Advertisement

Cell and Tissue Research

, Volume 347, Issue 3, pp 747–757 | Cite as

Engineering of vascularized adipose constructs

  • Paul S. Wiggenhauser
  • Daniel F. Müller
  • Ferry P. W. Melchels
  • José T. Egaña
  • Katharina Storck
  • Helena Mayer
  • Peter Leuthner
  • Daniel Skodacek
  • Ursula Hopfner
  • Hans G. Machens
  • Rainer Staudenmaier
  • Jan T. Schantz
Regular Article
First Online:
Received:
Accepted:

Abstract

Adipose tissue engineering offers a promising alternative to the current surgical techniques for the treatment of soft tissue defects. It is a challenge to find the appropriate scaffold that not only represents a suitable environment for cells but also allows fabrication of customized tissue constructs, particularly in breast surgery. We investigated two different scaffolds for their potential use in adipose tissue regeneration. Sponge-like polyurethane scaffolds were prepared by mold casting with methylal as foaming agent, whereas polycaprolactone scaffolds with highly regular stacked-fiber architecture were fabricated with fused deposition modeling. Both scaffold types were seeded with human adipose tissue-derived precursor cells, cultured and implanted in nude mice using a femoral arteriovenous flow-through vessel loop for angiogenesis. In vitro, cells attached to both scaffolds and differentiated into adipocytes. In vivo, angiogenesis and adipose tissue formation were observed throughout both constructs after 2 and 4 weeks, with angiogenesis being comparable in seeded and unseeded constructs. Fibrous tissue formation and adipogenesis were more pronounced on polyurethane foam scaffolds than on polycaprolactone prototyped scaffolds. In conclusion, both scaffold designs can be effectively used for adipose tissue engineering.

Keywords

Adipose tissue engineering Polycaprolactone Polyurethane Vessel loop Angiogenesis 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

This work is part of the MD thesis of Paul Wiggenhauser. We thank Professor Dietmar W. Hutmacher for critically reviewing the manuscript and Dr. Hinrich Wiese and Polymaterials AG for generously providing PU foam scaffolds.

References

  1. Borges J, Mueller MC, Padron NT, Tegtmeier F, Lang EM, Stark GB (2003) Engineered adipose tissue supplied by functional microvessels. Tissue Eng 9:1263–1270PubMedCrossRefGoogle Scholar
  2. Campa C, Costagliola C, Incorvaia C, Sheridan C, Semeraro F, De Nadai K, Sebastiani A, Parmeggiani F (2010) Inflammatory mediators and angiogenic factors in choroidal neovascularization: pathogenetic interactions and therapeutic implications. Mediators Inflamm. doi: 10.1155/2010/546826
  3. Carmi Y, Voronov E, Dotan S, Lahat N, Rahat MA, Fogel M, Huszar M, White MR, Dinarello CA, Apte RN (2009) The role of macrophage-derived IL-1 in induction and maintenance of angiogenesis. J Immunol 183:4705–4714PubMedCrossRefGoogle Scholar
  4. Carraro A, Hsu WM, Kulig KM, Cheung WS, Miller ML, Weinberg EJ, Swart EF, Kaazempur-Mofrad M, Borenstein JT, Vacanti JP, Neville C (2008) In vitro analysis of a hepatic device with intrinsic microvascular-based channels. Biomed Microdevices 10:795–805PubMedCrossRefGoogle Scholar
  5. Coleman SR (1997) Facial recontouring with lipostructure. Clin Plast Surg 24:347–367PubMedGoogle Scholar
  6. Cordeiro PG (2008) Breast reconstruction after surgery for breast cancer. N Engl J Med 359:1590–1601PubMedCrossRefGoogle Scholar
  7. Dolderer JH, Abberton KM, Thompson EW, Slavin JL, Stevens GW, Penington AJ, Morrison WA (2007) Spontaneous large volume adipose tissue generation from a vascularized pedicled fat flap inside a chamber space. Tissue Eng 13:673–681PubMedCrossRefGoogle Scholar
  8. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126:677–689PubMedCrossRefGoogle Scholar
  9. Exner K (2003) Kapitel 6: Gewebeexpansion. In: Berger A, Hierner R (eds) Plastische Chirurgie - Grundlagen, Prinzipien, Techniken. Springer, BerlinGoogle Scholar
  10. Eyrich D, Wiese H, Mailer G, Skodacek D, Appel B, Sarhan H, Tessmar J, Staudenmaier R, Wenzel MM, Goepferich A, Blunk T (2007) In vitro and in vivo cartilage engineering using a combination of chondrocyte-seeded long-term stable fibrin gels and polycaprolactone-based polyurethane scaffolds. Tissue Eng 13:2207–2218PubMedCrossRefGoogle Scholar
  11. Fagrell D, Enestrom S, Berggren A, Kniola B (1996) Fat cylinder transplantation: an experimental comparative study of three different kinds of fat transplants. Plast Reconstr Surg 98:90–96, discussion 97–98PubMedCrossRefGoogle Scholar
  12. Flynn P, Wongdagger M, Zavar M, Dean NM, Stokoe D (2000) Inhibition of PDK-1 activity causes a reduction in cell proliferation and survival. Curr Biol 10:1439–1442PubMedCrossRefGoogle Scholar
  13. Gleeson JP, Plunkett NA, O'Brien FJ (2010) Addition of hydroxyapatite improves stiffness, interconnectivity and osteogenic potential of a highly porous collagen-based scaffold for bone tissue regeneration. Eur Cell Mater 20:218–230PubMedGoogle Scholar
  14. Hijjawi JB, Blondeel PN (2010) Advancing deep inferior epigastric artery perforator flap breast reconstruction through multidetector row computed tomography: an evolution in preoperative imaging. J Reconstr Microsurg 26:11–20PubMedCrossRefGoogle Scholar
  15. Hofer SO, Knight KM, Cooper-White JJ, O'Connor AJ, Perera JM, Romeo-Meeuw R, Penington AJ, Knight KR, Morrison WA, Messina A (2003) Increasing the volume of vascularized tissue formation in engineered constructs: an experimental study in rats. Plast Reconstr Surg 111:1186–1192, discussion 1193–1184PubMedCrossRefGoogle Scholar
  16. Kanchwala SK, Glatt BS, Conant EF, Bucky LP (2009) Autologous fat grafting to the reconstructed breast: the management of acquired contour deformities. Plast Reconstr Surg 124:409–418PubMedCrossRefGoogle Scholar
  17. Kang X, Xie Y, Powell HM, James Lee L, Belury MA, Lannutti JJ, Kniss DA (2007) Adipogenesis of murine embryonic stem cells in a three-dimensional culture system using electrospun polymer scaffolds. Biomaterials 28:450–458PubMedCrossRefGoogle Scholar
  18. Klein JA (1990) Tumescent technique for regional anesthesia permits lidocaine doses of 35 mg/kg for liposuction. J Dermatol Surg Oncol 16:248–263PubMedGoogle Scholar
  19. Kononas TC, Bucky LP, Hurley C, May JW Jr (1993) The fate of suctioned and surgically removed fat after reimplantation for soft-tissue augmentation: a volumetric and histologic study in the rabbit. Plast Reconstr Surg 91:763–768PubMedCrossRefGoogle Scholar
  20. Kotch LE, Iyer NV, Laughner E, Semenza GL (1999) Defective vascularization of HIF-1alpha-null embryos is not associated with VEGF deficiency but with mesenchymal cell death. Dev Biol 209:254–267PubMedCrossRefGoogle Scholar
  21. Lam CX, Hutmacher DW, Schantz JT, Woodruff MA, Teoh SH (2009) Evaluation of polycaprolactone scaffold degradation for 6 months in vitro and in vivo. J Biomed Mater Res A 90:906–919PubMedGoogle Scholar
  22. Lokmic Z, Stillaert F, Morrison WA, Thompson EW, Mitchell GM (2007) An arteriovenous loop in a protected space generates a permanent, highly vascular, tissue-engineered construct. FASEB J 21:511–522PubMedCrossRefGoogle Scholar
  23. Macchiarini P, Walles T, Biancosino C, Mertsching H (2004) First human transplantation of a bioengineered airway tissue. J Thorac Cardiovasc Surg 128:638–641PubMedCrossRefGoogle Scholar
  24. McBride SH, Falls T, Knothe Tate ML (2008) Modulation of stem cell shape and fate B: mechanical modulation of cell shape and gene expression. Tissue Eng Part A 14:1573–1580PubMedCrossRefGoogle Scholar
  25. Mertsching H, Walles T, Hofmann M, Schanz J, Knapp WH (2005) Engineering of a vascularized scaffold for artificial tissue and organ generation. Biomaterials 26:6610–6617PubMedCrossRefGoogle Scholar
  26. Morrison WA, Penington AJ, Kumta SK, Callan P (1997) Clinical applications and technical limitations of prefabricated flaps. Plast Reconstr Surg 99:378–385PubMedCrossRefGoogle Scholar
  27. Nguyen A, Pasyk KA, Bouvier TN, Hassett CA, Argenta LC (1990) Comparative study of survival of autologous adipose tissue taken and transplanted by different techniques. Plast Reconstr Surg 85:378–386, discussion 387–379PubMedCrossRefGoogle Scholar
  28. Patrick CW Jr, Chauvin PB, Hobley J, Reece GP (1999) Preadipocyte seeded PLGA scaffolds for adipose tissue engineering. Tissue Eng 5:139–151PubMedCrossRefGoogle Scholar
  29. Presta M, Andres G, Leali D, Dell'Era P, Ronca R (2009) Inflammatory cells and chemokines sustain FGF2-induced angiogenesis. Eur Cytokine Netw 20:39–50PubMedGoogle Scholar
  30. Pugh CW, Ratcliffe PJ (2003) Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med 9:677–684PubMedCrossRefGoogle Scholar
  31. Rozen WM, Rajkomar AK, Anavekar NS, Ashton MW (2009) Post-mastectomy breast reconstruction: a history in evolution. Clin Breast Cancer 9:145–154PubMedCrossRefGoogle Scholar
  32. Sato T, Yamamoto M, Shimosato T, Klinman DM (2010) Accelerated wound healing mediated by activation of Toll-like receptor 9. Wound Repair Regen 18:586–593PubMedCrossRefGoogle Scholar
  33. Schantz J-T, Ng KW (2004) A manual for primary human cell culture. World Scientific, SingaporeGoogle Scholar
  34. Schreml S, Babilas P, Fruth S, Orso E, Schmitz G, Mueller MB, Nerlich M, Prantl L (2009) Harvesting human adipose tissue-derived adult stem cells: resection versus liposuction. Cytotherapy 11:947–957PubMedCrossRefGoogle Scholar
  35. Smahel J (1989) Experimental implantation of adipose tissue fragments. Br J Plast Surg 42:207–211PubMedCrossRefGoogle Scholar
  36. Spanholtz TA, Theodorou P, Holzbach T, Wutzler S, Giunta RE, Machens HG (2010) Vascular Endothelial Growth Factor (VEGF(165)) Plus Basic Fibroblast Growth Factor (bFGF) Producing Cells induce a Mature and Stable Vascular Network-a Future Therapy for Ischemically Challenged Tissue. J Surg Res (in press)Google Scholar
  37. Tachi M, Yamada A (2005) Choice of flaps for breast reconstruction. Int J Clin Oncol 10:289–297PubMedCrossRefGoogle Scholar
  38. Tanaka Y, Sung KC, Tsutsumi A, Ohba S, Ueda K, Morrison WA (2003) Tissue engineering skin flaps: which vascular carrier, arteriovenous shunt loop or arteriovenous bundle, has more potential for angiogenesis and tissue generation? Plast Reconstr Surg 112:1636–1644PubMedCrossRefGoogle Scholar
  39. Tanzi MC, Fare S (2009) Adipose tissue engineering: state of the art, recent advances and innovative approaches. Expert Rev Med Devices 6:533–551PubMedCrossRefGoogle Scholar
  40. Torio-Padron N, Baerlecken N, Momeni A, Stark GB, Borges J (2007) Engineering of adipose tissue by injection of human preadipocytes in fibrin. Aesthetic Plast Surg 31:285–293PubMedCrossRefGoogle Scholar
  41. Van RL, Roncari DA (1977) Isolation of fat cell precursors from adult rat adipose tissue. Cell Tissue Res 181:197–203PubMedGoogle Scholar
  42. Van RL, Roncari DA (1982) Complete differentiation in vivo of implanted cultured adipocyte precursors from adult rats. Cell Tissue Res 225:557–566PubMedGoogle Scholar
  43. von Heimburg D, Zachariah S, Heschel I, Kuhling H, Schoof H, Hafemann B, Pallua N (2001a) Human preadipocytes seeded on freeze-dried collagen scaffolds investigated in vitro and in vivo. Biomaterials 22:429–438CrossRefGoogle Scholar
  44. von Heimburg D, Zachariah S, Low A, Pallua N (2001b) Influence of different biodegradable carriers on the in vivo behavior of human adipose precursor cells. Plast Reconstr Surg 108:411–420, discussion 421–422CrossRefGoogle Scholar
  45. Weiser B, Prantl L, Schubert TE, Zellner J, Fischbach-Teschl C, Spruss T, Seitz AK, Tessmar J, Goepferich A, Blunk T (2008) In vivo development and long-term survival of engineered adipose tissue depend on in vitro precultivation strategy. Tissue Eng Part A 14:275–284PubMedCrossRefGoogle Scholar
  46. Wiese DH, Maier G, inventors; polyMaterials AG, assignee (2005) Open-Pored Polyurethane Foam without Skin formation, Formulation for the Production thereof and Use Thereof as a Carrier Material for Cell and Tissue Cultures or Medicaments. GermanyGoogle Scholar
  47. Wiggenhauser PS, Melchels FPW, Hutmacher DW, Machens HG, Ong FR, Schantz JT (2011) Fabrication of a customized tissue engineering scaffold for breast reconstruction. Histol Histopathol 26(supp 1):23Google Scholar
  48. Woodruff MA, Hutmacher DW (2010) The return of a forgotten polymer - Polycaprolactone in the 21st century. Prog Polym Sci 35:1217–1256CrossRefGoogle Scholar
  49. Yoshimura K, Sato K, Aoi N, Kurita M, Hirohi T, Harii K (2008) Cell-assisted lipotransfer for cosmetic breast augmentation: supportive use of adipose-derived stem/stromal cells. Aesthetic Plast Surg 32:48–55, discussion 56–57PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Paul S. Wiggenhauser
    • 1
  • Daniel F. Müller
    • 1
  • Ferry P. W. Melchels
    • 2
  • José T. Egaña
    • 1
  • Katharina Storck
    • 3
  • Helena Mayer
    • 3
  • Peter Leuthner
    • 3
  • Daniel Skodacek
    • 3
  • Ursula Hopfner
    • 1
  • Hans G. Machens
    • 1
  • Rainer Staudenmaier
    • 3
  • Jan T. Schantz
    • 1
  1. 1.Department for Plastic and Hand Surgery, Klinikum Rechts der IsarTechnische Universität MünchenMunichGermany
  2. 2.Institute of Health and Biomedical InnovationQueensland University of TechnologyKelvin GroveAustralia
  3. 3.Department for Ear-Nose-Throat, Klinikum Rechts der IsarTechnische Universität MünchenMunichGermany

Personalised recommendations