Current Stem Cell Reports

, Volume 4, Issue 2, pp 127–137 | Cite as

Therapeutic Applications for Adipose-Derived Stem Cells in Wound Healing and Tissue Engineering

  • Michelle E. McCarthy
  • Theodore A. Brown
  • Joanna Bukowska
  • Bruce A. Bunnell
  • Trivia Frazier
  • Xiying Wu
  • Jeffrey M. Gimble
Artificial Tissues (A Atala and JG Hunsberger, Section Editors)
Part of the following topical collections:
  1. Topical Collection on Artificial Tissues


Purpose of Review

The use of adipose-derived stem cells (ASCs) has garnered recent interest for their accessibility and potential utility in wound healing applications. The purpose of this review is to provide an overview of developments within the last 5 years regarding therapeutic use of ASCs in wound healing applications.

Recent Findings

Recent studies have demonstrated that ASCs do not exert the majority of their effects through differentiation, as previously believed. Rather, when they improve healing, it is via secreted factors that promote vascularization and control inflammation. New therapeutic approaches reflect this shift in belief.


ASC-based therapies can improve outcomes in the treatment of a variety of wound types. Questions about how to best implement ASCs in the clinical setting remain, and their answers will profoundly influence the utility and availability of ASC-based therapies.


Adipose-derived stem cells Cytokine Pressure ulcers Scaffold Skin wound healing Stromal vascular fraction 



The authors wish to thank Dr. Barbara Gawronska-Kozak, the staff of LaCell LLC, and the members of the Center for Stem Cell Research and Regenerative Medicine at Tulane University for their input and discussions during the preparation of this review article.

Author’s contributions

M.E.M., T.A.B., and J.M.G. researched data for the article and wrote the article. M.E.M., T.A.B., J.B., T.F., X.W., B.A.B, and J.M.G. made substantial contributions to discussions of the content and final revision of the manuscript. All authors reviewed and/or edited the manuscript before submission.

Compliance with Ethical Standards

Conflict of Interest

J.M.G. and X.W. are co-founders, co-owners and Chief Scientific Officer and Vice President for Research and Development, respectively, of LaCell LLC, a biotechnology company focusing on the clinical translation of stromal-cell and stem-cell science. J.M.G., X.W., and T.F. are the co-founders and co-owners of Obatala Sciences Inc., a biotechnology company focusing on humanized “fat on a chip” as a product for drug discovery where T.F. serves as the President and Chief Executive Officer.

J.M.G. is an inventor on multiple patents relating to adipose cells and products. X.W is about to submit a patent application from LaCell LLC on the use of adipose cells in therapy.

The other authors declare no competing interests.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.


Papers of particular interest, published recently, have been highlighted as:•  Of importance•• Of major importance

  1. 1.
    Takeo M, Lee W, Ito M. Wound healing and skin regeneration. Cold Spring Harb Perspect Med. 2015;5:a023267.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Singer AJ, Clark RAF. Cutaneous wound healing. N Engl J Med. 1999;341:738–46.CrossRefPubMedGoogle Scholar
  3. 3.
    Almine JF, Wise SG, Weiss AS. Elastin signaling in wound repair. Birth Defects Res Part C - Embryo Today Rev. 2012;96:248–57.CrossRefGoogle Scholar
  4. 4.
    Loder S, Peterson JR, Agarwal S, Eboda O, Brownley C, Delarosa S, et al. Wound healing after thermal injury is improved by fat and adipose-derived stem cell isografts. J Burn Care Res. 2015;36:70–6.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Goel A, Shrivastava P. Post-burn scars and scar contractures. Indian J Plast Surg. 2010;43:63.CrossRefGoogle Scholar
  6. 6.
    Xue M, Jackson CJ. Extracellular matrix reorganization during wound healing and its impact on abnormal scarring. Adv Wound Care. 2015;4:119–36.CrossRefGoogle Scholar
  7. 7.
    Ehrlich HP, Krummel TM. Regulation of wound healing from a connective tissue perspective. Wound Rep Reg. 1996;4:203–10.CrossRefGoogle Scholar
  8. 8.
    Lo DD, Zimmermann AS, Nauta A, Longaker MT, Lorenz HP. Scarless fetal skin wound healing update. Birth Defects Res Part C - Embryo Today Rev. 2012;96:237–47.CrossRefGoogle Scholar
  9. 9.
    Gawronska-Kozak B, Bogacki M, Rim JS, Monroe WT, Manuel JA. Scarless skin repair in immunodeficient mice. Wound Repair Regen. 2006;14:265–76.CrossRefPubMedGoogle Scholar
  10. 10.
    Yates CC, Hebda P, Wells A. Skin wound healing and scarring: fetal wounds and regenerative restitution. Birth Defects Res Part C - Embryo Today Rev. 2012;96:325–33.CrossRefGoogle Scholar
  11. 11.
    Kur-Piotrowska A, Kopcewicz M, Kozak LP, Sachadyn P, Grabowska A, Gawronska-Kozak B. Neotenic phenomenon in gene expression in the skin of Foxn1-deficient (nude) mice -a projection for regenerative skin wound healing. BMC Genomics. 2017;18:56.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Hassan WU, Greiser U, Wang W. Role of adipose-derived stem cells in wound healing. Wound Repair Regen. 2014;22:313–25.CrossRefPubMedGoogle Scholar
  13. 13.
    Frykberg RG, Banks J. Challenges in the treatment of chronic wounds. Adv Wound Care. 2015;4:560–82.CrossRefGoogle Scholar
  14. 14.
    Järbrink K, Ni G, Sönnergren H, Schmidtchen A, Pang C, Bajpai R, et al. The humanistic and economic burden of chronic wounds: a protocol for a systematic review. Syst Rev. 2017;6:15. Scholar
  15. 15.
    Skrepnek GH, Mills JL, Armstrong DG. A diabetic emergency one million feet long: disparities and burdens of illness among diabetic foot ulcer cases within emergency departments in the United States, 2006-2010. PLoS One. 2015;10:e0134914.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Eming SA, Martin P, Tomic-Canic M. Wound repair and regeneration: mechanisms, signaling, and translation. Sci Transl Med. 2014;6:265sr6.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 2001;7:211–28.CrossRefPubMedGoogle Scholar
  18. 18.
    Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284(80):143–7.CrossRefPubMedGoogle Scholar
  19. 19.
    Zuk PA. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell. 2002;13:4279–95.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Tsuji W, Rubin JP, Marra KG. Adipose-derived stem cells: implications in tissue regeneration. World J Stem Cells. 2014;6:312–21.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Toyserkani NM, Christensen ML, Sheikh SP, Sørensen JA. Adipose-derived stem cells: new treatment for wound healing? Ann Plast Surg. 2015;75:117–23.CrossRefPubMedGoogle Scholar
  22. 22.
    van den Broek LJ, Kroeze KL, Waaijman T, Breetveld M, Sampat-Sardjoepersad SC, Niessen FB, et al. Differential response of human adipose tissue-derived mesenchymal stem cells, dermal fibroblasts, and keratinocytes to burn wound exudates: potential role of skin-specific chemokine CCL27. Tissue Eng Part A. 2014;20:197–209.CrossRefPubMedGoogle Scholar
  23. 23.
    Bertozzi N, Simonacci F, Grieco MP, Grignaffini E, Raposio E. The biological and clinical basis for the use of adipose-derived stem cells in the field of wound healing. Ann Med Surg. 2017;20:41–8.CrossRefGoogle Scholar
  24. 24.
    Linero I, Chaparro O. Paracrine effect of mesenchymal stem cells derived from human adipose tissue in bone regeneration. PLoS One. 2014;9:e107001. Scholar
  25. 25.
    Blaber SP, Webster RA, Hill CJ, Breen EJ, Kuah D, Vesey G, et al. Analysis of in vitro secretion profiles from adipose-derived cell populations. J Transl Med. 2012;10:172.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Kuo Y-R, Wang C-T, Cheng J-T, Kao G-S, Chiang Y-C, Wang C-J. Adipose-derived stem cells accelerate diabetic wound healing through the induction of autocrine and paracrine effects. Cell Transplant. 2016;25:71–81.CrossRefPubMedGoogle Scholar
  27. 27.
    Kim WS, Park BS, Sung JH, Yang JM, Park SB, Kwak SJ, et al. Wound healing effect of adipose-derived stem cells: a critical role of secretory factors on human dermal fibroblasts. J Dermatol Sci. 2007;48:15–24.CrossRefPubMedGoogle Scholar
  28. 28.
    Kwon SH, Bhang SH, Jang HK, Rhim T, Kim BS. Conditioned medium of adipose-derived stromal cell culture in three-dimensional bioreactors for enhanced wound healing. J Surg Res. 2015;194:8–17.CrossRefPubMedGoogle Scholar
  29. 29.
    Deng C, He Y, Feng J, Dong Z. Extracellular matrix / stromal vascular fraction gel conditioned medium accelerates wound healing in a murine model. Wound Repair Regen. 2017;25:923–32. Scholar
  30. 30.
    Zhao L, Johnson T, Liu D. Therapeutic angiogenesis of adipose-derived stem cells for ischemic diseases. Stem Cell Res Ther. 2017;8:125.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Su N, Gao PL, Wang K, Wang JY, Zhong Y, Luo Y. Fibrous scaffolds potentiate the paracrine function of mesenchymal stem cells: a new dimension in cell-material interaction. Biomaterials. 2017;141:74–85.CrossRefPubMedGoogle Scholar
  32. 32.
    Dai R, Wang Z, Samanipour R, Koo K-I, Kim K. Adipose-derived stem cells for tissue engineering and regenerative medicine applications. Stem Cells Int. 2016;2016:1–19.Google Scholar
  33. 33.
    Hu L, Wang J, Zhou X, Xiong Z, Zhao J, Yu R, et al. Exosomes derived from human adipose mensenchymal stem cells accelerates cutaneous wound healing via optimizing the characteristics of fibroblasts. Sci Rep. 2016;6:32993.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Wang L, Hu L, Zhou X, Xiong Z, Zhang C, Shehada HMA, et al. Exosomes secreted by human adipose mesenchymal stem cells promote scarless cutaneous repair by regulating extracellular matrix remodelling. Sci Rep. 2017;7:13321.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Hiwatashi N, Hirano S, Mizuta M, Tateya I, Kanemaru SI, Nakamura T, et al. Adipose-derived stem cells versus bone marrow-derived stem cells for vocal fold regeneration. Laryngoscope. 2014;124:E461–9.CrossRefPubMedGoogle Scholar
  36. 36.
    Kokai LE, Marra K, Rubin JP. Adipose stem cells: biology and clinical applications for tissue repair and regeneration. Transl Res. 2014;163:399–408.CrossRefPubMedGoogle Scholar
  37. 37.
    McLaughlin MM, Marra KG. The use of adipose-derived stem cells as sheets for wound healing. Organ. 2013;9:79–81.Google Scholar
  38. 38.
    Koellensperger E, Lampe K, Beierfuss A, Gramley F, Germann G, Leimer U. Intracutaneously injected human adipose tissue-derived stem cells in a mouse model stay at the site of injection. J Plast Reconstr Aesthetic Surg. 2014;67:844–50.CrossRefGoogle Scholar
  39. 39.
    Huang S-MS-P, Huang C-H, Shyu J-F, Lee H-S, Chen S-G, Chan JY-H, et al. Promotion of wound healing using adipose-derived stem cells in radiation ulcer of a rat model. J Biomed Sci. 2013;20:51.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Ucuzian AA, Gassman AA, East AT, Greisler HP. Molecular mediators of angiogenesis. J Burn Care Res. 2010;31:158–75.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Cerqueira MT, Pirraco RP, Marques AP. Stem cells in skin wound healing: are we there yet? Adv Wound Care. 2016;5:164–75.CrossRefGoogle Scholar
  42. 42.
    Mi HM, Sun YK, Yeon JK, Su JK, Jae BL, Yong CB, et al. Human adipose tissue-derived mesenchymal stem cells improve postnatal neovascularization in a mouse model of hindlimb ischemia. Cell Physiol Biochem. 2006;17:279–90.CrossRefGoogle Scholar
  43. 43.
    Simpson RJ, Jensen SS, Lim JWE. Proteomic profiling of exosomes: current perspectives. Proteomics. 2008;8:4083–99.CrossRefPubMedGoogle Scholar
  44. 44.
    Lin R, Wang S, Zhao RC. Exosomes from human adipose-derived mesenchymal stem cells promote migration through Wnt signaling pathway in a breast cancer cell model. Mol Cell Biochem. 2013;383:13–20.CrossRefPubMedGoogle Scholar
  45. 45.
    Kang S, Kim S-M, Sung J-H. Cellular and molecular stimulation of adipose-derived stem cells under hypoxia. Cell Biol Int. 2014;38:553–62.CrossRefPubMedGoogle Scholar
  46. 46.
    Kakudo N, Morimoto N, Ogawa T, Taketani S, Kusumoto K. Hypoxia enhances proliferation of human adipose-derived stem cells via HIF-1α activation. PLoS One. 2015;10:e0139890.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Hsiao ST, Lokmic Z, Peshavariya H, Abberton KM, Dusting GJ, Lim SY, et al. Hypoxic conditioning enhances the Angiogenic paracrine activity of human adipose-derived stem cells. Stem Cells Dev. 2013;22:1614–23.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Markeson D, Pleat JM, Sharpe JR, Harris AL, Seifalian AM, Watt SM. Scarring, stem cells, scaffolds and skin repair. J Tissue Eng Regen Med. 2015;9:649–68.CrossRefPubMedGoogle Scholar
  49. 49.
    Bliley JM, Argenta A, Satish L, McLaughlin MM, Dees A, Tompkins-Rhoades C, et al. Administration of adipose-derived stem cells enhances vascularity, induces collagen deposition, and dermal adipogenesis in burn wounds. Burns. 2016;42:1212–22.CrossRefPubMedGoogle Scholar
  50. 50.
    Strong AL, Bowles AC, MacCrimmon CP, Frazier TP, Lee SJ, Wu X, et al. Adipose stromal cells repair pressure ulcers in both young and elderly mice: potential role of Adipogenesis in skin repair. Stem Cells Transl Med. 2015;4:632–42.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Park IS, Chung PS, Ahn JC. Enhanced angiogenic effect of adipose-derived stromal cell spheroid with low-level light therapy in hind limb ischemia mice. Biomaterials. 2014;35:9280–9.CrossRefPubMedGoogle Scholar
  52. 52.
    Sun M, He Y, Zhou T, Zhang P, Gao J, Lu F. Adipose extracellular matrix/stromal vascular fraction gel secretes Angiogenic factors and enhances skin wound healing in a murine model. Biomed Res Int. 2017;2017:1–11.Google Scholar
  53. 53.
    Feng J, Mineda K, Wu SH, Mashiko T, Doi K, Kuno S, et al. An injectable non-cross-linked hyaluronic-acid gel containing therapeutic spheroids of human adipose-derived stem cells. Sci Rep. 2017;7:1548.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Gentile P, Scioli MG, Bielli A, Orlandi A, Cervelli V. Concise review: the use of adipose-derived stromal vascular fraction cells and platelet rich plasma in regenerative plastic surgery. Stem Cells. 2017;35:117–34.CrossRefPubMedGoogle Scholar
  55. 55.
    Matsumoto D, Sato K, Gonda K, Takaki Y, Shigeura T, Sato T, et al. Cell-assisted Lipotransfer: supportive use of human adipose-derived cells for soft tissue augmentation with Lipoinjection. Tissue Eng. 2006;12:3375–82.CrossRefPubMedGoogle Scholar
  56. 56.
    Zielins ER, Brett EA, Longaker MT, Wan DC. Autologous fat grafting: the science behind the surgery. Aesthetic Surg J. 2016;36:488–96.CrossRefGoogle Scholar
  57. 57.
    Kølle SFT, Fischer-Nielsen A, Mathiasen AB, Elberg JJ, Oliveri RS, Glovinski PV, et al. Enrichment of autologous fat grafts with ex-vivo expanded adipose tissue-derived stem cells for graft survival: a randomised placebo-controlled trial. Lancet. 2013;382:1113–20.CrossRefPubMedGoogle Scholar
  58. 58.
    Gentile P, Orlandi A, Scioli MG, Di Pasquali C, Bocchini I, Curcio CB, et al. A comparative translational study: the combined use of enhanced stromal vascular fraction and platelet-rich plasma improves fat grafting maintenance in breast reconstruction. Stem Cells Transl Med. 2012;1:341–51.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Gentile P, De Angelis B, Pasin M, et al. Adipose-derived stromal vascular fraction cells and platelet-rich plasma: basic and clinical evaluation for cell-based therapies in patients with scars on the face. J Craniofac Surg. 2014;25:267–72.CrossRefPubMedGoogle Scholar
  60. 60.
    Rigotti G, Charles-De-Sá L, Gontijo-De-Amorim NF, Takiya CM, Amable PR, Borojevic R, et al. Expanded stem cells, stromal-vascular fraction, and platelet-rich plasma enriched fat: comparing results of different facial rejuvenation approaches in a clinical trial. Aesthetic Surg J. 2016;36:261–70.CrossRefGoogle Scholar
  61. 61.
    Sasaki GH. The safety and efficacy of cell-assisted fat grafting to traditional fat grafting in the anterior mid-face: an indirect assessment by 3D imaging. Aesthet Plast Surg. 2015;39:833–46.CrossRefGoogle Scholar
  62. 62.
    Lee HC, An SG, Lee HW, Park JS, Cha KS, Hong TJ, et al. Safety and effect of adipose tissue-derived stem cell implantation in patients with critical limb ischemia: a pilot study. Circ J. 2012;76:1750–60.CrossRefPubMedGoogle Scholar
  63. 63.
    Bura A, Planat-Benard V, Bourin P, Silvestre JS, Gross F, Grolleau JL, et al. Phase I trial: the use of autologous cultured adipose-derived stroma/stem cells to treat patients with non-revascularizable critical limb ischemia. Cytotherapy. 2014;16:245–57.CrossRefPubMedGoogle Scholar
  64. 64.
    Carstens MH, Gómez A, Cortés R, Turner E, Pérez C, Ocon M, et al. Non-reconstructable peripheral vascular disease of the lower extremity in ten patients treated with adipose-derived stromal vascular fraction cells. Stem Cell Res. 2017;18:14–21.CrossRefPubMedGoogle Scholar
  65. 65.
    Rheinwatd JG, Green H. Seria cultivation of strains of human epidemal keratinocytes: the formation keratinizin colonies from single cell is. Cell. 1975;6:331–43.CrossRefGoogle Scholar
  66. 66.
    Green H, Kehinde O, Thomas J. Growth of cultured human epidermal cells into multiple epithelia suitable for grafting. Proc Natl Acad Sci U S A. 1979;76:5665–8.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Souza CMCO, Mesquita LAF, Souza D, Irioda AC, Francisco JC, Souza CF, et al. Regeneration of skin tissue promoted by mesenchymal stem cells seeded in nanostructured membrane. Transplant Proc Elsevier. 2014;46:1882–6.CrossRefGoogle Scholar
  68. 68.
    •• Minjuan W, Jun X, Shiyun S, Sha X, Haitao N, Yue W, Kaihong J (2016) Hair follicle morphogenesis in the treatment of mouse full-thickness skin defects using composite human acellular amniotic membrane and adipose derived mesenchymal stem cells. Stem Cells Int 2016;2016:1–7. Dermagrafts used clinically currently lack complex tissue structures, such as hair follicles and sweat glands. This study found that adipose-derived MSCs were capable of differentiating into hair follicle-like structures. Google Scholar
  69. 69.
    • Kato Y, Iwata T, Morikawa S, Yamato M, Okano T, Uchigata Y. Allogeneic transplantation of an adipose-derived stem cell sheet combined with artificial skin accelerates wound healing in a rat wound model of type 2 diabetes and obesity. Diabetes. 2015;64:2723–34. Study demonstrated that allogeneic ASCs accelerated wound healing in diabetic foot ulcers through both direct and indirect actions CrossRefPubMedGoogle Scholar
  70. 70.
    Flynn LE. The use of decellularized adipose tissue to provide an inductive microenvironment for the adipogenic differentiation of human adipose-derived stem cells. Biomaterials. 2010;31:4715–24.CrossRefPubMedGoogle Scholar
  71. 71.
    Huang SPSMMSP, Hsu CCC, Chang SCC, Wang CHH, Deng SCC, Dai NTT, et al. Adipose-derived stem cells seeded on acellular dermal matrix grafts enhance wound healing in a murine model of a full-thickness defect. Ann Plast Surg. 2012;69:656–62.CrossRefPubMedGoogle Scholar
  72. 72.
    Nie C, Zhang G, Yang D, Liu T, Liu D, Xu J, et al. Targeted delivery of adipose-derived stem cells via acellular dermal matrix enhances wound repair in diabetic rats. J Tissue Eng Regen Med. 2015;9:224–35.CrossRefPubMedGoogle Scholar
  73. 73.
    Adams WP, Toriumi DM, Van Natta BW. Clinical use of GalaFLEX in facial and breast cosmetic plastic surgery. Aesthetic Surg J. 2016;36:S23–32.CrossRefGoogle Scholar
  74. 74.
    Lequeux C, Rodriguez J, Boucher F, Rouyer O, Damour O, Mojallal A, et al. In vitro and in vivo biocompatibility, bioavailability and tolerance of an injectable vehicle for adipose-derived stem/stromal cells for plastic surgery indications. J Plast Reconstr Aesthetic Surg. 2015;68:1491–7.CrossRefGoogle Scholar
  75. 75.
    Jin USS, Hong KYY, il HY-I. Effect of adipose-derived stem cells on acellular dermal matrix engraftment in a rabbit model of breast reconstruction. J Plast Reconstr Aesthetic Surg. 2017;70:806–13.CrossRefGoogle Scholar
  76. 76.
    Lin YC, Grahovac T, Oh SJ, Ieraci M, Rubin JP, Marra KG. Evaluation of a multi-layer adipose-derived stem cell sheet in a full-thickness wound healing model. Acta Biomater. 2013;9:5243–50.CrossRefPubMedGoogle Scholar
  77. 77.
    Kim YM, Oh SH, Choi JS, Lee S, Ra JC, Lee JH, et al. Adipose-derived stem cell-containing hyaluronic acid/alginate hydrogel improves vocal fold wound healing. Laryngoscope. 2014;124:64–72.CrossRefGoogle Scholar
  78. 78.
    Xu W, Hu R, Fan E, Han D. Adipose-derived mesenchymal stem cells in collagen-hyaluronic acid gel composite scaffolds for vocal fold regeneration. Ann Otol Rhinol Laryngol. 2011;120:123–30.CrossRefPubMedGoogle Scholar
  79. 79.
    Hu R, Ling W, Xu W, Han D. Fibroblast-like cells differentiated from adipose-derived mesenchymal stem cells for vocal fold wound healing. PLoS One. 2014;9:e92676.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Garg RK, Rennert RC, Duscher D, Sorkin M, Kosaraju R, Auerbach LJ, et al. Capillary force seeding of hydrogels for adipose-derived stem cell delivery in wounds. Stem Cells Transl Med. 2014;3:1079–89.CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Zonari A, Martins TMM, Paula ACC, Boeloni JN, Novikoff S, Marques AP, et al. Polyhydroxybutyrate-co-hydroxyvalerate structures loaded with adipose stem cells promote skin healing with reduced scarring. Acta Biomater. 2015;17:170–81.CrossRefPubMedGoogle Scholar
  82. 82.
    Lam MT, Nauta A, Meyer NP, Wu JC, Longaker MT. Effective delivery of stem cells using an extracellular matrix patch results in increased cell survival and proliferation and reduced scarring in skin wound healing. Tissue Eng Part A. 2013;19:738–47.CrossRefPubMedGoogle Scholar
  83. 83.
    Wang L, Johnson JA, Zhang Q, Beahm EK. Combining decellularized human adipose tissue extracellular matrix and adipose-derived stem cells for adipose tissue engineering. Acta Biomater. 2013;9:8921–31.CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Bayati V, Abbaspour MRR, Dehbashi FNN, Neisi N, Hashemitabar M. A dermal equivalent developed from adipose-derived stem cells and electrospun polycaprolactone matrix: an in vitro and in vivo study. Anat Sci Int. 2017;92:509–20.CrossRefPubMedGoogle Scholar
  85. 85.
    Wang JQ, Fan J, Gao JH, Zhang C, Bai SL. Comparison of in vivo adipogenic capabilities of two different extracellular matrix microparticle scaffolds. Plast Reconstr Surg. 2013;131:174e–87e.CrossRefPubMedGoogle Scholar
  86. 86.
    Kato Y, Iwata T, Washio K, Yoshida T, Kuroda H, Morikawa S, et al. Creation and transplantation of an Adipose-derived Stem Cell (ASC) sheet in a diabetic wound-healing model. J Vis Exp. 2017.
  87. 87.
    Fuentes-Julián S, Arnalich-Montiel F, Jaumandreu L, Leal M, Casado A, García-Tuñon I, et al. Adipose-derived mesenchymal stem cell administration does not improve corneal graft survival outcome. PLoS One. 2015;10:e0117945.CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Wu W, Niklason L, Steinbacher DM. The effect of age on human adipose-derived stem cells. Plast Reconstr Surg. 2013;131:27–37.CrossRefPubMedGoogle Scholar
  89. 89.
    Alt EU, Senst C, Murthy SN, Slakey DP, Dupin CL, Chaffin AE, et al. Aging alters tissue resident mesenchymal stem cell properties. Stem Cell Res. 2012;8:215–25.CrossRefPubMedGoogle Scholar
  90. 90.
    Duscher D, Rennert RC, Januszyk M, et al. Aging disrupts cell subpopulation dynamics and diminishes the function of mesenchymal stem cells. Sci Rep. 2014;4:7144.CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Cronk SM, Kelly-Goss MR, Ray HC, Mendel TA, Hoehn KL, Bruce AC, et al. Adipose-derived stem cells from diabetic mice show impaired vascular stabilization in a murine model of diabetic retinopathy. Stem Cells Transl Med. 2015;4:459–67.CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Chiu Y-J, Yang J-S, Hsu H-S, Tsai C-H, Ma H. Adipose-derived stem cell conditioned medium attenuates cisplatin-triggered apoptosis in tongue squamous cell carcinoma. Oncol Rep. 2018;39:651–8.PubMedGoogle Scholar
  93. 93.
    Harris WM, Zhang P, Plastini M, Ortiz T, Kappy N, Benites J, et al. Evaluation of function and recovery of adipose-derived stem cells after exposure to paclitaxel. Cytotherapy. 2017;19:211–21.CrossRefPubMedGoogle Scholar
  94. 94.
    Gong JH, Dong JY, Xie T, Lu SL. The influence of AGEs environment on proliferation, apoptosis, homeostasis, and endothelial cell differentiation of human adipose stem cells. Int J Low Extrem Wounds. 2017;16:94–103.CrossRefPubMedGoogle Scholar
  95. 95.
    Lopez MJ, McIntosh KR, Spencer ND, Borneman JN, Horswell R, Anderson P, et al. Acceleration of spinal fusion using syngeneic and allogeneic adult adipose derived stem cells in a rat model. J Orthop Res. 2009;27:366–73.CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    McIntosh KR, Lopez MJ, Borneman JN, Spencer ND, Anderson PA, Gimble JM. Immunogenicity of allogeneic adipose-derived stem cells in a rat spinal fusion model. Tissue Eng Part A. 2009;15:2677–86.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Michelle E. McCarthy
    • 1
  • Theodore A. Brown
    • 1
  • Joanna Bukowska
    • 1
    • 2
  • Bruce A. Bunnell
    • 1
    • 3
    • 4
  • Trivia Frazier
    • 5
    • 8
  • Xiying Wu
    • 8
  • Jeffrey M. Gimble
    • 1
    • 5
    • 6
    • 7
    • 8
  1. 1.Center for Stem Cell Research and Regenerative MedicineTulane UniversityNew OrleansUSA
  2. 2.Polish Academy of ScienceOlsztynPoland
  3. 3.Department of PharmacologyTulane UniversityNew OrleansUSA
  4. 4.Tulane National Primate Research CenterTulane UniversityNew OrleansUSA
  5. 5.Department of Structural and Cell BiologyTulane UniversityNew OrleansUSA
  6. 6.Department of MedicineTulane UniversityNew OrleansUSA
  7. 7.Department of SurgeryTulane UniversityNew OrleansUSA
  8. 8.LaCell LLC and Obatala Sciences Inc.New OrleansUSA

Personalised recommendations