Intra-subject variability in human bone marrow stromal cell (BMSC) replicative senescence: Molecular changes associated with BMSC senescence

Stem Cell Research

Volumn 11, Issue 3, 2013, Pages 1060-1073

  Ren, Jiaqiang ^a   Stroncek, David F ^a   Zhao, Yingdong ^b   Jin, Ping ^a   Castiello, Luciano ^a   Civini, Sara ^a   Wang, Huan ^a   Feng, Ji ^a   Tran, Katherine ^a   Kuznetsov, Sergei A ^c   Robey, Pamela G ^c   Sabatino, Marianna ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CHEMOKINE RECEPTOR CXCR4; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 8; MACROPHAGE DERIVED CHEMOKINE; OSTEOPROTEGERIN; TRANSFORMING GROWTH FACTOR BETA1; VASCULOTROPIN;

ARTICLE; BONE DEVELOPMENT; CELL GROWTH; CELL MATURATION; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; CYTOKINE RELEASE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOMODULATION; IN VITRO STUDY; LIFESPAN; MESENCHYMAL STROMA CELL; PRIORITY JOURNAL; SENESCENCE; UPREGULATION;

BIOLOGICAL MARKERS; BONE MARROW CELLS; CELL AGING; CELL PROLIFERATION; CELLS, CULTURED; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; HUMANS; MESENCHYMAL STROMAL CELLS; PHENOTYPE; REGRESSION ANALYSIS; SIGNAL TRANSDUCTION;

EID: 84882967491     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2013.07.005     Document Type: Article

References (51)

1. Acosta J.C., O'Loghlen A., Banito A., Guijarro M.V., Augert A., Raguz S., Fumagalli M., Da Costa M., Brown C., Popov N., et al. Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell 2008, 133:1006-1018.
2. Ashkar S., Weber G.F., Panoutsakopoulou V., Sanchirico M.E., Jansson M., Zawaideh S., Rittling S.R., Denhardt D.T., Glimcher M.J., Cantor H. Eta-1 (osteopontin): an early component of type-1 (cell-mediated) immunity. Science 2000, 287:860-864.
3. 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.
4. Benisch P., Schilling T., Klein-Hitpass L., Frey S.P., Seefried L., Raaijmakers N., Krug M., Regensburger M., Zeck S., Schinke T., et al. The transcriptional profile of mesenchymal stem cell populations in primary osteoporosis is distinct and shows overexpression of osteogenic inhibitors. PLoS One 2012, 7:e45142.
5. Ciccocioppo, R., Bernardo, M.E., Sgarella, A., Maccario, R., Avanzini, M.A., Ubezio, C., Minelli, A., Alvisi, C., Vanoli, A., Calliada, F., et al., 2011. Autologous bone marrow-derived mesenchymal stromal cells in the treatment of fistulising Crohn's disease. Gut 60, 788-798.
6. Coppe J.P., Patil C.K., Rodier F., Sun Y., Munoz D.P., Goldstein J., Nelson P.S., Desprez P.Y., Campisi J. Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol. 2008, 6:2853-2868.
7. Dash N.R., Dash S.N., Routray P., Mohapatra S., Mohapatra P.C. Targeting nonhealing ulcers of lower extremity in human through autologous bone marrow-derived mesenchymal stem cells. Rejuvenation Res. 2009, 12:359-366.
8. Digirolamo C.M., Stokes D., Colter D., Phinney D.G., Class R., Prockop D.J. Propagation and senescence of human marrow stromal cells in culture: a simple colony-forming assay identifies samples with the greatest potential to propagate and differentiate. Br. J. Haematol. 1999, 107:275-281.
9. Ducy P., Zhang R., Geoffroy V., Ridall A.L., Karsenty G. Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 1997, 89:747-754.
10. Efron B., Hastie T., Johnstone I., Tibshirani R. Least angle regression. Ann. Stat. 2004, 32:407-499.
11. Friedenstein A.J., Piatetzky S., Petrakova K.V. Osteogenesis in transplants of bone marrow cells. J. Embryol. Exp. Morphol. 1966, 16:381-390.
12. Galderisi U., Helmbold H., Squillaro T., Alessio N., Komm N., Khadang B., Cipollaro M., Bohn W., Giordano A. In vitro senescence of rat mesenchymal stem cells is accompanied by downregulation of stemness-related and DNA damage repair genes. Stem Cells Dev. 2009, 18:1033-1042.
13. Hare J.M., Traverse J.H., Henry T.D., Dib N., Strumpf R.K., Schulman S.P., Gerstenblith G., DeMaria A.N., Denktas A.E., Gammon R.S., et al. A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction. J. Am. Coll. Cardiol. 2009, 54:2277-2286.
14. Horwitz E.M., Gordon P.L., Koo W.K., Marx J.C., Neel M.D., McNall R.Y., Muul L., Hofmann T. Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: implications for cell therapy of bone. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:8932-8937.
15. Inkson C.A., Ono M., Bi Y., Kuznetsov S.A., Fisher L.W., Young M.F. The potential functional interaction of biglycan and WISP-1 in controlling differentiation and proliferation of osteogenic cells. Cells Tissues Organs 2009, 189:153-157.
16. Inkson C.A., Ono M., Kuznetsov S.A., Fisher L.W., Robey P.G., Young M.F. TGF-beta1 and WISP-1/CCN-4 can regulate each other's activity to cooperatively control osteoblast function. J. Cell. Biochem. 2008, 104:1865-1878.
17. Jiang S.S., Chen C.H., Tseng K.Y., Tsai F.Y., Wang M.J., Chang I.S., Lin J.L., Lin S. Gene expression profiling suggests a pathological role of human bone marrow-derived mesenchymal stem cells in aging-related skeletal diseases. Aging (Albany NY) 2011, 3:672-684.
18. Joyce, N., Annett, G., Wirthlin, L., Olson, S., Bauer, G., and Nolta, J.A., 2010. Mesenchymal stem cells for the treatment of neurodegenerative disease. Regen. Med. 5, 933-946.
19. Karussis, D., Karageorgiou, C., Vaknin-Dembinsky, A., Gowda-Kurkalli, B., Gomori, J.M., Kassis, I., Bulte, J.W., Petrou, P., Ben-Hur, T., Abramsky, O., et al., 2010. Safety and immunological effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis. Arch. Neurol. 67, 1187-1194.
20. Kobayashi K., Hernandez L.D., Galan J.E., Janeway C.A., Medzhitov R., Flavell R.A. IRAK-M is a negative regulator of Toll-like receptor signaling. Cell 2002, 110:191-202.
21. Koc O.N., Day J., Nieder M., Gerson S.L., Lazarus H.M., Krivit W. Allogeneic mesenchymal stem cell infusion for treatment of metachromatic leukodystrophy (MLD) and Hurler syndrome (MPS-IH). Bone Marrow Transplant. 2002, 30:215-222.
22. Koc O.N., Gerson S.L., Cooper B.W., Dyhouse S.M., Haynesworth S.E., Caplan A.I., Lazarus H.M. Rapid hematopoietic recovery after coinfusion of autologous-blood stem cells and culture-expanded marrow mesenchymal stem cells in advanced breast cancer patients receiving high-dose chemotherapy. J. Clin. Oncol. 2000, 18:307-316.
23. Ksiazek K. A comprehensive review on mesenchymal stem cell growth and senescence. Rejuvenation Res. 2009, 12:105-116.
24. Kuilman T., Michaloglou C., Vredeveld L.C., Douma S., van Doorn R., Desmet C.J., Aarden L.A., Mooi W.J., Peeper D.S. Oncogene-induced senescence relayed by an interleukin-dependent inflammatory network. Cell 2008, 133:1019-1031.
25. Kukita T., Wada N., Kukita A., Kakimoto T., Sandra F., Toh K., Nagata K., Iijima T., Horiuchi M., Matsusaki H., et al. RANKL-induced DC-STAMP is essential for osteoclastogenesis. J. Exp. Med. 2004, 200:941-946.
26. Lafferty-Whyte, K., Bilsland, A., Cairney, C.J., Hanley, L., Jamieson, N.B., Zaffaroni, N., Oien, K.A., Burns, S., Roffey, J., Boyd, S.M., et al., 2010. Scoring of senescence signalling in multiple human tumour gene expression datasets, identification of a correlation between senescence score and drug toxicity in the NCI60 panel and a pro-inflammatory signature correlating with survival advantage in peritoneal mesothelioma. BMC Genomics 11, 532.
27. Le Blanc K., Rasmusson I., Sundberg B., Gotherstrom C., Hassan M., Uzunel M., Ringden O. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 2004, 363:1439-1441.
28. Le Blanc K., Ringden O. Immunomodulation by mesenchymal stem cells and clinical experience. J. Intern. Med. 2007, 262:509-525.
29. Le Blanc K., Tammik L., Sundberg B., Haynesworth S.E., Ringden O. Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand. J. Immunol. 2003, 57:11-20.
30. Mazzini, L., Ferrero, I., Luparello, V., Rustichelli, D., Gunetti, M., Mareschi, K., Testa, L., Stecco, A., Tarletti, R., Miglioretti, M., et al., 2010. Mesenchymal stem cell transplantation in amyotrophic lateral sclerosis: A Phase I clinical trial. Exp. Neurol. 223, 229-237.
31. Okabe Y., Sano T., Nagata S. Regulation of the innate immune response by threonine-phosphatase of Eyes absent. Nature 2009, 460:520-524.
32. Ono, M., Inkson, C.A., Kilts, T.M., and Young, M.F., 2011. WISP-1/CCN4 regulates osteogenesis by enhancing BMP-2 activity. J. Bone Miner. Res. 26, 193-208.
33. Oskowitz, A., McFerrin, H., Gutschow, M., Carter, M.L., and Pochampally, R., 2011. Serum-deprived human multipotent mesenchymal stromal cells (MSCs) are highly angiogenic. Stem Cell Res. 6, 215-225.
34. Pal R., Venkataramana N.K., Bansal A., Balaraju S., Jan M., Chandra R., Dixit A., Rauthan A., Murgod U., Totey S. Ex vivo-expanded autologous bone marrow-derived mesenchymal stromal cells in human spinal cord injury/paraplegia: a pilot clinical study. Cytotherapy 2009, 11:897-911.
35. Pitto L., Rizzo M., Simili M., Colligiani D., Evangelista M., Mercatanti A., Mariani L., Cremisi F., Rainaldi G. miR-290 acts as a physiological effector of senescence in mouse embryo fibroblasts. Physiol. Genomics 2009, 39:210-218.
36. Ripperger T., von Neuhoff N., Kamphues K., Emura M., Lehmann U., Tauscher M., Schraders M., Groenen P., Skawran B., Rudolph C., et al. Promoter methylation of PARG1, a novel candidate tumor suppressor gene in mantle-cell lymphomas. Haematologica 2007, 92:460-468.
37. Sabatino, M., Ren, J., David-Ocampo, V., England, L., McGann, M., Tran, M., Kuznetsov, S.A., Khuu, H., Balakumaran, A., Klein, H.G., et al., 2012. The establishment of a bank of stored clinical bone marrow stromal cell products. J. Transl. Med. 10, 23.
38. Saeed A.I., Sharov V., White J., Li J., Liang W., Bhagabati N., Braisted J., Klapa M., Currier T., Thiagarajan M., et al. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 2003, 34:374-378.
39. Saleem K.S., Suzuki W., Tanaka K., Hashikawa T. Connections between anterior inferotemporal cortex and superior temporal sulcus regions in the macaque monkey. J. Neurosci. 2000, 20:5083-5101.
40. Schallmoser, K., Bartmann, C., Rohde, E., Bork, S., Guelly, C., Obenauf, A.C., Reinisch, A., Horn, P., Ho, A.D., Strunk, D., et al., 2010. Replicative senescence-associated gene expression changes in mesenchymal stromal cells are similar under different culture conditions. Haematologica 95, 867-874.
41. Sethe S., Scutt A., Stolzing A. Aging of mesenchymal stem cells. Ageing Res. Rev. 2006, 5:91-116.
42. Siddappa R., Licht R., van Blitterswijk C., de Boer J. Donor variation and loss of multipotency during in vitro expansion of human mesenchymal stem cells for bone tissue engineering. J. Orthop. Res. 2007, 25:1029-1041.
43. Simon R., Lam A., Li M.C., Ngan M., Menenzes S., Zhao Y. Analysis of gene expression data using BRB-ArrayTools. Cancer Inform. 2007, 3:11-17.
44. 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.
45. Tanabe S., Sato Y., Suzuki T., Suzuki K., Nagao T., Yamaguchi T. Gene expression profiling of human mesenchymal stem cells for identification of novel markers in early- and late-stage cell culture. J. Biochem. 2008, 144:399-408.
46. Wagner, W., Ho, A.D., and Zenke, M., 2010. Different facets of aging in human mesenchymal stem cells. Tissue Eng. Part B Rev. 16, 445-453.
47. Wagner W., Horn P., Castoldi M., Diehlmann A., Bork S., Saffrich R., Benes V., Blake J., Pfister S., Eckstein V., et al. Replicative senescence of mesenchymal stem cells: a continuous and organized process. PLoS One 2008, 3:e2213.
48. Wang D., Jang D.J. Protein kinase CK2 regulates cytoskeletal reorganization during ionizing radiation-induced senescence of human mesenchymal stem cells. Cancer Res. 2009, 69:8200-8207.
49. Wang H., Jin P., Sabatino M., Ren J., Civini S., Bogin V., Ichim T.E., Stroncek D.F. Comparison of endometrial regenerative cells and bone marrow stromal cells. J. Transl. Med. 2012, 10:207.
50. Wang X., Zheng M., Liu G., Xia W., McKeown-Longo P.J., Hung M.C., Zhao J. Kruppel-like factor 8 induces epithelial to mesenchymal transition and epithelial cell invasion. Cancer Res. 2007, 67:7184-7193.
51. Zhao, Y., and Simon, R., 2010. Development and validation of predictive indices for a continuous outcome using gene expression profiles. Cancer Inform. 9, 105-114.