Therapeutic applications of human adipose-derived stromal cells for soft tissue reconstruction

Discovery Medicine

Volumn 19, Issue 105, 2015, Pages 245-253

  Zielins, Elizabeth R ^a   Luan, Anna ^a   Brett, Elizabeth A ^a   Longaker, Michael T ^a   Wan, Derrick C ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; INTERLEUKIN 10; PLATELET DERIVED GROWTH FACTOR; SCATTER FACTOR; VASCULOTROPIN;

ANGIOGENESIS; ARTICLE; CANCER RADIOTHERAPY; CANCER SURGERY; CELL DIFFERENTIATION; CELL POPULATION; CLINICAL TRIAL (TOPIC); COMPOSITE SKIN GRAFT; COMPUTER ASSISTED TOMOGRAPHY; HEART FAILURE; HUMAN; HYPOXIA; ISCHEMIA; NECROSIS; OUTCOME ASSESSMENT; PARTIAL MASTECTOMY; PHOTOGRAPHY; PROTEIN EXPRESSION; SOFT TISSUE DEFECT; STROMA CELL; TUMOR RECURRENCE; WOUND HEALING; ADIPOCYTE; ADIPOSE TISSUE; ANIMAL; AUTOTRANSPLANTATION; BREAST RECONSTRUCTION; CYTOLOGY; FEMALE; LIPECTOMY; MOUSE; NEOPLASMS; PROCEDURES; RECONSTRUCTIVE SURGERY; RECURRENT DISEASE; SURGICAL FLAPS; TRANSPLANTATION;

ADIPOCYTES; ADIPOSE TISSUE; ANIMALS; CLINICAL TRIALS AS TOPIC; FEMALE; HUMANS; ISCHEMIA; LIPECTOMY; MAMMAPLASTY; MICE; NEOPLASMS; RECONSTRUCTIVE SURGICAL PROCEDURES; RECURRENCE; STROMAL CELLS; SURGICAL FLAPS; TRANSPLANTATION, AUTOLOGOUS;

EID: 84940548595     PISSN: 15396509     EISSN: 19447930     Source Type: Journal    
DOI: None     Document Type: Article

References (82)

1. Aguena M, Fanganiello RD, Tissiani LA, Ishiy FA, Atique R, Alonso N, Passos-Bueno MR. Optimization of parameters for a more efficient use of adipose-derived stem cells in regenerative medicine therapies. Stem Cells Int 2012:303610, 2012.
2. Ahn JO, Coh YR, Lee HW, Shin IS, Kang SK, Youn HY. Human adipose tissue-derived mesenchymal stem cells inhibit melanoma growth in vitro and in vivo. Anticancer Res 35(1):159-168, 2015.
3. Alperovich M, Lee ZH, Friedlander PL, Rowan BG, Gimble JM, Chiu ES. Adipose stem cell therapy in cancer reconstruction: a critical review. Ann Plast Surg 73 Suppl 1:S104-107, 2014.
4. American Society of Plastic Surgeons. Reconstructive Surgery Procedure Trends. Available online at: http://www.plasticsurgery.org/Documents/news-resources/statistics/2012-Plastic-Surgery-Statistics/Reconstructive-Surgery-Procedure-Trends-2012.pdf (accessed Mar. 17, 2015). 2012.
5. Aronowitz JA. NCT02116933: Grafting of Autologous Adipose Stromal Cell Trial (GAASC). Available online at: https://www.clinicaltrials.gov/ct2/show/NCT02116933 (accessed Mar. 17, 2015). 2014.
6. Atashroo D, Raphel J, Chung MT, Paik KJ, Parisi-Amon A, Mcardle A, Senarath-Yapa K, Zielins ER, Tevlin R, Duldulao C, Walmsley GG, Hu MS, Momeni A, Domecus B, Rimsa JR, Greenberg L, Gurtner GC, Longaker MT, Wan DC. Studies in fat grafting: Part II. Effects of injection mechanics on material properties of fat. Plast Reconstr Surg 134(1):39-46, 2014.
7. Carpaneda CA, Ribeiro MT. Study of the histologic alterations and viability of the adipose graft in humans. Aesthetic Plast Surg 17(1):43-47, 1993.
8. Castro-Govea Y, De La Garza-Pineda O, Lara-Arias J, Chacon-Martinez H, Mecott-Rivera G, Salazar-Lozano A, Valdes-Flores E. Cell-assisted lipotransfer for the treatment of parry-romberg syndrome. Arch Plast Surg 39(6):659-662, 2012.
9. Chandler EM, Seo BR, Califano JP, Andresen Eguiluz RC, Lee JS, Yoon CJ, Tims DT, Wang JX, Cheng L, Mohanan S, Buckley MR, Cohen I, Nikitin AY, Williams RM, Gourdon D, Reinhart-King CA, Fischbach C. Implanted adipose progenitor cells as physicochemical regulators of breast cancer. Proc Natl Acad Sci U S A 109(25):9786-9791, 2012.
10. Choudhery MS, Badowski M, Muise A, Pierce J, Harris DT. Donor age negatively impacts adipose tissue-derived mesenchymal stem cell expansion and differentiation. J Transl Med 12:8, 2014.
11. Chung MT, Liu C, Hyun JS, Lo DD, Montoro DT, Hasegawa M, Li S, Sorkin M, Rennert R, Keeney M, Yang F, Quarto N, Longaker MT, Wan DC. CD90 (Thy-1)-positive selection enhances osteogenic capacity of human adipose-derived stromal cells. Tissue Eng Part A 19(7-8):989-997, 2013a.
12. Chung MT, Paik KJ, Atashroo DA, Hyun JS, Mcardle A, Senarath-Yapa K, Zielins ER, Tevlin R, Duldulao C, Hu MS, Walmsley GG, Parisi-Amon A, Momeni A, Rimsa JR, Commons GW, Gurtner GC, Wan DC, Longaker MT. Studies in fat grafting: Part I. Effects of injection technique on in vitro fat viability and in vivo volume retention. Plast Reconstr Surg 134(1):29-38, 2014.
13. Chung MT, Zimmermann AS, Paik KJ, Morrison SD, Hyun JS, Lo DD, Mcardle A, Montoro DT, Walmsley GG, Senarath-Yapa K, Sorkin M, Rennert R, Chen HH, Chung AS, Vistnes D, Gurtner GC, Longaker MT, Wan DC. Isolation of human adipose-derived stromal cells using laser-assisted liposuction and their therapeutic potential in regenerative medicine. Stem Cells Transl Med 2(10):808-817, 2013b.
14. Clark N, Sherman R. Soft-tissue reconstruction of the foot and ankle. Orthop Clin North Am 24(3):489-503, 1993.
15. Claro F, Jr., Figueiredo JC, Zampar AG, Pinto-Neto AM. Applicability and safety of autologous fat for reconstruction of the breast. Br J Surg 99(6):768-780, 2012.
16. Coleman SR. Structural fat grafting: more than a permanent filler. Plast Reconstr Surg 118(3 Suppl):108S-120S, 2006.
17. Cousin B, Ravet E, Poglio S, De Toni F, Bertuzzi M, Lulka H, Touil I, Andre M, Grolleau JL, Peron JM, Chavoin JP, Bourin P, Penicaud L, Casteilla L, Buscail L, Cordelier P. Adult stromal cells derived from human adipose tissue provoke pancreatic cancer cell death both in vitro and in vivo. PLoS One 4(7):e6278, 2009.
18. Dong Z, Peng Z, Chang Q, Zhan W, Zeng Z, Zhang S, Lu F. The angiogenic and adipogenic modes of adipose tissue after free fat grafting. Plast Reconstr Surg 135(3):556e-567e, 2015.
19. El-Ftesi S, Chang EI, Longaker MT, Gurtner GC. Aging and diabetes impair the neovascular potential of adipose-derived stromal cells. Plast Reconstr Surg 123(2):475-485, 2009.
20. Eto H, Kato H, Suga H, Aoi N, Doi K, Kuno S, Yoshimura K. The fate of adipocytes after nonvascularized fat grafting: evidence of early death and replacement of adipocytes. Plast Reconstr Surg 129(5):1081-1092, 2012.
21. Fraser JK, Hicok KC, Shanahan R, Zhu M, Miller S, Arm DM. The Celution System: Automated Processing of Adipose-Derived Regenerative Cells in a Functionally Closed System. Adv Wound Care (New Rochelle) 3(1):38-45, 2014.
22. Gao W, Qiao X, Ma S, Cui L. Adipose-derived stem cells accelerate neovascularization in ischaemic diabetic skin flap via expression of hypoxia-inducible factor-1alpha. J Cell Mol Med 15(12):2575-2585, 2011.
23. Garza RM, Paik KJ, Chung MT, Duscher D, Gurtner GC, Longaker MT, Wan DC. Studies in fat grafting: Part III. Fat grafting irradiated tissue-improved skin quality and decreased fat graft retention. Plast Reconstr Surg 134(2):249-257, 2014a.
24. Garza RM, Rennert RC, Paik KJ, Atashroo D, Chung MT, Duscher D, Januszyk M, Gurtner GC, Longaker MT, Wan DC. Studies in Fat Grafting: Part IV. Adipose-derived stromal cell gene expression in cell-assisted lipotransfer. Plast Reconstr Surg 135(4):1045-1055, 2014b.
25. Goldstein RH, Reagan MR, Anderson K, Kaplan DL, Rosenblatt M. Human bone marrow-derived MSCs can home to orthotopic breast cancer tumors and promote bone metastasis. Cancer Res 70(24):10044-10050, 2010.
26. Herold C, Ueberreiter K, Busche MN, Vogt PM. Autologous fat transplantation: volumetric tools for estimation of volume survival. A systematic review. Aesthetic Plast Surg 37(2):380-387, 2013.
27. Hollenbeck ST, Senghaas A, Komatsu I, Zhang Y, Erdmann D, Klitzman B. Tissue engraftment of hypoxic-preconditioned adipose-derived stem cells improves flap viability. Wound Repair Regen 20(6):872-878, 2012.
28. Jurgens WJ, Oedayrajsingh-Varma MJ, Helder MN, Zandiehdoulabi B, Schouten TE, Kuik DJ, Ritt MJ, Van Milligen FJ. Effect of tissue-harvesting site on yield of stem cells derived from adipose tissue: implications for cell-based therapies. Cell Tissue Res 332(3):415-426, 2008.
29. Kapur SK, Katz AJ. Review of the adipose derived stem cell secretome. Biochimie 95(12):2222-2228, 2013.
30. Karacaoglu E, Zienowicz RJ, Balan I. Calf contouring with endoscopic fascial release, calf implant, and structural fat grafting. Plast Reconstr Surg Glob Open 1(5):e35, 2013.
31. Karam JP, Bonafe F, Sindji L, Muscari C, Montero-Menei CN. Adipose-derived stem cell adhesion on laminin-coated microcarriers improves commitment toward the cardiomyogenic lineage. J Biomed Mater Res A 103(5):1828-1839, 2014.
32. Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW, Richardson AL, Polyak K, Tubo R, Weinberg RA. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 449(7162):557-563, 2007.
33. Kato H, Mineda K, Eto H, Doi K, Kuno S, Kinoshita K, Kanayama K, Yoshimura K. Degeneration, regeneration, and cicatrization after fat grafting: dynamic total tissue remodeling during the first 3 months. Plast Reconstr Surg 133(3):303e-313e, 2014.
34. Kaufman MR, Bradley JP, Dickinson B, Heller JB, Wasson K, O'hara C, Huang C, Gabbay J, Ghadjar K, Miller TA. Autologous fat transfer national consensus survey: trends in techniques for harvest, preparation, and application, and perception of short- and long-term results. Plast Reconstr Surg 119(1):323-331, 2007.
35. Keck M, Kober J, Riedl O, Kitzinger HB, Wolf S, Stulnig TM, Zeyda M, Gugerell A. Power assisted liposuction to obtain adipose-derived stem cells: impact on viability and differentiation to adipocytes in comparison to manual aspiration. J Plast Reconstr Aesthet Surg 67(1):e1-e8, 2014.
36. Kim SK. Adipose stromal vascular fraction isolation: a head-to-head comparison of four commercial cell separation systems. Plast Reconstr Surg 133(6):889e, 2014.
37. Kitamura K, Kajitani K, Hedrick M. Stem cell augmented reconstruction: a new hope for reconstruction after breast conservation therapy. Breast Cancer Res Treat 106:S190, 2007.
38. Kolle SF, Fischer-Nielsen A, Mathiasen AB, Elberg JJ, Oliveri RS, Glovinski PV, Kastrup J, Kirchhoff M, Rasmussen BS, Talman ML, Thomsen C, Dickmeiss E, Drzewiecki KT. Enrichment of autologous fat grafts with ex-vivo expanded adipose tissue-derived stem cells for graft survival: a randomised placebo-controlled trial. Lancet 382(9898):1113-1120, 2013.
39. Kucerova L, Kovacovicova M, Polak S, Bohac M, Fedeles J, Palencar D, Matuskova M. Interaction of human adipose tissue-derived mesenchymal stromal cells with breast cancer cells. Neoplasma 58(5):361-370, 2011.
40. Kuhbier JW, Bucan V, Reimers K, Strauss S, Lazaridis A, Jahn S, Radtke C, Vogt PM. Observed changes in the morphology and phenotype of breast cancer cells in direct co-culture with adipose-derived stem cells. Plast Reconstr Surg 134(3):414-423, 2014.
41. Lazennec G, Jorgensen C. Concise review: adult multipotent stromal cells and cancer: risk or benefit? Stem Cells 26(6):1387-1394, 2008.
42. Lee JH, Kirkham JC, Mccormack MC, Nicholls AM, Randolph MA, Austen WG, Jr. The effect of pressure and shear on autologous fat grafting. Plast Reconstr Surg 131(5):1125-1136, 2013.
43. Levi B, James AW, Glotzbach JP, Wan DC, Commons GW, Longaker MT. Depot-specific variation in the osteogenic and adipogenic potential of human adipose-derived stromal cells. Plast Reconstr Surg 126(3):822-834, 2010.
44. Levi B, Wan DC, Glotzbach JP, Hyun J, Januszyk M, Montoro D, Sorkin M, James AW, Nelson ER, Li S, Quarto N, Lee M, Gurtner GC, Longaker MT. CD105 protein depletion enhances human adipose-derived stromal cell osteogenesis through reduction of transforming growth factor beta1 (TGF-beta1) signaling. J Biol Chem 286(45):39497-39509, 2011.
45. Li K, Li F, Li J, Wang H, Zheng X, Long J, Guo W, Tian W. Increased survival of human free fat grafts with varying densities of human adipose-derived stem cells and platelet-rich plasma. J Tissue Eng Regen Med, 2014.
46. Lim AA, Fan K, Allam KA, Wan D, Tabit C, Liao E, Kawamoto HK, Bradley JP. Autologous fat transplantation in the craniofacial patient: the UCLA experience. J Craniofac Surg 23(4):1061-1066, 2012.
47. Matsumoto D, Sato K, Gonda K, Takaki Y, Shigeura T, Sato T, Aiba-Kojima E, Iizuka F, Inoue K, Suga H, Yoshimura K. Cell-assisted lipotransfer: supportive use of human adipose-derived cells for soft tissue augmentation with lipoinjection. Tissue Eng 12(12):3375-3382, 2006.
48. Moseley TA, Zhu M, Hedrick MH. Adipose-derived stem and progenitor cells as fillers in plastic and reconstructive surgery. Plast Reconstr Surg 118(3 Suppl):121S-128S, 2006.
49. Muehlberg FL, Song YH, Krohn A, Pinilla SP, Droll LH, Leng X, Seidensticker M, Ricke J, Altman AM, Devarajan E, Liu W, Arlinghaus RB, Alt EU. Tissue-resident stem cells promote breast cancer growth and metastasis. Carcinogenesis 30(4):589-597, 2009.
50. Paik KJ, Zielins ER, Atashroo DA, Maan ZN, Duscher D, Luan A, Walmsley GG, Momeni A, Vistnes S, Gurtner GC, Longaker MT, Wan DC. Studies in Fat Grafting: Part V. Cell-Assisted Lipotransfer to Enhance Fat Graft Retention is Dose Dependent. Plast Reconstr Surg, epub ahead of print, Mar. 17, 2015.
51. Panetta NJ, Gupta DM, Kwan MD, Wan DC, Commons GW, Longaker MT. Tissue harvest by means of suction-assisted or third-generation ultrasound-assisted lipoaspiration has no effect on osteogenic potential of human adipose-derived stromal cells. Plast Reconstr Surg 124(1):65-73, 2009.
52. Peltoniemi HH, Salmi A, Miettinen S, Mannerstrom B, Saariniemi K, Mikkonen R, Kuokkanen H, Herold C. Stem cell enrichment does not warrant a higher graft survival in lipofilling of the breast: a prospective comparative study. J Plast Reconstr Aesthet Surg 66(11):1494-1503, 2013.
53. Perez-Cano R, Vranckx JJ, Lasso JM, Calabrese C, Merck B, Milstein AM, Sassoon E, Delay E, Weiler-Mithoff EM. Prospective trial of adipose-derived regenerative cell (ADRC)-enriched fat grafting for partial mastectomy defects: the RESTORE-2 trial. Eur J Surg Oncol 38(5):382-389, 2012.
54. Planat-Benard V, Silvestre JS, Cousin B, Andre M, Nibbelink M, Tamarat R, Clergue M, Manneville C, Saillan-Barreau C, Duriez M, Tedgui A, Levy B, Penicaud L, Casteilla L. Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives. Circulation 109(5):656-663, 2004.
55. 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 109(10):1292-1298, 2004.
56. Rosing JH, Wong G, Wong MS, Sahar D, Stevenson TR, Pu LL. Autologous fat grafting for primary breast augmentation: a systematic review. Aesthetic Plast Surg 35(5):882-890, 2011.
57. Ross RJ, Shayan R, Mutimer KL, Ashton MW. Autologous fat grafting: current state of the art and critical review. Ann Plast Surg 73(3):352-357, 2014.
58. Rowan BG, Gimble JM, Sheng M, Anbalagan M, Jones RK, Frazier TP, Asher M, Lacayo EA, Friedlander PL, Kutner R, Chiu ES. Human adipose tissue-derived stromal/stem cells promote migration and early metastasis of triple negative breast cancer xenografts. PLoS One 9(2):e89595, 2014.
59. Rubin JP. NCT01924364: Effect of Concentrating Endogenous Stromal Cells in the Fat Graft Using TGI Device (AFIRM-TGI). Available online at: https://www.clinicaltrials.gov/ct2/show/NCT01924364 (accessed Mar. 17, 2015). 2012.
60. Rubin JP, Marra KG. Soft tissue reconstruction. Methods Mol Biol 702:395-400, 2011.
61. Ryu H, Oh JE, Rhee KJ, Baik SK, Kim J, Kang SJ, Sohn JH, Choi E, Shin HC, Kim YM, Kim HS, Bae KS, Eom YW. Adipose tissue-derived mesenchymal stem cells cultured at high density express IFN-beta and suppress the growth of MCF-7 human breast cancer cells. Cancer Lett 352(2):220-227, 2014.
62. Siebert JW, Longaker MT, Angrigiani C. The inframammary extended circumflex scapular flap: an aesthetic improvement of the parascapular flap. Plast Reconstr Surg 99(1):70-77, 1997.
63. Sivan U, Jayakumar K, Krishnan LK. Constitution of fibrin-based niche for in vitro differentiation of adipose-derived mesenchymal stem cells to keratinocytes. Biores Open Access 3(6):339-347, 2014.
64. Slack GC, Tabit CJ, Allam KA, Kawamoto HK, Bradley JP. Parry-Romberg reconstruction: beneficial results despite poorer fat take. Ann Plast Surg 73(3):307-310, 2014.
65. Suga H, Eto H, Aoi N, Kato H, Araki J, Doi K, Higashino T, Yoshimura K. Adipose tissue remodeling under ischemia: death of adipocytes and activation of stem/progenitor cells. Plast Reconstr Surg 126(6):1911-1923, 2010.
66. Sultan SM, Stern CS, Allen RJ, Jr, Thanik VD, Chang CC, Nguyen PD, Canizares O, Szpalski C, Saadeh PB, Warren SM, Coleman SR, Hazen A. Human fat grafting alleviates radiation skin damage in a murine model. Plast Reconstr Surg 128(2):363-372, 2011.
67. Sun B, Roh KH, Park JR, Lee SR, Park SB, Jung JW, Kang SK, Lee YS, Kang KS. Therapeutic potential of mesenchymal stromal cells in a mouse breast cancer metastasis model. Cytotherapy 11(3):289-298, 281 p following 298, 2009.
68. Tabit CJ, Slack GC, Fan K, Wan DC, Bradley JP. Fat Grafting Versus Adipose-Derived Stem Cell Therapy: Distinguishing Indications, Techniques, and Outcomes. Aesthetic Plast Surg 36(3):704-713, 2011.
69. Tanikawa DY, Aguena M, Bueno DF, Passos-Bueno MR, Alonso N. Fat grafts supplemented with adipose-derived stromal cells in the rehabilitation of patients with craniofacial microsomia. Plast Reconstr Surg 132(1):141-152, 2013.
70. Thangarajah H, Vial IN, Chang E, El-Ftesi S, Januszyk M, Chang EI, Paterno J, Neofytou E, Longaker MT, Gurtner GC. IFATS collection: Adipose stromal cells adopt a proangiogenic phenotype under the influence of hypoxia. Stem Cells 27(1):266-274, 2009.
71. Van Harmelen V, Skurk T, Hauner H. Primary culture and differentiation of human adipocyte precursor cells. Methods Mol Med 107:125-135, 2005.
72. Wang L, Luo X, Lu Y, Fan ZH, Hu X. Is the Resorption of Grafted Fat Reduced in Cell-Assisted Lipotransfer for Breast Augmentation? Ann Plast Surg, epub ahead of print, Mar. 28, 2014.
73. Wetterau M, Szpalski C, Hazen A, Warren SM. Autologous fat grafting and facial reconstruction. J Craniofac Surg 23(1):315-318, 2012.
74. 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 16(2):169-175, 2010.
75. Yoshimura K, Sato K, Aoi N, Kurita M, Hirohi T, Harii K. Cell-assisted lipotransfer for cosmetic breast augmentation: supportive use of adipose-derived stem/stromal cells. Aesthetic Plast Surg 32(1):48-55; discussion 56-47, 2008a.
76. 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 34(9):1178-1185, 2008b.
77. Yoshimura K, Shigeura T, Matsumoto D, Sato T, Takaki Y, Aiba-Kojima E, Sato K, Inoue K, Nagase T, Koshima I, Gonda K. Characterization of freshly isolated and cultured cells derived from the fatty and fluid portions of liposuction aspirates. J Cell Physiol 208(1):64-76, 2006.
78. Yu G, Wu X, Dietrich MA, Polk P, Scott LK, Ptitsyn AA, Gimble JM. Yield and characterization of subcutaneous human adipose-derived stem cells by flow cytometric and adipogenic mRNA analyzes. Cytotherapy 12(4):538-546, 2010.
79. Zhang Z, Luo X, Xu H, Wang L, Jin X, Chen R, Ren X, Lu Y, Fu M, Huang Y, He J, Fan Z. Bone marrow stromal cell-derived extracellular matrix promotes osteogenesis of adipose-derived stem cells. Cell Biol Int 39(3):291-299, 2015.
80. 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 64(2):222-228, 2010.
81. Zhu Y, Sun Z, Han Q, Liao L, Wang J, Bian C, Li J, Yan X, Liu Y, Shao C, Zhao RC. Human mesenchymal stem cells inhibit cancer cell proliferation by secreting DKK-1. Leukemia 23(5):925-933, 2009.
82. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, Alfonso ZC, Fraser JK, Benhaim P, Hedrick MH. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13(12):4279-4295, 2002.