Mesenchymal Stem Cells Derived from Peripheral Blood Retain Their Pluripotency, but Undergo Senescence during Long-Term Culture

Tissue Engineering - Part C: Methods

Volumn 21, Issue 10, 2015, Pages 1088-1097

  Fu, Wei Li ^a   Li, Jian ^a   Chen, Gang ^a   Li, Qi ^a   Tang, Xin ^a   Zhang, Cheng Hao ^a  

^a SICHUAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD; CELL DEATH; FLOWCHARTING; STEM CELLS; TISSUE; TISSUE ENGINEERING;

APOPTOTIC CELLS; GALACTOSIDASES; GRANULOCYTE-COLONY STIMULATING FACTOR; LONG-TERM CULTURE; MESENCHYMAL STEM CELL; MINIMALLY INVASIVE; PERIPHERAL BLOOD; TELOMERASE ACTIVITY;

CELL CULTURE;

ADENINE NUCLEOTIDE TRANSLOCASE; BETA GALACTOSIDASE; GRANULOCYTE COLONY STIMULATING FACTOR; PLERIXAFOR; REACTIVE OXYGEN METABOLITE; TELOMERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL AGING; CELL CULTURE; CELL DIFFERENTIATION; CELL EXPANSION; CELL ISOLATION; CELL LINEAGE; CELL METABOLISM; CELL PLURIPOTENCY; CELL PROLIFERATION; CELL STRUCTURE; CELLULAR PARAMETERS; CONTROLLED STUDY; CULTURAL ANTHROPOLOGY; ENZYME ACTIVITY; G1 PHASE CELL CYCLE CHECKPOINT; MESENCHYMAL STEM CELL; NONHUMAN; OXIDATIVE STRESS; PERIPHERAL BLOOD DERIVED MESENCHYMAL STEM CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABBIT; ANIMAL; BLOOD CELL; CELL CULTURE TECHNIQUE; CYTOLOGY; MESENCHYMAL STROMA CELL; METABOLISM; TIME FACTOR;

ANIMALS; APOPTOSIS; BLOOD CELLS; CELL AGING; CELL CULTURE TECHNIQUES; CELL PROLIFERATION; CELLS, CULTURED; MESENCHYMAL STROMAL CELLS; RABBITS; TIME FACTORS;

EID: 84942897508     PISSN: 19373384     EISSN: 19373392     Source Type: Journal    
DOI: 10.1089/ten.tec.2014.0595     Document Type: Article

References (42)

1. English, K. , French, A. , and Wood, K. J. Mesenchymal stromal cells: facilitators of successful transplantation? Cell Stem Cell 7, 431, 2010.
2. Salem, H. K. , and Thiemermann, C. Mesenchymal stromal cells: current understanding and clinical status. Stem Cells 28, 585, 2010.
3. Caplan, A. I. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol 213, 341, 2007.
4. Fei, C. , Zhao, Y. , Guo, J. , Gu, S. , Li, X. , and Chang, C. Senescence of bone marrow mesenchymal stromal cells is accompanied by activation of p53/p21 pathway in myelodysplastic syndromes. Eur J Haematol 93, 476, 2014.
5. da Silva Meirelles, L. , Chagastelles, P. C. , and Nardi, N. B. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 119, 2204, 2006.
6. Saw, K. Y. , Anz, A. , Siew-Yoke Jee, C. , Merican, S. , Ching-Soong Ng, R. , Roohi, S. A. , et al. Articular cartilage regeneration with autologous peripheral blood stem cells versus hyaluronic acid: A randomized controlled trial. Arthroscopy 29, 684, 2013.
7. Turajane, T. , Chaweewannakorn, U. , Larbpaiboonpong, V. , Aojanepong, J. , Thitiset, T. , Honsawek, S. , et al. Combination of intra-articular autologous activated peripheral blood stem cells with growth factor addition/ preservation and hyaluronic acid in conjunction with arthroscopic microdrilling mesenchymal cell stimulation Improves quality of life and regenerates articular cartilage in early osteoarthritic knee disease. J Med Assoc Thai 96, 580, 2013.
8. Wan, C. , He, Q. , and Li, G. Allogenic peripheral blood derived mesenchymal stem cells (MSCs) enhance bone regeneration in rabbit ulna critical-sized bone defect model. J Orthop Res 24, 610, 2006.
9. Kumar, S. , and Ponnazhagan, S. Mobilization of bone marrow mesenchymal stem cells in vivo augments bone healing in a mouse model of segmental bone defect. Bone 50, 1012, 2012.
10. Dahl, J. A. , Duggal, S. , Coulston, N. , Millar, D. , Melki, J. , Shahdadfar, A. , et al. Genetic and epigenetic instability of human bone marrow mesenchymal stem cells expanded in autologous serum or fetal bovine serum. Int J Dev Biol 52, 1033, 2008.
11. Qin, Y. , Ji, H. , Wu, Y. , and Liu, H. Chromosomal instability of murine adipose tissue-derived mesenchymal stem cells in long-term culture and development of cloned embryos. Cloning Stem Cells 11, 445, 2009.
12. Rosland, G. V. , Svendsen, A. , Torsvik, A. , Sobala, E. , McCormack, E. , Immervoll, H. , et al. Long-term cultures of bone marrow-derived human mesenchymal stem cells frequently undergo spontaneous malignant transformation. CancerRes 69, 5331, 2009.
13. Otte, A. , Bucan, V. , Reimers, K. , and Hass, R. Mesenchymal stem cells maintain long-term in vitro stemness during explant culture. Tissue Eng Part C Methods 19, 937, 2013.
14. Danoviz, M. E. , Bassaneze, V. , Nakamuta, J. S. , dos Santos-Junior, G. R. , Saint-Clair, D. , Bajgelman, M. C. , et al. Adipose tissue-derived stem cells from humans and mice differ in proliferative capacity and genome stability in long-term cultures. Stem Cells Dev 20, 661, 2011.
15. Dai, L. , He, Z. , Zhang, X. , Hu, X. , Yuan, L. , Qiang, M. , et al. One-step repair for cartilage defects in a rabbit model: A technique combining the perforated decalcified corticalcancellous bone matrix scaffold with microfracture. Am J Sports Med 42, 583, 2014.
16. Fu, W. L. , Zhang, J. Y. , Fu, X. , Duan, X. N. , Leung, K. K. , Jia, Z. Q. , et al. Comparative study of the biological characteristics of mesenchymal stem cells from bone marrow and peripheral blood of rats. Tissue Eng Part A 18, 1793, 2012.
17. Chen, G. , Yue, A. , Ruan, Z. , Yin, Y. , Wang, R. , Ren, Y. , et al. Human umbilical cord-derived mesenchymal stem cells do not undergo malignant transformation during longterm culturing in serum-free medium. PLoS One 9, e98565, 2014.
18. Dominici, M. , Le Blanc, K. , Mueller, I. , Slaper-Cortenbach, I. , Marini, F. , Krause, D. , et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8, 315, 2006.
19. Bernardo, M. E. , Zaffaroni, N. , Novara, F. , Cometa, A. M. , Avanzini, M. A. , Moretta, A. , et al. Human bone marrow derived mesenchymal stem cells do not undergo transformation after long-term in vitro culture and do not exhibit telomere maintenance mechanisms. Cancer Res 67, 9142, 2007.
20. Nekanti, U. , Rao, V. B. , Bahirvani, A. G. , Jan, M. , Totey, S. , and Ta, M. Long-term expansion and pluripotent marker array analysis of Wharton's jelly-derived mesenchymal stem cells. Stem Cells Dev 19, 117, 2010.
21. Kretlow, J. D. , Jin, Y. Q. , Liu, W. , Zhang, W. J. , Hong, T. H. , Zhou, G. , et al. Donor age and cell passage affects differentiation potential of murine bone marrow-derived stem cells. BMC Cell Biol 9, 60, 2008.
22. Wagner, W. , Horn, P. , Castoldi, M. , Diehlmann, A. , Bork, S. , Saffrich, R. , et al. Replicative senescence of mesenchymal stem cells: A continuous and organized process. PLoS One 3, e2213, 2008.
23. Cheng, H. , Qiu, L. , Ma, J. , Zhang, H. , Cheng, M. , Li, W. , et al. Replicative senescence of human bone marrow and umbilical cord derived mesenchymal stem cells and their differentiation to adipocytes and osteoblasts. Mol Biol Rep 38, 5161, 2011.
24. Ahmadbeigi, N. , Shafiee, A. , Seyedjafari, E. , Gheisari, Y. , Vassei, M. , Amanpour, S. , et al. Early spontaneous immortalization and loss of plasticity of rabbit bone marrow mesenchymal stem cells. Cell Prolif 44, 67, 2011.
25. Gou, S. , Wang, C. , Liu, T. , Wu, H. , Xiong, J. , Zhou, F. , et al. Spontaneous differentiation of murine bone marrowderived mesenchymal stem cells into adipocytes without malignant transformation after long-term culture. Cells Tissues Organs 191, 185, 2010.
26. Deng, J. , Petersen, B. E. , Steindler, D. A. , Jorgensen, M. L. , and Laywell, E. D. Mesenchymal stem cells spontaneously express neural proteins in culture and are neurogenic after transplantation. Stem Cells 24, 1054, 2006.
27. Khoo, M. L. , Shen, B. , Tao, H. , and Ma, D. D. Long-term serial passage and neuronal differentiation capability of human bone marrow mesenchymal stem cells. Stem Cells Dev 17, 883, 2008.
28. He, L. , Zheng, Y. , Wan, Y. , and Song, J. A shorter telomere is the key factor in preventing cultured human mesenchymal stem cells from senescence escape. Histochem Cell Biol 142, 257, 2014.
29. Leontieva, O. V. , Lenzo, F. , Demidenko, Z. N. , and Blagosklonny, M. V. Hyper-mitogenic drive coexists with mitotic incompetence in senescent cells. Cell Cycle 11, 4642, 2012.
30. Ksiazek, K. A comprehensive review on mesenchymal stem cell growth and senescence. Rejuvenation Res 12, 105, 2009.
31. Kim, J. , Kang, J. W. , Park, J. H. , Choi, Y. , Choi, K. S. , Park, K. D. , et al. Biological characterization of long-term cultured human mesenchymal stem cells. Arch Pharm Res 32, 117, 2009.
32. Meza-Zepeda, L. A. , Noer, A. , Dahl, J. A. , Micci, F. , Myklebost, O. , and Collas, P. High-resolution analysis of genetic stability of human adipose tissue stem cells cultured to senescence. J Cell Mol Med 12, 553, 2008.
33. Grimes, B. R. , Steiner, C. M. , Merfeld-Clauss, S. , Traktuev, D. O. , Smith, D. , Reese, A. , et al. Interphase FISH demonstrates that human adipose stromal cells maintain a high level of genomic stability in long-term culture. Stem Cells Dev 18, 717, 2009.
34. Serakinci, N. , Graakjaer, J. , and Kolvraa, S. Telomere stability and telomerase in mesenchymal stem cells. Biochimie 90, 33, 2008.
35. Wagner, W. , Ho, A. D. , and Zenke, M. Different facets of aging in human mesenchymal stem cells. Tissue Eng Part B Rev 16, 445, 2010.
36. Bork, S. , Pfister, S. , Witt, H. , Horn, P. , Korn, B. , Ho, A. D. , et al. DNA methylation pattern changes upon long-term culture and aging of human mesenchymal stromal cells. Aging Cell 9, 54, 2010.
37. Galderisi, U. , Helmbold, H. , Squillaro, T. , Alessio, N. , Komm, N. , Khadang, B. , et al. In vitro senescence of rat mesenchymal stem cells is accompanied by downregulation of stemness-related and DNA damage repair genes. Stem Cells Dev 18, 1033, 2009.
38. Duggal, S. , and Brinchmann, J. E. Importance of serum source for the in vitro replicative senescence of human bone marrow derived mesenchymal stem cells. J Cell Physiol 226, 2908, 2011.
39. Colavitti, R. , and Finkel, T. Reactive oxygen species as mediators of cellular senescence. IUBMB Life 57, 277, 2005.
40. Hutter, E. , Renner, K. , Pfister, G. , Stockl, P. , Jansen-Durr, P. , and Gnaiger, E. Senescence-associated changes in respiration and oxidative phosphorylation in primary human fibroblasts. Biochem J 380, 919, 2004.
41. Hutter, E. , Unterluggauer, H. , Uberall, F. , Schramek, H. , and Jansen-Durr, P. Replicative senescence of human fibroblasts: The role of Ras-dependent signaling and oxidative stress. Exp Gerontol 37, 1165, 2002.
42. Stolzing, A. , and Scutt, A. Age-related impairment of mesenchymal progenitor cell function. Aging Cell 5, 213, 2006.