Myogel, a novel, basement membrane-rich, extracellular matrix derived from skeletal muscle, is highly adipogenic in vivo and in vitro

Cells Tissues Organs

Volumn 188, Issue 4, 2008, Pages 347-358

  Abberton, K M ^a,b   Bortolotto, S K ^a   Woods, A A ^a   Findlay, M ^a   Morrison, W A ^a   Thompson, E W ^a   Messina, A ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b Bernard O'Brien Institute of Microsurgery   (Australia)

Author keywords

Adipogenesis; Basement membrane; Extracellular matrix; Muscle

Indexed keywords

COLLAGEN TYPE 1; COLLAGEN TYPE 4; FIBROBLAST GROWTH FACTOR 2; LAMININ 1; LAMININ ALPHA2; LAMININ ALPHA4; MATRIGEL; VASCULOTROPIN A;

ADIPOGENESIS; ADIPOSE TISSUE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR MATRIX; FIBROBLAST CULTURE; HUMAN; HUMAN TISSUE; HYDROGEL; MOUSE; MYOGEL; NONHUMAN; PRIORITY JOURNAL; PROADIPOCYTE; PROTEIN ANALYSIS; RAT; SKELETAL MUSCLE; TISSUE ENGINEERING; WESTERN BLOTTING;

ADIPOGENESIS; ADIPOSE TISSUE; ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MUSCLE, SKELETAL; RATS; STROMAL CELLS; SWINE; TISSUE ENGINEERING;

ANIMALIA; MUS; RATTUS; SUIDAE;

EID: 53549093045     PISSN: 14226405     EISSN: None     Source Type: Journal    
DOI: 10.1159/000121575     Document Type: Article

References (92)

1. Bachmeier, M., G. Loffler (1995) Influence of growth factors on growth and differentiation of 3T3-L1 preadipocytes in serum-free conditions. Eur J Cell Biol 68: 323-329.
2. Badylak, S., J. Obermiller, L. Geddes, R. Matheny (2003) Extracellular matrix for myocardial repair. Heart Surg Forum 6: E20-E26.
3. Bae, S.N., G. Arand, H. Azzam, P. Pavasant, J. Torri, T.L. Frandsen, E.W. Thompson (1993) Molecular and cellular analysis of basement membrane invasion by human breast cancer cells in Matrigel-based in vitro assays. Breast Cancer Res Treat 24: 241-255.
4. Barbosa, I., S. Garcia, V. Barbier-Chassefiere, J.-P. Caruelle, I. Martelly, D. Papy-Garcia (2003) Improved and simple micro assay for sulfated glycosaminoglycans quantification in biological extracts and its use in skin and muscle tissue studies. Glycobiology 13: 647-653.
5. Beahm, E.K., R.L. Walton, C.W. Patrick Jr. (2003) Progress in adipose tissue construct development. Clin Plast Surg 30: 547-558.
6. Behravesh, E., A.G. Mikos (2003) Three-dimensional culture of differentiating marrow stromal osteoblasts in biomimetic poly (propylene fumarate-co-ethylene glycol)-based macroporous hydrogels. J Biomed Mater Res A 66: 698-706.
7. Bokhari, M.A., G. Akay, S. Zhang, M.A. Birch (2005) The enhancement of osteoblast growth and differentiation in vitro on a peptide hydrogel-polyHIPE polymer hybrid material. Biomaterials 26: 5198-5208.
8. Boney, C.M., B.M. Moats-Staats, A.D. Stiles, A.J. D'Ercole (1994) Expression of insulin-like growth factor-I (IGF-I) and IGF-binding proteins during adipogenesis. Endocrinology 35: 1863-1868.
9. Bradshaw, A.D., E.H. Sage (2001) SPARC, a matricellular protein that functions in cellular differentiation and tissue response to injury. J Clin Invest 107: 1049-1054.
10. Bradshaw, A.D., D.C. Graves, K. Motamed, E.H. Sage (2003) SPARC-null mice exhibit increased adiposity without significant differences in overall body weight. Proc Natl Acad Sci USA 100: 6045-6050
11. Bryant, S.J., K.S. Anseth (2001) Hydrogel properties influence ECM production by chondrocytes photoencapsulated in poly (ethylene glycol) hydrogels. J Biomed Mater Res 59: 63-72.
12. Burkhardt, D., S.Y. Hwa, P. Ghosh (2001) A novel microassay for the quantitation of the sulfated glycosaminoglycan content of histological sections: its application to determine the effects of Diacerhein on cartilage in an ovine model of osteoarthritis. Osteoarthritis Cartilage 9: 238-247.
13. Cao, Y., P. Linden, D. Shima, F. Browne, J. Folkman (1996) In vivo angiogenic activity and hypoxia induction of heterodimers of placenta growth factor/vascular endothelial growth factor J Clin Invest 208: 2507-2511.
14. Carbonetto, S.T., M.M. Gruver, D.C. Turner (1982) Nerve fiber growth on defined hydrogel substrates. Science 216: 897-899.
15. Chen, T., H.D. Embree, E.M. Brown, M.M. Taylor, G.F. Payne (2003) Enzyme-catalyzed gel formation of gelatin and chitosan: potential for in situ applications. Biomaterials 23: 2831-2841.
16. Cimini, M, D.R. Boughner, J.A. Ronald, D.E. Johnston, K.A. Rogers (2005) Dermal fibroblasts cultured on small intestinal submucosa: conditions for the formation of a neotissue. J Biomed Mater Res A 75: 895-906.
17. Cinti, S, Cigolini M., M. Morroni, M.C. Zingaretti (1989) S-100 protein in white preadipocytes: an immunoelectronmicroscopic study. Anat Rec 224: 466-472.
18. Colognato, H., P.D. Yurchenco (2000) Form and function: the laminin family of heterotrimers. Dev Dyn 218: 213-234.
19. Crandall, D.L., G.J. Hausman, J.G. Kral (1997) A review of the microcirculation of adipose tissue: anatomic, metabolic, and angiogenic perspectives. Microcirculation 4: 211-232.
20. Cronin, K.J., A. Messina, K.R. Knight, J.J. Cooper-White, G.W. Stevens, A.J. Penington, W.A. Morrison (2004) New murine model of spontaneous autologous tissue engineering combining an arteriovenous pedicle with matrix materials. Plast Reconstr Surg 113: 260-269.
21. Darkovich, S.L., M. Brown-Etris, M. Spencer (1990) Biofilm hydrogel dressing: a clinical evaluation in the treatment of pressure sores. Ostomy Wound Manage 29: 47-60.
22. Ding, L., I. Hennig, S.E. Evsyukov (2001) Nonionic hydrogels by copolymerization of vinylene carbonate and oligo(ethylene glycol) vinyl ethers. Polymer 42: 2745-2753
23. Distler, J.W., A. Hirth, M. Kurowska-Stolarska, R.E. Gay, S. Gay, O. Distler (2003) Angiogenic and angiostatic factors in the molecular control of angiogenesis. Q J Nucl Med 47: 149-161.
24. Drury, J.L., D.J. Mooney (2003) Hydrogels for tissue engineering: scaffold design variables and applications. Biomaterials 24: 4337-4351.
25. Eiselt, P., J. Yeh, R.K. Latvala, L.D. Shea, D.J. Mooney (2000) Porous carriers for biomedical applications based on alginate hydrogels. Biomaterials 21: 1921-1927.
26. Eisenbud, D., H. Hunter, L. Kessler, K. Zulkowski (2003) Hydrogel wound dressings: where do we stand in 2003? Ostomy Wound Manage 49: 52-57.
27. Farndale, R.W., D.J. Buttle, A.J. Barrett (1986) Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta 882: 173-177.
28. Gobin, A.S., J.L. West (2003) Effects of epidermal growth factor on fibroblast migration through biomimetic hydrogels Biotechnol Prog 19: 1781-1785.
29. Gullberg, D., C.F. Tiger, T. Velling (1999) Laminins during muscle development and in muscular dystrophies. Cell Mol Life Sci 56: 442-460.
30. Hagedorn, H.G., A.G. Nerlich (2000) Microvessel density and endothelial basement membrane composition in laryngeal squamous cell carcinomas. Acta Otolaryngol 120: 891-898.
31. Hallmann, R., N. Horn, M. Selg, O. Wendler, F. Pausch, L.M. Sorokin (2005) Expression and function of laminins in the embryonic and mature vasculature. Physiol Rev 85: 979-1000.
32. Hampton, S. (2004) A small study in healing rates and symptom control using a new sheet hydrogel dressing. J Wound Care 13: 297-300.
33. Hausman, G.J., J.T. Wright, R.L. Richardson (1996) The influence of extracellular matrix substrata on preadipocyte development in serum-free cultures of stromal-vascular cells. J Anim Sci 74: 2117-2128.
34. Hausman, G.J., R.L. Richardson (2004) Adipose tissue angiogenesis. J Anim Sci 82: 925-934.
35. Hendrix, M.J., E.A. Seftor, R.E. Seftor, I.J. Fidler (1987) A simple quantitative assay for studying the invasive potential of high and low human metastatic variants. Cancer Lett 38: 137-147.
36. Hemmrich, K., D. von Heimburg, R. Rendchen, C. Di Bartolo, E. Milella, N. Pallua (2005) Implantation of preadipocyte-loaded hyaluronic acid-based scaffolds into nude mice to evaluate potential for soft tissue engineering. Biomaterials 26: 7025-7037.
37. Hemmrich, K., M. Meersch, U. Wiesemann, J. Salber, D. Klee, T. Gries, N. Pallua (2006) Polyesteramide-derived nonwovens as innovative degradable matrices support preadipocyte adhesion, proliferation, and differentiation. Tissue Eng 12: 3557-3565.
38. Hemmrich, K., G.P.L. Thomas, K.M. Abberton, E.W. Thompson, J.A. Rophael, A.J. Penington, W.A. Morrison (2007) MCP-1 and NO promote adipogenesis in a model that mimics obesity. Obesity 15: 2951-2957.
39. Hoddle, J. (2002) Naturally occurring scaffolds for soft tissue repair and regeneration. Tissue Eng 8: 295-308.
40. Hofer, S.O., G.M. Mitchell, A.J. Penington, W.A. Morrison, R. RomeoMeeuw, E. Keramidaris, J. Palmer, K.R. Knight (2005) The use of pimonidazole to characterise hypoxia in the internal environment of an in vivo tissue engineering chamber. Br J Plast Surg 58: 1104-1114.
41. Hoffman, A.S. (2001) Hydrogels for biomedical applications. Ann NY Acad Sci 944: 62-73.
42. Hong, S.R., Y.M. Lee, T. Akaike (2002) Evaluation of a galactose-carrying gelatin sponge for hepatocytes culture and transplantation. J Biomed Mater Res A 67: 733-741
43. Jeong, B., K.M. Lee, A. Gutowska, Y.H. An (2002) Thermogelling biodegradable copolymer aqueous solutions for injectable protein delivery and tissue engineering. Biomacromolecules 3: 865-868.
44. Kang, X., Y. Xie, D.A. Kniss (2005) Adipose tissue model using three-dimensional cultivation of preadipocytes seeded onto fibrous polymer scaffolds. Tissue Eng 11: 458-468.
45. Kawaguchi, N., K. Toriyama, E. Nicodemou-Lena, K. Inou, S. Torii, Y. Kitagawa (1998) De novo adipogenesis in mice at the site of injection of basement membrane and basic fibroblast growth factor. Proc Natl Acad Sci USA 95: 1062-1066.
46. Kedeshian, P., M.D. Sternlicht, M. Nguyen, Z.M. Shao, S.H. Barsky (1998) Humatrix, a novel myoepithelial matrical gel with unique biochemical and biological properties. Cancer Lett 123: 215-226.
47. Kimura, Y., M. Ozeki, T. Inamoto, Y. Tabata (2002) Time course of de novo adipogenesis in Matrigel by gelatin microspheres incorporating basic fibroblast growth factor. Tissue Eng 8: 603-613.
48. Kimura, Y., M. Ozeki, T. Inamoto, Y. Tabata (2003) Adipose tissue engineering based on human preadipocytes combined with gelatin microspheres containing basic fibroblast growth factor. Biomaterials 24: 2513-2521.
49. Kirker, K.R., Y. Luo, S.E. Morris, J. Shelby, G.D. Prestwich (2004) Glycosaminoglycan hydrogels as supplemental wound dressings for donor sites. J Burn Care Rehabil 25: 276-286.
50. Kleinman, H.K., M.L. McGarvey, L.A. Liotta, P.G. Robey (1982) Isolation and characterization of type IV procollagen, laminin and heparan sulfate proteoglycan from the EHS sarcoma. Biochemistry 24: 6188-6193.
51. Kleinman, H.K., M.L. McGarvey, J.R. Hassell, V.L. Star, F.B. Cannon, G.W. Laurie, G.R. Martin (1986) Basement membrane complexes with biological activity. Biochemistry 25: 312-318.
52. Kleinman, H.K., G.R. Martin (2005) Matrigel: basement membrane matrix with biological activity. Semin Cancer Biol 15: 378-386.
53. Kuo, C.K., P.X. Ma (2001) Ionically crosslinked alginate hydrogels as scaffolds for tissue engineering. Part 1. Structure, gelation rate and mechanical properties. Biomaterials 2: 511-521.
54. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
55. Lokmic, Z., F. Stillaert, W.A. Morrison, E.W. Thompson, G.M. Mitchell (2007) An arteriovenous loop in a protected space generates a permanent, highly vascular, tissue engineered construct. FASEB J 21: 511-522.
56. Liu, Y., X.Z. Shu, S.D. Gray, G.D. Prestwich (2004) Disulfide-crosslinked hyaluronangelatin sponge: growth of fibrous tissue in vivo. J Biomed Mater Res A 68: 142-149.
57. Lutolf, M.P., J.L. Lauer-Fields, H.G. Schmoekel, A.T. Metters, F.E. Weber, G.B. Fields, J.A. Hubbell (2003) Synthetic matrix metalloproteinase- sensitive hydrogels for the conduction of tissue regeneration: engineering cell-invasion characteristics. Proc Natl Acad Sci USA 100: 5413-5418.
58. Malinda, K.M., H.K. Kleinman (1996) The laminins. Int J Biochem Cell Biol 28: 957-959.
59. Mann, B.K., J.L. West (2002) Cell adhesion peptides alter smooth muscle cell adhesion, proliferation, migration, and matrix protein synthesis on modified surfaces and in polymer scaffolds. J Biomed Mater Res 60: 86-93.
60. Marotta, M., G. Martino (1985) Sensitive spectrophotometric method for the quantitative estimation of collagen. Anal Biochem 150: 86-90.
61. Marx, M., R.A. Perlmutter, J.A. Madri (1984) Modulation of platelet-derived growth factor receptor expression in microvascular endothelial cells during in vitro angiogenesis. J Clin Invest 93: 131-139.
62. Messina, A., S.K. Bortolotto, O.C. Cassell, J. Kelly, K.M. Abberton, W.A. Morrison (2005) Generation of a vascularized organoid using skeletal muscle as the inductive source. FASEB J 19: 1570-1572.
63. Mian, R., W.A. Morrison, J.V. Hurley, A.J. Penington, R. Romeo, Y. Tanaka, K.R. Knight (2000) Formation of new tissue from an arteriovenous loop in the absence of added extracellular matrix. Tissue Eng 6: 595-603.
64. Navarro, X., F.J. Rodriguez, D. Ceballos, E. Verdu (2003) Engineering an artificial nerve graft for the repair of severe nerve injuries. Med Biol Eng Comput 41: 220-226.
65. Neubauer, M., C. Fischbach, P. Bauer-Kreisel, E. Lieb, M. Hacker, J. Tessmar, M.B. Schulz, A. Goepferich, T. Blunk (2004) Basic fibroblast growth factor enhances PPARγ ligand-induced adipogenesis of mesenchymal stem cells. FEBS Lett 577: 277-283.
66. Nicosia, R.F., A. Ottinetti (1990) Modulation of microvascular growth and morphogenesis by reconstituted basement membrane gel in three-dimensional cultures of rat aorta: a comparative study of angiogenesis in Matrigel, collagen, fibrin, and plasma clot. In Vitro Cell Dev Biol 26: 119-128.
67. Niimi, T., C. Kumagai, M. Okano, Y. Kitagawa (1997) Differentiation- dependent expression of laminin-8 (α4β1γ1) mRNAs in mouse 3T3-L1 adipocytes. Matrix Biol 16: 223-230.
68. Peer, L. (1956) The neglected free fat graft. Am J Surg 18: 233-250.
69. Powell, C.A., B.L. Smiley, J. Mills, H.H. Vandenburgh (2002) Mechanical stimulation improves tissue-engineered human skeletal muscle. Am J Physiol Cell Physiol 283: C1557-C1565.
70. Pratt, A.B., F.E. Weber, H.G. Schmoekel, R. Muller, J.A. Hubbell (2004) Synthetic extracellular matrices for in situ tissue engineering. Biotechnol Bioeng 86: 27-36.
71. Rossatti, B. (1960) Revascularisation and phagocytosis in free fat autografts: an experimental study. Br J Plast Surg 13: 35-41.
72. Rosso, F., A. Giordano, M. Barbarisi, A. Barbarisi (2004) From cell-ECM interactions to tissue engineering. J Cell Physiol 199: 174-180.
73. Schmedlen, R.H., K.S. Masters, J.L. West (2002) Photocrosslinkable polyvinyl alcohol hydrogels that can be modified with cell adhesion peptides for use in tissue engineering. Biomaterials 23: 4325-4332.
74. Siegal, G.P., M.H. Wang, C.A. Rinehart Jr., J.W. Kennedy, L.J. Goodly, Y. Miller, D.G. Kaufman, R.K. Singh (1993) Development of a novel human extracellular matrix for quantitation of the invasiveness of human cells. Cancer Lett 69: 123-132.
75. Smahel, J. (1986) Adipose tissue in plastic surgery. Ann Plast Surg 16: 444-453.
76. Smith, P.J., L.S. Wise, R. Berkowitz, C. Wan, C.S. Rubin (1988) Insulin-like growth factor-I is an essential regulator of the differentiation of 3T3-L1 adipocytes. J Biol Chem 263: 9402-9408.
77. Stark, H.J., M.J. Willhauck, N. Mirancea, K. Boehnke, I. Nord, D. Breitkreutz, Pavesio A., Boukamp P., Fusenig N.E. (2004) Authentic fibroblast matrix in dermal equivalents normalizes epidermal histogenesis and dermoepidermal junction in organotypic co-culture. Eur J Cell Biol 83: 631-645.
78. Stillaert, F., M. Findlay, J. Palmer, R. Idrizi, S. Cheang, A. Messina, K. Abberton, W. Morrison, E.W. Thompson (2007) Host rather than graft origin of Matrigel-induced adipose tissue in the murine tissue-engineering chamber. Tissue Eng 13: 2291-2300.
79. Tabata, Y. (2000) The importance of drug delivery systems in tissue engineering. Pharm Sci Technol Today 3: 80-89.
80. Tabata, Y. (2004) Tissue regeneration based on tissue engineering technology. Congenital Anomalies 44: 111-124.
81. Talts, J.F., Z. Andac, W. Gohring, A. Brancaccio, R. Timpl (1999) Binding of the G domains of laminin α1 and α2 chains and perlecan to heparin, sulfatides, α-dystroglycan and several extracellular matrix proteins. EMBO J 18: 863-870.
82. Talts, J.F., T. Sasaki, N. Miosge, W. Gohring, K. Mann, R. Mayne, R. Timpl (2000) Structural and functional analysis of the recombinant g domain of the laminin α4 chain and its proteolytic processing in tissues. J Biol Chem 275: 35192-35199.
83. Tartare-Deckert, S., C. Chavey, M.N. Monthouel, N. Gautier, E. Van Obberghen (2001) The matricellular protein SPARC/osteonectin as a newly identified factor up-regulated in obesity. J Biol Chem 276: 22231-22237.
84. Thomas, G.P., K. Hemmrich, K.M. Abberton, D. McCombe, A.J. Penington, E.W. Thompson, W.A. Morrison (2007) Zymosan-induced inflammation stimulates neo-adipogenesis. Int J Obes (Lond) [E-pub ahead of print].
85. Toti, P., M. Villanova, C. De Felice, T. Megha, S. Bartolommei, P. Tosi (1998) Expression of laminin 1 and 2 in brain tumor vessels: an immunohistochemical study. J Submicrosc Cytol Pathol 30: 227-230.
86. Vashi, A.V., K.M. Abberton, G.P. Thomas, W.A. Morrison, A.J. O'Connor, J.J. Cooper-White, E.W. Thompson (2006) Adipose tissue engineering based on the controlled release of fibroblast growth factor-2 in a collagen matrix. Tissue Eng 12: 3035-3043.
87. Veronese, F.M., C. Mammucari, F. Schiavon, O. Schiavon, S. Lora, F. Secundo, A. Chilin, A. Guiotto (2001) Pegylated enzyme entrapped in poly(vinyl alcohol) hydrogel for biocatalytic application. Farmaco 56: 541-547.
88. von Heimburg, D., M. Kuberka, R. Rendchen, K. Hemmrich, G. Rau, N. Pallua (2003) Preadipocyte-loaded collagen scaffolds with enlarged pore size for improved soft tissue engineering. Int J Artif Organs 26: 1064-1076.
89. Wang, L., R.M. Shelton, P.R. Cooper, M. Lawson, J.T. Triffitt, J.E. Barralet (2003) Evaluation of sodium alginate for bone marrow cell tissue engineering. Biomaterials 24: 3475-3481.
90. Wu, X., Black L., G. Santacana-Laffitte, C.W. Patrick Jr. (2007) Preparation and assessment of glutaraldehyde-crosslinked collagen-chitosan hydrogels for adipose tissue engineering. J Biomed Mater Res A 81: 59-65.
91. Zhang, Y, H.K. Lin, D. Frimberger, R.B. Epstein, B.P. Kropp (2005) Growth of bone marrow stromal cells on small intestinal submucosa: an alternative cell source for tissue engineered bladder. BJU Int 96: 1120-1125.
92. Zuk, P.A., M. Zhu, H. Mizuno, J. Juang, J.W. Futrell, A.J. Katz, P. Benhaim, H.P. Lorenz, M.H. Hedrick (2001) Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7: 211-228.