Proteomic analysis reveals novel common genes modulated in both replicative and stress-induced senescence

Journal of Proteomics

Volumn 128, Issue , 2015, Pages 18-29

  Succoio, Mariangela ^a,b   Comegna, Marika ^a,b   D'Ambrosio, Chiara ^c   Scaloni, Andrea ^c   Cimino, Filiberto ^a,b   Faraonio, Raffaella ^a,b  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^c CNR   (Italy)

Author keywords

2D DIGE; Cellular senescence; Chromatin immunoprecipitation; Gene regulation; Human primary fibroblasts; Oxidative stress

Indexed keywords

EPLIN PROTEIN; LEPRE1 PROTEIN; LIMA1 PROTEIN; MAGOHA PROTEIN; MAGOHB PROTEIN; MESSENGER RNA; PROTEIN; UNCLASSIFIED DRUG; PROTEOME;

ARTICLE; CELL AGING; CELL CYCLE ARREST; CELL MATURATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DOWN REGULATION; FIBROBLAST; GENE CONTROL; GENE REPLICATION; GENE SILENCING; GENETIC ASSOCIATION; HISTONE METHYLATION; HUMAN; HUMAN CELL; NORMAL HUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEOMICS; RNA INTERFERENCE; SENESCENCE; STRESS; TUMOR GROWTH; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; CYTOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PROCEDURES;

CELL AGING; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; FIBROBLASTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; PROTEOME; PROTEOMICS; STRESS, PHYSIOLOGICAL;

EID: 84938151091     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2015.07.010     Document Type: Article

References (70)

1. Hayflick L., Moorhead P.S. The serial cultivation of human diploid cell strains. Exp. Cell Res. 1961, 25:585-621.
2. 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.
3. Campisi J. Aging, cellular senescence, and cancer. Annu. Rev. Physiol. 2013, 75:685-705.
4. Collado M., Serrano M. Senescence in tumours: evidence from mice and humans. Nat. Rev. Cancer 2010, 10:51-57.
5. Kuilman T., Michaloglou C., Mooi W.J., Peeper D.S. The essence of senescence. Genes Dev. 2010, 24(22):2463-2479.
6. Michaloglou C., Vredeveld L.C., Soengas M.S., Denoyelle C., Kuilman T., van der Horst C.M., Majoor D.M., Shay J.W., Mooi W.J., Peeper D.S. BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature 2005, 436:720-724.
7. Chen Z., Trotman L.C., Shaffer D., Lin H.K., Dotan Z.A., Niki M., Koutcher J.A., Scher H.I., Ludwig T., Gerald W., Cordon-Cardo C., Pandolfi P.P. Crucial role of p53-dependent cellular senescence in suppression of Pten-deficient tumorigenesis. Nature 2005, 436:725-730.
8. Shamma A., Takegami Y., Miki T., Kitajima S., Noda M., Obara T., Okamoto T., Takahashi C. Rb Regulates DNA damage response and cellular senescence through E2F-dependent suppression of N-ras isoprenylation. Cancer Cell 2009, 15(4):255-269.
9. Young A.P., Schlisio S., Minamishima Y.A., Zhang Q., Li L., Grisanzio C., Signoretti S., Kaelin W.G. VHL loss actuates a HIF-independent senescence programme mediated by Rb and p400. Nat. Cell Biol. 2008, 10:361-369.
10. Nardella C., Clohessy J.G., Alimonti A., Pandolfi P.P. Pro-senescence therapy for cancer treatment. Nat. Rev. Cancer 2011, 11(7):503-511.
11. van Deursen J.M. The role of senescent cells in ageing. Nature 2014, 509(7501):439-446.
12. Jeyapalan J.C., Ferreira M., Sedivy J.M., Herbig U. Accumulation of senescent cells in mitotic tissue of aging primates. Mech. Ageing Dev. 2007, 128:36-44.
13. Sharpless N.E., DePinho R.A. How stem cells age and why this makes us grow old. Nat. Rev. Mol. Cell Biol. 2007, 8:703-713.
14. Baker D.J., Perez-Terzic C., Jin F., Pitel K.S., Niederländer N.J., Jeganathan K., Yamada S., Reyes S., Rowe L., Hiddinga H.J., Eberhardt N.L., Terzic A., van Deursen J.M. Opposing roles for p16Ink4a and p19Arf in senescence and ageing caused by BubR1 insufficiency. Nat. Cell Biol. 2008, 10:825-836.
15. Nat. Cell Biol. Jun 2012, 14(6):649. Erratum in.
16. Coppé J.P., Desprez P.Y., Krtolica A., Campisi J. The senescence-associated secretory phenotype: the dark side of tumor suppression. Annu. Rev. Pathol. 2010, 5:99-118.
17. Rodier F., Campisi J. Four faces of cellular senescence. J. Cell Biol. 2011, 192:547-556.
18. Acosta J.C., Banito A., Wuestefeld T., Georgilis A., Janich P., Morton J.P., Athineos D., Kang T.W., Lasitschka F., Andrulis M., Pascual G., Morris K.J., Khan S., Jin H., Dharmalingam G., Snijders A.P., Carroll T., Capper D., Pritchard C., Inman G.J., Longerich T., Sansom O.J., Benitah S.A., Zender L., Gil J. A complex secretory program orchestrated by the inflammasome controls paracrine senescence. Nat. Cell Biol. 2013, 15(8):978-990.
19. Baker D.J., Wijshake T., Tchkonia T., LeBrasseur N.K., Childs B.G., van de Sluis B., Kirkland J.L., van Deursen J.M. Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders. Nature 2011, 479(7372):232-236.
20. Naylor R.M., Baker D.J., van Deursen J.M. Senescent cells: a novel therapeutic target for aging and age-related diseases. Clin. Pharmacol. Ther. 2013, 93(1):105-116.
21. Muñoz-Espín D., Cañamero M., Maraver A., Gómez-López G., Contreras J., Murillo-Cuesta S., Rodríguez-Baeza A., Varela-Nieto I., Ruberte J., Collado M., Serrano M. Programmed cell senescence during mammalian embryonic development. Cell 2013, 155(5):1104-1118.
22. Storer M., Mas A., Robert-Moreno A., Pecoraro M., Ortells M.C., Di Giacomo V., Yosef R., Pilpel N., Krizhanovsky V., Sharpe J., Keyes W.M. Senescence is a developmental mechanism that contributes to embryonic growth and patterning. Cell 2013, 155(5):1119-1130.
23. D'Adda di Fagagna F. Living on a break: cellular senescence as a DNA-damage response. Nat. Rev. Cancer 2008, 8:512-522.
24. López-Otín C., Blasco M.A., Partridge L., Serrano M., Kroemer G. The hallmarks of aging. Cell 2013, 153(6):1194-1217.
25. Salama R., Sadaie M., Hoare M., Narita M. Cellular senescence and its effector programs. Genes Dev. 2014, 28(2):99-114.
26. Chan C.H., Gao Y., Moten A., Lin H.K. Novel ARF/p53-independent senescence pathways in cancer repression. J. Mol. Med. 2011, 89(9):857-867.
27. Lanigan F., Geraghty J.G., Bracken A.P. Transcriptional regulation of cellular senescence. Oncogene 2011, 30(26):2901-2911.
28. Berger S.L. The complex language of chromatin regulation during transcription. Nature 2007, 447:407-412.
29. Li B., Carey M., Workman J.L. The role of chromatin during transcription. Cell 2007, 128:707-719.
30. Cecco M., Criscione S.W., Peckham E.J., Hillenmeyer S., Hamm E.A., Manivannan J., Peterson A.L., Kreiling J.A., Neretti N., Sedivy J.M. Genomes of replicatively senescent cells undergo global epigenetic changes leading to gene silencing and activation of transposable elements. Aging Cell 2013, 12:247-256.
31. Corpet A., Stucki M. Chromatin maintenance and dynamics in senescence: a spotlight on SAHF formation and the epigenome of senescent cells. Chromosoma 2014, 123(5):423-436.
32. Narita M., Ñnez S., Heard E., Narita M., Lin A.W., Hearn S.A., Spector D.L., Hannon G.J., Lowe S.W. Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 2003, 113:703-716.
33. Bracken A.P., Kleine-Kohlbrecher D., Dietrich N., Pasini D., Gargiulo G., Beekman C., Theilgaard-Mönch K., Minucci S., Porse B.T., Marine J.C., Hansen K.H., Helin K. The Polycomb group proteins bind throughout the INK4A-ARF locus and are disassociated in senescent cells. Genes Dev. 2007, 21:525-530.
34. Kotake Y., Cao R., Viatour P., Sage J., Zhang Y., Xiong Y. pRB family proteins are required for H3K27 trimethylation and Polycomb repression complexes binding to and silencing p16INK4alpha tumor suppressor gene. Genes Dev. 2007, 21:49-54.
35. Sadaie M., Salama R., Carroll T., Tomimatsu K., Chandra T., Young A.R., Narita M., Pérez-Mancera P.A., Bennett D.C., Chong H., Kimura H., Narita M. Redistribution of the Lamin B1 genomic binding profile affects rearrangement of heterochromatic domains and SAHF formation during senescence. Genes Dev. 2013, 27:1800-1808.
36. Shah P.P., Donahue G., Otte G.L., Capell B.C., Nelson D.M., Cao K., Aggarwala V., Cruickshanks H.A., Rai T.S., McBryan T., Gregory B.D., Adams P.D., Berger S.L. Lamin B1 depletion in senescent cells triggers large-scale changes in gene expression and the chromatin landscape. Genes Dev. 2013, 27:1787-1799.
37. Li M., Durbin K.R., Sweet S.M., Tipton J.D., Zheng Y., Kelleher N.L. Oncogene induced cellular senescence elicits an anti-Warburg effect. Proteomics 2013, 13(17):2585-2596.
38. Faraonio R., Salerno P., Passaro F., Sedia C., Iaccio A., Bellelli R., Nappi T.C., Comegna M., Romano S., Salvatore G., Santoro M., Cimino F. A set of miRNAs participates in the cellular senescence program in human diploid fibroblasts. Cell Death Differ. 2012, 19(4):713-721.
39. Comegna M., Succoio M., Napolitano M., Vitale M., D'Ambrosio C., Scaloni A., Passaro F., Zambrano N., Cimino F., Faraonio R. Identification of miR-494 direct targets involved in senescence of human diploid fibroblasts. FASEB J. 2014, 28(8):3720-3733.
40. Monteleone F., Rosa R., Vitale M., D'Ambrosio C., Succoio M., Formisano L., Nappi L., Romano M.F., Scaloni A., Tortora G., Bianco R., Zambrano N. Increased anaerobic metabolism is a distinctive signature in a colorectal cancer cellular model of resistance to antiepidermal growth factor receptor antibody. Proteomics 2013, 13(5):866-877.
41. Talamo F., D'Ambrosio C., Arena S., Del Vecchio P., Ledda L., Zehender G., Ferrara L., Scaloni A. Proteins from bovine tissues and biological fluids: defining a reference electrophoresis map for liver, kidney, muscle, plasma and red blood cells. Proteomics 2003, 3:440-460.
42. Scippa G.S., Rocco M., Ialicicco M., Trupiano D., Viscosi V., Di Michele M., Arena S., Chiatante D., Scaloni A. The proteome of lentil (Lens culinaris Medik.) seeds: discriminating between landraces. Electrophoresis 2010, 31:497-506.
43. Perkins D.N., Pappin D.J., Creasy D.M., Cottrell J.S. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20:3551-3567.
44. Singh K.K., Wachsmuth L., Kulozik A.E., Gehring N.H. Two mammalian MAGOH genes contribute to exon junction complex composition and nonsense-mediated decay. RNA Biol. 2013, 10(8):1291-1298.
45. Chen S., Maul R.S., Kim H.R., Chang D.D. Characterization of the human EPLIN (epithelial protein lost in neoplasm) gene reveals distinct promoters for the two EPLIN isoforms. Gene 2000, 248:69-76.
46. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Methods 2001, 25(4):402-408.
47. Lanzafame M., Botta E., Teson M., Fortugno P., Zambruno G., Stefanini M., Orioli D. Reference genes for gene expression analysis in proliferating and differentiating human keratinocytes. Exp. Dermatol. 2015, 24:296-319.
48. Dimri G.P., 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.
49. Chakrabarti S.K., James J.C., Mirmira R.G. Quantitative assessment of gene targeting in vitro and in vivo by the pancreatic transcription factor, Pdx1. Importance of chromatin structure in directing promoter binding. J. Biol. Chem. 2002, 277(15):13286-13293.
50. Christenson L.K., Stouffer R.L., Strauss J.F. Quantitative analysis of the hormone-induced hyperacetylation of histone H3 associated with the steroidogenic acute regulatory protein gene promoter. J. Biol. Chem. 2001, 276:27392-27399.
51. Nishio K., Inoue A. Senescence-associated alterations of cytoskeleton: extraordinary production of vimentin that anchors cytoplasmic p53 in senescent human fibroblasts. Histochem. Cell Biol. 2005, 123(3):263-273.
52. Chrétien A., Delaive E., Dieu M., Demazy C., Ninane N., Raes M., Toussaint O. Upregulation of annexin A2 in H(2)O(2)-induced premature senescence as evidenced by 2D-DIGE proteome analysis. Exp. Gerontol. 2008, 43(4):353-359.
53. Aan G.J., Hairi H.A., Makpol S., Rahman M.A., Karsani S.A. Differences in protein changes between stress-induced premature senescence and replicative senescence states. Electrophoresis 2013, 34(15):2209-2217.
54. Li W., Wang W., Li Y., Wang W., Wang T., Li L., Han Z., Wang S., Ma D., Wang H. Proteomics analysis of normal and senescent NG108-15 cells: GRP78 plays a negative role in cisplatin-induced senescence in the NG108-15 cell line. PLoS One 2014, 9(3):e90114.
55. Keppler D., Walter R., Perez C., Sierra F. Increased expression of mature cathepsin B in aging rat liver. Cell Tissue Res. 2000, 302:181-188.
56. Fisher G.J., Quan T., Purohit T., Shao Y., Cho M.K., He T., Varani J., Kang S., Voorhees J.J. Collagen fragmentation promotes oxidative stress and elevates matrix metalloproteinase-1 in fibroblasts in aged human skin. Am. J. Pathol. 2009, 174(1):10114.
57. Bigot N., Beauchef G., Hervieu M., Oddos T., Demoor M., Boumediene K., Galéra P. NF-κB accumulation associated with COL1A1 transactivators defects during chronological aging represses type I collagen expression through a -112/-61-bp region of the COL1A1 promoter in human skin fibroblasts. J. Investig. Dermatol. 2012, 132(10):2360-2367.
58. Holcomb V.B., Vogel H., Hasty P. Deletion of Ku80 causes early aging independent of chronic inflammation and Rag-1-induced DSBs. Mech. Ageing Dev. 2007, 128:601-608.
59. Steder M., Alla V., Meier C., Spitschak A., Pahnke J., Fürst K., Kowtharapu B.S., Engelmann D., Petigk J., Egberts F., Schäd-Trcka S.G., Gross G., Nettelbeck D.M., Niemetz A., Pützer B.M. DNp73 exerts function in metastasis initiation by disconnecting the inhibitory role of EPLIN on IGF1R-AKT/STAT3 signaling. Cancer Cell 2013, 24(4):512-527.
60. Lin H.K., Chen Z., Wang G., Nardella C., Lee S.W., Chan C.H., Yang W.L., Wang J., Egia A., Nakayama K.I., Cordon-Cardo C., Teruya-Feldstein J., Pandolfi P.P. Skp2 targeting suppresses tumorigenesis by Arf-p53-independent cellular senescence. Nature 2010, 464:374-379.
61. Myllyharju J., Kivirikko K.I. Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet. 2004, 20(1):33-43.
62. Pokidysheva E., Zientek K.D., Ishikawa Y., Mizuno K., Vranka J.A., Montgomery N.T., Keene D.R., Kawaguchi T., Okuyama K., Bächinger H.P. Posttranslational modifications in type I collagen from different tissues extracted from wild type and prolyl 3-hydroxylase 1 null mice. J. Biol. Chem. 2013, 288(34):24742-24752.
63. Moul A., Alladin A., Navarrete C., Abdenour G., Rodriguez M.M. Osteogenesis imperfecta due to compound heterozygosity for the LEPRE1 Gene. Fetal Pediatr. Pathol. 2013, 32(5):319-325.
64. Ishikawa Y., Bächinger H.P. An additional function of the rough endoplasmic reticulum protein complex prolyl 3-hydroxylase 1·cartilage-associated protein·cyclophilin B: the CXXXC motif reveals disulfide isomerase activity in vitro. J. Biol. Chem. 2013, 288(44):31437-31446.
65. Jiang W.G., Martin T.A., Lewis-Russell J.M., Douglas-Jones A., Ye L., Mansel R.E. Eplin-alpha expression in human breast cancer, the impact on cellular migration and clinical outcome. Mol. Cancer 2008, 7:71.
66. Zhang S., Wang X., Osunkoya A.O., Iqbal S., Wang Y., Chen Z., Müller S., Chen Z., Josson S., Coleman I.M., Nelson P.S., Wang Y.A., Wang R., Shin D.M., Marshall F.F., Kucuk O., Chung L.W., Zhau H.E., Wu D. EPLIN downregulation promotes epithelial-mesenchymal transition in prostate cancer cells and correlates with clinical lymph node metastasis. Oncogene 2011, 30:4941-4952.
67. Bono F., Gehring N.H. Assembly, disassembly and recycling: the dynamics of exon junction complexes. RNA Biol. 2011, 8(1):24-29.
68. Le Hir H., Gatfield D., Izaurralde E., Moore M.J. The exon-exon junction complex provides a binding platform for factors involved in mRNA export and nonsense-mediated mRNA decay. EMBO J. 2001, 20(17):4987-4997.
69. Chazal P.E., Daguenet E., Wendling C., Ulryck N., Tomasetto C., Sargueil B., Le Hir H. EJC core component MLN51 interacts with eIF3 and activates translation. Proc. Natl. Acad. Sci. U. S. A. 2013, 110(15):5903-5908.
70. Silver D.L., Watkins-Chow D.E., Schreck K.C., Pierfelice T.J., Larson D.M., Burnetti A.J., Liaw H.J., Myung K., Walsh C.A., Gaiano N., Pavan W.J. The exon junction complex component Magoh controls brain size by regulating neural stem cell division. Nat. Neurosci. 2010, 13(5):551-558.