Senescence-inducing stress promotes proteolysis of phosphoglycerate mutase via ubiquitin ligase Mdm2

Journal of Cell Biology

Volumn 204, Issue 5, 2014, Pages 729-745

  Mikawa, Takumi ^a   Maruyama, Takeshi ^a   Okamoto, Koji ^b   Nakagama, Hitoshi ^b   Lleonart, Matilde E ^c   Tsusaka, Takeshi ^a   Hori, Kousuke ^a   Murakami, Itsuo ^a   Izumi, Taisuke ^d   Takaori Kondo, Akifumi ^a   Yokode, Masayuki ^e   Peters, Gordon ^f   Beach, David ^g   Kondoh, Hiroshi ^a  

^a KYOTO UNIVERSITY   (Japan)

^b NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^c HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^d FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^e KYOTO UNIVERSITY HOSPITAL   (Japan)

^f Cancer Research UK London Research Institute   (Germany)

^g Center for Cutaneous Biology Institute for Cell and Molecular Science   (Germany)

Author keywords

DKO, double knockout; MEF, mouse embryonic fibroblast; PGAM, phosphoglycerate mutase; SA Gal, senescence associated galactosidase; SIS, stress induced senescence

Indexed keywords

6 PHOSPHOFRUCTOKINASE; ENOLASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCOLYTIC ENZYME; P21 ACTIVATED KINASE 1; PHOSPHOGLYCERATE KINASE; PHOSPHOGLYCERATE MUTASE; PHOSPHOGLYCERATE MUTASE 1; PHOSPHOGLYCERATE MUTASE 2; PROTEIN MDM2; PROTEIN P53; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL AGING; CELL PROLIFERATION; CELL STRESS; DNA DAMAGE; DOWN REGULATION; EMBRYO; ENZYME DEGRADATION; ENZYME PHOSPHORYLATION; FIBROBLAST; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UBIQUITINATION;

ANIMALS; CELL AGING; CELL LINE; DNA DAMAGE; DOWN-REGULATION; HCT116 CELLS; HEK293 CELLS; HELA CELLS; HT29 CELLS; HUMANS; MICE; MICE, INBRED C57BL; MICE, NUDE; P21-ACTIVATED KINASES; PHOSPHOGLYCERATE MUTASE; PHOSPHORYLATION; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS C-MDM2; STRESS, PHYSIOLOGICAL; UBIQUITIN;

EID: 84895763135     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201306149     Document Type: Article

References (60)

1. Acosta, J.C., A. O'Loghlen, A. Banito, M.V. Guijarro, A. Augert, S. Raguz, M. Fumagalli, M. Da Costa, C. Brown, N. Popov, et al. 2008. Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell. 133:1006-1018. http://dx.doi.org/10.1016/j.cell.2008.03.038
2. Bensaad, K., A. Tsuruta, M.A. Selak, M.N. Vidal, K. Nakano, R. Bartrons, E. Gottlieb, K.H. Vousden. 2006. TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell. 126:107-120. http://dx.doi.org/10.1016/j.cell.2006.05.036
3. Brown, D.R., C.A. Thomas, and S.P. Deb. 1998. The human oncoprotein MDM2 arrests the cell cycle: elimination of its cell-cycle-inhibitory function induces tumorigenesis. EMBO J. 17:2513-2525. http://dx.doi.org/10.1093/emboj/17.9.2513
4. Brummelkamp, T.R., R. Bernards, and R. Agami. 2002. A system for stable expression of short interfering RNAs in mammalian cells. Science. 296:550-553. http://dx.doi.org/10.1126/science.1068999
5. Campisi, J. 2013. Aging, cellular senescence, and cancer. Annu. Rev. Physiol. 75:685-705. http://dx.doi.org/10.1146/annurev-physiol-030212-183653
6. Cancer Genome Atlas Research Network. 2008. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature. 455:1061-1068. http://dx.doi.org/10.1038/nature07385
7. Carnero, A., J.D. Hudson, C.M. Price, and D.H. Beach. 2000. p16INK4A and p19ARF act in overlapping pathways in cellular immortalization. Nat. Cell Biol. 2:148-155.
8. Chen, Q., and B.N. Ames. 1994. Senescence-like growth arrest induced by hydrogen peroxide in human diploid fibroblast F65 cells. Proc. Natl. Acad. Sci. USA. 91:4130-4134. http://dx.doi.org/10.1073/pnas.91.10.4130
9. Dimri, G.P., X. Lee, G. Basile, M. Acosta, G. Scott, C. Roskelley, E.E. Medrano, M. Linskens, I. Rubelj, O. Pereira-Smith, et al. 1995. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. USA. 92:9363-9367. http://dx.doi.org/10.1073/pnas.92.20.9363
10. Ding, L., G. Getz, D.A. Wheeler, E.R. Mardis, M.D. McLellan, K. Cibulskis, C. Sougnez, H. Greulich, D.M. Muzny, M.B. Morgan, et al. 2008. Somatic mutations affect key pathways in lung adenocarcinoma. Nature. 455:1069-1075. http://dx.doi.org/10.1038/nature07423
11. Durany, N., J. Joseph, E. Campo, R. Molina, and J. Carreras. 1997. Phosphoglycerate mutase, 2,3-bisphosphoglycerate phosphatase and enolase activity and isoenzymes in lung, colon and liver carcinomas. Br. J. Cancer. 75:969-977. http://dx.doi.org/10.1038/bjc.1997.168
12. Durany, N., J. Joseph, O.M. Jimenez, F. Climent, P.L. Fernández, F. Rivera, and J. Carreras. 2000. Phosphoglycerate mutase, 2,3-bisphosphoglycerate phosphatase, creatine kinase and enolase activity and isoenzymes in breast carcinoma. Br. J. Cancer. 82:20-27.
13. Evans, M.J., A. Saghatelian, E.J. Sorensen, and B.F. Cravatt. 2005. Target discovery in small-molecule cell-based screens by in situ proteome reactivity profiling. Nat. Biotechnol. 23:1303-1307. http://dx.doi.org/10.1038/nbt1149
14. Hagai, T., A. Tóth-Petróczy, A. Azia, and Y. Levy. 2012. The origins and evolution of ubiquitination sites. Mol. Biosyst. 8:1865-1877. http://dx.doi.org/10.1039/c2mb25052g
15. Haupt, Y., R. Maya, A. Kazaz, and M. Oren. 1997. Mdm2 promotes the rapid degradation of p53. Nature. 387:296-299. http://dx.doi.org/10.1038/387296a0
16. Hayflick, L. 1965. The limited in vitro lifetime of human diploid cell strains. Exp. Cell Res. 37:614-636. http://dx.doi.org/10.1016/0014-4827(65)90211-9
17. Hershko, A., A. Ciechanover. 1998. The ubiquitin system. Annu. Rev. Biochem. 67:425-479. http://dx.doi.org/10.1146/annurev.biochem.67.1.425
18. Hitosugi, T., L. Zhou, S. Elf, J. Fan, H.B. Kang, J.H. Seo, C. Shan, Q. Dai, L. Zhang, J. Xie, et al. 2012. Phosphoglycerate mutase 1 coordinates glycolysis and biosynthesis to promote tumor growth. Cancer Cell. 22:585-600. http://dx.doi.org/10.1016/j.ccr.2012.09.020
19. International Cancer Genome Consortium. 2010. International network of cancer genome projects. Nature. 464:993-998. (published erratum appears in Nature. 2010. 17:465) http://dx.doi.org/10.1038/nature08987
20. Itahana, K., H. Mao, A. Jin, Y. Itahana, H.V. Clegg, M.S. Lindström, K.P. Bhat, V.L. Godfrey, G.I. Evan, and Y. Zhang. 2007. Targeted inactivation of Mdm2 RING finger E3 ubiquitin ligase activity in the mouse reveals mechanistic insights into p53 regulation. Cancer Cell. 12:355-366. http://dx.doi.org/10.1016/j.ccr.2007.09.007
21. Iyer, N.V., L.E. Kotch, F. Agani, S.W. Leung, E. Laughner, R.H. Wenger, M. Gassmann, J.D. Gearhart, A.M. Lawler, A.Y. Yu, and G.L. Semenza. 1998. Cellular and developmental control of O2 homeostasis by hypoxiainducible factor 1 alpha. Genes Dev. 12:149-162. http://dx.doi.org/10.1101/gad.12.2.149
22. Jones, R.G., D.R. Plas, S. Kubek, M. Buzzai, J. Mu, Y. Xu, M.J. Birnbaum, and C.B. Thompson. 2005. AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol. Cell. 18:283-293. http://dx.doi.org/10.1016/j.molcel.2005.03.027
23. Kawauchi, K., K. Araki, K. Tobiume, and N. Tanaka. 2008. p53 regulates glucose metabolism through an IKK-NF-κB pathway and inhibits cell transformation. Nat. Cell Biol. 10:611-618. http://dx.doi.org/10.1038/ncb1724
24. Kondoh, H., M.E. Lleonart, J. Gil, J. Wang, P. Degan, G. Peters, D. Martinez, A. Carnero, and D. Beach. 2005. Glycolytic enzymes can modulate cellular life span. Cancer Res. 65:177-185.
25. Koppenol, W.H., P.L. Bounds, and C.V. Dang. 2011. Otto Warburg's contributions to current concepts of cancer metabolism. Nat. Rev. Cancer. 11:325-337. http://dx.doi.org/10.1038/nrc3038
26. Kubbutat, M.H., S.N. Jones, and K.H. Vousden. 1997. Regulation of p53 stability by Mdm2. Nature. 387:299-303. http://dx.doi.org/10.1038/387299a0
27. Kubbutat, M.H., R.L. Ludwig, A.J. Levine, and K.H. Vousden. 1999. Analysis of the degradation function of Mdm2. Cell Growth Differ. 10:87-92.
28. Kuilman, T., C. Michaloglou, L.C. Vredeveld, S. Douma, R. van Doorn, C.J. Desmet, L.A. Aarden, W.J. Mooi, and D.S. Peeper. 2008. Oncogeneinduced senescence relayed by an interleukin-dependent inflammatory network. Cell. 133:1019-1031. http://dx.doi.org/10.1016/j.cell.2008.03.039
29. Leach, F.S., T. Tokino, P. Meltzer, M. Burrell, J.D. Oliner, S. Smith, D.E. Hill, D. Sidransky, K.W. Kinzler, and B. Vogelstein. 1993. p53 Mutation and MDM2 amplification in human soft tissue sarcomas. Cancer Res. 53:2231-2234.
30. Li, M., C.L. Brooks, F. Wu-Baer, D. Chen, R. Baer, and W. Gu. 2003. Mono- versus polyubiquitination: differential control of p53 fate by Mdm2. Science. 302:1972-1975. http://dx.doi.org/10.1126/science.1091362
31. Lipkowitz, S., and A.M. Weissman. 2011. RINGs of good and evil: RING finger ubiquitin ligases at the crossroads of tumour suppression and oncogenesis. Nat. Rev. Cancer. 11:629-643. http://dx.doi.org/10.1038/nrc3120
32. Manfredi, J.J. 2010. The Mdm2-p53 relationship evolves: Mdm2 swings both ways as an oncogene and a tumor suppressor. Genes Dev. 24:1580-1589. http://dx.doi.org/10.1101/gad.1941710
33. McClatchey, A.I., I. Saotome, K. Mercer, D. Crowley, J.F. Gusella, R.T. Bronson, and T. Jacks. 1998. Mice heterozygous for a mutation at the Nf2 tumor suppressor locus develop a range of highly metastatic tumors. Genes Dev. 12:1121-1133. http://dx.doi.org/10.1101/gad.12.8.1121
34. Molli, P.R., D.Q. Li, B.W. Murray, S.K. Rayala, and R. Kumar. 2009. PAK signaling in oncogenesis. Oncogene. 28:2545-2555. http://dx.doi.org/10.1038/onc.2009.119
35. Niwa, H., K. Yamamura, and J. Miyazaki. 1991. Efficient selection for highexpression transfectants with a novel eukaryotic vector. Gene. 108:193-199. http://dx.doi.org/10.1016/0378-1119(91)90434-D
36. Ogawara, Y., S. Kishishita, T. Obata, Y. Isazawa, T. Suzuki, K. Tanaka, N. Masuyama, and Y. Gotoh. 2002. Akt enhances Mdm2-mediated ubiquitination and degradation of p53. J. Biol. Chem. 277:21843-21850. http://dx.doi.org/10.1074/jbc. M109745200
37. Osthus, R.C., H. Shim, S. Kim, Q. Li, R. Reddy, M. Mukherjee, Y. Xu, D. Wonsey, L.A. Lee, and C.V. Dang. 2000. Deregulation of glucose transporter 1 and glycolytic gene expression by c-Myc. J. Biol. Chem. 275:21797-21800. http://dx.doi.org/10.1074/jbc. C000023200
38. Parrinello, S., E. Samper, A. Krtolica, J. Goldstein, S. Melov, and J. Campisi. 2003. Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts. Nat. Cell Biol. 5:741-747. http://dx.doi.org/10.1038/ncb1024
39. Poyurovsky, M.V., X. Jacq, C. Ma, O. Karni-Schmidt, P.J. Parker, M. Chalfie, J.L. Manley, and C. Prives. 2003. Nucleotide binding by the Mdm2 RING domain facilitates Arf-independent Mdm2 nucleolar localization. Mol. Cell. 12:875-887. http://dx.doi.org/10.1016/S1097-2765(03)00400-3
40. Prives, C. 1998. Signaling to p53: breaking the MDM2-p53 circuit. Cell. 95:5-8. http://dx.doi.org/10.1016/S0092-8674(00)81774-2
41. Reifenberger, G., L. Liu, K. Ichimura, E.E. Schmidt, V.P. Collins. 1993. Amplification and overexpression of the MDM2 gene in a subset of human malignant gliomas without p53 mutations. Cancer Res. 53:2736-2739.
42. Ren, F., H. Wu, Y. Lei, H. Zhang, R. Liu, Y. Zhao, X. Chen, D. Zeng, A. Tong, L. Chen, et al. 2010. Quantitative proteomics identification of phosphoglycerate mutase 1 as a novel therapeutic target in hepatocellular carcinoma. Mol. Cancer. 9:81. http://dx.doi.org/10.1186/1476-4598-9-81
43. Rodrigues, N.R., A. Rowan, M.E. Smith, I.B. Kerr, W.F. Bodmer, J.V. Gannon, D.P. Lane. 1990. p53 mutations in colorectal cancer. Proc. Natl. Acad. Sci. USA. 87:7555-7559. http://dx.doi.org/10.1073/pnas.87.19.7555
44. Ruiz-Lozano, P., M.L. Hixon, M.W. Wagner, A.I. Flores, S. Ikawa, A.S. Baldwin Jr., K.R. Chien, and A. Gualberto. 1999. p53 is a transcriptional activator of the muscle-specific phosphoglycerate mutase gene and contributes in vivo to the control of its cardiac expression. Cell Growth Differ. 10:295-306.
45. Samuels-Lev, Y., D.J. O'Connor, D. Bergamaschi, G. Trigiante, J.K. Hsieh, S. Zhong, I. Campargue, L. Naumovski, T. Crook, and X. Lu. 2001. ASPP proteins specifically stimulate the apoptotic function of p53. Mol. Cell. 8:781-794. http://dx.doi.org/10.1016/S1097-2765(01)00367-7
46. Schraml, P., G. Schwerdtfeger, F. Burkhalter, A. Raggi, D. Schmidt, T. Ruffalo, W. King, K. Wilber, M.J. Mihatsch, and H. Moch. 2003. Combined array comparative genomic hybridization and tissue microarray analysis suggest PAK1 at 11q13.5-q14 as a critical oncogene target in ovarian carcinoma. Am. J. Pathol. 163:985-992. http://dx.doi.org/10.1016/S0002-9440(10)63458-X
47. Seger, Y.R., M. García-Cao, S. Piccinin, C.L. Cunsolo, C. Doglioni, M.A. Blasco, G.J. Hannon, and R. Maestro. 2002. Transformation of normal human cells in the absence of telomerase activation. Cancer Cell. 2: 401-413. http://dx.doi.org/10.1016/S1535-6108(02)00183-6
48. Serrano, M., H. Lee, L. Chin, C. Cordon-Cardo, D. Beach, and R.A. DePinho. 1996. Role of the INK4a locus in tumor suppression and cell mortality. Cell. 85:27-37. http://dx.doi.org/10.1016/S0092-8674(00)81079-X
49. Serrano, M., A.W. Lin, M.E. McCurrach, D. Beach, and S.W. Lowe. 1997. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell. 88:593-602. http://dx.doi.org/10.1016/S0092-8674(00)81902-9
50. Shalom-Barak, T., and U.G. Knaus. 2002. A p21-activated kinase-controlled metabolic switch up-regulates phagocyte NADPH oxidase. J. Biol. Chem. 277:40659-40665. http://dx.doi.org/10.1074/jbc. M206650200
51. Terzian, T., Y.A. Suh, T. Iwakuma, S.M. Post, M. Neumann, G.A. Lang, C.S. Van Pelt, and G. Lozano. 2008. The inherent instability of mutant p53 is alleviated by Mdm2 or p16INK4a loss. Genes Dev. 22:1337-1344. http://dx.doi.org/10.1101/gad.1662908
52. Thorslund, T., F. Esashi, and S.C. West. 2007. Interactions between human BRCA2 protein and the meiosis-specific recombinase DMC1. EMBO J. 26:2915-2922. http://dx.doi.org/10.1038/sj.emboj.7601739
53. Vadlamudi, R.K., L. Adam, R.A. Wang, M. Mandal, D. Nguyen, A. Sahin, J. Chernoff, M.C. Hung, and R. Kumar. 2000. Regulatable expression of p21-activated kinase-1 promotes anchorage-independent growth and abnormal organization of mitotic spindles in human epithelial breast cancer cells. J. Biol. Chem. 275:36238-36244. http://dx.doi.org/10.1074/jbc. M002138200
54. Vander Heiden, M.G., L.C. Cantley, and C.B. Thompson. 2009. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 324:1029-1033. http://dx.doi.org/10.1126/science.1160809
55. Vander Heiden, M.G., J.W. Locasale, K.D. Swanson, H. Sharfi, G.J. Heffron, D. Amador-Noguez, H.R. Christofk, G. Wagner, J.D. Rabinowitz, J.M. Asara, and L.C. Cantley. 2010. Evidence for an alternative glycolytic pathway in rapidly proliferating cells. Science. 329:1492-1499. http://dx.doi.org/10.1126/science.1188015
56. Wang, R.A., A. Mazumdar, R.K. Vadlamudi, and R. Kumar. 2002. P21-activated kinase-1 phosphorylates and transactivates estrogen receptor-α and promotes hyperplasia in mammary epithelium. EMBO J. 21:5437-5447. http://dx.doi.org/10.1093/emboj/cdf543
57. Warburg, O. 1956. On respiratory impairment in cancer cells. Science. 124: 269-270.
58. Zhang, S., J. Han, M.A. Sells, J. Chernoff, U.G. Knaus, R.J. Ulevitch, G.M. Bokoch. 1995. Rho family GTPases regulate p38 mitogen-activated protein kinase through the downstream mediator Pak1. J. Biol. Chem. 270:23934-23936. http://dx.doi.org/10.1074/jbc.270.41.23934
59. Zhang, J., L. Yu, Q. Fu, J. Gao, Y. Xie, J. Chen, P. Zhang, Q. Liu, and S. Zhao. 2001. Mouse phosphoglycerate mutase M and B isozymes: cDNA cloning, enzyme activity assay and mapping. Gene. 264:273-279. http://dx.doi.org/10.1016/S0378-1119(00)00597-7
60. Zwerschke, W., S. Mazurek, P. Stöckl, E. Hütter, E. Eigenbrodt, and P. Jansen- Dürr. 2003. Metabolic analysis of senescent human fibroblasts reveals a role for AMP in cellular senescence. Biochem. J. 376:403-411. http://dx.doi.org/10.1042/BJ20030816