Clinical and preclinical translation of cell-based therapies using adipose tissue-derived cells

Jeffrey M Gimble, Farshid Guilak, Bruce A Bunnell, Jeffrey M Gimble, Farshid Guilak, Bruce A Bunnell

Abstract

Adipose tissue is now recognized as an accessible, abundant, and reliable site for the isolation of adult stem cells suitable for tissue engineering and regenerative medicine applications. The past decade has witnessed an explosion of preclinical data relating to the isolation, characterization, cryopreservation, differentiation, and transplantation of freshly isolated stromal vascular fraction cells and adherent, culture-expanded, adipose-derived stromal/stem cells in vitro and in animal models. This body of work has provided evidence supporting clinical translational applications of adipose-derived cells in safety and efficacy trials. The present article reviews the case reports and phase I-III clinical evidence using autologous adipose-derived cells that have been published, to date, in the fields of gastroenterology, neurology, orthopedics, reconstructive surgery, and related clinical disciplines. Future directions and challenges facing the field are discussed and evaluated.

References

    1. Gimble J, Guilak F. Adipose-derived adult stem cells: isolation, characterization, and differentiation potential. Cytotherapy. 2003;5:362–369. doi: 10.1080/14653240310003026.
    1. Gimble JM, Katz AJ, Bunnell BA. Adipose-derived stem cells for regenerative medicine. Circ Res. 2007;100:1249–1260. doi: 10.1161/01.RES.0000265074.83288.09.
    1. Gimble JM, Guilak F, Nutall ME, Sathishkumar S, Vidal MA, Bunnell BA. In vitro differentiation potential of mesenchymal stem cells. Transfus Med Hemother. 2008;35:228–238. doi: 10.1159/000124281.
    1. Locke M, Windsor J, Dunbar PR. Human adipose-derived stem cells: isolation, characterization and applications in surgery. ANZ J Surg. 2009;79:235–244. doi: 10.1111/j.1445-2197.2009.04852.x.
    1. Food and Drug Administration.
    1. European Medicines Agency.
    1. Lin K, Matsubara Y, Masuda Y, Togashi K, Ohno T, Tamura T, Toyoshima Y, Sugimachi K, Toyoda M, Marc H, Douglas A. Characterization of adipose tissue-derived cells isolated with the Celution system. Cytotherapy. 2008;10:417–426. doi: 10.1080/14653240801982979.
    1. Zhu M, Zhou Z, Chen Y, Schreiber R, Ransom JT, Fraser JK, Hedrick MH, Pinkernell K, Kuo HC. Supplementation of fat grafts with adipose-derived regenerative cells improves long-term graft retention. Ann Plast Surg. 2010;64:222–228. doi: 10.1097/SAP.0b013e31819ae05c.
    1. Matsumoto D, Sato K, Gonda K, Takaki Y, Shigeura T, Sato T, Aiba-Kojima E, Iizuka F, Inoue I, Suga H, Yoshimura K. Cell-assisted lipotransfer (CAL): supportive use of human adipose-derived cells for soft tissue augmentation with lipoinjection. Tissue Eng. 2006;12:3375–3382. doi: 10.1089/ten.2006.12.3375.
    1. Yoshimura K, Sato K, Aoi N, Kurita M, Inoue K, Suga H, Eto H, Kato H, Hirohi T, Harii K. Cell-assisted lipotransfer for cosmetic breast augmentation: supportive use of adipose-derived stem/stromal cells. Aesthetic Plast Surg. 2008;32:48–55. doi: 10.1007/s00266-007-9019-4. discussion 56-57.
    1. Yoshimura K, Asano Y, Aoi N, Kurita M, Oshima Y, Sato K, Inoue K, Suga H, Eto H, Kato H, Harii K. Progenitor-enriched adipose tissue transplantation as rescue for breast implant complications. Breast J. 2010;16:169–175. doi: 10.1111/j.1524-4741.2009.00873.x.
    1. Kim MH, Kim I, Kim SH, Jung MK, Han S, Lee JE, Nam JS, Lee SK, Bang SI. Cryopreserved human adipogenic-differentiated pre-adipocytes: a potential new source for adipose tissue regeneration. Cytotherapy. 2007;9:468–476. doi: 10.1080/14653240701358452.
    1. Mojallal A, Saint-Cyr M, Garrido I. Autologous fat transfer: controversies and current indications for breast surgery. J Plast Reconstr Aesthet Surg. 2009;62:708–710. doi: 10.1016/j.bjps.2009.01.037.
    1. McIntosh K, Zvonic S, Garrett S, Mitchell JB, Floyd ZE, Hammill L, Kloster A, Di Halvorsen Y, Ting JP, Storms RW, Goh B, Kilroy G, Wu X, Gimble JM. The immunogenicity of human adipose derived cells: temporal changes in vitro. Stem Cells. 2006;24:1245–1253. doi: 10.1634/stemcells.2005-0235.
    1. Cui L, Yin S, Liu W, Li N, Zhang W, Cao Y. Expanded adipose-derived stem cells suppress mixed lymphocyte reaction by secretion of prostaglandin E2. Tissue Eng. 2007;13:1185–1195. doi: 10.1089/ten.2006.0315.
    1. Puissant B, Barreau C, Bourin P, Clavel C, Corre J, Bousquet C, Taureau C, Cousin B, Abbal M, Laharrague P, Penicaud L, Casteilla L, Blancher A. Immunomodulatory effect of human adipose tissue-derived adult stem cells: comparison with bone marrow mesenchymal stem cells. Br J Haematol. 2005;129:118–129. doi: 10.1111/j.1365-2141.2005.05409.x.
    1. Xu F, Gomillion C, Maxson S, Burg KJ. In vitro interaction between mouse breast cancer cells and mouse mesenchymal stem cells during adipocyte differentiation. J Tissue Eng Regen Med. 2009;3:338–347. doi: 10.1002/term.158.
    1. Rigotti G, Marchi A, Galiè M, Baroni G, Benati D, Krampera M, Pasini A, Sbarbati A. Clinical treatment of radiotherapy tissue damage by lipoaspirate transplant: a healing process mediated by adipose-derived adult stem cells. Plast Reconstr Surg. 2007;119:1409–1422. doi: 10.1097/01.prs.0000256047.47909.71. discussion 1423-1424.
    1. Billings E Jr, May JW Jr. Historical review and present status of free fat graftautotransplantation in plastic and reconstructive surgery. Plast Reconstr Surg. 1989;83:368–381. doi: 10.1097/00006534-198902000-00033.
    1. Ellenbogen R. Free autogenous pearl fat grafts in the face - a preliminary report of a rediscovered technique. Ann Plast Surg. 1986;16:179–194. doi: 10.1097/00000637-198603000-00001.
    1. Yoshimura K, Sato K, Aoi N, Kurita M, Inoue K, Suga H, Eto H, Kato H, Hirohi T, Harii K. Cell-assisted lipotransfer for facial lipoatrophy: efficacy of clinical use of adipose-derived stem cells. Dermatol Surg. 2008;34:1178–1185. doi: 10.1111/j.1524-4725.2008.34256.x.
    1. Gimble JM. The function of adipocytes in the bone marrow stroma. New Biol. 1990;2:304–312.
    1. Gimble JM, Robinson CE, Wu X, Kelly KA. The function of adipocytes in the bone marrow stroma: an update. Bone. 1996;19:421–428. doi: 10.1016/S8756-3282(96)00258-X.
    1. Gimble JM, Zvonic S, Floyd ZE, Kassem M, Nuttall ME. Playing with bone and fat. J Cell Biochem. 2006;98:251–266. doi: 10.1002/jcb.20777.
    1. Mesimäki K, Lindroos B, Törnwall J, Mauno J, Lindqvist C, Kontio R, Miettinen S, Suuronen R. Novel maxillary reconstruction with ectopic bone formation by GMP adipose stem cells. Int J Oral Maxillofac Surg. 2009;38:201–209. doi: 10.1016/j.ijom.2009.01.001.
    1. Lendeckel S, Jödicke A, Christophis P, Heidinger K, Wolff J, Fraser JK, Hedrick MH, Berthold L, Howaldt HP. Autologous stem cells (adipose) and fibrin glue used to treat widespread traumatic calvarial defects: case report. J Craniomaxillofac Surg. 2004;32:370–373.
    1. García-Olmo D, García-Arranz M, García LG, Cuellar ES, Blanco IF, Prianes LA, Montes JA, Pinto FL, Marcos DH, García-Sancho L. Autologous stem cell transplantation for treatment of rectovaginal fistula in perianal Crohn's disease: a new cell-based therapy. Int J Colorectal Dis. 2003;18:451–454. doi: 10.1007/s00384-003-0490-3.
    1. Garcia-Olmo D, Garcia-Arranz M, Herreros D. Expanded adipose-derived stem cells for the treatment of complex perianal fistula including Crohn's disease. Expert Opin Biol Ther. 2008;8:1417–1423. doi: 10.1517/14712598.8.9.1417.
    1. García-Olmo D, García-Arranz M, Herreros D, Pascual I, Peiro C, Rodríguez-Montes JA. A phase I clinical trial of the treatment of Crohn's fistula by adipose mesenchymal stem cell transplantation. Dis Colon Rectum. 2005;48:1416–1423. doi: 10.1007/s10350-005-0052-6.
    1. Garcia-Olmo D, Herreros D, Pascual I, Pascual JA, Del-Valle E, Zorrilla J, De-La-Quintana P, Garcia-Arranz M, Pascual M. Expanded adipose-derived stem cells for the treatment of complex perianal fistula: a phase II clinical trial. Dis Colon Rectum. 2009;52:79–86.
    1. Garcia-Olmo D, Herreros D, Pascual M, Pascual I, De-La-Quintana P, Trebol J, Garcia-Arranz M. Treatment of enterocutaneous fistula in Crohn's disease with adipose-derived stem cells: a comparison of protocols with and without cell expansion. Int J Colorectal Dis. 2009;24:27–30. doi: 10.1007/s00384-008-0559-0.
    1. Taxonera C, Schwartz DA, Garcia-Olmo D. Emerging treatments for complex perianal fistula in Crohn's disease. World J Gastroenterol. 2009;15:4263–4272. doi: 10.3748/wjg.15.4263.
    1. Constantin G, Marconi S, Rossi B, Angiari S, Calderan L, Anghileri E, Gini B, Bach SD, Martinello M, Bifari F, Galiè M, Turano E, Budui S, Sbarbati A, Krampera M, Bonetti B. Adipose-derived mesenchymal stem cells ameliorate chronic experimental autoimmune encephalomyelitis. Stem Cells. 2009;27:2624–2635. doi: 10.1002/stem.194.
    1. Riordan NH, Ichim TE, Min WP, Wang H, Solano F, Lara F, Alfaro M, Rodriguez JP, Harman RJ, Patel AN, Murphy MP, Lee RR, Minev B. Non-expanded adipose stromal vascular fraction cell therapy for multiple sclerosis. J Transl Med. 2009;7:29. doi: 10.1186/1479-5876-7-29.
    1. Miranville A, Heeschen C, Sengenès C, Curat CA, Busse R, Bouloumié A. Improvement of postnatal neovascularization by human adipose tissuederived stem cells. Circulation. 2004;110:349–355. doi: 10.1161/01.CIR.0000135466.16823.D0.
    1. Planat-Benard V, Silvestre JS, Cousin B, André M, Nibbelink M, Tamarat R, Clergue M, Manneville C, Saillan-Barreau C, Duriez M, Tedgui A, Levy B, Pénicaud L, Casteilla L. Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives. Circulation. 2004;109:656–663. doi: 10.1161/01.CIR.0000114522.38265.61.
    1. Rehman J, Traktuev D, Li J, Merfeld-Clauss S, Temm-Grove CJ, Bovenkerk JE, Pell CL, Johnstone BH, Considine RV, March KL. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation. 2004;109:1292–1298. doi: 10.1161/01.CIR.0000121425.42966.F1.
    1. Nakagami H, Maeda K, Morishita R, Iguchi S, Nishikawa T, Takami Y, Kikuchi Y, Saito Y, Tamai K, Ogihara T, Kaneda Y. Novel autologous cell therapy in ischemic limb disease through growth factor secretion by cultured adipose tissue-derived stromal cells. Arterioscler Thromb Vasc Biol. 2005;25:2542–2547. doi: 10.1161/01.ATV.0000190701.92007.6d.
    1. Nakagami H, Morishita R, Maeda K, Kikuchi Y, Ogihara T, Kaneda Y. Adipose tissue-derived stromal cells as a novel option for regenerative cell therapy. J Atheroscler Thromb. 2006;13:77–81.
    1. Bhang SH, Cho SW, Lim JM, Kang JM, Lee TJ, Yang HS, Song YS, Park MH, Kim HS, Yoo KJ, Jang Y, Langer R, Anderson DG, Kim BS. Locally delivered growth factor enhances the angiogenic efficacy of adipose-derived stromal cells transplanted to ischemic limbs. Stem Cells. 2009;27:1976–1986. doi: 10.1002/stem.115.
    1. Moon MH, Kim SY, Kim YJ, Kim SJ, Lee JB, Bae YC, Sung SM, Jung JS. Human adipose tissue-derived mesenchymal stem cells improve postnatal neovascularization in a mouse model of hindlimb ischemia. Cell Physiol Biochem. 2006;17:279–290. doi: 10.1159/000094140.
    1. Cai L, Johnstone BH, Cook TG, Tan J, Fishbein MC, Chen PS, March KL. IFATS collection: human adipose tissue-derived stem cells induce angiogenesis and nerve sprouting following myocardial infarction, in conjunction with potent preservation of cardiac function. Stem Cells. 2009;27:230–237. doi: 10.1634/stemcells.2008-0273.
    1. Bai X, Yan Y, Song YH, Seidensticker M, Rabinovich B, Metzele R, Bankson JA, Vykoukal D, Alt E. Both cultured and freshly isolated adipose tissue-derived stem cells enhance cardiac function after acute myocardial infarction. Eur Heart J. pp. 489–501.
    1. Kim JM, Lee ST, Chu K, Jung KH, Song EC, Kim SJ, Sinn DI, Kim JH, Park DK, Kang KM, Hyung Hong N, Park HK, Won CH, Kim KH, Kim M, Kun Lee S, Roh JK. Systemic transplantation of human adipose stem cells attenuated cerebral inflammation and degeneration in a hemorrhagic stroke model. Brain Res. 2007;1183:43–50. doi: 10.1016/j.brainres.2007.09.005.
    1. Kim Y, Kim H, Cho H, Bae Y, Suh K, Jung J. Direct comparison of human mesenchymal stem cells derived from adipose tissues and bone marrow in mediating neovascularization in response to vascular ischemia. Cell Physiol Biochem. 2007;20:867–876. doi: 10.1159/000110447.
    1. Kang SK, Lee DH, Bae YC, Kim HK, Baik SY, Jung JS. Improvement of neurological deficits by intracerebral transplantation of human adipose tissue-derived stromal cells after cerebral ischemia in rats. Exp Neurol. 2003;183:355–366. doi: 10.1016/S0014-4886(03)00089-X.
    1. Kang SK, Shin MJ, Jung JS, Kim YG, Kim CH. Autologous adipose tissuederived stromal cells for treatment of spinal cord injury. Stem Cells Dev. 2006;15:583–594. doi: 10.1089/scd.2006.15.583.
    1. Tran TT, Kahn CR. Transplantation of adipose tissue and stem cells: role in metabolism and disease. Nat Rev Endocrinol. pp. 195–213.
    1. Trivedi HL, Vanikar AV, Thakker U, Firoze A, Dave SD, Patel CN, Patel JV, Bhargava AB, Shankar V. Human adipose tissue-derived mesenchymal stem cells combined with hematopoietic stem cell transplantation synthesize insulin. Transplant Proc. 2008;40:1135–1139. doi: 10.1016/j.transproceed.2008.03.113.
    1. Rubio D, Garcia-Castro J, Martín MC, de la Fuente R, Cigudosa JC, Lloyd AC, Bernad A. Spontaneous human adult stem cell transformation. Cancer Res. 2005;65:3035–3039.
    1. Halberstadt C, Austin C, Rowley J, Culberson C, Loebsack A, Wyatt S, Coleman S, Blacksten L, Burg K, Mooney D, Holder W Jr. A hydrogel material for plastic and reconstructive applications injected into the subcutaneous space of a sheep. Tissue Eng. 2002;8:309–319. doi: 10.1089/107632702753725067.
    1. Patrick CW Jr, Chauvin PB, Hobley J, Reece GP. Preadipocyte seeded PLGA scaffolds for adipose tissue engineering. Tissue Eng. 1999;5:139–151. doi: 10.1089/ten.1999.5.139.
    1. Patrick CW Jr, Wu X. Integrin-mediated preadipocyte adhesion and migration on laminin-1. Ann Biomed Eng. 2003;31:505–514. doi: 10.1114/1.1566446.
    1. Patrick CW Jr, Zheng B, Johnston C, Reece GP. Long-term implantation of preadipocyte-seeded PLGA scaffolds. Tissue Eng. 2002;8:283–293. doi: 10.1089/107632702753725049.
    1. 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. doi: 10.1073/pnas.95.3.1062.
    1. Mauney JR, Nguyen T, Gillen K, Kirker-Head C, Gimble JM, Kaplan DL. Engineering adipose-like tissue in vitro and in vivo utilizing human bone marrow and adipose-derived mesenchymal stem cells with silk fibroin 3D scaffolds. Biomaterials. 2007;28:5280–5290. doi: 10.1016/j.biomaterials.2007.08.017.
    1. Tabata Y, Miyao M, Inamoto T, Ishii T, Hirano Y, Yamaoki Y, Ikada Y. De novo formation of adipose tissue by controlled release of basic fibroblast growth factor. Tissue Eng. 2000;6:279–289. doi: 10.1089/10763270050044452.
    1. Toriyama K, Kawaguchi N, Kitoh J, Tajima R, Inou K, Kitagawa Y, Torii S. Endogenous adipocyte precursor cells for regenerative soft-tissue engineering. Tissue Eng. 2002;8:157–165. doi: 10.1089/107632702753503144.
    1. Kimura Y, Ozeki M, Inamoto T, Tabata Y. Time course of de novo adipogenesis in matrigel by gelatin microspheres incorporating basic fibroblast growth factor. Tissue Eng. 2002;8:603–613. doi: 10.1089/107632702760240526.
    1. Kimura Y, Ozeki M, Inamoto T, Tabata Y. Adipose tissue engineering based on human preadipocytes combined with gelatin microspheres containing basic fibroblast growth factor. Biomaterials. 2003;24:2513–2521. doi: 10.1016/S0142-9612(03)00049-8.
    1. Rodeheffer MS, Birsoy K, Friedman JM. Identification of white adipocyte progenitor cells in vivo. Cell. 2008;135:240–249. doi: 10.1016/j.cell.2008.09.036.
    1. Ebrahimian TG, Pouzoulet F, Squiban C, Buard V, André M, Cousin B, Gourmelon P, Benderitter M, Casteilla L, Tamarat R. Cell therapy based on adipose tissue-derived stromal cells promotes physiological and pathological wound healing. Arterioscler Thromb Vasc Biol. 2009;29:503–510. doi: 10.1161/ATVBAHA.108.178962.
    1. Poglio S, Galvani S, Bour S, André M, Prunet-Marcassus B, Pénicaud L, Casteilla L, Cousin B. Adipose tissue sensitivity to radiation exposure. Am J Pathol. 2009;174:44–53. doi: 10.2353/ajpath.2009.080505.
    1. Altman AM, Yan Y, Matthias N, Bai X, Rios C, Mathur AB, Song YH, Alt EU. IFATS collection: human adipose-derived stem cells seeded on a silk fibroinchitosan scaffold enhance wound repair in a murine soft tissue injury model. Stem Cells. 2009;27:250–258. doi: 10.1634/stemcells.2008-0178.
    1. Cowan CM, Aalami OO, Shi YY, Chou YF, Mari C, Thomas R, Quarto N, Nacamuli RP, Contag CH, Wu B, Longaker MT. Bone morphogenetic protein 2 and retinoic acid accelerate in vivo bone formation, osteoclast recruitment, and bone turnover. Tissue Eng. 2005;11:645–658. doi: 10.1089/ten.2005.11.645.
    1. Cowan CM, Shi YY, Aalami OO, Chou YF, Mari C, Thomas R, Quarto N, Contag CH, Wu B, Longaker MT. Adipose-derived adult stromal cells heal criticalsize mouse calvarial defects. Nat Biotechnol. 2004;22:560–567. doi: 10.1038/nbt958.
    1. Dragoo JL, Choi JY, Lieberman JR, Huang J, Zuk PA, Zhang J, Hedrick MH, Benhaim P. Bone induction by BMP-2 transduced stem cells derived from human fat. J Orthop Res. 2003;21:622–629. doi: 10.1016/S0736-0266(02)00238-3.
    1. Lopez MJ, McIntosh KR, Spencer ND, Borneman JN, Horswell R, Anderson P, Yu G, Gaschen L, Gimble JM. Acceleration of spinal fusion using syngeneic and allogeneic adult adipose derived stem cells in a rat model. J Orthop Res. 2009;27:366–373. doi: 10.1002/jor.20735.
    1. 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;15:2677–2686. doi: 10.1089/ten.tea.2008.0566.
    1. Miyahara Y, Nagaya N, Kataoka M, Yanagawa B, Tanaka K, Hao H, Ishino K, Ishida H, Shimizu T, Kangawa K, Sano S, Okano T, Kitamura S, Mori H. Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat Med. 2006;12:459–465. doi: 10.1038/nm1391.
    1. Choi YS, Matsuda K, Dusting GJ, Morrison WA, Dilley RJ. Engineering cardiac tissue in vivo from human adipose-derived stem cells. Biomaterials. pp. 2236–2242.
    1. Kubis N, Tomita Y, Tran-Dinh A, Planat-Benard V, André M, Karaszewski B, Waeckel L, Pénicaud L, Silvestre JS, Casteilla L, Seylaz J, Pinard E. Vascular fate of adipose tissue-derived adult stromal cells in the ischemic murine brain: a combined imaging-histological study. Neuroimage. 2007;34:1–11. doi: 10.1016/j.neuroimage.2006.09.014.
    1. González MA, Gonzalez-Rey E, Rico L, Büscher D, Delgado M. Adiposederived mesenchymal stem cells alleviate experimental colitis by inhibiting inflammatory and autoimmune responses. Gastroenterology. 2009;136:978–989. doi: 10.1053/j.gastro.2008.11.041.
    1. Kim SJ, Cho HH, Kim YJ, Seo SY, Kim HN, Lee JB, Kim JH, Chung JS, Jung JS. Human adipose stromal cells expanded in human serum promote engraftment of human peripheral blood hematopoietic stem cells in NOD/SCID mice. Biochem Biophys Res Commun. 2005;329:25–31. doi: 10.1016/j.bbrc.2005.01.092.
    1. Cousin B, André M, Arnaud E, Pénicaud L, Casteilla L. Reconstitution of lethally irradiated mice by cells isolated from adipose tissue. Biochem Biophys Res Commun. 2003;301:1016–1022. doi: 10.1016/S0006-291X(03)00061-5.
    1. Murphy JM, Fink DJ, Hunziker EB, Barry FP. Stem cell therapy in a caprine model of osteoarthritis. Arthritis Rheum. 2003;48:3464–3474. doi: 10.1002/art.11365.
    1. Black LL, Gaynor J, Gahring D, Adams C, Aron D, Harman S, Gingerich DA, Harman R. Effect of adipose-derived mesenchymal stem and regenerative cells on lameness in dogs with chronic osteoarthritis of the coxofemoral joints: a randomized, double-blinded, multicenter, controlled trial. Vet Ther. 2007;8:272–284.
    1. Black LL, Gaynor J, Adams C, Dhupa S, Sams AE, Taylor R, Harman S, Gingerich DA, Harman R. Effect of intraarticular injection of autologous adiposederived mesenchymal stem and regenerative cells on clinical signs of chronic osteoarthritis of the elbow joint in dogs. Vet Ther. 2008;9:192–200.
    1. Frisbie DD, Kisiday JD, Kawcak CE, Werpy NM, McIlwraith CW. Evaluation of adipose-derived stromal vascular fraction or bone marrow-derived mesenchymal stem cells for treatment of osteoarthritis. J Orthop Res. 2009;27:1675–1680. doi: 10.1002/jor.20933.
    1. Banas A, Teratani T, Yamamoto Y, Tokuhara M, Takeshita F, Quinn G, Okochi H, Ochiya T. Adipose tissue-derived mesenchymal stem cells as a source of human hepatocytes. Hepatology. 2007;46:219–228. doi: 10.1002/hep.21704.
    1. Ishikawa T, Banas A, Hagiwara K, Iwaguro H, Ochiya T. Stem cells for hepatic regeneration: the role of adipose tissue derived mesenchymal stem cells. Curr Stem Cell Res Ther. 2010;5:182–189. doi: 10.2174/157488810791268636.
    1. Ochiya T, Yamamoto Y, Banas A. Commitment of stem cells into functional hepatocytes. Differentiation. 2010;79:65–73. doi: 10.1016/j.diff.2009.10.002.
    1. Banas A, Teratani T, Yamamoto Y, Tokuhara M, Takeshita F, Osaki M, Kato T, Okochi H, Ochiya T. Rapid hepatic fate specification of adipose-derived stem cells and their therapeutic potential for liver failure. J Gastroenterol Hepatol. 2009;24:70–77. doi: 10.1111/j.1440-1746.2008.05496.x.
    1. Banas A, Teratani T, Yamamoto Y, Tokuhara M, Takeshita F, Osaki M, Kawamata M, Kato T, Okochi H, Ochiya T. IFATS collection: in vivo therapeutic potential of human adipose tissue mesenchymal stem cells after transplantation into mice with liver injury. Stem Cells. 2008;26:2705–2712. doi: 10.1634/stemcells.2008-0034.
    1. Seo MJ, Suh SY, Bae YC, Jung JS. Differentiation of human adipose stromal cells into hepatic lineage in vitro and in vivo. Biochem Biophys Res Commun. 2005;328:258–264. doi: 10.1016/j.bbrc.2004.12.158.
    1. Aurich H, Sgodda M, Kaltwasser P, Vetter M, Weise A, Liehr T, Brulport M, Hengstler JG, Dollinger MM, Fleig WE, Christ B. Hepatocyte differentiation of mesenchymal stem cells from human adipose tissue in vitro promotes hepatic integration in vivo. Gut. 2009;58:570–581. doi: 10.1136/gut.2008.154880.
    1. Taléns-Visconti R, Bonora A, Jover R, Mirabet V, Carbonell F, Castell JV, Gómez-Lechón MJ. Hepatogenic differentiation of human mesenchymal stem cells from adipose tissue in comparison with bone marrow mesenchymal stem cells. World J Gastroenterol. 2006;12:5834–5845.
    1. Ruiz JC, Ludlow JW, Sherwood S, Yu G, Wu X, Gimble JM. Differentiated human adipose-derived stem cells exhibit hepatogenic capability in vitro and in vivo. J Cell Physiol. in press .
    1. Kajiyama H, Hamazaki TS, Tokuhara M, Masui S, Okabayashi K, Ohnuma K, Yabe S, Yasuda K, Ishiura S, Okochi H, Asashima M. Pdx1-transfected adipose tissue-derived stem cells differentiate into insulin-producing cells in vivo and reduce hyperglycemia in diabetic mice. Int J Dev Biol. 2010;54:699–705. doi: 10.1387/ijdb.092953hk.
    1. Chandra V, Swetha G, Phadris S, Nair PD, Bhonde RR. Generation of pancreatic hormone-expressing islet-like cell aggregates from murine adipose tissue-derived stem cells. Stem Cells. 2009;27:1941–1953. doi: 10.1002/stem.117.
    1. Blanton MW, Hadad I, Johnstone BH, Mund JA, Rogers PI, Eppley BL, March KL. Adipose stromal cells and platelet-rich plasma therapies synergistically increase revascularization during wound healing. Plast Reconstr Surg. 2009;123:56S–64S. doi: 10.1097/PRS.0b013e318191be2d.
    1. Nixon AJ, Dahlgren LA, Haupt JL, Yeager AE, Ward DL. Effect of adiposederived nucleated cell fractions on tendon repair in horses with collagenase-induced tendinitis. Am J Vet Res. 2008;69:928–937. doi: 10.2460/ajvr.69.7.928.
    1. Jack GS, Almeida FG, Zhang R, Alfonso ZC, Zuk PA, Rodríguez LV. Processed lipoaspirate cells for tissue engineering of the lower urinary tract: implications for the treatment of stress urinary incontinence and bladder reconstruction. J Urol. 2005;174:2041–2045. doi: 10.1097/01.ju.0000176489.96993.84.

Source: PubMed

Patrocinadores e Colaboradores

Condições médicas

Intervenções de drogas

3
Se inscrever