Insulin-like growth factor binding proteins 4 and 7 released by senescent cells promote premature senescence in mesenchymal stem cells

Cell Death and Disease

Volumn 4, Issue 11, 2013, Pages

  Severino, V ^a,b,c   Alessio, N ^a   Farina, A ^d   Sandomenico, A ^b,c   Cipollaro, M ^a   Peluso, G ^b,e   Galderisi, U ^a,e,f,g   Chambery, A ^a,c  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

^b CNR   (Italy)

^c Centro Interuniversitario di Ricerca Sui Peptidi Bioattivi (CIRPEB)   (Italy)

^d UNIVERSITY OF GENEVA   (Switzerland)

^e INSTITUTE OF PROTEIN BIOCHEMISTRY   (Italy)

^f TEMPLE UNIVERSITY   (United States)

^g ERCIYES UNIVERSITY   (Turkey)

Author keywords

IGFBP4; IGFBP7; Mass spectrometry; Mesenchymal stem cells; Secretome; Senescence

Indexed keywords

SOMATOMEDIN BINDING PROTEIN; SOMATOMEDIN BINDING PROTEIN 4; SOMATOMEDIN BINDING PROTEIN 7; UNCLASSIFIED DRUG; INSULIN LIKE GROWTH FACTOR BINDING PROTEIN RELATED PROTEIN 1; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN-RELATED PROTEIN 1;

APOPTOSIS; ARTICLE; CELL GROWTH; CELL MATURATION; CONTROLLED STUDY; CULTURE MEDIUM; CYTOLOGY; DNA DAMAGE; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLEIOTROPY; PRIORITY JOURNAL; SENESCENCE; WESTERN BLOTTING; BIOLOGY; CELL AGING; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; DRUG EFFECT; GENETICS; IMMUNOHISTOCHEMISTRY; LIQUID CHROMATOGRAPHY; METABOLISM; TANDEM MASS SPECTROMETRY;

APOPTOSIS; BLOTTING, WESTERN; CELL AGING; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CHROMATOGRAPHY, LIQUID; COMPUTATIONAL BIOLOGY; CULTURE MEDIA, CONDITIONED; HUMANS; IMMUNOHISTOCHEMISTRY; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 4; INSULIN-LIKE GROWTH FACTOR BINDING PROTEINS; TANDEM MASS SPECTROMETRY;

EID: 84889571932     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.445     Document Type: Article

References (56)

1. Campisi J, d'Adda di Fagagna F. Cellular senescence: When bad things happen to good cells. Nat Rev Mol Cell Biol 2007; 8: 729-740
2. d'Adda di Fagagna F. Living on a break: Cellular senescence as a DNA-damage response. Nat Rev Cancer 2008; 8: 512-522
3. Beyer Nardi N, da Silva Meirelles L. Mesenchymal stem cells: Isolation, in vitro expansion and characterization. Handb Exp Pharmacol 2006; 174: 249-282
4. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, et al. Multineage potential of adult human mesenchimal stem cell. Science 1999; 284: 143-147
5. Valtieri M, Sorrentino A. The mesenchymal stromal cell contribution to homeostasis. J Cell Physiol 2008; 217: 296-300
6. Kuilman T, Peeper DS. Senescence-messaging secretome: SMS-ing cellular stress. Nat Rev Cancer 2009; 9: 81-94
7. Coppe JP, Patil CK, Rodier F, Sun Y, Munoz DP, Goldstein J, et al. Senescence-Associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol 2008; 6: 2853-2868
8. Fumagalli M, d'Adda di Fagagna F. SASPense and DDRama in cancer and ageing. Nat Cell Biol 2009; 11: 921-923
9. Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators. J Cell Biochem 2006; 98: 1076-1084
10. Hsiao ST, Asgari A, Lokmic Z, Sinclair R, Dusting GJ, Lim SY, et al. Comparative analysis of paracrine factor expression in human adult mesenchymal stem cells derived from bone marrow, adipose, and dermal tissue. Stem cells Dev 2012; 21: 2189-2203
11. Ranganath SH, Levy O, Inamdar MS, Karp JM. Harnessing the mesenchymal stem cell secretome for the treatment of cardiovascular disease. Cell Stem Cell 2012; 10: 244-258
12. van Koppen A, Joles JA, van Balkom BW, Lim SK, de Kleijn D, Giles RH, et al. Human embryonic mesenchymal stem cell-derived conditioned medium rescues kidney function in rats with established chronic kidney disease. PLoS One 2012; 7: E38746
13. Pollina EA, Brunet A. Epigenetic regulation of aging stem cells. Oncogene 2011; 30: 3105-3126
14. Walter P, Gilmore R, Blobel G. Protein translocation across the endoplasmic reticulum. Cell 1984; 38: 5-8
15. Nickel W. The mystery of nonclassical protein secretion. A current view on cargo proteins and potential export routes. Eur J Biochem 2003; 270: 2109-2119
16. Narita M, Nunez S, Heard E, Narita M, Lin AW, Hearn SA, et al. Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 2003; 113: 703-716
17. Lombard DB, Chua KF, Mostoslavsky R, Franco S, Gostissa M, Alt FW. DNA repair, genome stability, and aging. Cell 2005; 120: 497-512
18. Roos WP, Kaina B. DNA damage-induced cell death by apoptosis. Trends Mol Med 2006; 12: 440-450
19. Alessio N, Squillaro T, Cipollaro M, Bagella L, Giordano A, Galderisi U. The BRG1 ATPase of chromatin remodeling complexes is involved in modulation of mesenchymal stem cell senescence through RB-P53 pathways. Oncogene 2013; 29: 5452-5463
20. Cagnol S, Chambard JC. ERK and cell death: Mechanisms of ERK-induced cell death-Apoptosis, autophagy and senescence. Febs J 2010; 277: 2-21.
21. Tresini M, Lorenzini A, Torres C, Cristofalo VJ. Modulation of replicative senescence of diploid human cells by nuclear ERK signaling. J Biol Chem 2007; 282: 4136-4151
22. Rodier F, Campisi J. Four faces of cellular senescence. J Cell Biol 2011; 192: 547-556
23. Frantz C, Stewart KM, Weaver VM. The extracellular matrix at a glance. J Cell Sci 2010; 123: 4195-4200
24. Zhao CQ, Wang LM, Jiang LS, Dai LY. The cell biology of intervertebral disc aging and degeneration. Ageing Res Rev 2007; 6: 247-261
25. Yang KE, Kwon J, Rhim JH, Choi JS, Kim SI, Lee SH, et al. Differential expression of extracellular matrix proteins in senescent and young human fibroblasts: A comparative proteomics and microarray study. Mol Cells 2011; 32: 99-106
26. Hauser N, Paulsson M, Heinegard D, Morgelin M. Interaction of cartilage matrix protein with aggrecan. Increased covalent cross-linking with tissue maturation. J Biol Chem 1996; 271: 32247-32252
27. Soti C, Csermely P. Molecular chaperones and the aging process. Biogerontology 2000; 1: 225-233
28. Holt SE, Aisner DL, Baur J, Tesmer VM, Dy M, Ouellette M, et al. Functional requirement of p23 and Hsp90 in telomerase complexes. Genes Dev 1999; 13: 817-826
29. Kim KS, Kim MS, Seu YB, Chung HY, Kim JH, Kim Jr. Regulation of replicative senescence by insulin-like growth factor-binding protein 3 in human umbilical vein endothelial cells. Aging Cell 2007; 6: 535-545
30. Elzi DJ, Lai Y, Song M, Hakala K, Weintraub ST, Shiio Y. Plasminogen activator inhibitor 1-insulin-like growth factor binding protein 3 cascade regulates stress-induced senescence. Proc Natl Acad Sci USA 2012; 109: 12052-12057
31. Kim KS, Seu YB, Baek SH, Kim MJ, Kim KJ, Kim JH, et al. Induction of cellular senescence by insulin-like growth factor binding protein-5 through a p53-dependent mechanism. Mol Biol Cell 2007; 18: 4543-4552
32. Kojima H, Kunimoto H, Inoue T, Nakajima K. The STAT3-IGFBP5 axis is critical for IL-6/ gp130-induced premature senescence in human fibroblasts. Cell Cycle 2012; 11: 730-739
33. Wajapeyee N, Serra RW, Zhu X, Mahalingam M, Green MR. Oncogenic BRAF induces senescence and apoptosis through pathways mediated by the secreted protein IGFBP7. Cell 2008; 132: 363-374
34. Wajapeyee N, Serra RW, Zhu X, Mahalingam M, Green MR. Role for IGFBP7 in senescence induction by BRAF. Cell 2010; 141: 746-747
35. Benatar T, Yang W, Amemiya Y, Evdokimova V, Kahn H, Holloway C, et al. IGFBP7 reduces breast tumor growth by induction of senescence and apoptosis pathways. Breast Cancer Res Treat 2012; 133: 563-573
36. Schnabl B, Purbeck CA, Choi YH, Hagedorn CH, Brenner D. Replicative senescence of activated human hepatic stellate cells is accompanied by a pronounced inflammatory but less fibrogenic phenotype. Hepatology 2003; 37: 653-664
37. Suzuki T, Minagawa S, Michishita E, Ogino H, Fujii M, Mitsui Y, et al. Induction of senescence-Associated genes by 5-bromodeoxyuridine in HeLa cells. Exp Gerontol 2001; 36: 465-474
38. Denoyelle C, Abou-Rjaily G, Bezrookove V, Verhaegen M, Johnson TM, Fullen DR, et al. Anti-oncogenic role of the endoplasmic reticulum differentially activated by mutations in the MAPK pathway. Nat Cell Biol 2006; 8: 1053-1063
39. Alessio N, Bohn W, Rauchberger V, Rizzolio F, Cipollaro M, Rosemann M, et al. Silencing of RB1 but not of RB2/P130 induces cellular senescence and impairs the differentiation potential of human mesenchymal stem cells. Cell Mol Life Sci 2013; 70: 1637-1651
40. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8: 315-317
41. Farina A, D'Aniello C, Severino V, Hochstrasser DF, Parente A, Minchiotti G, et al. Temporal proteomic profiling of embryonic stem cell secretome during cardiac and neural differentiation. Proteomics 2011; 11: 3972-3982
42. Severino V, Farina A, Colucci-D'Amato L, Reccia MG, Volpicelli F, Parente A, et al. Secretome profiling of differentiated neural mes-c-myc A1 cell line endowed with stem cell properties. Biochim Biophys Acta 2013; 1834: 2385-2395
43. Severino V, Farina A, Chambery A. Analysis of secreted proteins. Methods Mol Biol 2013; 1002: 37-60
44. Scherl A, Tsai YS, Shaffer SA, Goodlett DR. Increasing information from shotgun proteomic data by accounting for misassigned precursor ion masses. Proteomics 2008; 8: 2791-2797
45. Mueller LN, Rinner O, Schmidt A, Letarte S, Bodenmiller B, Brusniak MY, et al. SuperHirn-A novel tool for high resolution LC-MS-based peptide/protein profiling. Proteomics 2007; 7: 3470-3480
46. Keller A, Nesvizhskii AI, Kolker E, Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 2002; 74: 5383-5392
47. Nesvizhskii AI, Keller A, Kolker E, Aebersold R. A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 2003; 75: 4646-4658
48. Kulasingam V, Diamandis EP. Proteomics analysis of conditioned media from three breast cancer cell lines: A mine for biomarkers and therapeutic targets. Mol Cell Proteomics 2007; 6: 1997-2011
49. Wilson R, Diseberg AF, Gordon L, Zivkovic S, Tatarczuch L, Mackie EJ, et al. Comprehensive profiling of cartilage extracellular matrix formation and maturation using sequential extraction and label-free quantitative proteomics. Mol Cell Proteomics 2010; 9: 1296-1313
50. Rocco M, Malorni L, Cozzolino R, Palmieri G, Rozzo C, Manca A, et al. Proteomic profiling of human melanoma metastatic cell line secretomes. J Proteome Res 2011; 10: 4703-4714
51. Bendtsen JD, Nielsen H, von Heijne G, Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 2004; 340: 783-795
52. Bendtsen JD, Jensen LJ, Blom N, Von Heijne G, Brunak S. Feature-based prediction of non-classical and leaderless protein secretion. Protein Eng Des Sel 2004; 17: 349-356
53. Nakamura S, Yamada Y, Baba S, Kato H, Kogami H, Takao M, et al. Culture medium study of human mesenchymal stem cells for practical use of tissue engineering and regenerative medicine. Biomed Mater Eng 2008; 18: 129-136
54. Debacq-Chainiaux F, Erusalimsky JD, Campisi J, Toussaint O. Protocols to detect senescence-Associated beta-galactosidase (SA-betagal) activity, a biomarker of senescent cells in culture and in vivo. Nat Protoc 2009; 4: 1798-1806
55. Gary RK, Kindell SM. Quantitative assay of senescence-Associated beta-galactosidase activity in mammalian cell extracts. Anal Biochem 2005; 343: 329-334
56. Liu H, Kang H, Liu R, Chen X, Zhao K. Maximal induction of a subset of interferon target genes requires the chromatin-remodeling activity of the BAF complex. Mol Cell Biol 2002; 22: 6471-6479