Adult stem cell and mesenchymal progenitor theories of aging

Frontiers in Cell and Developmental Biology

Volumn 2, Issue MAR, 2014, Pages

  Fukada, So ichiro ^a   Ma, Yuran ^a   Uezumi, Akiyoshi ^b  

^a OSAKA UNIVERSITY   (Japan)

^b FUJITA HEALTH UNIVERSITY   (Japan)

Author keywords

Adult stem cells; Aging; DNA damage; Mesenchymal progenitors; Niche; Oxidative stress; Telomere

Indexed keywords

EID: 84977985902     PISSN: None     EISSN: 2296634X     Source Type: Journal    
DOI: 10.3389/fcell.2014.00010     Document Type: Review

References (87)

1. Alves, H., Munoz-Najar, U., De Wit, J., Renard, A. J., Hoeijmakers, J. H., Sedivy, J. M., et al. (2010). A link between the accumulation of DNA damage and loss of multi-potency of human mesenchymal stromal cells. J. Cell. Mol. Med. 14, 2729-2738. doi: 10.1111/j.1582-4934.2009.00931.x
2. Bjornson, C. R., Cheung, T. H., Liu, L., Tripathi, P. V., Steeper, K. M., and Rando, T. A. (2012). Notch signaling is necessary to maintain quiescence in adult muscle stem cells. Stem Cells 30, 232-242. doi: 10.1002/stem.773
3. Blasco, M. A., Lee, H. W., Hande, M. P., Samper, E., Lansdorp, P. M., DePinho, R. A., et al. (1997). Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91, 25-34. doi: 10.1016/S0092-8674(01)80006-4
4. Bortoli, S., Renault, V., Eveno, E., Auffray, C., Butler-Browne, G., and Pietu, G. (2003). Gene expression profiling of human satellite cells during muscular aging using cDNA arrays. Gene 321, 145-154. doi: 10.1016/j.gene.2003.08.025
5. Boutten, A., Goven, D., Boczkowski, J., and Bonay, M. (2010). Oxidative stress targets in pulmonary emphysema: focus on the Nrf2 pathway. Exp. Opin. Ther. Targets 14, 329-346. doi: 10.1517/14728221003629750
6. Brack, A. S., Conboy, M. J., Roy, S., Lee, M., Kuo, C. J., Keller, C., et al. (2007). Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 317, 807-810. doi: 10.1126/science.1144090
7. Bulfield, G., Siller, W. G., Wight, P. A., and Moore, K. J. (1984). X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc. Natl. Acad. Sci. U.S.A. 81, 1189-1192. doi: 10.1073/pnas.81.4.1189
8. Campisi, J., Andersen, J. K., Kapahi, P., and Melov, S. (2011). Cellular senescence: a link between cancer and age-related degenerative disease? Sem. Cancer Biol. 21, 354-359. doi: 10.1016/j.semcancer.2011.09.001
9. Caplan, A. I., and Dennis, J. E. (2006). Mesenchymal stem cells as trophic mediators. J. Cell Biochem. 98, 1076-1084. doi: 10.1002/jcb.20886
10. Cheung, T. H., and Rando, T. A. (2013). Molecular regulation of stem cell quiescence. Nat. Rev. Mol. Cell Biol. 14, 329-340. doi: 10.1038/nrm3591
11. Christov, C., Chretien, F., Abou-Khalil, R., Bassez, G., Vallet, G., Authier, F. J., et al. (2007). Muscle satellite cells and endothelial cells: close neighbors and privileged partners. Mol. Biol. Cell 18, 1397-1409. doi: 10.1091/mbc. E06-08-0693
12. Collins, C. A., Zammit, P. S., Ruiz, A. P., Morgan, J. E., and Partridge, T. A. (2007). A population of myogenic stem cells that survives skeletal muscle aging. Stem Cells 25, 885-894. doi: 10.1634/stemcells.2006-0372
13. Conboy, I. M., Conboy, M. J., Wagers, A. J., Girma, E. R., Weissman, I. L., and Rando, T. A. (2005). Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433, 760-764. doi: 10.1038/nature03260
14. de Boer, J., Andressoo, J. O., de Wit, J., Huijmans, J., Beems, R. B., van Steeg, H., et al. (2002). Premature aging in mice deficient in DNA repair and transcription. Science 296, 1276-1279. doi: 10.1126/science.1070174
15. Freter, R., Osawa, M., and Nishikawa, S. (2010). Adult stem cells exhibit global suppression of RNA polymerase II serine-2 phosphorylation. Stem Cells 28, 1571-1580. doi: 10.1002/stem.476
16. Friedman, D. B., and Johnson, T. E. (1988). A mutation in the age-1 gene in Caenorhabditis elegans lengthens life and reduces hermaphrodite fertility. Genetics 118, 75-86.
17. Fukada, S., Ma, Y., Ohtani, T., Watanabe, Y., Murakami, S., and Yamaguchi, M. (2013). Isolation, characterization, and molecular regulation of muscle stem cells. Front. Physiol. 4:317. doi: 10.3389/fphys.2013.00317
18. Fukada, S., Morikawa, D., Yamamoto, Y., Yoshida, T., Sumie, N., Yamaguchi, M., et al. (2010). Genetic background affects properties of satellite cells and mdx phenotypes. Am. J. Pathol. 176, 2414-2424. doi: 10.2353/ajpath.2010.090887
19. Fukada, S., Yamaguchi, M., Kokubo, H., Ogawa, R., Uezumi, A., Yoneda, T., et al. (2011). Hesr1 and Hesr3 are essential to generate undifferentiated quiescent satellite cells and to maintain satellite cell numbers. Development 138, 4609-4619. doi: 10.1242/dev.067165
20. Harley, C. B., Futcher, A. B., and Greider, C. W. (1990). Telomeres shorten during ageing of human fibroblasts. Nature 345, 458-460. doi: 10.1038/345458a0
21. Harman, D. (1956). Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 11, 298-300. doi: 10.1093/geronj/11.3.298
22. Hochmuth, C. E., Biteau, B., Bohmann, D., and Jasper, H. (2011). Redox regulation by Keap1 and Nrf2 controls intestinal stem cell proliferation in Drosophila. Cell Stem Cell 8, 188-199. doi: 10.1016/j.stem.2010.12.006
23. Imayoshi, I., Sakamoto, M., Yamaguchi, M., Mori, K., and Kageyama, R. (2010). Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. J. Neurosci. 30, 3489-3498. doi: 10.1523/JNEUROSCI.4987-09.2010
24. Itoh, K., Wakabayashi, N., Katoh, Y., Ishii, T., Igarashi, K., Engel, J. D., et al. (1999). Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 13, 76-86. doi: 10.1101/gad.13.1.76
25. Janzen, V., Forkert, R., Fleming, H. E., Saito, Y., Waring, M. T., Dombkowski, D. M., et al. (2006). Stem-cell ageing modified by the cyclin-dependent kinase inhibitor p16INK4a. Nature 443, 421-426. doi: 10.1038/nature05159
26. Joe, A. W., Yi, L., Natarajan, A., Le Grand, F., So, L., Wang, J., et al. (2010). Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat. Cell Biol. 12, 153-163. doi: 10.1038/ncb2015
27. Ju, Z., Jiang, H., Jaworski, M., Rathinam, C., Gompf, A., Klein, C., et al. (2007). Telomere dysfunction induces environmental alterations limiting hematopoietic stem cell function and engraftment. Nat. Med. 13, 742-747. doi: 10.1038/nm1578
28. Kadi, F., Charifi, N., Denis, C., and Lexell, J. (2004). Satellite cells and myonuclei in young and elderly women and men. Muscle Nerve 29, 120-127. doi: 10.1002/mus.10510
29. Kasai, H. (1997). Analysis of a form of oxidative DNA damage, 8-hydroxy-2'-deoxyguanosine, as a marker of cellular oxidative stress during carcinogenesis. Mutation research 387, 147-163. doi: 10.1016/S1383-5742(97)00035-5
30. Kawaguchi, D., Furutachi, S., Kawai, H., Hozumi, K., and Gotoh, Y. (2013). Dll1 maintains quiescence of adult neural stem cells and segregates asymmetrically during mitosis. Nat. Commun. 4, 1880. doi: 10.1038/ncomms2895
31. Kenyon, C., Chang, J., Gensch, E., Rudner, A., and Tabtiang, R. (1993). A C. elegans mutant that lives twice as long as wild type. Nature 366, 461-464. doi: 10.1038/366461a0
32. Kiel, M. J., Yilmaz, O. H., Iwashita, T., Yilmaz, O. H., Terhorst, C., and Morrison, S. J. (2005). SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121, 1109-1121. doi: 10.1016/j.cell.2005.05.026
33. Lama, V. N., Smith, L., Badri, L., Flint, A., Andrei, A. C., Murray, S., et al. (2007). Evidence for tissue-resident mesenchymal stem cells in human adult lung from studies of transplanted allografts. J. Clin. Invest. 117, 989-996. doi: 10.1172/JCI29713
34. Le Blanc, K., and Ringden, O. (2007). Immunomodulation by mesenchymal stem cells and clinical experience. J. Int. Med. 262, 509-525. doi: 10.1111/j.1365-2796.2007.01844.x
35. Lee, H. W., Blasco, M. A., Gottlieb, G. J., Horner, J. W. 2nd., Greider, C. W., and DePinho, R. A. (1998). Essential role of mouse telomerase in highly proliferative organs. Nature 392, 569-574. doi: 10.1038/33345
36. Li, L., and Clevers, H. (2010). Coexistence of quiescent and active adult stem cells in mammals. Science 327, 542-545. doi: 10.1126/science.1180794
37. Linton, P. J., and Dorshkind, K. (2004). Age-related changes in lymphocyte development and function. Nat. Immunol. 5, 133-139. doi: 10.1038/ni1033
38. Liu, H., Fergusson, M. M., Castilho, R. M., Liu, J., Cao, L., Chen, J., et al. (2007). Augmented Wnt signaling in a mammalian model of accelerated aging. Science 317, 803-806. doi: 10.1126/science.1143578
39. Liu, W., Liu, Y., Lai, X., and Kuang, S. (2012). Intramuscular adipose is derived from a non-Pax3 lineage and required for efficient regeneration of skeletal muscles. Dev. Biol. 361, 27-38. doi: 10.1016/j.ydbio.2011.10.011
40. Mateos, J., De la Fuente, A., Lesende-Rodriguez, I., Fernandez-Pernas, P., Arufe, M. C., and Blanco, F. J. (2013). Lamin A deregulation in human mesenchymal stem cells promotes an impairment in their chondrogenic potential and imbalance in their response to oxidative stress. Stem Cell Res. 11, 1137-1148. doi: 10.1016/j.scr.2013.07.004
41. Miyamoto, K., Araki, K. Y., Naka, K., Arai, F., Takubo, K., Yamazaki, S., et al. (2007). Foxo3a is essential for maintenance of the hematopoietic stem cell pool. Cell Stem Cell 1, 101-112. doi: 10.1016/j.stem.2007.02.001
42. Molofsky, A. V., Slutsky, S. G., Joseph, N. M., He, S., Pardal, R., Krishnamurthy, J., et al. (2006). Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing. Nature 443, 448-452. doi: 10.1038/nature05091
43. Morikawa, S., Mabuchi, Y., Kubota, Y., Nagai, Y., Niibe, K., Hiratsu, E., et al. (2009a). Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. J. Exp. Med. 206, 2483-2496. doi: 10.1084/jem.20091046
44. Morikawa, S., Mabuchi, Y., Niibe, K., Suzuki, S., Nagoshi, N., Sunabori, T., et al. (2009b). Development of mesenchymal stem cells partially originate from the neural crest. Biochem. Biophys. Res. Commun. 379, 1114-1119. doi: 10.1016/j.bbrc.2009.01.031
45. Moriyama, M., Osawa, M., Mak, S. S., Ohtsuka, T., Yamamoto, N., Han, H., et al. (2006). Notch signaling via Hes1 transcription factor maintains survival of melanoblasts and melanocyte stem cells. J. Cell Biol. 173, 333-339. doi: 10.1083/jcb.200509084
46. Morrison, S. J., Wandycz, A. M., Akashi, K., Globerson, A., and Weissman, I. L. (1996). The aging of hematopoietic stem cells. Nat. Med. 2, 1011-1016. doi: 10.1038/nm0996-1011
47. Mourikis, P., Sambasivan, R., Castel, D., Rocheteau, P., Bizzarro, V., and Tajbakhsh, S. (2012). A critical requirement for notch signaling in maintenance of the quiescent skeletal muscle stem cell state. Stem Cells 30, 243-252. doi: 10.1002/stem.775
48. Naito, A. T., Sumida, T., Nomura, S., Liu, M. L., Higo, T., Nakagawa, A., et al. (2012). Complement C1q activates canonical Wnt signaling and promotes aging-related phenotypes. Cell 149, 1298-1313. doi: 10.1016/j.cell.2012.03.047
49. Nijnik, A., Woodbine, L., Marchetti, C., Dawson, S., Lambe, T., Liu, C., et al. (2007). DNA repair is limiting for haematopoietic stem cells during ageing. Nature 447, 686-690. doi: 10.1038/nature05875
50. Nishimura, E. K. (2011). Melanocyte stem cells: a melanocyte reservoir in hair follicles for hair and skin pigmentation. Pigment Cell Melanoma Res. 24, 401-410. doi: 10.1111/j.1755-148X.2011.00855.x
51. Nishimura, E. K., Granter, S. R., and Fisher, D. E. (2005). Mechanisms of hair graying: incomplete melanocyte stem cell maintenance in the niche. Science 307, 720-724. doi: 10.1126/science.1099593
52. Ogg, S., Paradis, S., Gottlieb, S., Patterson, G. I., Lee, L., Tissenbaum, H. A., et al. (1997). The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389, 994-999. doi: 10.1038/40194
53. Omatsu, Y., Sugiyama, T., Kohara, H., Kondoh, G., Fujii, N., Kohno, K., et al. (2010). The essential functions of adipo-osteogenic progenitors as the hematopoietic stem and progenitor cell niche. Immunity 33, 387-399. doi: 10.1016/j.immuni.2010.08.017
54. Paik, J. H., Ding, Z., Narurkar, R., Ramkissoon, S., Muller, F., Kamoun, W. S., et al. (2009). FoxOs cooperatively regulate diverse pathways governing neural stem cell homeostasis. Cell Stem Cell 5, 540-553. doi: 10.1016/j.stem.2009.09.013
55. Pallafacchina, G., Francois, S., Regnault, B., Czarny, B., Dive, V., Cumano, A., et al. (2010). An adult tissue-specific stem cell in its niche: a gene profiling analysis of in vivo quiescent and activated muscle satellite cells. Stem Cell Res. 4, 77-91. doi: 10.1016/j.scr.2009.10.003
56. Pan, L., Chen, S., Weng, C., Call, G., Zhu, D., Tang, H., et al. (2007). Stem cell aging is controlled both intrinsically and extrinsically in the Drosophila ovary. Cell Stem Cell 1, 458-469. doi: 10.1016/j.stem.2007.09.010
57. Pang, W. W., Price, E. A., Sahoo, D., Beerman, I., Maloney, W. J., Rossi, D. J., et al. (2011). Human bone marrow hematopoietic stem cells are increased in frequency and myeloid-biased with age. Proc. Natl. Acad. Sci. U.S.A. 108, 20012-20017. doi: 10.1073/pnas.1116110108
58. Pellegrinet, L., Rodilla, V., Liu, Z., Chen, S., Koch, U., Espinosa, L., et al. (2011). Dll1-and dll4-mediated notch signaling are required for homeostasis of intestinal stem cells. Gastroenterology 140, 1230-1240.e1-7. doi: 10.1053/j.gastro.2011.01.005
59. Poyton, R. O., Ball, K. A., and Castello, P. R. (2009). Mitochondrial generation of free radicals and hypoxic signaling. Trends Endocrinol. Metab. 20, 332-340. doi: 10.1016/j.tem.2009.04.001
60. Renault, V. M., Rafalski, V. A., Morgan, A. A., Salih, D. A., Brett, J. O., Webb, A. E., et al. (2009). FoxO3 regulates neural stem cell homeostasis. Cell Stem Cell 5, 527-539. doi: 10.1016/j.stem.2009.09.014
61. Reuter, S., Gupta, S. C., Chaturvedi, M. M., and Aggarwal, B. B. (2010). Oxidative stress, inflammation, and cancer: how are they linked? Free Radic. Biol. Med. 49, 1603-1616. doi: 10.1016/j.freeradbiomed.2010.09.006
62. Roberts, E. W., Deonarine, A., Jones, J. O., Denton, A. E., Feig, C., Lyons, S. K., et al. (2013). Depletion of stromal cells expressing fibroblast activation protein-alpha from skeletal muscle and bone marrow results in cachexia and anemia. J. Exp. Med. 210, 1137-1151. doi: 10.1084/jem.20122344
63. Rompolas, P., Mesa, K. R., and Greco, V. (2013). Spatial organization within a niche as a determinant of stem-cell fate. Nature 502, 513-518. doi: 10.1038/nature12602
64. Rossi, D. J., Bryder, D., Seita, J., Nussenzweig, A., Hoeijmakers, J., and Weissman, I. L. (2007). Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age. Nature 447, 725-729. doi: 10.1038/nature05862
65. Rube, C. E., Fricke, A., Widmann, T. A., Furst, T., Madry, H., Pfreundschuh, M., et al. (2011). Accumulation of DNA damage in hematopoietic stem and progenitor cells during human aging. PLoS ONE 6:e17487. doi: 10.1371/journal.pone.0017487
66. Sacco, A., Mourkioti, F., Tran, R., Choi, J., Llewellyn, M., Kraft, P., et al. (2010). Short telomeres and stem cell exhaustion model Duchenne muscular dystrophy in mdx/mTR mice. Cell 143, 1059-1071. doi: 10.1016/j.cell.2010.11.039
67. Saeed, H., and Iqtedar, M. (2013). Stem cell function and maintenance - ends that matter: role of telomeres and telomerase. J. Biosci. 38, 641-649. doi: 10.1007/s12038-013-9346-3
68. Scaffidi, P., and Misteli, T. (2006). Lamin A-dependent nuclear defects in human aging. Science 312, 1059-1063. doi: 10.1126/science.1127168
69. Shibata, K. R., Aoyama, T., Shima, Y., Fukiage, K., Otsuka, S., Furu, M., et al. (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. doi: 10.1634/stemcells.2007-0225
70. Shiloh, Y., and Kastan, M. B. (2001). ATM: genome stability, neuronal development, and cancer cross paths. Adv. Cancer Res. 83, 209-254. doi: 10.1016/S0065-230X(01)83007-4
71. Sousa-Victor, P., Gutarra, S., Garcia-Prat, L., Rodriguez-Ubreva, J., Ortet, L., Ruiz-Bonilla, V., et al. (2014). Geriatric muscle stem cells switch reversible quiescence into senescence. Nature 50, 316-321. doi: 10.1038/nature13013
72. Sudo, K., Kanno, M., Miharada, K., Ogawa, S., Hiroyama, T., Saijo, K., et al. (2007). Mesenchymal progenitors able to differentiate into osteogenic, chondrogenic, and/or adipogenic cells in vitro are present in most primary fibroblast-like cell populations. Stem Cells 25, 1610-1617. doi: 10.1634/stemcells.2006-0504
73. Takashima, Y., Era, T., Nakao, K., Kondo, S., Kasuga, M., Smith, A. G., et al. (2007). Neuroepithelial cells supply an initial transient wave of MSC differentiation. Cell 129, 1377-1388. doi: 10.1016/j.cell.2007.04.028
74. Tavazoie, M., Van der Veken, L., Silva-Vargas, V., Louissaint, M., Colonna, L., Zaidi, B., et al. (2008). A specialized vascular niche for adult neural stem cells. Cell Stem Cell 3, 279-288. doi: 10.1016/j.stem.2008.07.025
75. Tothova, Z., Kollipara, R., Huntly, B. J., Lee, B. H., Castrillon, D. H., Cullen, D. E., et al. (2007). FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 128, 325-339. doi: 10.1016/j.cell.2007.01.003
76. Tsai, J. J., Dudakov, J. A., Takahashi, K., Shieh, J. H., Velardi, E., Holland, A. M., et al. (2013). Nrf2 regulates haematopoietic stem cell function. Nat. Cell Biol. 15, 309-316. doi: 10.1038/ncb2699
77. Tullet, J. M., Hertweck, M., An, J. H., Baker, J., Hwang, J. Y., Liu, S., et al. (2008). Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans. Cell 132, 1025-1038. doi: 10.1016/j.cell.2008.01.030
78. Uezumi, A., Fukada, S., Yamamoto, N., Takeda, S., and Tsuchida, K. (2010). Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat. Cell Biol. 12, 143-152. doi: 10.1038/ncb2014
79. Uezumi, A., Ikemoto-Uezumi, M., and Tsuchida, K. (2014). Roles of nonmyogenic mesenchymal progenitors in pathogenesis and regeneration of skeletal muscle. Front. Physiol. 5:68. doi: 10.3389/fphys.2014.00068
80. Uezumi, A., Ito, T., Morikawa, D., Shimizu, N., Yoneda, T., Segawa, M., et al. (2011). Fibrosis and adipogenesis originate from a common mesenchymal progenitor in skeletal muscle. J. Cell Sci. 124, 3654-3664. doi: 10.1242/jcs.086629
81. Vaziri, H., and Benchimol, S. (1996). From telomere loss to p53 induction and activation of a DNA-damage pathway at senescence: the telomere loss/DNA damage model of cell aging. Exp. Gerontol. 31, 295-301. doi: 10.1016/0531-5565(95)02025-X
82. von Zglinicki, T. (2002). Oxidative stress shortens telomeres. Trends Biochem. Sci. 27, 339-344. doi: 10.1016/S0968-0004(02)02110-2
83. Wong, K. K., Maser, R. S., Bachoo, R. M., Menon, J., Carrasco, D. R., Gu, Y., et al. (2003). Telomere dysfunction and Atm deficiency compromises organ homeostasis and accelerates ageing. Nature 421, 643-648. doi: 10.1038/nature01385
84. Yoshida, S., Sukeno, M., and Nabeshima, Y. (2007). A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science 317, 1722-1726. doi: 10.1126/science.1144885
85. Zhang, D. Y., Wang, H. J., and Tan, Y. Z. (2011a). Wnt/beta-catenin signaling induces the aging of mesenchymal stem cells through the DNA damage response and the p53/p21 pathway. PLoS ONE 6:e21397. doi: 10.1371/journal.pone.0021397
86. Zhang, J., Lian, Q., Zhu, G., Zhou, F., Sui, L., Tan, C., et al. (2011b). A human iPSC model of Hutchinson Gilford Progeria reveals vascular smooth muscle and mesenchymal stem cell defects. Cell Stem Cell 8, 31-45. doi: 10.1016/j.stem.2010.12.002
87. Zuk, P. A., Zhu, M., Ashjian, P., De Ugarte, D. A., Huang, J. I., Mizuno, H., et al. (2002). Human adipose tissue is a source of multipotent stem cells. Mol. Biol. Cell 13, 4279-4295. doi: 10.1091/mbc. E02-02-0105