C., Barocas V.H., Tranquillo R.T. Functional tissue-engineered valves from cell-remodeled fibrin with commissural alignment of cell-produced collagen. Tissue Eng. Part A 2008, 14(1):83-95.
29. Ross J.J., Tranquillo R.T. ECM gene expression correlates with in vitro tissue growth and development in fibrin gel remodeled by neonatal smooth muscle cells. Matrix Biol. 2003, 22(6):477-490.
30. Sato M., Shegogue D., Gore E.A., Smith E.A., McDermott P.J., Trojanowska M. Role of p38 MAPK in transforming growth factor beta stimulation of collagen production by scleroderma and healthy dermal fibroblasts. J. Invest. Dermatol. 2002, 118(4):704-711.
31. Starcher B.C., Galione M.J. Purification and comparison of elastins from different animal species. Anal. Biochem. 1976, 74(2):441-447.
32. Stegemann H., Stalder K. Determination of hydroxyproline. Clin. Chim. Acta 1967, 18:267-273.
33. Syedain Z.H., Meier L.A., Bjork J.W., Lee A., Tranquillo R.T. Implantable arterial grafts from human fibroblasts and fibrin using a multi-graft pulsed flow-stretch bioreactor with noninvasive strength monitoring. Biomaterials 2010, 32(3):714-722.
34. Syedain Z.H., Tranquillo R.T. Controlled cyclic stretch bioreactor for tissue-engineered heart valves. Biomaterials 2009, 30(25):4078-4084.
35. Syedain Z.H., Weinberg J.S., Tranquillo R.T. Cyclic distension of fibrin-based tissue constructs: evidence of adaptation during growth of engineered connective tissue. Proc. Natl. Acad. Sci. USA 2008, 105(18):6537-6542.
36. Thom T., Haase N., Rosamond W., Howard V.J., Rumsfeld J., Manolio T., Zheng Z.J., Flegal K., O'Donnell C., Kittner S., Lloyd-Jones D., Goff D.C., Hong Y., Adams R., Friday G., Furie K., Gorelick P., Kissela B., Marler J., Meigs J., Roger V., Sidney S., Sorlie P., Steinberger J., Wasserthiel-Smoller S., Wilson M., Wolf P. Heart disease and stroke statistics--2006 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 2006, 113(6):e85-151.
37. Tuan T.L., Song A., Chang S., Younai S., Nimni M.E. In vitro fibroplasia: matrix contraction, cell growth, and collagen production of fibroblasts cultured in fibrin gels. Exp. Cell Res. 1996, 223(1):127-134.
38. Walker G.A., Masters K.S., Shah D.N., Anseth K.S., Leinwand L.A. Valvular myofibroblast activation by transforming growth factor-beta: implications for pathological extracellular matrix remodeling in heart valve disease. Circ. Res. 2004, 95(3):253-260.
39. Yacoub M., Nerem R. Introduction. Bioengineering the heart. Philos. Trans. R. Soc. London B. Biol. Sci. 2007, 362(1484):1253-1255.
40. Yang G., Crawford R.C., Wang J.H. Proliferation and collagen production of human patellar tendon fibroblasts in response to cyclic uniaxial stretching in serum-free conditions. J. Biomech. 2004, 37(10):1543-1550.
41. Yao L., Liu J., Andreadis S.T. Composite fibrin scaffolds increase mechanical strength and preserve contractility of tissue engineered blood vessels. Pharm. Res. 2008, 25(5):1212-1221.