Journal of Tissue Viability
Volume 20, Issue 2 , Pages 37-48 , May 2011

Materials for engineering vascularized adipose tissue

  • Yu-Chieh Chiu

      Affiliations

    • Pritzker Institute of Biomedical Science and Engineering, Department of Biomedical Engineering, Illinois Institute of Technology Chicago, IL, USA
  • ,
  • Ming-Huei Cheng

      Affiliations

    • Department of Plastic and Reconstructive Surgery, Chang Gung Memorial Hospital, College of Medicine, Chang Gung University, Taoyuan, Taiwan
  • ,
  • Shiri Uriel

      Affiliations

    • Pritzker Institute of Biomedical Science and Engineering, Department of Biomedical Engineering, Illinois Institute of Technology Chicago, IL, USA
  • ,
  • Eric M. Brey

      Affiliations

    • Pritzker Institute of Biomedical Science and Engineering, Department of Biomedical Engineering, Illinois Institute of Technology Chicago, IL, USA
    • Research Service, Hines Veterans Administration Hospital, Hines, IL, USA
    • Corresponding Author InformationCorresponding author. Pritzker Institute of Biomedical Science and Engineering, Department of Biomedical Engineering, Illinois Institute of Technology Chicago, IL 60616, USA.

References 

  1. Boris S, Gerhard S. Current concepts of fat graft survival: histology of aspirated adipose tissue and review of the literature. Dermatol Surg. 2000;26:1159–1166
  2. Crandall DL, Hausman GJ, Kral JG. A review of the microcirculation of adipose tissue: anatomic, metabolic, and angiogenic perspectives. Microcirculation. 1997;4:211–232
  3. Cheng MH, Uriel S, Brey EM. Tissue derived materials for adipose regeneration. Bioengineering research in chronic wounds. In:  Gefen A editors. Springer; 2009;
  4. Lutolf MP, Hubbell JA. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol. 2005;23:47–55
  5. Miner JH, Yurchenco PD. Laminin functions in tissue morphogenesis. Ann Rev Cell Development Biol. 2004;20:255–284
  6. Uriel S, Labay E, Francis-Sedlak M, Moya ML, Weichselbaum RR, Ervin N, et al. Extraction and assembly of tissue-derived gels for cell culture and tissue engineering. Tissue Eng Part C Methods. 2009;15:309–321
  7. Kleinman HK, Martin GR. Matrigel: basement membrane matrix with biological activity. Semin Cancer Biol. 2005;15:378–386
  8. Aumailley M, Bruckner-Tuderman L, Carter WG, Deutzmann R, Edgar D, Ekblom P, et al. A simplified laminin nomenclature. Matrix Biol. 2005;24:326–332
  9. Kleinman HK, McGarvey ML, Liotta LA, Robey PG, Tryggvason K, Martin GR. Isolation and characterization of type IV procollagen, laminin, and heparan sulfate proteoglycan from the EHS sarcoma. Biochemistry. 1982;21:6188–6193
  10. Patarroyo M, Tryggvason K, Virtanen I. Laminin isoforms in tumor invasion, angiogenesis and metastasis. Semin Cancer Biol. 2002;12:197–207
  11. Kleinman HK, McGarvey ML, Hassell JR, Star VL, Cannon FB, Laurie GW, et al. Basement membrane complexes with biological activity. Biochemistry. 1986;25:312–318
  12. Kawaguchi N, Toriyama K, Nicodemou-Lena E, Inou K, Torii S, Kitagawa Y. De novo adipogenesis in mice at the site of injection of basement membrane and basic fibroblast growth factor. Proc Natl Acad Sci USA. 1998;95:1062–1066
  13. Tzu J, Marinkovich MP. Bridging structure with function: structural, regulatory, and developmental role of laminins. Int J Biochem Cell Biol. 2008;40:199–214
  14. Kawaguchi N, Toriyama K, Nicodemou-Lena E, Inou K, Torii S, Kitagawa Y. Reconstituted basement membrane potentiates in vivo adipogenesis of 3T3-F442A cells. Cytotechnology. 1999;31:215–220
  15. Chavey C, Mari B, Monthouel MN, Bonnafous S, Anglard P, Van Obberghen E, et al. Matrix metalloproteinases are differentially expressed in adipose tissue during obesity and modulate adipocyte differentiation. J Biol Chem. 2003;278:11888–11896
  16. Kubo Y, Kaidzu S, Nakajima I, Takenouchi K, Nakamura F. Organization of extracellular matrix components during differentiation of adipocytes in long-term culture. Vitro Cell Dev Biol Anim. 2000;36:38–44
  17. Nie J, Sage EH. SPARC inhibits adipogenesis by its enhancement of Î2-catenin signaling. J Biol Chem. 2009;284:1279–1290
  18. Aratani Y, Kitagawa Y. Enhanced synthesis and secretion of type IV collagen and entactin during adipose conversion of 3T3-L1 cells and production of unorthodox laminin complex. J Biol Chem. 1988;263:16163–16169
  19. Niimi T, Kumagai C, Okano M, Kitagawa Y. Differentiation-dependent expression of laminin-8 (alpha 4 beta 1 gamma 1) mRNAs in mouse 3T3-L1 adipocytes. Matrix Biol. 1997;16:223–230
  20. Patrick CW, Wu X. Integrin-mediated preadipocyte adhesion and migration on laminin-1. Ann Biomed Eng. 2003;31:505–514
  21. Francis ME, Uriel S, Brey EM. Endothelial cell-matrix interactions in neovascularization. Tissue Eng Part B Rev. 2008;14:19–32
  22. Parekh A, Weaver AM. Regulation of cancer invasiveness by the physical extracellular matrix environment. Cell Adh Migr. 2009;3:288–292
  23. Chun TH, Hotary KB, Sabeh F, Saltiel AR, Allen ED, Weiss SJ. A pericellular collagenase directs the 3-dimensional development of white adipose tissue. Cell. 2006;125:577–591
  24. Li Q, Hosaka T, Jambaldorj B, Nakaya Y, Funaki M. Extracellular matrix with the rigidity of adipose tissue helps 3T3-L1 adipocytes maintain insulin responsiveness. J Med Invest. 2009;56:142–149
  25. Rophael JA, Craft RO, Palmer JA, Hussey AJ, Thomas GP, Morrison WA, et al. Angiogenic growth factor synergism in a murine tissue engineering model of angiogenesis and adipogenesis. Am J Pathol. 2007;171:2048–2057
  26. Vashi AV, Abberton KM, Thomas GP, Morrison WA, O'Connor AJ, Cooper-White JJ, et al. Adipose tissue engineering based on the controlled release of fibroblast growth factor-2 in a collagen matrix. Tissue Eng. 2006;12:3035–3043
  27. Cronin KJ, Messina A, Thompson EW, Morrison WA, Stevens GW, Knight KR. The role of biological extracellular matrix scaffolds in vascularized three-dimensional tissue growth in vivo. J Biomed Mater Res B Appl Biomater. 2007;82:122–128
  28. Knight KR, Uda Y, Findlay MW, Brown DL, Cronin KJ, Jamieson E, et al. Vascularized tissue-engineered chambers promote survival and function of transplanted islets and improve glycemic control. FASEB J. 2006;20:565–567
  29. Cronin KJ, Messina A, Knight KR, Cooper-White JJ, Stevens GW, Penington AJ, et al. New murine model of spontaneous autologous tissue engineering, combining an arteriovenous pedicle with matrix materials. Plast Reconstr Surg. 2004;113:260–269
  30. Piasecki JH, Gutowski KA, Lahvis GP, Moreno KI. An experimental model for improving fat graft viability and purity. Plast Reconstr Surg. 2007;119:1571–1583
  31. Piasecki JH, Gutowski KA, Moreno KM, Lahvis GL. Purified viable fat suspended in matrigel improves volume longevity. Aesthet Surg J. 2008;28:24–32
  32. Cheng MH, Uriel S, Moya ML, Francis-Sedlak M, Wang R, Huang JJ, et al. Dermis-derived hydrogels support adipogenesis in vivo. J Biomed Mater Res, in press.
  33. Abberton KM, Bortolotto SK, Woods AA, Findlay M, Morrison WA, Thompson EW, et al. Myogel, a novel, basement membrane-rich, extracellular matrix derived from skeletal muscle, is highly adipogenic in vivo and in vitro. Cell Tissues Organs. 2008;188:347–358
  34. Hiraoka Y, Yamashiro H, Yasuda K, Kimura Y, Inamoto T, Tabata Y. In situ regeneration of adipose tissue in rat fat pad by combining a collagen scaffold with gelatin microspheres containing basic fibroblast growth factor. Tissue Eng. 2006;12:1475–1487
  35. Cho SW, Song KW, Rhie JW, Park MH, Choi CY, Kim BS. Engineered adipose tissue formation enhanced by basic fibroblast growth factor and a mechanically stable environment. Cell Transplant. 2007;16:421–434
  36. Torio-Padron N, Baerlecken N, Momeni A, Stark GB, Borges J. Engineering of adipose tissue by injection of human preadipocytes in fibrin. Aesthetic Plast Surg. 2007;31:285–293
  37. Patel PN, Gobin AS, West JL, Patrick CW. Poly(ethylene glycol) hydrogel system supports preadipocyte viability, adhesion, and proliferation. Tissue Eng. 2005;11:1498–1505
  38. Hillel AT, Varghese S, Petsche J, Shamblott MJ, Elisseeff JH. Embryonic germ cells are capable of adipogenic differentiation in vitro and in vivo. Tissue Eng Part A. 2008;
  39. Stacey DH, Hanson SE, Lahvis G, Gutowski KA, Masters KS. In vitro adipogenic differentiation of preadipocytes varies with differentiation stimulus, culture dimensionality, and scaffold composition. Tissue Eng Part A; 0.
  40. Stosich MS, Bastian B, Marion NW, Clark PA, Reilly G, Mao JJ. Vascularized adipose tissue grafts from human mesenchymal stem cells with bioactive cues and microchannel conduits. Tissue Eng. 2007;13:2881–2890
  41. Dolderer JH, Abberton KM, Thompson EW, Slavin JL, Stevens GW, Penington AJ, et al. Spontaneous large volume adipose tissue generation from a vascularized pedicled fat flap inside a chamber space. Tissue Eng. 2007;13:673–681
  42. Chaubey A, Ross KJ, Leadbetter RM, Burg KJ. Surface patterning: tool to modulate stem cell differentiation in an adipose system. J Biomed Mater Res B Appl Biomater. 2008;84:70–78
  43. Uriel S, Labay E, Francis-Sedlak M, Moya ML, Weichselbaum RR, Ervin N, et al. Extraction and assembly of tissue-derived gels for cell culture and tissue engineering. Tissue Eng Part C Methods. 2009;15(3):309–321
  44. Uriel S, Huang JJ, Moya ML, Francis ME, Wang R, Chang SY, et al. The role of adipose protein derived hydrogels in adipogenesis. Biomaterials. 2008;29:3712–3719
  45. Uriel S. Isolation and characterization of tissue specific basement membrane extracts. In: Biomedical engineering. Chicago: Illinois Institute of Technology; 2009;
  46. Barroso MM, Freire E, Limaverde GS, Rocha GM, Batista EJ, Weissmuller G, et al. Artificial laminin polymers assembled in acidic pH mimic basement membrane organization. J Biol Chem. 2008;283:11714–11720
  47. Freire E, Coelho-Sampaio T. Self-assembly of laminin induced by acidic pH. J Biol Chem. 2000;275:817–822
  48. Frye CA, Wu X, Patrick CW. Microvascular endothelial cells sustain preadipocyte viability under hypoxic conditions. In Vitro Cell Dev Biol Anim. 2005;41:160–164
  49. Dallabrida SM, Zurakowski D, Shih SC, Smith LE, Folkman J, Moulton KS, et al. Adipose tissue growth and regression are regulated by angiopoietin-1. Biochem Biophys Res Commun. 2003;311:563–571
  50. Tang W, Zeve D, Suh JM, Bosnakovski D, Kyba M, Hammer RE, et al. White fat progenitor cells reside in the adipose vasculature. Science. 2008;322:583–586
  51. Zhong X, Yan W, He X, Ni Y. Improved fat graft viability by delayed fat flap with ischaemic pretreatment. J Plast Reconstr Aesthet Surg. 2009;62:526–531
  52. Yi CG, Xia W, Zhang LX, Zhen Y, Shu MG, Han Y, et al. VEGF gene therapy for the survival of transplanted fat tissue in nude mice. J Plast Reconstr Aesthet Surg. 2007;60:272–278
  53. Ozaki H, Seo M-S, Ozaki K, Yamada H, Yamada E, Okamoto N, et al. Blockade of vascular endothelial cell growth factor receptor signaling is sufficient to completely prevent retinal neovascularization. Am J Pathol. 2000;156:697–707
  54. Nikol S, Baumgartner I, Van Belle E, Diehm C, Visona A, Capogrossi MC, et al. Therapeutic angiogenesis with intramuscular NV1FGF improves amputation-free survival in patients with critical limb ischemia. Mol Ther. 2008;16:972–978
  55. Liu Z, Kobayashi K, van Dinther M, van Heiningen SH, Valdimarsdottir G, van Laar T, et al. VEGF and inhibitors of TGF{beta} type-I receptor kinase synergistically promote blood-vessel formation by inducing {alpha}5-integrin expression. J Cell Sci. 2009;122:3294–3302
  56. Pierce EA, Avery RL, Foley ED, Aiello LP, Smith LE. Vascular endothelial growth factor/vascular permeability factor expression in a mouse model of retinal neovascularization. Proc Natl Acad Sci U S A. 1995;92:905–909
  57. Nor JE, Christensen J, Mooney DJ, Polverini PJ. Vascular endothelial growth factor (VEGF)-mediated angiogenesis is associated with enhanced endothelial cell survival and induction of Bcl-2 expression. Am J Pathol. 1999;154:375–384
  58. Dvorak HF, Brown LF, Detmar M, Dvorak AM. Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am J Pathol. 1995;146:1029–1039
  59. Ozawa CR, Banfi A, Glazer NL, Thurston G, Springer ML, Kraft PE, et al. Microenvironmental VEGF concentration, not total dose, determines a threshold between normal and aberrant angiogenesis. J Clin Invest. 2004;113:516–527
  60. Seliktar D, Zisch AH, Lutolf MP, Wrana JL, Hubbell JA. MMP-2 sensitive, VEGF-bearing bioactive hydrogels for promotion of vascular healing. J Biomed Mater Res A. 2004;68:704–716
  61. Ehrbar M, Metters A, Zammaretti P, Hubbell JA, Zisch AH. Endothelial cell proliferation and progenitor maturation by fibrin-bound VEGF variants with differential susceptibilities to local cellular activity. J Control Release. 2005;101:93–109
  62. Moya ML, Lucas S, Francis-Sedlak M, Liu X, Garfinkel MR, Huang J-J, et al. Sustained delivery of FGF-1 increases vascular density in comparison to bolus administration. Microvasc Res. 2009;78:142–147
  63. Monica LM. Optimizing alginate microbead delivery system for release of angiogenic protein for neovascularization. In: Biomedical engineering. Chicago: Illinois Institute if Technology; December 2009;p. 120
  64. Uriel S, Brey EM, Greisler HP. Sustained low levels of fibroblast growth factor-1 promote persistent microvascular network formation. Am J Surg. 2006;192:604–609
  65. Yancopoulos GD, Davis S, Gale NW, Rudge JS, Wiegand SJ, Holash J. Vascular-specific growth factors and blood vessel formation. Nature. 2000;407:242–248
  66. Richardson TP, Peters MC, Ennett AB, Mooney DJ. Polymeric system for dual growth factor delivery. Nat Biotechnol. 2001;19:1029–1034
  67. Peirce SM, Price RJ, Skalak TC. Spatial and temporal control of angiogenesis and arterialization using focal applications of VEGF164 and Ang-1. Am J Physiol Heart Circ Physiol. 2004;286:H918–H925
  68. Brey EM, Uriel S, Greisler HP, McIntire LV. Therapeutic neovascularization: contributions from bioengineering. Tissue Eng. 2005;11:567–584
  69. Nor JE, Peters MC, Christensen JB, Sutorik MM, Linn S, Khan MK, et al. Engineering and characterization of functional human microvessels in immunodeficient mice. Lab Invest. 2001;81:453–463
  70. Ghajar CM, Blevins KS, Hughes CCW, George SC, Putnam AJ. Mesenchymal stem cells enhance angiogenesis in mechanically viable prevascularized tissues via early matrix metalloproteinase upregulation. Tissue Eng. 2006;12:2875–2888
  71. Koike N, Fukumura D, Gralla O, Au P, Schechner JS, Jain RK. Tissue engineering: creation of long-lasting blood vessels. Nature. 2004;428:138–139
  72. Chen X, Aledia AS, Ghajar CM, Griffith CK, Putnam AJ, Hughes CCW, et al. Prevascularization of a fibrin-based tissue construct accelerates the formation of functional anastomosis with host vasculature. Tissue Eng Part A. 2008;15:1363–1371
  73. Levenberg S, Rouwkema J, Macdonald M, Garfein ES, Kohane DS, Darland DC, et al. Engineering vascularized skeletal muscle tissue. Nat Biotechnol. 2005;23:879–884
  74. Kaihara S, Borenstein J, Koka R, Lalan S, Ochoa ER, Ravens M, et al. Silicon micromachining to tissue engineer branched vascular channels for liver fabrication. Tissue Eng. 2000;6:105–117
  75. Hahn MS, Taite LJ, Moon JJ, Rowland MC, Ruffino KA, West JL. Photolithographic patterning of polyethylene glycol hydrogels. Biomaterials. 2006;27:2519–2524
  76. Kaihara S, Borenstein J, Koka R, Lalan S, Ochoa ER, Ravens M, et al. Silicon micromachining to tissue engineer branched vascular channels for liver fabrication. Tissue Eng. 2004;6:105–117
  77. Liu Tsang V, Chen AA, Cho LM, Jadin KD, Sah RL, DeLong S, et al. Fabrication of 3D hepatic tissues by additive photopatterning of cellular hydrogels. FASEB J. 2007;21:790–801
  78. Papavasiliou G, Songprawat P, Pérez-Luna V, Hammes E, Morris M, Chiu YC, et al. Three-dimensional patterning of poly(ethylene glycol) hydrogels through surface-initiated photopolymerization. Tissue Eng. 2008;14:129–140
  79. Chiu YC, Larson JC, Perez-Luna VH, Brey EM. Formation of microchannels in poly(ethylene glycol) hydrogels by selective degradation of patterned microstructures. Chem Mater. 2009;21:1677–1682
  80. Tsuda Y, Shimizu T, Yamato M, Kikuchi A, Sasagawa T, Sekiya S, et al. Cellular control of tissue architectures using a three-dimensional tissue fabrication technique. Biomaterials. 2007;28:4939–4946
  81. Golden AP, Tien J. Fabrication of microfluidic hydrogels using molded gelatin as a sacrificial element. Lab Chip. 2007;7:720–725
  82. Chrobak KM, Potter DR, Tien J. Formation of perfused, functional microvascular tubes in vitro. Microvasc Res. 2006;71:185–196
  83. Chiu YC. Microchannel generation by selective degradation of patterned hydrogels. Chicago: Illinois Institute of Technology; July 2009;p. 60

PII: S0965-206X(09)00057-6

doi: 10.1016/j.jtv.2009.11.005

Journal of Tissue Viability
Volume 20, Issue 2 , Pages 37-48 , May 2011