C-Maf regulates pluripotency genes, proliferation/self-renewal, and lineage commitment in ROS-mediated senescence of human mesenchymal stem cells

Oncotarget

Volumn 6, Issue 34, 2015, Pages 35404-35418

  Chen, Pei Min ^a   Lin, Chia Hua ^a   Li, Nan Ting ^a   Wu, Yao Ming ^b,c   Lin, Ming Tsan ^a,c   Hung, Shih Chieh ^d,e   Yen, Men Luh ^a,b  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^d NATIONAL YANG MING UNIVERSITY   (Taiwan)

^e TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

Author keywords

C Maf; Gerotarget; human adipose tissue derived MSCs (hAMSCs); Lineage commitment; ROS mediated senescence; Self renewal

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; CYCLIN DEPENDENT KINASE INHIBITOR 2B; HYDROGEN PEROXIDE; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR C MAF; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; MAF PROTEIN, HUMAN;

ADIPOGENESIS; ADIPOSE TISSUE DERIVED MESENCHYMAL STEM CELL; ARTICLE; BIOACCUMULATION; BONE DEVELOPMENT; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CELL RENEWAL; DOWN REGULATION; EX VIVO STUDY; GENE CONTROL; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VITRO STUDY; MESENCHYMAL STEM CELL; OXIDATIVE STRESS; PLURIPOTENT STEM CELL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; SENESCENCE; STEM CELL EXPANSION; UPREGULATION; CELL AGING; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; PHYSIOLOGY;

CELL AGING; CELL PROLIFERATION; GENE EXPRESSION REGULATION; HUMANS; MESENCHYMAL STROMAL CELLS; PLURIPOTENT STEM CELLS; PROTO-ONCOGENE PROTEINS C-MAF; REACTIVE OXYGEN SPECIES;

EID: 84946828425     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6178     Document Type: Article

References (46)

1. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, Alfonso ZC, Fraser JK, Benhaim P and Hedrick MH. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell. 2002; 13:4279-4295.
2. Komoda H, Okura H, Lee CM, Sougawa N, Iwayama T, Hashikawa T, Saga A, Yamamoto-Kakuta A, Ichinose A, Murakami S, Sawa Y and Matsuyama A. Reduction of N-glycolylneuraminic acid xenoantigen on human adipose tissue-derived stromal cells/mesenchymal stem cells leads to safer and more useful cell sources for various stem cell therapies. Tissue Eng Part A. 2010; 16:1143-1155.
3. Wagner W, Bork S, Lepperdinger G, Joussen S, Ma N, Strunk D and Koch C. How to track cellular aging of mesenchymal stromal cells? Aging (Albany NY). 2010; 2:224-230.
4. Lepperdinger G, Brunauer R, Jamnig A, Laschober G and Kassem M. Controversial issue: is it safe to employ mesenchymal stem cells in cell-based therapies? Exp Gerontol. 2008; 43:1018-1023.
5. Lopez-Otin C, Blasco MA, Partridge L, Serrano M and Kroemer G. The hallmarks of aging. Cell. 2013; 153:1194-1217.
6. Ho PJ, Yen ML, Tang BC, Chen CT and Yen BL. H2O2 accumulation mediates differentiation capacity alteration, but not proliferative decline, in senescent human fetal mesenchymal stem cells. Antioxid Redox Signal. 2013; 18:11.
7. Stenderup K, Justesen J, Eriksen EF, Rattan SI and Kassem M. Number and proliferative capacity of osteogenic stem cells are maintained during aging and in patients with osteoporosis. J Bone Miner Res. 2001; 16:1120-1129.
8. D'Ippolito G, Schiller PC, Ricordi C, Roos BA and Howard GA. Age-related osteogenic potential of mesenchymal stromal stem cells from human vertebral bone marrow. J Bone Miner Res. 1999; 14:1115-1122.
9. Zhou S, Greenberger JS, Epperly MW, Goff JP, Adler C, Leboff MS and 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.
10. Benz CC and Yau C. Ageing, oxidative stress and cancer: paradigms in parallax. Nat Rev Cancer. 2008; 8:875-879.
11. Finkel T and Holbrook NJ. Oxidants, oxidative stress and the biology of ageing. Nature. 2000; 408:239-247.
12. Kataoka K. Multiple mechanisms and functions of maf transcription factors in the regulation of tissue-specific genes. J Biochem. 2007; 141:775-781.
13. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D and Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006; 8:315-317.
14. Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, Medrano EE, Linskens M, Rubelj I, Pereira-Smith O and et al. 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.
15. Stenderup K, Justesen J, Clausen C and Kassem M. Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone. 2003; 33:919-926.
16. Lee JS, Lee MO, Moon BH, Shim SH, Fornace AJ, Jr. and Cha HJ. Senescent growth arrest in mesenchymal stem cells is bypassed by Wip1-mediated downregulation of intrinsic stress signaling pathways. Stem Cells. 2009; 27:1963-1975.
17. Sethe S, Scutt A and Stolzing A. Aging of mesenchymal stem cells. Ageing Res Rev. 2006; 5:91-116.
18. Glimcher LH. Lineage commitment in lymphocytes: controlling the immune response. J Clin Invest. 2001; 108:s25-s30.
19. Nishikawa K, Nakashima T, Takeda S, Isogai M, Hamada M, Kimura A, Kodama T, Yamaguchi A, Owen MJ, Takahashi S and Takayanagi H. Maf promotes osteoblast differentiation in mice by mediating the age-related switch in mesenchymal cell differentiation. J Clin Invest. 2010; 120:3455-3465.
20. Beltrami AP, Cesselli D and Beltrami CA. Stem cell senescence and regenerative paradigms. Clin Pharmacol Ther. 2012; 91:21-29.
21. Takahashi K and Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006; 126:663-676.
22. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, Guenther MG, Kumar RM, Murray HL, Jenner RG, Gifford DK, Melton DA, Jaenisch R and Young RA. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell. 2005; 122:947-956.
23. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin, II and Thomson JA. Induced pluripotent stem cell lines derived from human somatic cells. Science. 2007; 318:1917-1920.
24. Giorgio M, Trinei M, Migliaccio E and Pelicci PG. Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals? Nat Rev Mol Cell Biol. 2007; 8:722-728.
25. Yoshida T, Ohkumo T, Ishibashi S and Yasuda K. The 5'-AT-rich half-site of Maf recognition element: a functional target for bZIP transcription factor Maf. Nucleic Acids Res. 2005; 33:3465-3478.
26. Eychene A, Rocques N and Pouponnot C. A new MAFia in cancer. Nat Rev Cancer. 2008; 8:683-693.
27. Caplan AI and Correa D. The MSC: an injury drugstore. Cell Stem Cell. 2011; 9:11-15.
28. Chamberlain G, Fox J, Ashton B and Middleton J. Mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells. 2007; 25:2739-2749.
29. Hegde SP, Zhao J, Ashmun RA and Shapiro LH. c-Maf induces monocytic differentiation and apoptosis in bipotent myeloid progenitors. Blood. 1999; 94:1578-1589.
30. Hansen L, Mikkelsen A, Nurnberg P, Nurnberg G, Anjum I, Eiberg H and Rosenberg T. Comprehensive mutational screening in a cohort of Danish families with hereditary congenital cataract. Invest Ophthalmol Vis Sci. 2009; 50:3291-3303.
31. Ring BZ, Cordes SP, Overbeek PA and Barsh GS. Regulation of mouse lens fiber cell development and differentiation by the Maf gene. Development. 2000; 127:307-317.
32. Tsai CC, Su PF, Huang YF, Yew TL and Hung SC. Oct4 and Nanog directly regulate Dnmt1 to maintain self-renewal and undifferentiated state in mesenchymal stem cells. Mol Cell. 2012; 47:169-182.
33. Li Z, Liu C, Xie Z, Song P, Zhao RC, Guo L, Liu Z and Wu Y. Epigenetic dysregulation in mesenchymal stem cell aging and spontaneous differentiation. PLoS One. 2011; 6:e20526.
34. Yew TL, Chiu FY, Tsai CC, Chen HL, Lee WP, Chen YJ, Chang MC and Hung SC. Knockdown of p21(Cip1/Waf1) enhances proliferation, the expression of stemness markers, and osteogenic potential in human mesenchymal stem cells. Aging Cell. 2011; 10:349-361.
35. Maslov AY, Barone TA, Plunkett RJ and Pruitt SC. Neural stem cell detection, characterization, and age-related changes in the subventricular zone of mice. J Neurosci. 2004; 24:1726-1733.
36. Molofsky AV, Slutsky SG, Joseph NM, He S, Pardal R, Krishnamurthy J, Sharpless NE and Morrison SJ. Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing. Nature. 2006; 443:448-452.
37. Yoshida Y, Takahashi K, Okita K, Ichisaka T and Yamanaka S. Hypoxia enhances the generation of induced pluripotent stem cells. Cell Stem Cell. 2009; 5:237-241.
38. Sherr CJ and DePinho RA. Cellular senescence: mitotic clock or culture shock? Cell. 2000; 102:407-410.
39. Janzen V, Forkert R, Fleming HE, Saito Y, Waring MT, Dombkowski DM, Cheng T, DePinho RA, Sharpless NE and Scadden DT. Stem-cell ageing modified by the cyclindependent kinase inhibitor p16INK4a. Nature. 2006; 443:421-426.
40. Shibata KR, Aoyama T, Shima Y, Fukiage K, Otsuka S, Furu M, Kohno Y, Ito K, Fujibayashi S, Neo M, Nakayama T, Nakamura T and 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.
41. Lee RH, Kim B, Choi I, Kim H, Choi HS, Suh K, Bae YC and Jung JS. Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue. Cell Physiol Biochem. 2004; 14:311-324.
42. Wang CH, Wang TM, Young TH, Lai YK and Yen ML. The critical role of ECM proteins within the human MSC niche in endothelial differentiation. Biomaterials. 2013; 34:4223-4234.
43. Yen ML, Hou CH, Peng KY, Tseng PC, Jiang SS, Shun CT, Chen YC and Kuo ML. Efficient derivation and concise gene expression profiling of human embryonic stem cellderived mesenchymal progenitors (EMPs). Cell Transplant. 2011; 20:1529-1545.
44. Tseng PC, Young TH, Wang TM, Peng HW, Hou SM and Yen ML. Spontaneous osteogenesis of MSCs cultured on 3D microcarriers through alteration of cytoskeletal tension. Biomaterials. 2012; 33:556-564.
45. Wu CC, Chao YC, Chen CN, Chien S, Chen YC, Chien CC, Chiu JJ and Linju Yen B. Synergism of biochemical and mechanical stimuli in the differentiation of human placentaderived multipotent cells into endothelial cells. J Biomech. 2008; 41:813-821.
46. Tseng PC, Hou SM, Chen RJ, Peng HW, Hsieh CF, Kuo ML and Yen ML. Resveratrol promotes osteogenesis of human mesenchymal stem cells by upregulating RUNX2 gene expression via the SIRT1/FOXO3A axis. J Bone Miner Res. 2011; 26:2552-2563.