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Donor age and long-term culture affect differentiation and proliferation of human bone marrow mesenchymal stem cells
Abstract
Bone marrow-derived human mesenchymal stem cells (BM-hMSCs) represent a promising cell-based therapy for a number of degenerative conditions. Many applications require cell expansion and involve the treatment of diseases and conditions found in an aging population. Therefore, the effects of donor age and long-term passage must be clarified. In this study, the effects of donor age and long-term passage on the morphology, proliferation potential, characteristics, mesodermal differentiation ability, and transdifferentiation potential of hMSCs towards neurogenic lineage were evaluated. Cells from child donors (0-12 years, n = 6) maintained their fibroblast-like morphology up to higher passages and proliferated in a greater number than those from adult (25-50 years, n = 6) and old (over 60 years, n = 6) donors. Adipogenic, osteogenic, and neurogenic differentiation potential decreased with age, while chondrogenic potential did not change. Long-term passage affected the morphology and proliferation of hMSCs from all ages. With increasing passage number, proliferation rate decreased and cells lost their typical morphology. Expression levels of neural markers (β III tubulin and NSE) and topo II isoforms in populations of nondifferentiated hMSCs were investigated by reverse transcription polymerase chain reaction analysis. While neural marker and topo IIβ expression levels increased due to increasing passage number in adult hMSCs compared to child hMSCs, topo IIα decreased in both. These results indicated that, even under highly standardized culture conditions, donor age and long-term passage have effects on hMSC characteristics, which should be taken into account prior to stem cell-based therapies.
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“with older donors of BM-MSCs having lower proliferation rates [246], [249] and osteogenic [246], [248], adipogenic and neurogenic [248] capacities.”
From Mesenchymal stem cell secretome for regenerative medicine: Where do we stand? (2025) · cites this paper as [248]
In the citing paper
“In addition, the number of MSC passage [246], [247], [248] and the donor variability [246], [247], [248] cannot be ignored since MSC activity and, thus, the properties of MSC-secretome can be affected by donor age and sex [246], [248], [249]”
From Mesenchymal stem cell secretome for regenerative medicine: Where do we stand? (2025) · cites this paper as [248]
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“Zaim et al.(26) found that the adipogenic, osteogenic, and neurogenic differentiation potentials of hBMSCs declined with age, but that the chondrogenic potential did not.”
BackgroundLiu, X., Hu, D., Zeng, Z., Zhu, W., Zhang, N., Yu, H., Chen, H., Wang, K., Wang, Y., Wang, L., et al. (2017) · Cell Death and Disease · doi:10.1038/cddis.2017.107 · Cited by 40
New Challenge: Mitochondrial Epigenetics?
Štimpfel, M., Jančar, N., & Virant‐Klun, I. (2017) · Stem Cell Reviews and Reports · doi:10.1007/s12015-017-9771-z · Cited by 41
Charif, N., Li, Y., Targa, L., Zhang, L., Ye, J., Li, Y., Stoltz, J. F., Han, H. Z., & de Isla, N. (2017) · Bio-Medical Materials and Engineering · doi:10.3233/bme-171624 · Cited by 40
“Other authors showed that adipogenic and osteogenic differentiation would decrease with the increase in the donors age but no effect was observed in chondrogenic differentiation [27].”
Quality by design to define critical process parameters for mesenchymal stem cell expansion
Maillot, C., Sion, C., de Isla, N., Toye, D., & Olmos, É. (2021) · Biotechnology Advances · doi:10.1016/j.biotechadv.2021.107765 · Cited by 40
Effect of UV Photofunctionalization on Osseointegration in Aged Rats
Ishijima, M., Ghassemi, A., Soltanzadeh, P., Tanaka, M., Nakhaei, K., Park, W., Hirota, M., Tsukimura, N., & Ogawa, T. (2016) · Implant Dentistry · doi:10.1097/id.0000000000000459 · Cited by 38
“In regard to osteoblastic phenotype, a previous studyof humanbonemarrow– derived mesenchymal stem cells found decreased osteogenic differentiation potential with increased cell donor age.(11) Aging has also been associated with a marked decline in the ability to regenerate tissues and maintain homeostasis in adult ste…”
BackgroundResultInfluence of age on stem cells depends on the sex of the bone marrow donor
Selle, M., Koch, J. D., Ongsiek, A., Ulbrich, L., Ye, W., Jiang, Z., Krettek, C., Neunaber, C., & Noack, S. (2022) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.17201 · Cited by 37
Mesenchymal Stromal Cell Secretome Is Affected by Tissue Source and Donor Age
Turło, A., Hammond, D. E., Ramsbottom, K. A., Soul, J., Gillen, A. M., McDonald, K., Peffers, M. J., & Clegg, P. (2023) · Stem Cells · doi:10.1093/stmcls/sxad060 · Cited by 37
Alghazali, K. M., Nima, Z. A., Hamzah, R. N., Dhar, M. S., Anderson, D. E., & Biris, A. S. (2015) · Drug Metabolism Reviews · doi:10.3109/03602532.2015.1115871 · Cited by 37
“Thus, MSCs from one source may be better than the other in therapy (Katsara et al., 2011; Phinney et al., 1999; Phinney & Sensebe, 2013; Sakaguchi et al., 2005; Wagner, 2012; Zaim et al., 1999).”
BackgroundAlves, E. G. L., Serákides, R., Boeloni, J. N., Rosado, I. R., Ocarino, N. M., Oliveira, H. P., Goes, A. M., & Rezende, C. M. F. (2014) · BMC Veterinary Research · doi:10.1186/s12917-014-0190-y · Cited by 35
“Some studies have shown that the osteogenic potential of MSCs may vary as a function of tissue type [3,4], collection site [5], animal species [6], age [7,8], state of health [9], and performance of physical activity on a daily basis [7,10].”
BackgroundSlamecka, J., Salimova, L., McClellan, S. B., van Kelle, M. A. J., Kehl, D., Laurini, J. A., Cinelli, P., Owen, L. B., Hoerstrup, S. P., & Weber, B. (2015) · Cell Cycle · doi:10.1080/15384101.2015.1121332 · Cited by 35
Taguchi, T., Borjesson, D. L., Osmond, C., & Griffon, D. J. (2019) · Stem Cells and Development · doi:10.1089/scd.2019.0118 · Cited by 36
“This finding was in general agreement with previous reports, where age had a negative effect on the DT and the number of CFUs in cAD-MSCs [17,18], canine BM-MSCs [19], and hBM-MSCs [14,23,24].”
Huang, Y., Zhao, H., Wang, Y., Bi, S., Zhou, K., Li, H., Zhou, C., Wang, Y., Wu, W., Peng, B., et al. (2023) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2023.1089031 · Cited by 34
“01%) and that their differentiation capability decreases with age, which may impair the effectiveness of BMSCs in stem cell treatment (Zaim et al., 2012).”
BackgroundLi, Y., Charif, N., Mainard, D., Bensoussan, D., Stoltz, J., & de Isla, N. (2014) · Bio-Medical Materials and Engineering · doi:10.3233/bme-140973 · Cited by 34
“This study was consistent with previous ones [7,10,11].”
Stem cell passage affects directional migration of stem cells in electrotaxis
Hong, S. H., Lee, M. H., Koo, M.-A., Seon, G. M., Park, Y. J., Kim, D., & Park, J. (2019) · Stem Cell Research · doi:10.1016/j.scr.2019.101475 · Cited by 34
“Long-term serial passaging of MSCs causes the cells to become senescent with reduced osteogenic differentiation potential and decreased proliferation potential (Zaim et al., 2012; Siddappa et al., 2007).”
BackgroundNémeth, K. (2014) · Experimental Dermatology · doi:10.1111/exd.12459 · Cited by 33
Animal mesenchymal stem cell research in cartilage regenerative medicine – a review
Gugjoo, M. B., Fazili, M. R., Gayas, M. A., Ahmad, R. A., & Dhama, K. (2019) · Veterinary Quarterly · doi:10.1080/01652176.2019.1643051 · Cited by 33
“This has implications on the healing potential and health status of the individuals as degeneration of the tissues ensues subsequently with aging (Zaim et al. 2012).”
BackgroundDerivation and growth characteristics of dental pulp stem cells from patients of different ages
Wu, W., Zhou, J. P., XU, C.-T., Zhang, J., JIN, Y.-J., & Geng-lin, S. (2015) · Molecular Medicine Reports · doi:10.3892/mmr.2015.4106 · Cited by 33
“Similar results were obtained for human bone marrow mesenchymal stem cells by Zaim et al (31).”
Physoxia alters human mesenchymal stem cell secretome
Merkhan, M. M., Shephard, M. T., & Forsyth, N. R. (2021) · Journal of Tissue Engineering · doi:10.1177/20417314211056132 · Cited by 36
Rejuvenation of Mesenchymal Stem Cells to Ameliorate Skeletal Aging
Cheng, M., Yuan, W., Moshaverinia, A., & Yu, B. (2023) · Cells · doi:10.3390/cells12070998 · Cited by 33
“A similar increase in cell size is also correlated to donor age in primary MSCs [36].”
BackgroundGao, P., Han, P., Jiang, D., Yang, S., Cui, Q., & Li, Z. (2017) · Cytotechnology · doi:10.1007/s10616-017-0084-5 · Cited by 32
Mehrian, M., Lambrechts, T., Maréchal, M., Luyten, F. P., Papantoniou, I., & Geris, L. (2020) · Cytotherapy · doi:10.1016/j.jcyt.2019.12.006 · Cited by 33
“Inherent variability coming from the cells is a major source of variation in the autologous cell expansion process, where natural factors such as the age and gender of the donor have been shown to influence the expansion characteristics such as population doubling time (PDT) [6, 7].”
BackgroundJulavijitphong, S., Wichitwiengrat, S., Tirawanchai, N., Ruangvutilert, P., Vantanasiri, C., & Phermthai, T. (2013) · Cytotherapy · doi:10.1016/j.jcyt.2013.07.012 · Cited by 32
Age-related Changes in the Energy of Human Mesenchymal Stem Cells
Barilani, M., Lovejoy, C., Piras, R., Abramov, A. Y., Lazzari, L., & Angelova, P. R. (2022) · Journal of Cellular Physiology · doi:10.1002/jcp.30638 · Cited by 31
“…proliferation and differentiation (Beane et al., 2014; Ganguly et al., 2019; Kretlow et al., 2008; Lund et al., 2010; Stolzing et al., 2008; Zaim et al., 2012); c) use of MSC in diverse clinical applications, such as bone reconstruction (Gómez‐Barrena et al., 2020); and d) lack of…”
MethodEffects of Hypoxia and Chitosan on Equine Umbilical Cord‐Derived Mesenchymal Stem Cells
Griffon, D. J., Cho, J., Wagner, J. R., Charavaryamath, C., Wei, J., & Johnson, A. J. W. (2016) · Stem Cells International · doi:10.1155/2016/2987140 · Cited by 31
“However, this approach remains limited by the morbidity associated with tissue collection, delayed administration due to processing or reprogramming of cells, and the influence of the patient’s health status and age on the properties of stem cells [14, 15].”
Qu, H., Liu, X., Ni, Y., Jiang, Y. Z., Feng, X., Xiao, J., Guo, Y., Kong, D., Ai, L., Li, X., et al. (2014) · Journal of Translational Medicine · doi:10.1186/1479-5876-12-135 · Cited by 31
“Thereafter, generation of IPCs from human neural progenitor cell [22], ESCs [23], liver cells [24,25], pancreatic non-endocrine cells [26], placenta-derived multipotent stem cells [27], gene modified BM-MSC [5], and pancreatic cells [28] have been reported.”
BackgroundInfluentialRole of Aquaporins in the Physiological Functions of Mesenchymal Stem Cells
Zannetti, A., Benga, G., Brunetti, A., Napolitano, F., Avallone, L., & Pelagalli, A. (2020) · Cells · doi:10.3390/cells9122678 · Cited by 31
Peffers, M. J., Goljanek‐Whysall, K., Collins, J., Fang, Y., Rushton, M. D., Loughlin, J. A., Proctor, C. J., & Clegg, P. (2016) · PLoS ONE · doi:10.1371/journal.pone.0160517 · Cited by 30
“One study found a reduction in glycosaminoglycans in chondrogenesis with age [7] whereas another experiment using a wider donor agerange found no change [8].”
ResultPeffers, M. J., Collins, J., Loughlin, J. A., Proctor, C. J., & Clegg, P. (2016) · Stem Cell Research & Therapy · doi:10.1186/s13287-016-0384-2 · Cited by 30
“For instance, relating to chondrogenic differentiation of MSCs, one study identified a reduction in glycosaminoglycan with age [7] whereas another found no change [5].”
BackgroundLee, B., Li, Q., Song, W., Chae, H., Kweon, K., Ahn, J., & Youn, H. (2018) · Journal of Veterinary Medical Science · doi:10.1292/jvms.17-0563 · Cited by 30
“A decrease in proliferation rate with sequential passages has been reported in cats and various other species [27, 35, 38, 39].”
Background
Metadata
- Authors
- Zaim, M., Karaman, S., Cetin, G., & Isik, S.
- Affiliations
- Fatih University (TR)
- Şişli Etfal Eğitim ve Araştırma Hastanesi (TR)
- Venue
- Annals of Hematology
- Published
- 2012-03-08
- Volume
- 91
- Issue
- 8
- Pages
- 1175-1186
- ISSN
- 0939-5555 (ISSN-L)
- 1432-0584
- OpenAlex
- W1978468353
- Cited by
- 294
- References
- 41
- Citations by year
- 2026: 8 · 2025: 15 · 2024: 15 · 2023: 24 · 2022: 19 · 2021: 35 · 2020: 27 · 2019: 23 · 2018: 19 · 2017: 28 · 2016: 23 · 2015: 18 · 2014: 24 · 2013: 12 · 2012: 4
- FWCI
- 8.84
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Annals of Hematology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Mesenchymal stem cell research
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Keywords
- mesenchymal stem cells, bone marrow, donor age, cellular aging, cell proliferation, multilineage differentiation, neurogenic differentiation, transdifferentiation, topoisomerase II, neural markers, stem cell therapy
- MeSH terms
- Adult, Age Factors, Aged, Aging, Bone Marrow Cells, Cell Differentiation, Cells, Cultured, Child, Child, Preschool, Female, Humans, Male, Middle Aged, Time Factors, Tissue Donors, Cell Proliferation, Mesenchymal Stem Cells, Primary Cell Culture
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