Characterisation and In Vivo Safety of Canine Adipose-Derived Stem Cells

Abdi, R., Fiorina, P., Adra, C. N., Atkinson, M., Sayegh, M. H. (2008). Immunomodulation by mesenchymal stem cells. Diabetes,57, 1759–1767.10.2337/db08-0180245363118586907Search in Google Scholar

Anjos-Afonso, F., Siapati, E. K., Bonnet, D. (2004). In vivo contribution of murine mesenchymal stem cells into multiple cell-types under minimal damage conditions. J. Cell Sci.,117, 5655–5664.10.1242/jcs.0148815494370Search in Google Scholar

Anonymous (2007). No. 1394/2007 of the European Parliament and of the Council of 13 November 2007 on advanced therapy medicinal products and amending directive 2001/83/EC and regulation (EC) no 726/2004. J. Eur. Union, 324, 121–137.Search in Google Scholar

Anonymous (2014). Report from the commission to the European Parliament and the Council in accordance with article 25 of regulation (EC) no 1394/2007 of the European Parliament and of the Council on advanced therapy medicinal products and amending directive 2001/83/EC and regulation (EC) no 726/2004. Available from: https://publications.europa.eu/en/publication-detail/-/publication/2dc18b82-b6c8-11e3-86f9-01aa75ed71a1 (accessed 30.01.2018).Search in Google Scholar

Anonymous (2015). General Secretariat of the Council to Delegations; Document number 15054/15: Personalised medicine for patients: Council conclusions. 07.12.2015. Available from: http://data.consilium.europa.eu/doc/document/ST-15054-2015-INIT/en/pdf (accessed 30.01.2018).Search in Google Scholar

Basciano, L., Nemos, C., Foliguet, B., de Isla, N., de Carvalho, M., Tran, N., Dalloul, A. (2011). Long term culture of mesenchymal stem cells in hypoxia promotes a genetic program maintaining their undifferentiated and multipotent status. BMC Cell Biol.,12, 12.10.1186/1471-2121-12-12307390021450070Search in Google Scholar

Bentzon, J. F., Stenderup, K., Hansen, F. D., Schroder, H. D., Abdallah, B. M., Jensen, T. G., Kassem, M. (2005). Tissue distribution and engraftment of human mesenchymal stem cells immortalized by human telomerase reverse transcriptase gene. Biochem. Biophys. Res. Comm.,330, 633–640.10.1016/j.bbrc.2005.03.07215809044Search in Google Scholar

Blythe, L. L., Craig, A. M., Christensen, J. M., Appell, L. H., Slizeski, M. L. (1986). Pharmacokinetic disposition of dimethyl sulfoxide administered intravenously to horses. Amer. J. Vet. Res.,47, 1739–1743.Search in Google Scholar

Bogdanova, A., Berzins, U., Nikulshin, S., Skrastina, D., Ezerta, A., Legzdina, D., Kozlovska, T. (2014). Characterization of human adipose-derived stem cells cultured in autologous serum after subsequent passaging and long term cryopreservation. J. Stem Cells,9, 135–148.Search in Google Scholar

Carrade, D. D., Borjesson, D. L. (2013). Immunomodulation by mesenchymal stem cells in veterinary species. Compar. Med.,63, 207–217.Search in Google Scholar

Corcione, A., Benvenuto, F., Ferretti, E., Giunti, D., Cappiello, V., Cazzanti, F., Risso, M., Gualandi, F., Mancardi, G. L., Pistoia, V., Uccelli, A. (2006). Human mesenchymal stem cells modulate B-cell functions. Blood, 107, 367–372.10.1182/blood-2005-07-265716141348Search in Google Scholar

Cyranoski, D. (2010). Korean deaths spark inquiry. Nature, 468, 485.10.1038/468485a21107396Search in Google Scholar

de Bakker, E., Van Ryssen, B., De Schauwer, C., Meyer, E. (2013). Canine mesenchymal stem cells: State of the art, perspectives as therapy for dogs and as a model for man. Vet. Quart., 33, 225–233.10.1080/01652176.2013.87396324404887Search in Google Scholar

De Jesus, M. M., Santiago, J. S., Trinidad, C. V., See, M. E., Semon, K. R., Fernandez, M. O., Jr., Chung, F. S. (2016). Autologous adipose-derived mesenchymal stromal cells for the treatment of Psoriasis vulgaris and psoriatic arthritis: A case report. Cell Transplant., 25, 2063–2069.10.3727/096368916X69199827301844Search in Google Scholar

Desiderio, V., De Francesco, F., Schiraldi, C., De Rosa, A., La Gatta, A., Paino, F., d’Aquino, R., Ferraro, G. A., Tirino, V., Papaccio, G. (2013). Human Ng2+ adipose stem cells loaded in vivo on a new crosslinked hyaluronic acid-Lys scaffold fabricate a skeletal muscle tissue. J. Cell. Physiol., 228, 1762–1773.10.1002/jcp.2433623359523Search in Google Scholar

Di Nicola, M., Carlo-Stella, C., Magni, M., Milanesi, M., Longoni, P. D., Matteucci, P., Grisanti, S., Gianni, A. M. (2002). Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood, 99, 3838–3843.10.1182/blood.V99.10.383811986244Search in Google Scholar

Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F., Krause, D., Deans, R., Keating, A., Prockop, D., Horwitz, E. (2006). Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy, 8, 315–-317.Search in Google Scholar

Eggenhofer, E., Benseler, V., Kroemer, A., Popp, F. C., Geissler, E. K., Schlitt, H. J., Baan, C. C., Dahlke, M. H., Hoogduijn, M. J. (2012). Mesenchymal stem cells are short-lived and do not migrate beyond the lungs after intravenous infusion. Frontiers Immunol., 3, 297.10.3389/fimmu.2012.00297345830523056000Search in Google Scholar

Eggenhofer, E., Luk, F., Dahlke, M. H., Hoogduijn, M. J. (2014). The life and fate of mesenchymal stem cells. Frontiers Immunol., 5, 148.10.3389/fimmu.2014.00148403290124904568Search in Google Scholar

Fang, B., Li, N., Song, Y., Li, J., Zhao, R. C., Ma, Y. (2009). Cotransplantation of haploidentical mesenchymal stem cells to enhance engraftment of hematopoietic stem cells and to reduce the risk of graft failure in two children with severe aplastic anemia. Pediatric Transplant., 13, 499–502.10.1111/j.1399-3046.2008.01002.x18673358Search in Google Scholar

Fang, B., Song, Y., Liao, L., Zhang, Y., Zhao, R. C. (2007). Favorable response to human adipose tissue-derived mesenchymal stem cells in steroid-refractory acute graft-versus-host disease. Transplant. Proc., 39, 3358–3362.10.1016/j.transproceed.2007.08.10318089385Search in Google Scholar

Fischer, U. M., Harting, M. T., Jimenez, F., Monzon-Posadas, W. O., Xue, H., Savitz, S. I., Laine, G. A., Cox, C. S., Jr. (2009). Pulmonary passage is a major obstacle for intravenous stem cell delivery: The pulmonary first-pass effect. Stem Cells Devel., 18, 683–692.10.1089/scd.2008.0253319029219099374Search in Google Scholar

Furlani, D., Ugurlucan, M., Ong, L., Bieback, K., Pittermann, E., Westien, I., Wang, W., Yerebakan, C., Li, W., Gaebel, R., Li, R. K., Vollmar, B., Steinhoff, G., Ma, N. (2009). Is the intravascular administration of mesenchymal stem cells safe? Mesenchymal stem cells and intravital microscopy. Microvasc. Res., 77, 370–376.10.1016/j.mvr.2009.02.00119249320Search in Google Scholar

Ghannam, S., Bouffi, C., Djouad, F., Jorgensen, C., Noel, D. (2010). Immunosuppression by mesenchymal stem cells: Mechanisms and clinical applications. Stem Cell Res. Ther., 1, 2.10.1186/scrt2287369820504283Search in Google Scholar

Hall, M. N., Rosenkrantz, W. S., Hong, J. H., Griffin, C. E., Mendelsohn, C. M. (2010). Evaluation of the potential use of adipose-derived mesenchymal stromal cells in the treatment of canine atopic dermatitis: A pilot study. Vet. Ther. Res. Appl. Vet. Med., 11, E1–14.Search in Google Scholar

Han, S. M., Kim, H. T., Kim, K. W., Jeon, K. O., Seo, K. W., Choi, E. W., Youn, H. Y. (2015). CTLA4 overexpressing adipose tissue-derived mesenchymal stem cell therapy in a dog with steroid-refractory pemphigus foliaceus. BMC Vet. Res., 11, 49.10.1186/s12917-015-0371-3441722225889154Search in Google Scholar

Hoffman, A. M., Dow, S. W. (2016). Concise review: Stem cell trials using companion animal disease models. Stem Cells (Dayton, Ohio), 34, 1709–1729.10.1002/stem.237727066769Search in Google Scholar

Honmou, O., Houkin, K., Matsunaga, T., Niitsu, Y., Ishiai, S., Onodera, R., Waxman, S. G., Kocsis, J. D. (2011). Intravenous administration of auto serum-expanded autologous mesenchymal stem cells in stroke. Brain, 134, 1790–1807.10.1093/brain/awr063310223721493695Search in Google Scholar

Hu, X., Yu, S. P., Fraser, J. L., Lu, Z., Ogle, M. E., Wang, J. A., Wei, L. (2008). Transplantation of hypoxia-preconditioned mesenchymal stem cells improves infarcted heart function via enhanced survival of implanted cells and angiogenesis. J. Thor. Cardiovasc. Surg., 135, 799–808.10.1016/j.jtcvs.2007.07.07118374759Search in Google Scholar

Hung, S. C., Pochampally, R. R., Hsu, S. C., Sanchez, C., Chen, S. C., Spees, J., Prockop, D. J. (2007). Short-term exposure of multipotent stromal cells to low oxygen increases their expression of CX3CR1 and CXCR4 and their engraftment in vivo. PloS One, 2, e416.10.1371/journal.pone.0000416185507717476338Search in Google Scholar

Ivanovic, Z. (2009). Hypoxia or in situ normoxia: The stem cell paradigm. J. Cell. Physiol., 219, 271–275.10.1002/jcp.2169019160417Search in Google Scholar

Jung, J. W., Kwon, M., Choi, J. C., Shin, J. W., Park, I. W., Choi, B. W., Kim, J. Y. (2013). Familial occurrence of pulmonary embolism after intravenous, adipose tissue-derived stem cell therapy. Yonsei Med. J.,54, 1293–1296.10.3349/ymj.2013.54.5.1293374320423918585Search in Google Scholar

Kang, J. W., Kang, K. S., Koo, H. C., Park, J. R., Choi, E. W., Park Y. H. (2008). Soluble factors-mediated immunomodulatory effects of canine adipose tissue-derived mesenchymal stem cells. Stem Cells Devel., 17, 681–694.10.1089/scd.2007.015318717642Search in Google Scholar

Kang, M. H., Park, H. M. (2014). Evaluation of adverse reactions in dogs following intravenous mesenchymal stem cell transplantation. Acta Vet. Scand., 56, 16.10.1186/1751-0147-56-16399452224655411Search in Google Scholar

Karagiannis, K., Proklou, A., Tsitoura, E., Lasithiotaki, I. (2017). Impaired mRNA expression of the migration related chemokine receptor CXCR4 in mesenchymal stem cells of COPD patients. Int. J. Inflam., 2017, 6089425.10.1155/2017/6089425553994228804668Search in Google Scholar

Kim, M., Kim, D. I., Kim, E. K., Kim, C. W. (2017). CXCR4 overexpression in human adipose tissue-derived stem cells improves homing and engraftment in an animal limb ischemia model. Cell Transplant.,26, 191–204.10.3727/096368916X692708565775827501830Search in Google Scholar

Kisiel, A. H., McDuffee, L. A., Masaoud, E., Bailey, T. R., Esparza Gonzalez, B. P., Nino-Fong, R. (2012). Isolation, characterization, and in vitro proliferation of canine mesenchymal stem cells derived from bone marrow, adipose tissue, muscle, and periosteum. Amer. J. Vet. Res., 73, 1305–1317.10.2460/ajvr.73.8.130522849692Search in Google Scholar

Kraitchman, D. L., Tatsumi, M., Gilson, W. D., Ishimori, T., Kedziorek, D., Walczak, P., Segars, W. P., Chen, H. H., Fritzges, D., Izbudak, I., Young, R. G., Marcelino, M., Pittenger, M. F., Solaiyappan, M., Boston, R. C., Tsui, B. M., Wahl, R. L., Bulte, J. W. (2005). Dynamic imaging of allogeneic mesenchymal stem cells trafficking to myocardial infarction. Circulation, 112, 1451–1461.10.1161/CIRCULATIONAHA.105.537480145673116129797Search in Google Scholar

Le Blanc, K., Tammik, L., Sundberg, B., Haynesworth, S. E., Ringden, O. (2003). Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand. J. Immunol., 57, 11–20.10.1046/j.1365-3083.2003.01176.x12542793Search in Google Scholar

Lee, E. Y., Xia, Y., Kim, W. S., Kim, M. H., Kim, T. H., Kim, K. J., Park, B. S., Sung, J. H. (2009). Hypoxia-enhanced wound-healing function of adipose-derived stem cells: Increase in stem cell proliferation and up-regulation of VEGF and bFGF. Wound Repair Regen.,17, 540–547.10.1111/j.1524-475X.2009.00499.x19614919Search in Google Scholar

Legzdina, D., Romanauska, A., Nikulshin, S., Kozlovska, T., Berzins, U. (2016). Characterization of senescence of culture-expanded human adipose-derived mesenchymal stem cells. Int. J. Stem Cells, 9, 124–136.10.15283/ijsc.2016.9.1.124496111227426094Search in Google Scholar

Leroux, L., Descamps, B., Tojais, N. F., Seguy, B., Oses, P., Moreau, C., Daret, D., Ivanovic, Z., Boiron, J. M., Lamaziere, J.M., Dufourcq, P., Couffinhal, T., Duplaa, C. (2010). Hypoxia preconditioned mesenchymal stem cells improve vascular and skeletal muscle fiber regeneration after ischemia through a Wnt4-dependent pathway. Mol. Ther.,18, 1545–1552.10.1038/mt.2010.108292705920551912Search in Google Scholar

Li, Q., Zhang, A., Tao, C., Li, X., Jin, P. (2013). The role of SDF-1-CXCR4/CXCR7 axis in biological behaviors of adipose tissue-derived mesenchymal stem cells in vitro. Biochem. Biophys. Res. Comm., 441, 675–680.10.1016/j.bbrc.2013.10.07124184476Search in Google Scholar

Lim, J. Y., Ra, J. C., Shin, I. S., Jang, Y. H., An, H. Y., Choi, J. S., Kim, W. C., Kim, Y. M. (2013). Systemic transplantation of human adipose tissue-derived mesenchymal stem cells for the regeneration of irradiation-induced salivary gland damage. PloS One, 8, e71167.10.1371/journal.pone.0071167373979523951100Search in Google Scholar

Liu, H., Liu, S., Li, Y., Wang, X., Xue, W., Ge, G., Luo, X. (2012). The role of SDF-1-CXCR4/CXCR7 axis in the therapeutic effects of hypoxia-pre-conditioned mesenchymal stem cells for renal ischemia/reperfusion injury. PloS One, 7, e34608.Search in Google Scholar

Lo Sicco, C., Reverberi, D., Balbi, C., Ulivi, V., Principi, E., Pascucci, L., Becherini, P., Bosco, M. C., Varesio, L., Franzin, C., Pozzobon, M., Cancedda, R., Tasso, R. (2017). Mesenchymal stem cell-derived extracellular vesicles as mediators of anti-inflammatory effects: Endorsement of macrophage polarization. Stem Cells Transl. Med., 6, 1018–1028.10.1002/sctm.16-0363544278328186708Search in Google Scholar

Lysaght, T., Lipworth, W., Hendl, T., Kerridge, I., Lee, T.L., Munsie, M., Waldby, C., Stewart, C. (2017). The deadly business of an unregulated global stem cell industry. J. Med. Ethics, 43 (11).10.1136/medethics-2016-10404628356490Search in Google Scholar

Martinello, T., Bronzini, I., Maccatrozzo, L., Mollo, A., Sampaolesi, M., Mascarello, F., Decaminada, M., Patruno, M. (2011). Canine adipose-derived-mesenchymal stem cells do not lose stem features after a long-term cryopreservation. Res. Vet. Sci.,91, 18–24.10.1016/j.rvsc.2010.07.02420732703Search in Google Scholar

McIntosh, K. R., Frazier, T., Rowan, B. G., Gimble, J. M. (2013). Evolution and future prospects of adipose-derived immunomodulatory cell therapeutics. Expert Rev. Clin. Immunol., 9, 175–184.10.1586/eci.12.9623390948Search in Google Scholar

Moll, G., Le Blanc, K. (2015). Engineering more efficient multipotent mesenchymal stromal (stem) cells for systemic delivery as cellular therapy. ISBT Science Series, 10, 357–365.10.1111/voxs.12133Search in Google Scholar

Muzes, G., Sipos, F. (2016). Heterogeneity of stem cells: A brief overview. Meth. Mol. biol. (Clifton, N.J.), 1516, 1–12.10.1007/7651_2016_34527044045Search in Google Scholar

Neupane, M., Chang, C.C., Kiupel, M., Yuzbasiyan-Gurkan, V. (2008). Isolation and characterization of canine adipose-derived mesenchymal stem cells. Tissue Eng. Part A, 14, 1007–1015.10.1089/ten.tea.2007.0207Search in Google Scholar

O’Kell, A. L., Wasserfall, C., Catchpole, B., Davison, L. J., Hess, R. S., Kushner, J. A., Atkinson, M. A. (2017). Comparative pathogenesis of autoimmune diabetes in humans, NOD mice, and canines: Has a valuable animal model of Type 1 Diabetes been overlooked? Diabetes, 66, 1443–1452.10.2337/db16-1551544002228533295Search in Google Scholar

Prologo, J. D., Hawkins, M., Gilliland, C., Chinnadurai, R., Harkey, P., Chadid, T., Lee, Z., Brewster, L. (2016). Interventional stem cell therapy. Clin. Radiol., 71, 307–311.10.1016/j.crad.2016.01.00526874660Search in Google Scholar

Ra, J. C., Kang, S. K., Shin, I. S., Park, H. G., Joo, S. A., Kim, J. G., Kang, B.-C., Lee, Y. S., Nakama, K., Piao, M. (2011a). Stem cell treatment for patients with autoimmune disease by systemic infusion of culture-expanded autologous adipose tissue derived mesenchymal stem cells. J. Translat. Med., 9, 181.10.1186/1479-5876-9-181322261722017805Search in Google Scholar

Ra, J. C., Shin, I. S., Kim, S. H., Kang, S. K., Kang, B. C., Lee, H. Y., Kim, Y. J., Jo, J. Y., Yoon, E. J., Choi, H. J. (2011b). Safety of intravenous infusion of human adipose tissue-derived mesenchymal stem cells in animals and humans. Stem Cells Devel., 20, 1297–1308.10.1089/scd.2010.046621303266Search in Google Scholar

Reich, C. M., Raabe, O., Wenisch, S., Bridger, P. S., Kramer, M., Arnhold, S. (2012). Isolation, culture and chondrogenic differentiation of canine adipose tissue-and bone marrow-derived mesenchymal stem cells—a comparative study. Vet. Res. Comm., 36, 139–148.10.1007/s11259-012-9523-022392598Search in Google Scholar

Rosova, I., Dao, M., Capoccia, B., Link, D., Nolta, J. A. (2008) Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells. Stem Cells (Dayton, Ohio), 26, 2173–2182.10.1634/stemcells.2007-1104301747718511601Search in Google Scholar

Russell, K. A., Chow, N. H. C., Dukoff, D., Gibson, T. W. G., LaMarre, J., Betts, D. H., Koch, T. G. (2016). Characterization and immunomodulatory effects of canine adipose tissue- and bone marrow-derived mesenchymal stromal cells. PLoS One, 11, e0167442.10.1371/journal.pone.0167442513197727907211Search in Google Scholar

Sato, J., Doi, T., Wako, Y., Hamamura, M., Kanno, T., Tsuchitani, M., Narama, I. (2012). Histopathology of incidental findings in beagles used in toxicity studies. J. Toxicol. Pathol., 25, 103–134.10.1293/tox.25.103332016022481862Search in Google Scholar

Shapiro, H. M., Shapiro, H. M. (2003). Practical Flow Cytometry. 4th edn. Wiley-Liss. 736 pp.10.1002/0471722731Search in Google Scholar

Sparrow, R. L., Tippett, E. (2005). Discrimination of live and early apoptotic mononuclear cells by the fluorescent SYTO 16 vital dye. J. Immunol. Meth., 305, 173–187.10.1016/j.jim.2005.07.01716165150Search in Google Scholar

Spees, J. L., Gregory, C. A., Singh, H., Tucker, H. A., Peister, A., Lynch, P. J., Hsu, S. C., Smith, J., Prockop, D. J. (2004). Internalized antigens must be removed to prepare hypoimmunogenic mesenchymal stem cells for cell and gene therapy. Mol. Ther.,9, 747–756.10.1016/j.ymthe.2004.02.01215120336Search in Google Scholar

Stepien, A., Dabrowska, N. L., Maciagowska, M., Macoch, R. P. (2016). Clinical application of autologous adipose stem cells in patients with multiple sclerosis: Preliminary results, Mediators Inflamm., 2016, 5302120.10.1155/2016/5302120505957627761060Search in Google Scholar

Sullivan, M. O., Gordon-Evans, W. J., Fredericks, L. P., Kiefer, K., Conzemius, M. G., Griffon, D. J. (2016). Comparison of mesenchymal stem cell surface markers from bone marrow aspirates and adipose stromal vascular fraction sites. Frontiers Vet. Sci., 2, 82.10.3389/fvets.2015.00082471384026835460Search in Google Scholar

Takemitsu, H., Zhao, D., Yamamoto, I., Harada, Y., Michishita, M., Arai, T. (2012). Comparison of bone marrow and adipose tissue-derived canine mesenchymal stem cells. BMC Vet. Res., 8, 150.10.1186/1746-6148-8-150344296122937862Search in Google Scholar

Tatsumi, K., Ohashi, K., Matsubara, Y., Kohori, A., Ohno, T., Kakidachi, H., Horii, A., Kanegae, K., Utoh, R., Iwata, T., Okano, T. (2013). Tissue factor triggers procoagulation in transplanted mesenchymal stem cells leading to thromboembolism. Biochem. Biophys. Res. Comm., 431, 203–209.10.1016/j.bbrc.2012.12.13423313481Search in Google Scholar

Tsai, C. C., Chen, Y. J., Yew, T. L., Chen, L. L., Wang, J. Y., Chiu, C. H., Hung, S. C. (2011). Hypoxia inhibits senescence and maintains mesenchymal stem cell properties through down-regulation of E2A-p21 by HIF-TWIST. Blood, 117, 459–469.10.1182/blood-2010-05-28750820952688Search in Google Scholar

Tsuji, W., Rubin, J. P., Marra, K. G. (2014). Adipose-derived stem cells: Implications in tissue regeneration. World J. Stem Cells, 6, 312–321.10.4252/wjsc.v6.i3.312413127325126381Search in Google Scholar

Tyndall, A., Uccelli, A. (2009). Multipotent mesenchymal stromal cells for autoimmune diseases: Teaching new dogs old tricks. Bone Marrow Transplantation, 43, 821–828.10.1038/bmt.2009.6319308035Search in Google Scholar

Veriter, S., Andre, W., Aouassar, N., Poirel, H. A., Lafosse, A., Docquier, P. L., Dufrane, D. (2015). Human adipose-derived mesenchymal stem cells in Cell therapy: Safety and feasibility in different “Hospital Exemption” clinical applications. PloS One, 10, e0139566.10.1371/journal.pone.0139566461562026485394Search in Google Scholar

Vieira, N. M., Brandalise, V., Zucconi, E., Secco, M., Strauss, B. E., Zatz, M. (2010). Isolation, characterization, and differentiation potential of canine adipose-derived stem cells. Cell Transplant., 19, 279–289.10.3727/096368909X48176419995482Search in Google Scholar

Vives, J., Carmona, G. (2015). Guide to Cell Therapy GxP: Quality Standards in the Development of Cell-Based Medicines in Non-pharmaceutical Environments. Academic Press. 266 pp.Search in Google Scholar

Zuk, P. A., Zhu, M., Ashjian, P., De Ugarte, D. A., Huang, J. I., Mizuno, H., Alfonso, Z. C., Fraser, J. K., Benhaim, P., Hedrick, M. H. (2002). Human adipose tissue is a source of multipotent stem cells. Mol. Biol. Cell, 13, 4279–4295.10.1091/mbc.e02-02-010513863312475952Search in Google Scholar

Zuk, P. A., Zhu, M., Mizuno, H., Huang, J., Futrell, J. W., Katz, A. J., Benhaim, P., Lorenz, H. P., Hedrick, M. H. (2001). Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng., 7, 211–228.10.1089/10763270130006285911304456Search in Google Scholar