Evaluation of senescence in mesenchymal stem cells isolated from equine bone marrow, adipose tissue, and umbilical cord tissue

Stem Cells and Development

Volumn 21, Issue 2, 2012, Pages 273-283

  Vidal, Martin A ^a   Walker, Naomi J ^a   Napoli, Eleonora ^a   Borjesson, Dori L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; SMOOTH MUSCLE ACTIN; TRANSCRIPTION FACTOR SOX2; VIMENTIN;

ADIPOSE DERIVED STEM CELL; ADIPOSE TISSUE; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; CELL AGING; CELL ISOLATION; CELL LINEAGE; CELL POPULATION; CELL PROLIFERATION; CELL TYPE; CONTROLLED STUDY; GENE EXPRESSION; HEMATOPOIETIC STEM CELL; HORSE; IMMUNOCYTOCHEMISTRY; MESENCHYMAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; STEM CELL; TELOMERE; TELOMERE LENGTH; UMBILICAL CORD; UMBILICAL CORD STEM CELL;

ACTINS; ADIPOSE TISSUE; ANIMALS; BIOLOGICAL MARKERS; BONE MARROW CELLS; CELL AGING; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; GENE EXPRESSION; HORSES; MESENCHYMAL STEM CELLS; OSTEONECTIN; SOXB1 TRANSCRIPTION FACTORS; TELOMERE; TELOMERE HOMEOSTASIS; TISSUE BANKS; UMBILICAL CORD; VIMENTIN;

EQUIDAE;

EID: 84855858430     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2010.0589     Document Type: Article

References (62)

1. Passeri S, F Nocchi, R Lamanna, S Lapi, V Miragliotta, E Giannessi, F Abramo, MR Stornelli, M Matarazzo, D Plen-teda, P Urciuoli, F Scatena and A Coli. (2009). Isolation and expansion of equine umbilical cord-derived matrix cells (EUCMCs). Cell Biol Int 33:100-105.
2. Hoynowski SM, MM Fry, BM Gardner, MT Leming, JR Tucker, L Black, T Sand and KE Mitchell. (2007). Characterization and differentiation of equine umbilical cord-derived matrix cells. Biochem Biophys Res Commun 362: 347-353. (Pubitemid 47334921)
3. Cremonesi F, S Violini, A Lange Consiglio, P Ramelli, G Ranzenigo and P Mariani. (2008). Isolation, in vitro culture and characterization of foal umbilical cord stem cells at birth. Vet Res Commun 32 Suppl 1:S139-S142.
4. Toupadakis CA, A Wong, DC Genetos, WK Cheung, DL Borjesson, GL Ferraro, LD Galuppo, JK Leach, SD Owens and CE Yellowley. (2010). Comparison of the osteogenic potential of equine mesenchymal stem cells from bone marrow, adipose tissue, umbilical cord blood, and umbilical cord tissue. Am J Vet Res 71:1237-1245.
5. Berg L, T Koch, T Heerkens, K Bessonov, P Thomsen and D Betts. (2009). Chondrogenic potential of mesenchymal stro-mal cells derived from equine bone marrow and umbilical cord blood. Vet Comp Orthop Traumatol 22:363-370.
6. Koch TG, PD Thomsen and DH Betts. (2009). Improved isolation protocol for equine cord blood-derived mesenchy-mal stromal cells. Cytotherapy 11:443-447.
7. Bartholomew S, SD Owens, GL Ferraro, DD Carrade, DJ Lara, FA Librach, DL Borjesson and LD Galuppo. (2009). Collection of equine cord blood and placental tissues in 40 thoroughbred mares. Equine Vet J 41:724-728.
8. Schuh EM, MS Friedman, DD Carrade, J Li, D Heeke, SM Oyserman, LD Galuppo, DJ Lara, NJ Walker, GL Ferraro, SD Owens and DL Borjesson. (2009). Identification of variables that optimize isolation and culture of multipotent mesen-chymal stem cells from equine umbilical-cord blood. Am J Vet Res 70:1526-1535.
9. Reed SA and SE Johnson. (2008). Equine umbilical cord blood contains a population of stem cells that express Oct4 and differentiate into mesodermal and endodermal cell types. J Cell Physiol 215:329-336. (Pubitemid 351468944)
10. Koch TG, T Heerkens, PD Thomsen and DH Betts. (2007). Isolation of mesenchymal stem cells from equine umbilical cord blood. BMC Biotechnol 7:26.
11. Vidal MA, SO Robinson, MJ Lopez, DB Paulsen, O Borkh-senious, JR Johnson, RM Moore and JM Gimble. (2008). Comparison of chondrogenic potential in equine mesen-chymal stromal cells derived from adipose tissue and bone marrow. Vet Surg 37:713-724.
12. Kisiday JD, PW Kopesky, CH Evans, AJ Grodzinsky, CW McIlwraith and DD Frisbie. (2008). Evaluation of adult equine bone marrow- and adipose-derived progenitor cell chondrogenesis in hydrogel cultures. J Orthop Res 26:322-331.
13. Schnabel LV, ME Lynch, MC van der Meulen, AE Yeager, MA Kornatowski and AJ Nixon. (2009). Mesenchymal stem cells and insulin-like growth factor-I gene-enhanced mes-enchymal stem cells improve structural aspects of healing in equine flexor digitorum superficialis tendons. J Orthop Res 27:1392-1398.
14. Nixon AJ, LA Dahlgren, JL Haupt, AE Yeager and DL Ward. (2008). Effect of adipose-derived nucleated cell fractions on tendon repair in horses with collagenase-induced tendinitis. Am J Vet Res 69:928-937.
15. Smith RK. (2008). Mesenchymal stem cell therapy for equine tendinopathy. Disabil Rehabil 30(20-22):1752-1758.
16. Ferris DJ, DD Frisbie, JD Kisiday, CW McIlwraith, BA Hague, MD Major, RK Schneider, CJ Zubrod, JJ Watkins, CE Kawcak and LR Goodrich. (2009). Clinical follow-up of horses treated with bone marrow derived mesenchymal stem cells for musculoskeletal lesions. In: Proceedings of American Association of Equine Practitioners, Las Vegas, NV, pP 59-60.
17. Muschler GF and RJ Midura. (2002). Connective tissue progenitors: practical concepts for clinical applications. Clin Orthop Relat Res (395):66-80. (Pubitemid 34136658)
18. Vidal MA, GE Kilroy, JR Johnson, MJ Lopez, RM Moore and JM Gimble. (2006). Cell growth characteristics and differentiation frequency of adherent equine bone marrow-derived mesenchymal stromal cells: adipogenic and osteo-genic capacity. Vet Surg 35:601-610. (Pubitemid 44526659)
19. Vidal MA, GE Kilroy, MJ Lopez, JR Johnson, RM Moore and JM Gimble. (2007). Characterization of equine adipose tissue-derived stromal cells: adipogenic and osteogenic capacity and comparison with bone marrow-derived mesen-chymal stromal cells. Vet Surg 36:613-622. (Pubitemid 47480926)
20. Lepperdinger G, R Brunauer, A Jamnig, G Laschober and M Kassem. (2008). Controversial issue: is it safe to employ mesenchymal stem cells in cell-based therapies? Exp Ger-ontol 43:1018-1023.
21. Radcliffe CH, MJ Flaminio and LA Fortier. (2010). Temporal analysis of equine bone marrow aspirate during establishment of putative mesenchymal progenitor cell populations. Stem Cells Dev 19:269-282.
22. Hayflick L and PS Moorhead. (1961). The serial cultivation of human diploid cell strains. Exp Cell Res 25:585-621.
23. Shay JW and WE Wright. (2000). Hayflick, his limit, and cellular ageing. Nat Rev Mol Cell Biol 1:72-76.
24. Stenderup K, J Justesen, C Clausen and M Kassem. (2003). Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 33:919-926. (Pubitemid 37543568)
25. Braun J, A Hack, M Weis-Klemm, S Conrad, S Treml, K Kohler, U Walliser, T Skutella and WK Aicher. (2010). Evaluation of the osteogenic and chondrogenic differentiation capacities of equine adipose tissue-derived mesenchymal stem cells. Am J Vet Res 71:1228-1236.
26. Ksiazek K. (2009). A comprehensive review on mesenchy-mal stem cell growth and senescence. Rejuvenation Res 12:105-116.
27. Masutomi K, EY Yu, S Khurts, I Ben-Porath, JL Currier, GB Metz, MW Brooks, S Kaneko, S Murakami, JA DeCaprio, RA Weinberg, SA Stewart and WC Hahn. (2003). Telomerase maintains telomere structure in normal human cells. Cell 114:241-253. (Pubitemid 36936917)
28. Shibata KR, T Aoyama, Y Shima, K Fukiage, S Otsuka, M Furu, Y Kohno, K Ito, S Fujibayashi, M Neo, T Nakayama, T Nakamura and J Toguchida. (2007). Expression of the p16INK4A gene is associated closely with senescence of human mesenchymal stem cells and is potentially silenced by DNA methylation during in vitro expansion. Stem Cells 25:2371-2382. (Pubitemid 47480497)
29. Dumont P, M Burton, QM Chen, ES Gonos, C Frippiat, JB Mazarati, F Eliaers, J Remacle and O Toussaint. (2000). Induction of replicative senescence biomarkers by sublethal oxidative stresses in normal human fibroblast. Free Radic Biol Med 28:361-373. (Pubitemid 30110651)
30. Gonos ES, A Derventzi, M Kveiborg, G Agiostratidou, M Kassem, BF Clark, PS Jat and SI Rattan. (1998). Cloning and identification of genes that associate with mammalian rep-licative senescence. Exp Cell Res 240:66-74. (Pubitemid 28366611)
31. Boiani M and HR Scholer. (2005). Regulatory networks in embryo-derived pluripotent stem cells. Nat Rev Mol Cell Biol 6:872-884. (Pubitemid 41568736)
32. Boyer LA, TI Lee, MF Cole, SE Johnstone, SS Levine, JP Zucker, MG Guenther, RM Kumar, HL Murray, RG Jenner, DK Gifford, DA Melton, R Jaenisch and RA Young. (2005). Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122:947-956. (Pubitemid 41345211)
33. Potdar PD and SB D'Souza. (2010). Ascorbic acid induces in vitro proliferation of human subcutaneous adipose tissue derived mesenchymal stem cells with upregulation of embryonic stem cell pluripotency markers Oct4 and SOX 2. Human Cell 23:152-155.
34. Pierantozzi E, B Gava, I Manini, F Roviello, G Marotta, M Chiavarelli and V Sorrentino. (2010). Pluripotency regulators in human mesenchymal stem cells: expression of NANOG but not of OCT-4 and SOX-2. Stem cells Dev [Epub ahead of print]; DOI:10.1089/scd.2010.0353.
35. Violini S, P Ramelli, LF Pisani, C Gorni and P Mariani. (2009). Horse bone marrow mesenchymal stem cells express embryo stem cell markers and show the ability for tenogenic differentiation by in vitro exposure to BMP-12. BMC Cell Biol 10:29.
36. Fisher DJ, D Naydan, LL Werner and PF Moore. (1995). Immunophenotyping lymphomas in dogs: a comparison of results from fine needle aspirate and needle biopsy samples. Vet Clin Pathol 24:118-123.
37. Singer NG and AI Caplan. (2011). Mesenchymal stem cells: mechanisms of inflammation. Annu Rev Pathol 6:457-478.
38. Krtolica A, S Parrinello, S Lockett, PY Desprez and J Cam-pisi. (2001). Senescent fibroblasts promote epithelial cell growth and tumorigenesis: a link between cancer and aging. Proc Natl Acad Sci USA 98:12072-12077. (Pubitemid 32959828)
39. Zhou YF, M Bosch-Marce, H Okuyama, B Krishnamachary, H Kimura, L Zhang, DL Huso and GL Semenza. (2006). Spontaneous transformation of cultured mouse bone marrow-derived stromal cells. Cancer Res 66:10849-10854. (Pubitemid 44876981)
40. Meza-Zepeda LA, A Noer, JA Dahl, F Micci, O Myklebost and P Collas. (2008). High-resolution analysis of genetic stability of human adipose tissue stem cells cultured to senescence. J Cell Mol Med 12:553-563. (Pubitemid 351555134)
41. Bauer G, MA Dao, SS Case, T Meyerrose, L Wirthlin, P Zhou, X Wang, P Herrbrich, J Arevalo, S Csik, DC Skelton, J Walker, K Pepper, DB Kohn and JA Nolta. (2008). In vivo biosafety model to assess the risk of adverse events from retroviral and lentiviral vectors. Mol Ther 16:1308-1315. (Pubitemid 351866063)
42. Takubo K, J Aida, N Izumiyama, N Ishikawa, M Fujiwara, SS Poon, H Kondo, M Kammori, M Matsuura, M Sawabe, T Arai, DM Baird and K Nakamura. (2010). Chromosomal instability and telomere lengths of each chromosomal arm measured by Q-FISH in human fibroblast strains prior to replicative senescence. Mech Ageing Dev 131:614-624.
43. Dimri GP, X Lee, G Basile, M Acosta, G Scott, C Roskelley, EE Medrano, M Linskens, I Rubelj, O Pereira-Smith, et al. (1995). A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA 92:9363-9367.
44. Campisi J and F d'Adda di Fagagna. (2007). Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol 8:729-740. (Pubitemid 47312822)
45. Krtolica A and J Campisi. (2002). Cancer and aging: a model for the cancer promoting effects of the aging stroma. Int J Biochem Cell Biol 34:1401-1414. (Pubitemid 35251811)
46. Baxter MA, RF Wynn, SN Jowitt, JE Wraith, LJ Fairbairn and I Bellantuono. (2004). Study of telomere length reveals rapid aging of human marrow stromal cells following in vitro expansion. Stem Cells 22:675-682. (Pubitemid 39172200)
47. Wagner W, P Horn, M Castoldi, A Diehlmann, S Bork, R Saffrich, V Benes, J Blake, S Pfister, V Eckstein and AD Ho. (2008). Replicative senescence of mesenchymal stem cells: a continuous and organized process. PLoS One 3:e2213.
48. Bourzac C, LC Smith, P Vincent, G Beauchamp, JP Lavoie and S Laverty. (2010). Isolation of equine bone marrow-derived mesenchymal stem cells: a comparison between three protocols. Equine Vet J 42:519-527.
49. Liu Y, X Xu, X Ma, E Martin-Rendon, S Watt and Z Cui. (2010). Cryopreservation of human bone marrow-derived mesenchymal stem cells with reduced dimethylsulfoxide and well-defined freezing solutions. Biotechnol Prog 26:1635-1643.
50. Martinello T, I Bronzini, L Maccatrozzo, I Iacopetti, M Sampaolesi, F Mascarello and M Patruno. (2010). Cryopre-servation does not affect the stem characteristics of multipotent cells isolated from equine peripheral blood. Tissue Eng Part C Methods 16:771-781.
51. Martinello T, I Bronzini, L Maccatrozzo, A Mollo, M Sam-paolesi, F Mascarello, M Decaminada and M Patruno. (2010). Canine adipose-derived- mesenchymal stem cells do not lose stem features after a long-term cryopreservation. Res Vet Sci [Epub ahead of print]; DOI:10.1016/j.rvsc.2010.07. 024.
52. Gonda K, T Shigeura, T Sato, D Matsumoto, H Suga, K In-oue, N Aoi, H Kato, K Sato, S Murase, I Koshima and K Yoshimura. (2008). Preserved proliferative capacity and multipotency of human adipose-derived stem cells after long-term cryopreservation. Plast Reconstr Surg 121:401-410. (Pubitemid 351642899)
53. Fehrer C and G Lepperdinger. (2005). Mesenchymal stem cell aging. Exp Gerontol 40:926-930. (Pubitemid 41682392)
54. Serakinci N, R Christensen, J Graakjaer, CJ Cairney, WN Keith, J Alsner, G Saretzki and S Kolvraa. (2007). Ectopically hTERT expressing adult human mesenchymal stem cells are less radiosensitive than their telomerase negative counterpart. Exp Cell Res 313:1056-1067. (Pubitemid 46273450)
55. Bonab MM, K Alimoghaddam, F Talebian, SH Ghaffari, A Ghavamzadeh and B Nikbin. (2006). Aging of mesenchymal stem cell in vitro. BMC Cell Biol 7:14.
56. Parsch D, J Fellenberg, TH Brummendorf, AM Eschlbeck and W Richter. (2004). Telomere length and telomerase activity during expansion and differentiation of human mes-enchymal stem cells and chondrocytes. J Mol Med 82:49-55. (Pubitemid 38168101)
57. Harley CB, AB Futcher and CW Greider. (1990). Telomeres shorten during ageing of human fibroblasts. Nature 345:458-460.
58. Shiba H, K Nakanishi, M Sakata, T Fujita, Y Uchida and H Kurihara. (2000). Effects of ageing on proliferative ability, and the expressions of secreted protein, acidic and rich in cysteine (SPARC) and osteoprotegerin (osteoclastogenesis inhibitory factor) in cultures of human periodontal ligament cells. Mech Ageing Dev 117:69-77. (Pubitemid 30665794)
59. Lane TF and EH Sage. (1994). The biology of SPARC, a protein that modulates cell-matrix interactions. FASEB J 8:163-173. (Pubitemid 24067139)
60. Bradshaw AD and EH Sage. (2001). SPARC, a matricellular protein that functions in cellular differentiation and tissue response to injury. J Clin Invest 107:1049-1054. (Pubitemid 32422898)
61. Clark CJ and EH Sage. (2008). A prototypic matricellular protein in the tumor microenvironment-where there's SPARC, there's fire. J Cell Biochem 104:721-732. (Pubitemid 351830824)
62. Mambelli LI, EJ Santos, PJ Frazao, MB Chaparro, A Kerkis, AL Zoppa and I Kerkis. (2009). Characterization of equine adipose tissue-derived progenitor cells before and after cryopreservation. Tissue Eng Part C Methods 15:87-94.