DNA methylation pattern changes upon long-term culture and aging of human mesenchymal stromal cells

Aging Cell

Volumn 9, Issue 1, 2010, Pages 54-63

  Bork, Simone ^a,b   Pfister, Stefan ^a,b,c   Witt, Hendrik ^a,c   Horn, Patrick ^a   Korn, Bernhard ^c   Ho, Anthony D ^a,b   Wagner, Wolfgang ^a,b,d  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b HEIDELBERG ACADEMY OF SCIENCES AND HUMANITIES   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Aging; DNA methylation; Human mesenchymal stromal cells; Long term culture; Pyrosequencing; Senescence

Indexed keywords

BISULFITE; HOMEODOMAIN PROTEIN;

ADULT; AGE DISTRIBUTION; AGED; ARTICLE; CELL AGING; CELL DIFFERENTIATION; CELL DIVISION; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EPIGENETICS; GENE EXPRESSION; HOMEOBOX; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; MESENCHYME CELL; MICROARRAY ANALYSIS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PYROSEQUENCING; STROMA CELL; AGING; CELL CULTURE; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; METABOLISM; MIDDLE AGED; TIME;

ADULT; AGED; AGED, 80 AND OVER; AGING; CELL AGING; CELLS, CULTURED; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; HUMANS; MIDDLE AGED; STROMAL CELLS; TIME FACTORS; YOUNG ADULT;

EID: 76249107254     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2009.00535.x     Document Type: Article

References (55)

1. Banfi A, Muraglia A, Dozin B, Mastrogiacomo M, Cancedda R, Quarto R. Proliferation kinetics and differentiation potential of ex vivo expanded human bone marrow stromal cells: implications for their use in cell therapy. Exp. Hematol. 2000, 28:707-715.
2. Baxter MA, Wynn RF, Jowitt SN, Wraith JE, Fairbairn LJ, Bellantuono I. Study of telomere length reveals rapid aging of human marrow stromal cells following in vitro expansion. Stem Cells 2004, 22:675-682.
3. Bonab MM, Alimoghaddam K, Talebian F, Ghaffari SH, Ghavamzadeh A, Nikbin B. Aging of mesenchymal stem cell in vitro. BMC Cell Biol. 2006, 7:14.
4. Brandeis M, Frank D, Keshet I, Siegfried Z, Mendelsohn M, Nemes A, Temper V, Razin A, Cedar H. Sp1 elements protect a CpG island from de novo methylation. Nature 1994, 371:435-438.
5. Chambers SM, Shaw CA, Gatza C, Fisk CJ, Donehower LA, Goodell MA. Aging hematopoietic stem cells decline in function and exhibit epigenetic dysregulation. PLoS Biol. 2007, 5:201.
6. Cristofalo VJ, Allen RG, Pignolo RJ, Martin BG, Beck JC. Relationship between donor age and the replicative lifespan of human cells in culture: a reevaluation. Proc. Natl Acad. Sci. U.S.A. 1998, 95:10614-10619.
7. Deng G, Chen A, Hong J, Chae HS, Kim YS. Methylation of CpG in a small region of the hMLH1 promoter invariably correlates with the absence of gene expression. Cancer Res. 1999, 59:2029-2033.
8. Di Donna S, Mamchaoui K, Cooper RN, Seigneurin-Venin S, Tremblay J, Butler-Browne GS, Mouly V. Telomerase can extend the proliferative capacity of human myoblasts, but does not lead to their immortalization. Mol. Cancer Res. 2003, 1:643-653.
9. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006, 8:315-317.
10. Gonzalgo ML, Hayashida T, Bender CM, Pao MM, Tsai YC, Gonzales FA, Nguyen HD, Nguyen TT, Jones PA. The role of DNA methylation in expression of the p19/p16 locus in human bladder cancer cell lines. Cancer Res. 1998, 58:1245-1252.
11. Hayflick L. The limited in vitro lifetime of human diploid cell strains. Exp. Cell Res. 1965, 37:614-636.
12. Ho AD, Wagner W, Mahlknecht U. Stem cells and ageing. The potential of stem cells to overcome age-related deteriorations of the body in regenerative medicine. EMBO Rep. 2005, 6:35-38.
13. Horwitz EM, Le BK, Dominici M, Mueller I, Slaper-Cortenbach I, Marini FC, Deans RJ, Krause DS, Keating A. Clarification of the nomenclature for MSC: the International Society for Cellular Therapy position statement. Cytotherapy 2005, 7:393-395.
14. Illingworth R, Kerr A, Desousa D, Jorgensen H, Ellis P, Stalker J, Jackson D, Clee C, Plumb R, Rogers J, Humphray S, Cox T, Langford C, Bird A. A novel CpG island set identifies tissue-specific methylation at developmental gene loci. PLoS Biol. 2008, 6:e22.
15. Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet. 2003, 33(Suppl):245-254.
16. Janzen V, Forkert R, Fleming HE, Saito Y, Waring MT, Dombkowski DM, Cheng T, DePinho RA, Sharpless NE, Scadden DT. Stem-cell ageing modified by the cyclin-dependent kinase inhibitor p16INK4a. Nature 2006, 443:421-426.
17. Kangaspeska S, Stride B, Metivier R, Polycarpou-Schwarz M, Ibberson D, Carmouche RP, Benes V, Gannon F, Reid G. Transient cyclical methylation of promoter DNA. Nature 2008, 452:112-115.
18. Kirkwood TB, Austad SN. Why do we age? Nature 2000, 408:233-238.
19. Kiyono T, Foster SA, Koop JI, McDougall JK, Galloway DA, Klingelhutz AJ. Both Rb/p16INK4a inactivation and telomerase activity are required to immortalize human epithelial cells. Nature 1998, 396:84-88.
20. Lee MH, Kim YJ, Yoon WJ, Kim JI, Kim BG, Hwang YS, Wozney JM, Chi XZ, Bae SC, Choi KY, Cho JY, Choi JY, Ryoo HM. Dlx5 specifically regulates Runx2 type II expression by binding to homeodomain-response elements in the Runx2 distal promoter. J. Biol. Chem. 2005, 280:35579-35587.
21. Macleod D, Charlton J, Mullins J, Bird AP. Sp1 sites in the mouse aprt gene promoter are required to prevent methylation of the CpG island. Genes Dev. 1994, 8:2282-2292.
22. de Magalhaes JP, Church GM. Genomes optimize reproduction: aging as a consequence of the developmental program. Physiology (Bethesda) 2005, 20:252-259.
23. Marciniak-Czochra A, Stiehl T, Wagner W. Modeling of replicative senescence in hematopoietic development. Aging 2009, 1:723-732.
24. Mareschi K, Ferrero I, Rustichelli D, Aschero S, Gammaitoni L, Aglietta M, Madon E, Fagioli F. Expansion of mesenchymal stem cells isolated from pediatric and adult donor bone marrow. J. Cell. Biochem. 2006, 97:744-754.
25. Metivier R, Gallais R, Tiffoche C, Le Peron C, Jurkowska RZ, Carmouche RP, Ibberson D, Barath P, Demay F, Reid G, Benes V, Jeltsch A, Gannon F, Salbert G. Cyclical DNA methylation of a transcriptionally active promoter. Nature 2008, 452:45-50.
26. Moerman EJ, Teng K, Lipschitz DA, Lecka-Czernik B. Aging activates adipogenic and suppresses osteogenic programs in mesenchymal marrow stroma/stem cells: the role of PPAR-gamma2 transcription factor and TGF-beta/BMP signaling pathways. Aging Cell 2004, 3:379-389.
27. Nilsson O, Mitchum RD, Schrier L, Ferns SP, Barnes KM, Troendle JF, Baron J. Growth plate senescence is associated with loss of DNA methylation. J. Endocrinol. 2005, 186:241-249.
28. Noer A, Boquest AC, Collas P. Dynamics of adipogenic promoter DNA methylation during clonal culture of human adipose stem cells to senescence. BMC Cell Biol. 2007, 8:18.
29. O'Hare MJ, Bond J, Clarke C, Takeuchi Y, Atherton AJ, Berry C, Moody J, Silver AR, Davies DC, Alsop AE, Neville AM, Jat PS. Conditional immortalization of freshly isolated human mammary fibroblasts and endothelial cells. Proc. Natl Acad. Sci. U.S.A. 2001, 98:646-651.
30. Prinzinger R. Programmed ageing: the theory of maximal metabolic scope. How does the biological clock tick? EMBO Rep. 2005, 6:S14-S19.
31. Reyes M, Lund T, Lenvik T, Aguiar D, Koodie L, Verfaillie CM. Purification and ex vivo expansion of postnatal human marrow mesodermal progenitor cells. Blood 2001, 98:2615-2625.
32. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, Rezantsev A, Popov D, Ryltsov A, Kostukovich E, Borisovsky I, Liu Z, Vinsavich A, Trush V, Quackenbush J. TM4: a free, open-source system for microarray data management and analysis. BioTechniques 2003, 34:374-378.
33. Schallmoser K, Bartmann C, Rohde E, Bork S, Guelly C, Obenauf AC, Reinisch A, Horn P, Ho AD, Strunk D, Wagner W. Replicative senescence-associated gene expression changes in mesenchymal stromal cells are similar under different culture conditions. Haematologica 2009, (in press)
34. Schneider EL, Mitsui Y. The relationship between in vitro cellular aging and in vivo human age. Proc. Natl Acad. Sci. U.S.A. 1976, 73:3584-3588.
35. Shibata KR, 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.
36. So K, Tamura G, Honda T, Homma N, Waki T, Togawa N, Nishizuka S, Motoyama T. Multiple tumor suppressor genes are increasingly methylated with age in non-neoplastic gastric epithelia. Cancer Sci. 2006, 97:1155-1158.
37. Song JZ, Stirzaker C, Harrison J, Melki JR, Clark SJ. Hypermethylation trigger of the glutathione-S-transferase gene (GSTP1) in prostate cancer cells. Oncogene 2002, 21:1048-1061.
38. Soshnikova N, Duboule D. Epigenetic temporal control of mouse Hox genes in vivo. Science 2009, 324:1320-1323.
39. Steemers FJ, Chang W, Lee G, Barker DL, Shen R, Gunderson KL. Whole-genome genotyping with the single-base extension assay. Nat. Methods 2006, 3:31-33.
40. Stelnicki EJ, Komuves LG, Kwong AO, Holmes D, Klein P, Rozenfeld S, Lawrence HJ, Adzick NS, Harrison M, Largman C. HOX homeobox genes exhibit spatial and temporal changes in expression during human skin development. J. Invest. Dermatol. 1998, 110:110-115.
41. Stenderup K, Justesen J, Clausen C, Kassem M. Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 2003, 33:919-926.
42. Stirzaker C, Song JZ, Davidson B, Clark SJ. Transcriptional gene silencing promotes DNA hypermethylation through a sequential change in chromatin modifications in cancer cells. Cancer Res. 2004, 64:3871-3877.
43. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. U.S.A. 2005, 102:15545-15550.
44. Suzuki T, Farrar JE, Yegnasubramanian S, Zahed M, Suzuki N, Arceci RJ. Stable knockdown of PASG enhances DNA demethylation but does not accelerate cellular senescence in TIG-7 human fibroblasts. Epigenetics 2008, 3:281-291.
45. Ushijima T, Okochi-Takada E. Aberrant methylations in cancer cells: where do they come from? Cancer Sci. 2005, 96:206-211.
46. Vogt M, Haggblom C, Yeargin J, Christiansen-Weber T, Haas M. Independent induction of senescence by p16INK4a and p21CIP1 in spontaneously immortalized human fibroblasts. Cell Growth Differ. 1998, 9:139-146.
47. Wagner W, Ho AD. Mesenchymal stem cell preparations-comparing apples and oranges. Stem Cell Rev. 2007, 3:239-248.
48. Wagner W, Wein F, Seckinger A, Frankhauser M, Wirkner U, Krause U, Blake J, Schwager C, Eckstein V, Ansorge W, Ho AD. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp. Hematol. 2005, 33:1402-1416.
49. Wagner W, Horn P, Castoldi M, Diehlmann A, Bork S, Saffrich R, Benes V, Blake J, Pfister S, Eckstein V, Ho AD. Replicative senescence of mesenchymal stem cells - a continuous and organized process. PLoS ONE 2008, 5:e2213.
50. Wagner W, Bork S, Horn P, Krunic D, Walenda T, Diehlmann A, Benes V, Blake J, Huber FX, Eckstein V, Boukamp P, Ho AD. Aging and replicative senescence have related effects on human stem and progenitor cells. PLoS ONE 2009, 4:e5846.
51. Wilson VL, Jones PA. DNA methylation decreases in aging but not in immortal cells. Science 1983, 220:1055-1057.
52. Young JI, Smith JR. DNA methyltransferase inhibition in normal human fibroblasts induces a p21-dependent cell cycle withdrawal. J. Biol. Chem. 2001, 276:19610-19616.
53. Zeng X. Human embryonic stem cells: mechanisms to escape replicative senescence? Stem Cell Rev. 2007, 3:270-279.
54. Zhou S, Greenberger JS, Epperly MW, Goff JP, Adler C, Leboff MS, 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.
55. Zimmermann P, Boeuf S, Dickhut A, Boehmer S, Olek S, Richter W. Correlation of COL10A1 induction during chondrogenesis of mesenchymal stem cells with demethylation of two CpG sites in the COL10A1 promoter. Arthritis Rheum. 2008, 58:2743-2753.