Hypoxia enhances proliferation and stemness of human adipose-derived mesenchymal stem cells

Cytotechnology

Volumn 67, Issue 6, 2015, Pages 1073-1084

  Fotia, Caterina ^a   Massa, Annamaria ^a   Boriani, Filippo ^a   Baldini, Nicola ^a,b   Granchi, Donatella ^a  

^a RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Adipose derived MSC; Hypoxia; Intact adipose tissue; Proliferation; Regenerative medicine; Stemness

Indexed keywords

ANTIGEN; CD140 ANTIGEN; CD34 ANTIGEN; CD45 ANTIGEN; COLLAGENASE; COLLAGENASE 2; UNCLASSIFIED DRUG;

ADIPOCYTE; ADIPOSE DERIVED MESENCHYMAL STEM CELL; ADULT; ARTICLE; BETA ACTIN GENE; CELL CLONING; CELL FUNCTION; CELL HETEROGENEITY; CELL ISOLATION; CELL LINEAGE; CELL PROLIFERATION; CELL STEMNESS; ENDOTHELIUM CELL; FEMALE; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; IMMUNOPHENOTYPING; LEUKOCYTE; MALE; MESENCHYMAL STEM CELL; OCTAMER TRANSCRIPTION FACTOR 4 GENE; OSTEOBLAST; OXYGEN TENSION; PERICYTE; PROTEIN EXPRESSION; TRANSCRIPTION FACTOR NANOG GENE; TRANSCRIPTION FACTOR SOX2 GENE;

EID: 84946478812     PISSN: 09209069     EISSN: 15730778     Source Type: Journal    
DOI: 10.1007/s10616-014-9731-2     Document Type: Article

References (47)

1. Arvidson K, Abdallah BM, Applegate LA, Baldini N, Cenni E, Gomez-Barrena E, Granchi D, Kassem M, Konttinen YT, Mustafa K, Pioletti DP, Sillat T, Finne-Wistrand A (2011) Bone regeneration and stem cells. J Cell Mol Med 15:718–746
2. Baer PC, Kuçi S, Krause M, Kuçi Z, Zielen S, Geiger H, Bader P, Schubert R (2013) Comprehensive phenotypic characterization of human adipose-derived stromal/stem cells and their subsets by a high throughput technology. Stem Cells Dev 22:330–339
3. Baksh D, Davies JE, Zandstra PW (2003) Adult human bone marrow-derived mesenchymal progenitor cells are capable of adhesion-independent survival and expansion. Exp Hematol 31:723–732
4. Baptista LS, do Amaral RJ, Carias RB, Aniceto M, Claudio-da-Silva C, Borojevic R (2009) An alternative method for the isolation of mesenchymal stromal cells derived from lipoaspirate samples. Cytotherapy 11:706–715
5. Barrilleaux B, Phinney DG, Prockop DJ, O’Connor KC (2006) Review: ex vivo engineering of living tissues with adult stem cells. Tissue Eng 12:3007–3019
6. Berg JS, Goodell MA (2007) An argument against a role for Oct4 in somatic stem cells. Cell Stem Cell 1:359–360
7. Bourin P, Bunnell BA, Casteilla L, Dominici M, Katz AJ, March KL, Redl H, Rubin JP, Yoshimura K, Gimble JM (2013) Stromal cells from the adipose tissue-derived stromal vascular fraction and culture expanded adipose tissue-derived stromal/stem cells: a joint statement of the International Federation for Adipose Therapeutics and Science (IFATS) and the International Society for Cellular Therapy (ISCT). Cytotherapy 15:641–648
8. Bruder SP, Jaiswal N, Ricalton NS, Mosca JD, Kraus KH, Kadiyala S (1998) Mesenchymal stem cells in osteobiology and applied bone regeneration. Clin Orthop Relat Res 355:S247–S256
9. Bunnell BA, Flaat M, Gagliardi C, Patel B, Ripoll C (2008) Adipose-derived stem cells: isolation, expansion and differentiation. Methods 45:115–120
10. Ciapetti G, Granchi D, Baldini N (2012) The combined use of mesenchymal stromal cells and scaffolds for bone repair. Curr Pharm Des 18:1796–1820
11. Covello KL, Kehler J, Yu H, Gordan JD, Arsham AM, Hu CJ, Labosky PA, Simon MC, Keith B (2006) HIF-2alpha regulates Oct-4: effects of hypoxia on stem cell function, embryonic development, and tumor growth. Genes Dev 20:557–570
12. D’Ippolito G, Diabira S, Howard GA, Roos BA, Schiller PC (2006) Low oxygen tension inhibits osteogenic differentiation and enhances stemness of human MIAMI cells. Bone 39:513–522
13. Eto H, Suga H, Matsumoto D, Inoue K, Aoi N, Kato H, Araki J, Yoshimura K (2009) Characterization of structure and cellular components of aspirated and excised adipose tissue. Plast Reconstr Surg 124:1087–1097
14. Fehrer C, Brunauer R, Laschober G, Unterluggauer H, Reitinger S, Kloss F, Gülly C, Gassner R, Lepperdinger G (2007) Reduced oxygen tension attenuates differentiation capacity of human mesenchymal stem cells and prolongs their lifespan. Aging Cell 6:745–757
15. Forristal CE, Wright KL, Hanley NA, Oreffo RO, Houghton FD (2010) Hypoxia inducible factors regulate pluripotency and proliferation in human embryonic stem cells cultured at reduced oxygen tensions. Reproduction 139:85–97
16. Fraccalvieri M, Datta G, Bogetti P, Verna G, Pedrale R, Bocchiotti MA, Boriani F, Obbialero FD, Kefalas N, Bruschi S (2007) Abdominoplasty after weight loss in morbidly obese patients: a 4-year clinical experience. Obes Surg 17:1319–1324
17. Gimble JM, Bunnell BA, Chiu ES, Guilak F (2011) Concise review: adipose-derived stromal vascular fraction cells and stem cells: let’s not get lost in translation. Stem Cells 29:749–754
18. Granchi D, Ochoa G, Leonardi E, Devescovi V, Baglìo SR, Osaba L, Baldini N, Ciapetti G (2010) Gene expression patterns related to osteogenic differentiation of bone marrow-derived mesenchymal stem cells during ex vivo expansion. Tissue Eng Part C Methods 16:511–524
19. Grayson WL, Zhao F, Bunnell B, Ma T (2007) Hypoxia enhances proliferation and tissue formation of human mesenchymal stem cells. Biochem Biophys Res Commun 358:948–953
20. Gumbiner BM (1996) Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84:345–357
21. http://clinicaltrials.gov (date last accessed 03 June 2013)
22. Huang GTJ, Gronthos S, Shi S (2009) Mesenchymal stem cells derived from dental tissues vs. those from other sources. Their biology and role in regenerative medicine. J Dent Res 88:792–806
23. Isern J, Martín-Antonio B, Ghazanfari R, Martín AM, López JA, Del Toro R, Sánchez-Aguilera A, Arranz L, Martín-Pérez D, Suárez-Lledó M, Marín P, Van Pel M, Fibbe WE, Vázquez J, Scheding S, Urbano-Ispizúa A, Méndez-Ferrer S (2013) Self-renewing human bone marrow mesenspheres promote hematopoietic stem cell expansion. Cell Rep 3:1714–1724
24. 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
25. Kim JH, Park SG, Song SY, Kim JK, Sung JH (2013) Reactive oxygen species-responsive miR-210 regulates proliferation and migration of adipose-derived stem cells via PTPN2. Cell Death Dis 4:e588. doi:10.1038/cddis.2013.117
26. Lecourt S, Vanneaux V, Cras A, Freida D, Heraoui D, Herbi L, Caillaud C, Chomienne C, Marolleau JP, Belmatoug N, Larghero J (2012) Bone marrow microenvironment in an in vitro model of Gaucher disease: consequences of glucocerebrosidase deficiency. Stem Cells Dev 21:239–248
27. Leonardi E, Ciapetti G, Baglìo SR, Devescovi V, Baldini N, Granchi D (2009) Osteogenic properties of late adherent subpopulations of human bone marrow stromal cells. Histochem Cell Biol 132:547–557
28. Liedtke S, Stephan M, Kögler G (2008) Oct4 expression revisited: potential pitfalls for data misinterpretation in stem cell research. Biol Chem 389:845–850
29. Mansilla E, Drago H, Sturla F, Bossi S, Salas E, Marín GH, Ibar R, Soratti C (2007) Matrix superhighways configurations: new concepts for complex organ regeneration. Transpl Proc 39:2431–2433
30. Mohyeldin A, Garzón-Muvdi T, Quiñones-Hinojosa A (2010) Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell 7:150–161
31. Otte A, Bucan V, Reimers K, Hass R (2013) Mesenchymal stem cells maintain long-term in vitro stemness during explant culture. Tissue Eng Part C Methods 19:937–948
32. Pawitan JA (2011) Future research in adipose stem cell engineering. In: Illouz YG, Sterodimas A (eds) Adipose Stem Cells and Regenerative Medicine. Springer, Berlin, pp 257–272
33. Pierantozzi E, Gava B, Manini I, Roviello F, Marotta G, Chiavarelli M, Sorrentino V (2011) Pluripotency regulators in human mesenchymal stem cells: expression of NANOG but not of OCT-4 and SOX-2. Stem Cells Dev 20:915–923
34. Salem HK, Thiemermann C (2010) Mesenchymal stromal cells: current understanding and clinical status. Stem Cells 28:585–596
35. Schäffler A, Büchler C (2007) Concise review: adipose tissue-derived stromal cells—basic and clinical implications for novel cell-based therapies. Stem Cells 25:818–827
36. Schreml S, Babilas P, Fruth S, Orsó E, Schmitz G, Mueller MB, Nerlich M, Prantl L (2009) Harvesting human adipose tissue-derived adult stem cells: resection versus liposuction. Cytotherapy 11:947–957
37. Schroeder JE, Beyth S, Liebergall M (2011) Orthopedic use of adipose-derived stem cells. In: Illouz YG, Sterodimas A (eds) Adipose Stem Cells and Regenerative Medicine. Springer, Berlin, pp 181–191
38. Scotti C, Piccinini E, Takizawa H, Todorov A, Bourgine P, Papadimitropoulos A, Barbero A, Manz MG, Martin I (2013) Engineering of a functional bone organ through endochondral ossification. Proc Natl Acad Sci USA 110:3997–4002
39. Stocchero IN, Stocchero GF (2011) Isolation of stem cells from human adipose tissue: technique, problems and pearls. In: Illouz YG, Sterodimas A (eds) Adipose Stem Cells and Regenerative Medicine. Springer, Berlin, pp 13–18
40. Strioga M, Viswanathan S, Darinskas A, Slaby O, Michalek J (2012) Same or not the same? Comparison of adipose tissue-derived versus bone marrow-derived mesenchymal stem and stromal cells. Stem Cells Dev 21:2724–2752
41. Suga H, Matsumoto D, Eto H, Inoue K, Aoi N, Kato H, Araki J, Yoshimura K (2009) Functional implications of CD34 expression in human adipose-derived stem/progenitor cells. Stem Cells Dev 18:1201–1210
42. Valorani MG, Montelatici E, Germani A, Biddle A, D’Alessandro D, Strollo R, Patrizi MP, Lazzari L, Nye E, Otto WR, Pozzilli P, Alison MR (2012) Pre-culturing human adipose tissue mesenchymal stem cells under hypoxia increases their adipogenic and osteogenic differentiation potentials. Cell Prolif 45:225–238
43. Wang DW, Fermor B, Gimble JM, Awad HA, Guilak F (2005) Influence of oxygen on the proliferation and metabolism of adipose derived adult stem cells. J Cell Physiol 204:184–191
44. Weijers EM, Van Den Broek LJ, Waaijman T, Van Hinsbergh VW, Gibbs S, Koolwijk P (2011) The influence of hypoxia and fibrinogen variants on the expansion and differentiation of adipose tissue-derived mesenchymal stem cells. Tissue Eng Part A 17:2675–2685
45. Zachar V, Rasmussen JG, Fink T (2011) Isolation and growth of adipose tissue-derived stem cells. Methods Mol Biol 698:37–49
46. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH (2001) Multi-lineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7:211–228
47. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, Alfonso ZC, Fraser JK, Benhaim P, Hedrick MH (2002) Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13:4279–4295