P16INK4A mediates age-related changes in mesenchymal stem cells derived from human dental pulp through the DNA damage and stress response

Mechanisms of Ageing and Development

Volumn 141-142, Issue , 2014, Pages 46-55

  Feng, Xingmei ^a   Xing, Jing ^a   Feng, Guijuan ^a   Huang, Dan ^a   Lu, Xiaohui ^a   Liu, Suzhe ^a   Tan, Wei ^a   Li, Liren ^a   Gu, Zhifeng ^a  

^a NANTONG UNIVERSITY   (China)

Author keywords

Age related; Dental pulp; Mesenchymal stem cell; P16INK4A; Senescence

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A;

ADOLESCENT; ADULT; AGING; CELL AGING; CHILD; DNA DAMAGE; FEMALE; GENE EXPRESSION REGULATION; HUMAN; MALE; MESENCHYMAL STROMA CELL; METABOLISM; MIDDLE AGED; PATHOLOGY; PRESCHOOL CHILD; SIGNAL TRANSDUCTION; TOOTH PULP;

ADOLESCENT; ADULT; AGING; CELL AGING; CHILD; CHILD, PRESCHOOL; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DENTAL PULP; DNA DAMAGE; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MALE; MESENCHYMAL STROMAL CELLS; MIDDLE AGED; SIGNAL TRANSDUCTION;

EID: 84908502157     PISSN: 00476374     EISSN: 18726216     Source Type: Journal    
DOI: 10.1016/j.mad.2014.09.004     Document Type: Article

References (43)

1. Armanios M., Alder J.K., Parry E.M., Karim B., Strong M.A., Greider C.W. Short telomeres are sufficient to cause the degenerative defects associated with aging. Am. J. Hum. Genet. 2009, 85:823-832.
2. Alge D.L., Zhou D., Adams L.L., Wyss B.K., Shadday M.D., Woods E.J., Gabriel Chu T.M., Goebel W.S. Donor-matches comparison of dental pulp stem cells and bone marrow-derived mesenchymal stem cells in a rat model. J. Tissue Eng. Regen. Med. 2010, 4:73-81.
3. Beauséjour C. Bone marrow-derived cells: the influence of aging and cellular senescence. Handb. Exp. Pharmacol. 2007, 180:67-88.
4. Campisi J. Cancer and aging: yin, yang, and p53. Sci. Aging Knowl. Environ. 2002, 2002:pe1.
5. Campisi J. Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors. Cell 2005, 120:513-522.
6. Collins C.J., Sedivy J.M. Involvement of the INK4a/Arf gene locus in senescence. Aging Cell 2003, 2:145-150.
7. Dimri G., Lee X., Basile G., Acosta M., Scott G., Roskelley C., Medrano E.E., Linskens M., Rubelj I., Pereira-Smith O., Peacocke M., Campisi J. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:9363-9367.
8. Feng X., Xing J., Feng G., Sang A., Shen B., Xu Y., Jiang J., Liu S., Tan W., Gu Z., Li L. Age-dependent impaired neurogenic differentiation capacity of dental stem cell is associated with Wnt/β-Catenin signaling. Cell. Mol. Neurobiol. 2013, 33:1023-1031.
9. Finkel T., Serrano M., Blasco M.A. The common biology of cancer and ageing. Nature 2007, 448:767-774.
10. Gu Z., Cao X., Jiang J., Li L., Da Z., Liu H., Cheng C. Upregulation of p16INK4A promotes cellular senescence of bone marrow-derived mesenchymal stem cells from systemic lupus erythematosus patients. Cell. Signal. 2012, 24:2307-2314.
11. Hall D.M., Xu L., Drake V.J., Oberley L.W., Oberley T.D., Moseley P.L., Kregel K.C. Aging reduces adaptive capacity and stress protein expression in the liver after heat stress. J. Appl. Physiol. 2000, 89:749-759.
12. Huang G.T., Gronthos S., Shi S. Mesenchymal stem cells derived from dental tissues vs. those from other sources: their biologyand role in regenerative medicine. J. Dent. Res. 2009, 88:792-806.
13. Heo J.Y., Jing K., Song K.S., Seo K.S., Park J.H., Kim J.S., Jung Y.J., Hur G.M., Jo D.Y., Kweon G.R., Yoon W.H., Lim K., Hwang B.D., Jeon B.H., Park J.I. Downregulation of APE1/Ref-1 is involved in the senescence of mesenchymal stem cells. Stem Cells 2009, 27:1455-1462.
14. Inoue T., Kato K., Kato H., Asanoma K., Kuboyama A., Ueoka Y., Yamaguchi S., Ohgami T., Wake N. Level of reactive oxygen species induced by p21Waf1/CIP1 is critical for the determination of cell fate. Cancer Sci. 2009, 100:1275-1283.
15. Jaiswal N., Haynesworth S.E., Caplan A.I., Bruder S.P. Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. J. Cell. Biochem. 1997, 64:295-312.
16. Johnstone B., Hering T.M., Caplan A.I., Goldberg V.M., Yoo J.U. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp. Cell Res. 1998, 238:265-272.
17. Kasper G., Mao L., Geissler S., Draycheva A., Trippens J., Kuhnisch J., Tschirschmann M., Kaspar K., Perka C., Duda G.N., Klose J. Insights into mesenchymal stem cell aging: involvement of antioxidant defense and actin cytoskeleton. Stem Cells 2009, 27:1288-1297.
18. Kosar M., Bartkova J., Hubackova S., Hodny Z., Lukas J., Bartek J. Senescence-associated heterochromatin foci are dispensable for cellular senescence, occur in a cell type- and insult-dependent manner and follow expression of p16 (ink4a). Cell Cycle 2011, 10:457-468.
19. Kretlow J.D., Jin Y.Q., Liu W., Zhang W.J., Hong T.H., Zhou G., Baggett L.S., Mikos A.G., Cao Y. Donor age and cell passage affects differentiation potential of murine bone marrow derived stem cells. BMC Cell Biol. 2008, 9:60.
20. Maynard S., Schurman S.H., Harboe C., de Souza-Pinto N.C., Bohr V.A. Base excision repair of oxidative DNA damage and association with cancer and aging. Carcinogenesis 2009, 30:2-10.
21. Melk A., Schmidt B.M., Takeuchi O., Sawitzki B., Rayner D.C., Halloran P.F. Expression of p16INK4a and other cell cycle regulator and senescence associated genes in aging human kidney. Kidney Int. 2004, 65:510-520.
22. Muller M. Cellular senescence: molecular mechanisms, in vivo significance, and redox considerations. Antioxid. Redox Signal. 2009, 11:59-98.
23. Park J.S., Kim H.Y., Kim H.W., Chae G.N., Oh H.T., Park J.Y., Shim H., Seo M., Shin E.Y., Kim E.G., Park S.C., Kwak S.J. Increased caveolin-1, a cause for the declined adipogenic potential of senescent human mesenchymal stem cells. Mech. Ageing Dev. 2005, 126:551-559.
24. Pierdomenico L., Bonsi L., Calvitti M., Rondelli D., Arpinati M., Chirumbolo G., Becchetti E., Marchionni C., Alviano F., Fossati V., Staffolani N., Franchina M., Grossi A., Bagnara G.P. Multipotent mesenchymal stem cells with immunosuppressive activity can be easily isolated from dental pulp. Transplantation 2005, 80:836-842.
25. Purpura K.A., Aubin J.E., Zandstra P.W. Sustained in vitro expansion of bone progenitors is cell density dependent. Stem Cells 2004, 22:39-50.
26. Rodriguez-Vargas J.M., Ruiz-Magana M.J., Ruiz-Ruiz C., Majuelos-Melguizo J., Peralta-Leal A., Rodriguez M.I., Munoz-Gamez J.A., de Almodovar M.R., Siles E., Rivas A.L., Jaattela M., Oliver F.J. ROS-induced DNA damage and PARP-1 are required for optimal induction of starvation-induced autophagy. Cell Res. 2012, 22:1181-1198.
27. Seoane M., Iglesias P., Gonzalez T., Dominguez F., Fraga M., Aliste C., Forteza J., Costoya J.A. Retinoblastoma loss modulates DNA damage response favoring tumor progression. PLoS ONE 2008, 3:e3632.
28. Serrano M., Hannon G.J., Beach D. A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature 1993, 366:704-707.
29. Sethe S., Scutt A., Stolzing A. Aging of mesenchymal stem cells. Ageing Res. Rev. 2006, 5:91-116.
30. Shibata K.R., Aoyama T., Shima Y., Fukiage K., Otsuka S., Furu M., Kohno Y., Ito K., Fujibayashi S., Neo M., Nakayama T., Nakamura T., Toguchida J. 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 2007, 25:2371-2382.
31. Stolzing A., Scutt A. Age-related impairment of mesenchymal progenitor cell function. Aging Cell 2006, 5:213-224.
32. Swanlund J.M., Kregel K.C., Oberley T.D. Autophagy following heat stress: the role of aging and protein nitration. Autophagy 2008, 4:936-939.
33. Tokalov S.V., Gruner S., Schindler S., Wolf G., Baumann M., Abolmaali N. Age-related changes in the frequency of mesenchymal stem cells in the bone marrow of rats. Stem Cells Dev. 2007, 16:439-446.
34. Wallenfang M.R. Aging within the stem cell niche. Dev. Cell 2007, 13:603-604.
35. Wang C., Jurk D., Maddick M., Nelson G., Martin-Ruiz C., von Zglinicki T. DNA damage response and cellular senescence in tissues of aging mice. Aging Cell 2009, 8:311-323.
36. Wang H., Zhou W., Zheng Z., Zhang P., Tu B., He Q., Zhu W.G. The HDAC inhibitor depsipeptide transactivates the p53/p21 pathway by inducing DNA damage. DNA Repair 2012, 11:146-156.
37. Wang J., Liu X., Jin X., Ma H., Hu J., Ni L., Ma P.X. The odontogenic differentiation of human dental pulp stem cells on nanofibrous poly(l-lactic acid) scaffolds in vitro and in vivo. Acta Biomater. 2010, 6:3856-3863.
38. Wang J., Ma H., Jin X., Hu J., Liu X., Ni L., Ma P.X. The effect of scaffold architecture on odontogenic differentiation of human dental pulp stem cells. Biomaterials 2011, 32:7822-7830.
39. Zhang H., Fazel S., Tian H., Mickle D.A., Weisel R.D., Fujii T., Li R.K. Increasing donor age adversely impacts beneficial effects of bone marrow but not smooth muscle myocardial cell therapy. Am. J. Physiol. Heart Circ. Physiol. 2005, 289:2089-2096.
40. Zhang H. Molecular signaling and genetic pathways of senescence: its role in tumorigenesis and aging. J. Cell. Physiol. 2007, 210:567-574.
41. Zhang J., An Y., Gao L.N., Zhang Y.J., Jin Y., Chen F.M. The effect of aging on the pluripotential capacity and regenerative potential of human periodontal ligament stem cells. Biomaterials 2012, 33:6974-6986.
42. Zheng Y., Liu Y., Zhang C.M., Zhang H.Y., Li W.H., Shi S., Le A.D., Wang S.L. Stem cells from deciduous tooth repair mandibular defect in swine. J. Dent. Res. 2009, 88:249-254.
43. Zhou S., Greenberger J.S., Epperly M.W., Goff J.P., Adler C., Leboff M.S., Glowacki J. Age-related intrinsic changes in human bone-marrow-derived mesenchymal stem cells and their differentiation to osteoblasts. Aging Cell 2008, 7:335-343.