Advertisement

Cytotechnology

, Volume 65, Issue 3, pp 437–445 | Cite as

Harvest site influences the growth properties of adipose derived stem cells

  • Patricia E. Engels
  • Mathias Tremp
  • Paul J. Kingham
  • Pietro G. di Summa
  • René D. Largo
  • Dirk J. Schaefer
  • Daniel F. Kalbermatten
Original Research

Abstract

The therapeutic potential of adult stem cells may become a relevant option in clinical care in the future. In hand and plastic surgery, cell therapy might be used to enhance nerve regeneration and help surgeons and clinicians to repair debilitating nerve injuries. Adipose-derived stem cells (ASCs) are found in abundant quantities and can be harvested with a low morbidity. In order to define the optimal fat harvest location and detect any potential differences in ASC proliferation properties, we compared biopsies from different anatomical sites (inguinal, flank, pericardiac, omentum, neck) in Sprague–Dawley rats. ASCs were expanded from each biopsy and a proliferation assay using different mitogenic factors, basic fibroblast growth factor (bFGF) and platelet-derived growth factor (PDGF) was performed. Our results show that when compared with the pericardiac region, cells isolated from the inguinal, flank, omental and neck regions grow significantly better in growth medium alone. bFGF significantly enhanced the growth rate of ASCs isolated from all regions except the omentum. PDGF had minimal effect on ASC proliferation rate but increases the growth of ASCs from the neck region. Analysis of all the data suggests that ASCs from the neck region may be the ideal stem cell sources for tissue engineering approaches for the regeneration of nervous tissue.

Keywords

Growth factor ASC Proliferation Stem cell Tissue engineering 

Notes

Conflict of interest

No competing financial interests exist.

References

  1. Aguena M, Fanganiello RD, Tissiani LA, Ishiy FA, Atique R, Alonso N, Passos-Bueno MR (2012) Optimization of parameters for a more efficient use of adipose-derived stem cells in regenerative medicine therapies. Stem Cells Int 2012:303610Google Scholar
  2. Bayes-Genis A, Galvez-Monton C, Prat-Vidal C, Soler-Botija C (2012) Cardiac adipose tissue: a new frontier for cardiac regeneration? Int J Cardiol. doi: 10.1016/j.ijcard.2012.05.082
  3. Buhring HJ, Battula VL, Treml S, Schewe B, Kanz L, Vogel W (2007) Novel markers for the prospective isolation of human MSC. Ann N Y Acad Sci 1106:262–271CrossRefGoogle Scholar
  4. Deng J, Petersen BE, Steindler DA, Jorgensen ML, Laywell ED (2006) Mesenchymal stem cells spontaneously express neural proteins in culture and are neurogenic after transplantation. Stem Cells 24:1054–1064CrossRefGoogle Scholar
  5. Dezawa M, Takahashi I, Esaki M, Takano M, Sawada H (2001) Sciatic nerve regeneration in rats induced by transplantation of in vitro differentiated bone-marrow stromal cells. Eur J Neurosci 14:1771–1776CrossRefGoogle Scholar
  6. Dhanasekaran M, Indumathi S, Kanmani A, Poojitha R, Revathy KM, Rajkumar JS, Sudarsanam D (2012) Surface antigenic profiling of stem cells from human omentum fat in comparison with subcutaneous fat and bone marrow. Cytotechnology 5:497–509Google Scholar
  7. di Summa PG, Kingham PJ, Raffoul W, Wiberg M, Terenghi G, Kalbermatten DF (2010) Adipose-derived stem cells enhance peripheral nerve regeneration. J Plast Reconstr Aesthet Surg 63:1544–1552CrossRefGoogle Scholar
  8. Hankemeier S, Keus M, Zeichen J, Jagodzinski M, Barkhausen T, Bosch U, Krettek C, Van Griensven M (2005) Modulation of proliferation and differentiation of human bone marrow stromal cells by fibroblast growth factor 2: potential implications for tissue engineering of tendons and ligaments. Tissue Eng 11:41–49CrossRefGoogle Scholar
  9. Hauner H, Rohrig K, Petruschke T (1995) Effects of epidermal growth factor (EGF), platelet-derived growth factor (PDGF) and fibroblast growth factor (FGF) on human adipocyte development and function. Eur J Clin Investig 25:90–96CrossRefGoogle Scholar
  10. Hausman GJ, Richardson RL (2004) Adipose tissue angiogenesis. J Animal Sci 82:925–934Google Scholar
  11. Helder MN, Knippenberg M, Klein-Nulend J, Wuisman PI (2007) Stem cells from adipose tissue allow challenging new concepts for regenerative medicine. Tissue Eng 13:1799–1808CrossRefGoogle Scholar
  12. Jiang L, Zhu JK, Liu XL, Xiang P, Hu J, Yu WH (2008) Differentiation of rat adipose tissue-derived stem cells into Schwann-like cells in vitro. NeuroReport 19:1015–1019CrossRefGoogle Scholar
  13. Kaewkhaw R, Scutt AM, Haycock JW (2011) Anatomical site influences the differentiation of adipose-derived stem cells for Schwann-cell phenotype and function. Glia 59:734–749CrossRefGoogle Scholar
  14. Kalbermatten DF, Schaakxs D, Kingham PJ, Wiberg M (2011) Neurotrophic activity of human adipose stem cells isolated from deep and superficial layers of abdominal fat. Cell Tissue Res 344:251–260CrossRefGoogle Scholar
  15. Kimura Y, Hokugo A, Takamoto T, Tabata Y, Kurosawa H (2008) Regeneration of anterior cruciate ligament by biodegradable scaffold combined with local controlled release of basic fibroblast growth factor and collagen wrapping. Tissue Eng Part C Methods 14:47–57CrossRefGoogle Scholar
  16. Kingham PJ, Kalbermatten DF, Mahay D, Armstrong SJ, Wiberg M, Terenghi G (2007) Adipose-derived stem cells differentiate into a Schwann cell phenotype and promote neurite outgrowth in vitro. Exp Neurol 207:267–274CrossRefGoogle Scholar
  17. Kitamura M, Akamatsu M, Machigashira M, Hara Y, Sakagami R, Hirofuji T, Hamachi T, Maeda K, Yokota M, Kido J, Nagata T, Kurihara H, Takashiba S, Sibutani T, Fukuda M, Noguchi T, Yamazaki K, Yoshie H, Ioroi K, Arai T, Nakagawa T, Ito K, Oda S, Izumi Y, Ogata Y, Yamada S, Shimauchi H, Kunimatsu K, Kawanami M, Fujii T, Furuichi Y, Furuuchi T, Sasano T, Imai E, Omae M, Yamada S, Watanuki M, Murakami S (2011) FGF-2 stimulates periodontal regeneration: results of a multi-center randomized clinical trial. J Dent Res 90:35–40CrossRefGoogle Scholar
  18. Kohler N, Lipton A (1974) Platelets as a source of fibroblast growth-promoting activity. Exp Cell Res 87:297–301CrossRefGoogle Scholar
  19. Labouyrie E, Dubus P, Groppi A, Mahon FX, Ferrer J, Parrens M, Reiffers J, de Mascarel A, Merlio JP (1999) Expression of neurotrophins and their receptors in human bone marrow. Am J Pathol 154:405–415CrossRefGoogle Scholar
  20. Lattanzi W, Geloso MC, Saulnier N, Giannetti S, Puglisi MA, Corvino V, Gasbarrini A, Michetti F (2011) Neurotrophic features of human adipose tissue-derived stromal cells: in vitro and in vivo studies. J Biomed Biotechnol 2011:468705CrossRefGoogle Scholar
  21. Liang W, Xia H, Li J, Zhao RC (2011) Human adipose tissue derived mesenchymal stem cells are resistant to several chemotherapeutic agents. Cytotechnology 63:523–530CrossRefGoogle Scholar
  22. Lundborg G (2000) A 25-year perspective of peripheral nerve surgery: evolving neuroscientific concepts and clinical significance. J Hand Surg Am 25:391–414CrossRefGoogle Scholar
  23. Lutton C, Young YW, Williams R, Meedeniya AC, Mackay-Sim A, Goss B (2012) Combined VEGF and PDGF treatment reduces secondary degeneration after spinal cord injury. J Neurotrauma 29:957–970CrossRefGoogle Scholar
  24. Martin I, Suetterlin R, Baschong W, Heberer M, Vunjak-Novakovic G, Freed LE (2001) Enhanced cartilage tissue engineering by sequential exposure of chondrocytes to FGF-2 during 2D expansion and BMP-2 during 3D cultivation. J Cell Biochem 83:121–128CrossRefGoogle Scholar
  25. Meyer-Franke A, Wilkinson GA, Kruttgen A, Hu M, Munro E, Hanson MG Jr, Reichardt LF, Barres BA (1998) Depolarization and cAMP elevation rapidly recruit TrkB to the plasma membrane of CNS neurons. Neuron 21:681–693CrossRefGoogle Scholar
  26. Mohamet L, Lea ML, Ward CM (2010) Abrogation of E-cadherin-mediated cellular aggregation allows proliferation of pluripotent mouse embryonic stem cells in shake flask bioreactors. PLoS ONE 5:e12921CrossRefGoogle Scholar
  27. Mohammadi R, Azizi S, Amini K (2012) Effects of undifferentiated cultured omental adipose-derived stem cells on peripheral nerve regeneration. J Surg Res. doi: 10.1016/j.jss.2012.04.011
  28. Morgan L, Jessen KR, Mirsky R (1991) The effects of cAMP on differentiation of cultured Schwann cells: progression from an early phenotype (04+) to a myelin phenotype (P0+, GFAP-, N-CAM-, NGF-receptor-) depends on growth inhibition. J Cell Biol 112:457–467CrossRefGoogle Scholar
  29. Oedayrajsingh-Varma MJ, van Ham SM, Knippenberg M, Helder MN, Klein-Nulend J, Schouten TE, Ritt MJ, van Milligen FJ (2006) Adipose tissue-derived mesenchymal stem cell yield and growth characteristics are affected by the tissue-harvesting procedure. Cytotherapy 8:166–177CrossRefGoogle Scholar
  30. Padoin AV, Braga-Silva J, Martins P, Rezende K, Rezende AR, Grechi B, Gehlen D, Machado DC (2008) Sources of processed lipoaspirate cells: influence of donor site on cell concentration. Plast Reconstr Surg 122:614–618CrossRefGoogle Scholar
  31. Phinney DG, Prockop DJ (2007) Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair–current views. Stem Cells 25:2896–2902CrossRefGoogle Scholar
  32. Prockop DJ (1997) Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276:71–74CrossRefGoogle Scholar
  33. Ross R, Raines EW, Bowen-Pope DF (1986) The biology of platelet-derived growth factor. Cell 46:155–169CrossRefGoogle Scholar
  34. Sato N, Beitz JG, Kato J, Yamamoto M, Clark JW, Calabresi P, Raymond A, Frackelton AR Jr (1993) Platelet-derived growth factor indirectly stimulates angiogenesis in vitro. Am J Pathol 142:1119–1130Google Scholar
  35. Strem BM, Hicok KC, Zhu M, Wulur I, Alfonso Z, Schreiber RE, Fraser JK, Hedrick MH (2005) Multipotential differentiation of adipose tissue-derived stem cells. Keio J Med 54:132–141CrossRefGoogle Scholar
  36. Strioga M, Viswanathan S, Darinskas A, Slaby O, Michalek J (2012) Same or not the same? Comparison of adipose tissue-derived versus bone marrow-derived mesenchymal stem and stromal cells. Stem Cells Dev 21:2724–2752Google Scholar
  37. Tabata Y, Miyao M, Inamoto T, Ishii T, Hirano Y, Yamaoki Y, Ikada Y (2000) De novo formation of adipose tissue by controlled release of basic fibroblast growth factor. Tissue Eng 6:279–289CrossRefGoogle Scholar
  38. Taha MF, Hedayati V (2010) Isolation, identification and multipotential differentiation of mouse adipose tissue-derived stem cells. Tissue Cell 42:211–216CrossRefGoogle Scholar
  39. Tassi E, McDonnell K, Gibby KA, Tilan JU, Kim SE, Kodack DP, Schmidt MO, Sharif GM, Wilcox CS, Welch WJ, Gallicano GI, Johnson MD, Riegel AT, Wellstein A (2011) Impact of fibroblast growth factor-binding protein-1 expression on angiogenesis and wound healing. Am J Pathol 179:2220–2232CrossRefGoogle Scholar
  40. Wislet-Gendebien S, Leprince P, Moonen G, Rogister B (2003) Regulation of neural markers nestin and GFAP expression by cultivated bone marrow stromal cells. J Cell Sci 116:3295–3302CrossRefGoogle Scholar
  41. Witkowska-Zimny M, Walenko K (2011) Stem cells from adipose tissue. Cell Mol Biol Lett 16:236–257CrossRefGoogle Scholar
  42. Wu G, Song Y, Zheng X, Jiang Z (2011) Adipose-derived stromal cell transplantation for treatment of stress urinary incontinence. Tissue Cell 43:246–253CrossRefGoogle Scholar
  43. Yuan Q, Zeng X, Chen L, Peng E, Ye Z (2010) Comparison of myogenic differentiation ability of adipose-derived stem cells from different sites in rabbit. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi 24:1228–1232Google Scholar
  44. Yun YR, Won JE, Jeon E, Lee S, Kang W, Jo H, Jang JH, Shin US, Kim HW (2010) Fibroblast growth factors: biology, function, and application for tissue regeneration. J Tissue Eng 2010:218142Google Scholar
  45. Zhang Y, Wang F, Chen J, Ning Z, Yang L (2012) Bone marrow-derived mesenchymal stem cells versus bone marrow nucleated cells in the treatment of chondral defects. Int Orthop 36:1079–1086CrossRefGoogle Scholar
  46. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, Alfonso ZC, Fraser JK, Benhaim P, Hedrick MH (2002) Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13:4279–4295CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Patricia E. Engels
    • 1
  • Mathias Tremp
    • 1
  • Paul J. Kingham
    • 3
  • Pietro G. di Summa
    • 2
  • René D. Largo
    • 1
  • Dirk J. Schaefer
    • 1
  • Daniel F. Kalbermatten
    • 1
    • 2
  1. 1.Department of Plastic, Reconstructive and Aesthetic Surgery, University Hospital BaselUniversity BaselBaselSwitzerland
  2. 2.Division of Plastic, Reconstructive and Aesthetic SurgeryCHUV, University Hospital of LausanneLausanneSwitzerland
  3. 3.Department of Integrative Medical Biology, Section of AnatomyUmeå UniversityUmeåSweden

Personalised recommendations