Deleterious effects of freezing on osteogenic differentiation of human adipose-derived stromal cells in vitro and in vivo

Stem Cells and Development

Volumn 20, Issue 3, 2011, Pages 427-439

  James, Aaron W ^a   Levi, Benjamin ^a   Nelson, Emily R ^a   Peng, Michelle ^a   Commons, George W ^a   Lee, Min ^b   Wu, Benjamin ^b   Longaker, Michael T ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROXYAPATITE; RECOMBINANT BONE MORPHOGENETIC PROTEIN 4; RECOMBINANT GROWTH FACTOR; RECOMBINANT SOMATOMEDIN C; UNCLASSIFIED DRUG;

ADIPOGENESIS; ADIPOSE TISSUE; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; CELL STRUCTURE; CELL VIABILITY; ENGRAFTMENT; FEMALE; FRACTURE HEALING; FREEZE THAWING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SKULL DEFECT; STORAGE TEMPERATURE; STROMA CELL;

ADIPOSE TISSUE; ALKALINE PHOSPHATASE; ANIMALS; BONE REGENERATION; CELL ADHESION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; CRYOPRESERVATION; FEMALE; FREEZING; GENE EXPRESSION; HUMANS; MALE; MICE; MICE, NUDE; MIDDLE AGED; MULTIPOTENT STEM CELLS; OSTEOCYTES; SKULL; TRANSPLANTATION, HETEROLOGOUS;

BOVINAE; MUS;

EID: 79952146857     PISSN: 15473287     EISSN: None     Source Type: Journal    
DOI: 10.1089/scd.2010.0082     Document Type: Article

References (55)

1. Kwan MD, BJ Slater, DC Wan and MT Longaker. (2008). Cell-based therapies for skeletal regenerative medicine. Hum Mol Genet 17:R93-R98.
2. Zuk PA, M Zhu, P Ashjian, DA De Ugarte, JI Huang, H Mizuno, ZC Alfonso, JK Fraser, P Benhaim and MH Hedrick. (2002). Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13:4279-4295. (Pubitemid 35471185)
3. Zuk PA, M Zhu, H Mizuno, J Huang, JW Futrell, AJ Katz, P Benhaim, HP Lorenz and MH Hedrick. (2001). Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7:211-228. (Pubitemid 32295155)
4. Xu Y, KE Hammerick, AW James, AL Carre, P Leucht, AJ Giaccia and MT Longaker. (2009). Inhibition of histone deacetylase activity in reduced oxygen environment enhances the osteogenesis of mouse adipose-derived stromal cells. Tissue Eng Part A 15:3697-3707.
5. Wan DC, JH Pomerantz, LJ Brunet, JB Kim, YF Chou, BM Wu, R Harland, HM Blau and MT Longaker. (2007). Noggin suppression enhances in vitro osteogenesis and accelerates in vivo bone formation. J Biol Chem 282: 26450-26459. (Pubitemid 47443797)
6. Wan DC, YY Shi, RP Nacamuli, N Quarto, KM Lyons and MT Longaker. (2006). Osteogenic differentiation of mouse adipose-derived adult stromal cells requires retinoic acid and bone morphogenetic protein receptor type IB signaling. Proc Natl Acad Sci U S A 103:12335-12340. (Pubitemid 44267260)
7. Wan DC, MT Siedhoff, MD Kwan, RP Nacamuli, BM Wu and MT Longaker. (2007). Refining retinoic acid stimulation for osteogenic differentiation of murine adipose-derived adult stromal cells. Tissue Eng 13:1623-1631. (Pubitemid 47105769)
8. Skillington J, L Choy and R Derynck. (2002). Bone morphogenetic protein and retinoic acid signaling cooperate to induce osteoblast differentiation of preadipocytes. J Cell Biol 159:135-146. (Pubitemid 35191525)
9. Cho HH, HT Park, YJ Kim, YC Bae, KT Suh and JS Jung. (2005). Induction of osteogenic differentiation of human mesenchymal stem cells by histone deacetylase inhibitors. J Cell Biochem 96:533-542. (Pubitemid 41504651)
10. Dragoo JL, JY Choi, JR Lieberman, J Huang, PA Zuk, J Zhang, MH Hedrick and P Benhaim. (2003). Bone induction by BMP-2 transduced stem cells derived from human fat. J Orthop Res 21:622-629. (Pubitemid 36758206)
11. Cowan CM, YY Shi, OO Aalami, YF Chou, C Mari, R Thomas, N Quarto, CH Contag, B Wu and MT Longaker. (2004). Adipose-derived adult stromal cells heal critical-size mouse calvarial defects. Nat Biotechnol 22:560-567. (Pubitemid 38585908)
12. Levi B, AW James, ER Nelson, D Vistnes, B Wu, M Lee, A Gupta and M Longaker. (2010). Human adipose derived stromal cells heal critical size mouse calvarial defects. PLoS ONE 5:e11177.
13. Gupta DM, MD Kwan, BJ Slater, DC Wan and MT Longaker. (2008). Applications of an athymic nude mouse model of nonhealing critical-sized calvarial defects. J Craniofac Surg 19:192-197. (Pubitemid 351158821)
14. Peterson B, J Zhang, R Iglesias, M Kabo, M Hedrick, P Benhaim and JR Lieberman. (2005). Healing of critically sized femoral defects, using genetically modified mesenchymal stem cells from human adipose tissue. Tissue Eng 11:120-129. (Pubitemid 40515180)
15. Dragoo JL, JR Lieberman, RS Lee, DA Deugarte, Y Lee, PA Zuk, MH Hedrick and P Benhaim. (2005). Tissueengineered bone from BMP-2-transduced stem cells derived from human fat. Plast Reconstr Surg 115:1665-1673. (Pubitemid 40604737)
16. Knippenberg M, MN Helder, B Zandieh Doulabi, PI Wuisman and J Klein-Nulend. (2006). Osteogenesis versus chondrogenesis by BMP-2 and BMP-7 in adipose stem cells. Biochem Biophys Res Commun 342:902-908. (Pubitemid 43320483)
17. Cowan CM, OO Aalami, YY Shi, YF Chou, C Mari, R Thomas, N Quarto, RP Nacamuli, CH Contag, B Wu and MT Longaker. (2005). Bone morphogenetic protein 2 and retinoic acid accelerate in vivo bone formation, osteoclast recruitment, and bone turnover. Tissue Eng 11:645-658. (Pubitemid 40632579)
18. Xu Y, P Malladi, DR Wagner and MT Longaker. (2005). Adipose-derived mesenchymal cells as a potential cell source for skeletal regeneration. Curr Opin Mol Ther 7:300-305. (Pubitemid 41103049)
19. Levi B, AW James, DC Wan, JP Glotzbach, GW Commons and MT Longaker. (2010). Regulation of human adiposederived stromal cell osteogenic differentiation by insulin-like growth factor-1 and platelet-derived growth factor-alpha. Plast Reconstr Surg 126:41-52.
20. Xu Y, DR Wagner, E Bekerman, M Chiou, AW James, D Carter and M Longaker. (2010). Connective tissue growth factor in regulation of rhoA mediated cytoskeletal tension associated osteogenesis of mouse adipose-derived stromal cells. PLoS ONE 5:e11279.
21. Edwards PC, S Ruggiero, J Fantasia, R Burakoff, SM Moorji, E Paric, P Razzano, DA Grande and JM Mason. (2005). Sonic hedgehog gene-enhanced tissue engineering for bone regeneration. Gene Ther 12:75-86. (Pubitemid 40090047)
22. Jager M, C Zilkens, B Bittersohl and R Krauspe. (2009). Cord blood-an alternative source for bone regeneration. Stem Cell Rev 5:266-277.
23. Valeri CR and LE Pivacek. (1996). Effects of the temperature, the duration of frozen storage, and the freezing container on in vitro measurements in human peripheral blood mononuclear cells. Transfusion 36:303-308. (Pubitemid 26141053)
24. Bakken AM. (2006). Cryopreserving human peripheral blood progenitor cells. Curr Stem Cell Res Ther 1:47-54.
25. Fleming KK and A Hubel. (2006). Cryopreservation of hematopoietic and non-hematopoietic stem cells. Transfus Apher Sci 34:309-315. (Pubitemid 44247908)
26. Thirumala S, S Zvonic, E Floyd, JM Gimble and RV Devireddy. (2005). Effect of various freezing parameters on the immediate post-thaw membrane integrity of adipose tissue derived adult stem cells. Biotechnol Prog 21:1511-1524. (Pubitemid 41443006)
27. Devireddy RV, S Thirumala and JM Gimble. (2005). Cellular response of adipose derived passage-4 adult stem cells to freezing stress. J Biomech Eng 127:1081-1086. (Pubitemid 43067263)
28. Oishi K, H Noguchi, H Yukawa, T Miyazaki, R Kato, Y Kitagawa, M Ueda and S Hayashi. (2008). Cryopreservation of mouse adipose tissue-derived stem=progenitor cells. Cell Transpl 17:35-41. (Pubitemid 351551378)
29. Liu G, H Zhou, Y Li, G Li, L Cui, W Liu and Y Cao. (2008). Evaluation of the viability and osteogenic differentiation of cryopreserved human adipose-derived stem cells. Cryobiology 57:18-24.
30. Thirumala S, X Wu, J Gimble and R Devireddy. (2009). Evaluation of polyvinylpyrollidone (PVP) as a cryoprotectant for adipose derived adult stem cells (ASCs). Tissue Eng Part C Methods Oct 19 [Epub ahead of print].
31. Thirumala S, JM Gimble and RV Devireddy. (2010). Cryopreservation of stromal vascular fraction of adipose tissue in a serum-free freezing medium. J Tissue Eng Regen Med 4:224-232.
32. James AW, Y Xu, R Wang and MT Longaker. (2008). Proliferation, osteogenic differentiation, and fgf-2 modulation of posterofrontal=sagittal suture-derived mesenchymal cells in vitro. Plast Reconstr Surg 122:53-63.
33. Levi B, AW James, J Glotzbach, D Wan, GW Commons and MT Longaker. (2010). Depot specific variation in the osteogenic and adipogenic potential of human adipose-derived stromal cells. Plast Reconstr Surg 126:822-834.
34. Xu Y, AW James and MT Longaker. (2008). Transforming growth factor-beta1 stimulates chondrogenic differentiation of posterofrontal suture-derived mesenchymal cells in vitro. Plast Reconstr Surg 122:1649-1659.
35. James AW, Y Xu, JK Lee, R Wang and MT Longaker. (2009). Differential effects of TGF-beta1 and TGF-beta3 on chondrogenesis in posterofrontal cranial suture-derived mesenchymal cells in vitro. Plast Reconstr Surg 123:31-43.
36. James AW, AA Theologis, SA Brugmann, Y Xu, AL Carre, P Leucht, K Hamilton, KS Korach and MT Longaker. (2009). Estrogen=estrogen receptor alpha signaling in mouse posterofrontal cranial suture fusion. PLoS ONE 4:e7120.
37. Panetta NJ, DM Gupta, JK Lee, DC Wan, GW Commons and MT Longaker. (2010). Human adipose-derived stromal cells respond to and elaborate bone morphogenetic protein-2 during in vitro osteogenic differentiation. Plast Reconstr Surg 125:483-493.
38. Malladi P, Y Xu, M Chiou, AJ Giaccia and MT Longaker. (2006). Effect of reduced oxygen tension on chondrogenesis and osteogenesis in adipose-derived mesenchymal cells. Am J Physiol 290:C1139-C1146.
39. Xu Y, P Malladi, M Chiou, E Bekerman, AJ Giaccia and MT Longaker. (2007). In vitro expansion of adipose-derived adult stromal cells in hypoxia enhances early chondrogenesis. Tissue Eng 13:2981-2993. (Pubitemid 350233076)
40. Mvula B, TJ Moore and H Abrahamse. (2010). Effect of lowlevel laser irradiation and epidermal growth factor on adult human adipose-derived stem cells. Lasers Med Sci 25:33-39.
41. Lee JK, DM Gupta, NJ Pannetta, B Levi, AW James, D Wan and M Longaker. (2010). Elucidating mechanisms of osteogenesis in human adipose-derived stromal cells via microarray analysis. J Craniofac Surg Jul 2 [Epub ahead of print].
42. Lecoeur L and JP Ouhayoun. (1997). In vitro induction of osteogenic differentiation from non-osteogenic mesenchymal cells. Biomaterials 18:989-993. (Pubitemid 27296559)
43. Canalis E. (1980). Effect of insulinlike growth factor I on DNA and protein synthesis in cultured rat calvaria. J Clin Invest 66:709-719. (Pubitemid 10060939)
44. Schlechter NL, SM Russell, EM Spencer and CS Nicoll. (1986). Evidence suggesting that the direct growthpromoting effect of growth hormone on cartilage in vivo is mediated by local production of somatomedin. Proc Natl Acad Sci U S A 83:7932-7934. (Pubitemid 17183957)
45. Schoenle E, J Zapf, RE Humbel and ER Froesch. (1982). Insulin- like growth factor I stimulates growth in hypophysectomized rats. Nature 296:252-253. (Pubitemid 12072141)
46. Tanaka H, R Quarto, S Williams, J Barnes and CT Liang. (1994). In vivo and in vitro effects of insulin-like growth factor-I (IGF-I) on femoral mRNA expression in old rats. Bone 15:647-653. (Pubitemid 24332657)
47. Canalis E, TL McCarthy and M Centrella. (1991). Growth factors and cytokines in bone cell metabolism. Annu Rev Med 42:17-24.
48. Rodan GA. (1992). Introduction to bone biology. Bone 13 (Suppl. 1):S3-S6.
49. Machwate M, E Zerath, X Holy, P Pastoureau and PJ Marie. (1994). Insulin-like growth factor-I increases trabecular bone formation and osteoblastic cell proliferation in unloaded rats. Endocrinology 134:1031-1038. (Pubitemid 24085547)
50. Dudas JR, KG Marra, GM Cooper, VM Penascino, MP Mooney, S Jiang, JP Rubin and JE Losee. (2006). The osteogenic potential of adipose-derived stem cells for the repair of rabbit calvarial defects. Ann Plast Surg 56:543-548. (Pubitemid 43970240)
51. Tchkonia T, M Lenburg, T Thomou, N Giorgadze, G Frampton, T Pirtskhalava, A Cartwright, M Cartwright, J Flanagan, I Karagiannides, N Gerry, RA Forse, Y Tchoukalova, MD Jensen, C Pothoulakis and JL Kirkland. (2007). Identification of depot-specific human fat cell progenitors through distinct expression profiles and developmental gene patterns. Am J Physiol Endocrinol Metab 292:E298-E307. (Pubitemid 46052953)
52. van Beek EA, AH Bakker, PM Kruyt, MH Hofker, WH Saris and J Keijer. (2007). Intra- and interindividual variation in gene expression in human adipose tissue. Pflugers Arch 453:851-861. (Pubitemid 46294932)
53. Samulin J, S Lien, E Grindflek, I Berget, B Ruyter and H Sundvold. (2008). Depot specific differences during adipogenesis of porcine stromal-vascular cells. Cell Biol Int 32:525-531.
54. Schipper BM, KG Marra, W Zhang, AD Donnenberg and JP Rubin. (2008). Regional anatomic and age effects on cell function of human adipose-derived stem cells. Ann Plast Surg 60:538-544. (Pubitemid 351591463)
55. Aksu AE, JP Rubin, JR Dudas and KG Marra. (2008). Role of gender and anatomical region on induction of osteogenic differentiation of human adipose-derived stem cells. Ann Plast Surg 60:306-322.