A Xenogeneic-Free Protocol for Isolation and Expansion of Human Adipose Stem Cells for Clinical Uses

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Escobedo Lucea, Carmen ^a,b   Bellver, Carmen ^a   Gandia, Carolina ^b   Sanz Garcia, Andres ^b   Esteban, Francisco J ^c   Mirabet, Vicente ^d   Forte, Giancarlo ^e,f   Moreno, Isabel ^g   Lezameta, Melissa ^a   Ayuso Sacido, Angel ^b,h   Garcia Verdugo, José M ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF JAÉN   (Spain)

^d Cell and Tissue Bank   (Spain)

^e NATIONAL INSTITUTE FOR MATERIALS SCIENCE   (Japan)

^f ST ANNE S UNIVERSITY HOSPITAL   (Czech Republic)

^g UNIVERSITY OF VALENCIA   (Spain)

^h Hospital de Madrid   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; HUMAN SERUM ALBUMIN;

ADIPOSE DERIVED STEM CELL; ADIPOSE TISSUE; ADULT; ARTICLE; CELL DIFFERENTIATION; CELL EXPANSION; CELL ISOLATION; CELL PROLIFERATION; CELL STRUCTURE; CELL THERAPY; CLINICAL ARTICLE; CLINICAL PROTOCOL; CYTOKINE RELEASE; FEMALE; GENE EXPRESSION; GROWTH CURVE; HUMAN; HUMAN CELL; MALE; MICROARRAY ANALYSIS; REGENERATIVE MEDICINE; TISSUE ENGINEERING; XENOGRAFT;

ADIPOCYTES; ADOLESCENT; ADULT; ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SEPARATION; CELL- AND TISSUE-BASED THERAPY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; HUMANS; METABOLIC NETWORKS AND PATHWAYS; PRIMARY CELL CULTURE; REGENERATIVE MEDICINE; STEM CELLS; TISSUE ENGINEERING; YOUNG ADULT;

ANIMALIA;

EID: 84879940296     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0067870     Document Type: Article

References (53)

1. Alvarez PD, Garcia-Arranz M, Georgiev-Hristov T, Garcia-Olmo DA, (2008) New bronchoscopic treatment of tracheomediastinal fistula using autologous adipose-derived stem cells. Thorax 63: 374-376.
2. Bensidhoum M, Gobin S, Chapel A, Lemaitre G, Bouet S, et al. (2005) Therapeutic effect of human mesenchymal stem cells in skin after radiation damage. J Soc Biol 199: 337-341.
3. Bieback K, Ha VA, Hecker A, Grassi M, Kinzebach S, et al. (2010) Altered gene expression in human adipose stem cells cultured with fetal bovine serum compared to human supplements. Tissue Eng Part A 16: 3467-3484.
4. Bieback K, Hecker A, Kocaömer A, Lannert H, Schallmoser K, et al. (2009) Human alternatives to fetal bovine serum for the expansion of mesenchymal stromal cells from bone marrow. Stem Cells 27: 2331-2341.
5. Bieback K, Kern S, Kocaomer A, Ferlik K, Bugert P, (2008) Comparing mesenchymal stromal cells from different human tissues: bone marrow, adipose tissue and umbilical cord blood. Biomed Mater Eng 18: S71-76.
6. Phinney DG, Prockop DJ, (2007) Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair-current views. Stem Cells 25: 2896-2902.
7. Planat-Benard V, Menard C, Andre M, Puceat M, Perez A, et al. (2004) Spontaneous cardiomyocyte differentiation from adipose tissue stroma cells. Circ Res 94: 223-229.
8. Kern S, Eichler H, Stoeve J, Klüter H, Bieback K, (2006) Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 24: 1294-1301.
9. Yen BL, Huang HI, Chien CC, Jui HK, Ko BS, et al. (2005) Isolation of multipotent cells from human term placenta. Stem Cells 23: 3-9.
10. Young HE, Steele TA, Bray RA, Hudson J, Floyd JA, et al. (2001) Human reserve pluripotent mesenchymal stem cells are present in the connective tissues of skeletal muscle and dermis derived from fetal, adult, and geriatric donors. Anat Rec 264: 51-62.
11. Zuk PAZM, Ashjian P, De Ugarte DA, Huang JI, Alfonso ZC, et al. (2002) Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13: 4279-4295.
12. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, et al. (2001) Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7: 211-228.
13. Friedenstein AJ, Gorskaja JF, Kulagina NN, (1976) Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol 4: 267-274.
14. Garcia-Olmo D, Garcia-Arranz M, Garcia LG, Cuellar ES, Blanco IF, et al. (2003) Autologous stem cell transplantation for treatment of rectovaginal fistula in perianal Crohn's disease: a new cell-based therapy. Int J Colorectal Dis 18: 451-454.
15. Garcia-Olmo D, Herreros D, De-La-Quintana P, Guadalajara H, Trébol J, et al. (2010) Adipose-derived stem cells in Crohn's rectovaginal fistula. Case Report Med 2010: 617-658.
16. Horwitz EM, Prockop DJ, Fitzpatrick LA, Koo WW, Gordon PL, et al. (1999) Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med 5: 309-313.
17. Nie C, Yang D, Xu J, Si Z, Jing X, et al. (2011) Locally administered adipose-derived stem cells accelerate wound healing through differentiation and vasculogenesis. Cell Transplant 20: 205-216.
18. Sanz-Ruiz R, Fernández-Santos E, Domínguez-Muñoa M, Parma R, Villa A, et al. (2009) Early translation of adipose-derived cell therapy for cardiovascular disease. Cell Transplant 18: 245-254.
19. Fraser JK, Zhu M, Wulur I, Alfonso Z (2008) Adipose-derived stem cells. In: D.J. Prockop DGP, and B.A Bunnell, editor. Methods in Molecular Biology. Totowa, NJ: Humana Press. 59-57.
20. Kuhbier JW, Weyand B, Radtke C, Vogt PM, Casper C, et al. (2010) Isolation, characterization, differentiation, and application of adipose-derived stem cells. Adv Biochem Eng Biotechnol 123: 55-105.
21. Kocaoemer A, Kern S, Klüter H, Bieback K, (2007) Human AB serum and thrombin-activated platelet-rich plasma are suitable alternatives to fetal calf serum for the expansion of mesenchymal stem cells from adipose tissue. Stem Cells 25: 1270-1278.
22. Yanez R, Oviedo A, Aldea M, Bueren JA, Lamana ML, (2010) Prostaglandin E2 plays a key role in the immunosuppressive properties of adipose and bone marrow tissue-derived mesenchymal stromal cells. Exp Cell Res 316: 3109-3123.
23. Puissant B, Barreau C, Bourin P, Clavel C, Corre J, et al. (2005) Immunomodulatory effect of human adipose tissue-derived adult stem cells: comparison with bone marrow mesenchymal stem cells. Br J Haematol 129: 118-129.
24. Gimble JM, Katz AJ, Bunnell BA, (2007) Adipose-derived stem cells for regenerative medicine. Circ Res 100: 1249-1260.
25. Fang B, Song YP, Li N, Li J, Han Q, et al. (2009) Mesenchymal stem cells for the treatment of refractory pure red cell aplasia after major ABO-incompatible hematopoietic stem cell transplantation. Ann Hematol 88: 261-266.
26. Fang B, Song Y, Zhao RC, Han Q, Lin Q, (2007) Using human adipose tissue-derived mesenchymal stem cells as salvage therapy for hepatic graft-versus-host disease resembling acute hepatitis. Transplant Proc 39: 1710-1713.
27. National Institute of Health website. Available: http://www.clinicaltrials.gov. Accessed 2013 Jun 3.
28. Matsumoto D, Sato K, Gonda K, Takaki Y, Shigeura T, et al. (2006) Cell-assisted lipotransfer: supportive use of human adipose-derived cells for soft tissue augmentation with lipoinjection. Tissue Eng Part A 12: 3375-3382.
29. Yoshimura K, Sato K, Aoi N, Kurita M, Hirohi T, et al. (2008) Cell-assisted lipotransfer for cosmetic breast augmentation: supportive use of adipose-derived stem/stromal cells. Aesthetic Plast Surg 32: 48-55.
30. Mannello F, Tonti GA, (2007) Concise review: no breakthroughs for human mesenchymal and embryonic stem cell culture: conditioned medium, feeder layer, or feeder-free; medium with fetal calf serum, human serum, or enriched plasma; serum-free, serum replacement nonconditioned medium, or ad hoc formula? All that glitters is not gold! Stem Cells 25: 1603-1609.
31. Martin MJ, Muotri A, Gage F, Varki A, (2005) Human embryonic stem cells express an immunogenic nonhuman sialic acid. Nat Med 11: 228-232.
32. Bihl F, Negro F, (2010) Hepatitis E virus: a zoonosis adapting to humans. J Antimicrob Chemother 65: 817-821.
33. Erickson GA, Bolin SR, Landgraf JG, (1991) Viral contamination of fetal bovine serum used for tissue culture: risks and concerns. Dev Biol Stand 75: 173-175.
34. Knight R, (2010) The risk of transmitting prion disease by blood or plasma products. Transfus Apher Sci 43: 387-391.
35. Willkommen H, Scheiblauer H, Lower J, (1999) Serum and serum substitutes: virus safety by inactivation or removal. Dev Biol Stand 99: 131-138.
36. Organization WH (1997) Medicinal and other products and human and animal transmissible spongiform encephalopaties: Memorandum from a WHO meeting. BullWorld Health Organ 75: 505-513.
37. Selvaggi TA, Walker RE, Fleisher TA, (1997) Development of antibodies to fetal calf serum with arthus-like reactions in human immunodeficiency virus-infected patients given syngeneic lymphocyte infusions. Blood 89: 776-779.
38. Mackensen A, Drager R, Schlesier M, Mertelsmann R, Lindemann A, (2000) Presence of IgE antibodies to bovine serum albumin in a patient developing anaphylaxis after vaccination with human peptide-pulsed dendritic cells. Cancer Immunol Immunother 49: 152-156.
39. R-project software website. Available: http://www.r-project.org/. Accessed 2013 Jun 3.
40. Bioconductor packages website. Available: http://www.bioconductor.org/. Accessed 2013 Jun 3.
41. Wettenhall JM, Smyth GK, (2004) limmaGUI: a graphical user interface for linear modeling of microarray data. Bioinformatics 20: 3705-3706.
42. Huang W, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
43. Ingenuity Pathway Analysis website. Available: http://www.ingenuity.com/. Accessed 2013 Jun 3.
44. Sherman BT, Huang dW, Tan Q, Guo Y, Bour S, et al. (2007) DAVID Knowledgebase: a gene-centered database integrating heterogeneous gene annotation resources to facilitate high-throughput gene functional analysis. BMC Bioinformatics 8: 426.
45. Sundin M, Ringden O, Sundberg B, Nava S, Götherström C, et al. (2007) No alloantibodies against mesenchymal stromal cells, but presence of anti-fetal calf serum antibodies, after transplantation in allogeneic hematopoietic stem cell recipients. Haematologica 92: 1208-1215.
46. Spees JL, Gregory CA, Singh H, Tucker HA, Peister A, et al. (2004) Internalized antigens must be removed to prepare hypoimmunogenic mesenchymal stem cells for cell and gene therapy. Mol Ther 9: 747-756.
47. Shahdadfar A, Fronsdal K, Haug T, (2005) In vitro expansion of human mesenchymal stem cells: choice of serum is a determinant of cell proliferation, differentiation, gene expression, and transcriptome stability. Stem Cells 23: 1357-1366.
48. Lindroos B, Aho K-L, Kuokkanen H, Räty S, Huhtala H, et al. (2010) Differential gene expression in adipose stem cells cultured in allogeneic human serum versus fetal bovine serum. Tissue Eng Part A 7: 2281-2294.
49. Stute N, Holtz K, Bubenheim M, Lange C, Blake F, et al. (2004) Autologous serum for isolation and expansion of human mesenchymal stem cells for clinical use. Exp Hematol 32: 1212-1225.
50. Muller I, Kordowich S, Holzwarth C, Spano C, Isensee G, et al. (2006) Animal serum-free culture conditions for isolation and expansion of multipotent mesenchymal stromal cells from human BM. Cytotherapy 8: 437-444.
51. Dromard C, Bourin P, Andre M, De Barros S, Casteilla L, et al. (2011) Human adipose derived stroma/stem cells grow in serum-free medium as floating spheres. Exp Cell Res 317: 770-780.
52. Le Blanc K, Gotherstrom C, Ringden O, Hassan M, McMahon R, et al. (2005) Fetal mesenchymal stem-cell engraftment in bone after in utero transplantation in a patient with severe osteogenesis imperfecta. Transplantation 79: 1607-1614.
53. Yanez R, Lamana ML, Garcia-Castro J, Colmenero I, Ramirez M, et al. (2006) Adipose tissue-derived mesenchymal stem cells have in vivo immunosuppressive properties applicable for the control of the graft-versus-host disease. Stem Cells 24: 2582-2591.