The molecular scaffold kinase suppressor of Ras 1 is a modifier of Ras V12-induced and replicative senescence

Molecular and Cellular Biology

Volumn 26, Issue 6, 2006, Pages 2202-2214

  Kortum, Robert L ^a   Johnson, Heidi J ^a   Costanzo, Diane L ^a   Volle, Deanna J ^a   Razidlo, Gina L ^a   Fusello, Angela M ^b   Shaw, Andrey S ^b   Lewis, Robert E ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2B; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOTRANSFERASE; PROTEIN P15; PROTEIN P16INK4A; PROTEIN P19; PROTEIN P19ARF; PROTEIN P53; RAF PROTEIN; RAS PROTEIN; RAS V12 PROTEIN; RAS1 PROTEIN; RETINOBLASTOMA PROTEIN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL AGING; CELL DIVISION; CELL GROWTH; CELL IMMORTALIZATION; CELL PROLIFERATION; CELL TRANSFORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; GENE DELETION; GENE DISRUPTION; GENE MUTATION; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SENESCENCE; WILD TYPE;

ANIMALS; CELL AGING; CELL LINE, TRANSFORMED; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P15; CYCLIN-DEPENDENT KINASE INHIBITOR P16; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLASTS; GENE EXPRESSION REGULATION; MAP KINASE KINASE 1; MICE; MUTATION; PROTEIN KINASES; RAS PROTEINS; TUMOR SUPPRESSOR PROTEIN P14ARF; TUMOR SUPPRESSOR PROTEIN P53;

ANIMALIA;

EID: 33644758575     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.26.6.2202-2214.2006     Document Type: Article

References (76)

1. Alani, R. M., A. Z. Young, and C. B. Shifflett. 2001. Id1 regulation of cellular senescence through transcriptional repression of p16/Ink4a. Proc. Natl. Acad. Sci. USA 98:7812-7816.
2. Barak, Y., T. Juven, R. Haffner, and M. Oren. 1993. mdm2 expression is induced by wild type p53 activity. EMBO J. 12:461-468.
3. Barbacid, M. 1987. ras genes. Annu. Rev. Biochem. 56:779-827.
4. Beausejour, C. M., A. Krtolica, F. Galimi, M. Narita, S. W. Lowe, P. Yaswen, and J. Campisi. 2003. Reversal of human cellular senescence: roles of the p53 and p16 pathways. EMBO J. 22:4212-4222.
5. Brennan, J. A., D. J. Volle, O. V. Chaika, and R. E. Lewis. 2002. Phosphorylation regulates the nucleocytoplasmic distribution of kinase suppressor of Ras. J. Biol. Chem. 277:5369-5377.
6. Brookes, S., J. Rowe, M. Ruas, S. Llanos, P. A. Clark, M. Lomax, M. C. James, R. Vatcheva, S. Bates, K. H. Vousden, D. Parry, N. Gruis, N. Smit, W. Bergman, and G. Peters. 2002. INK4a-deficient human diploid fibroblasts are resistant to RAS-induced senescence. EMBO J. 21:2936-2945.
7. Brunet, A., G. Pages, and J. Pouyssegur. 1994. Constitutively active mutants of MAP kinase kinase (MEK1) induce growth factor-relaxation and oncogenicity when expressed in fibroblasts. Oncogene 9:3379-3387.
8. Burack, W. R., and A. S. Shaw. 2000. Signal transduction: hanging on a scaffold. Curr. Opin. Cell Biol. 12:211-216.
9. Campisi, J. 2001. Cellular senescence as a tumor-suppressor mechanism. Trends Cell Biol. 11:S27-31.
10. 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.
11. Chang, E. H., M. E. Furth, E. M. Scolnick, and D. R. Lowy. 1982. Tumorigenic transformation of mammalian cells induced by a normal human gene homologous to the oncogene of Harvey murine sarcoma virus. Nature 297: 479-483.
12. Cowley, S., H. Paterson, P. Kemp, and C. J. Marshall. 1994. Activation of MAP kinase kinase is necessary and sufficient for PC12 differentiation and for transformation of NIH 3T3 cells. Cell 77:841-852.
13. 1 control causing immortalization and increased cell turnover under growth-restricting conditions. Genes Dev. 14:3051-3064.
14. Der, C. J., T. G. Krontiris, and G. M. Cooper. 1982. Transforming genes of human bladder and lung carcinoma cell lines are homologous to the ras genes of Harvey and Kirsten sarcoma viruses. Proc. Natl. Acad. Sci. USA 79:3637-3640.
15. de Stanchina, E., E. Querido, M. Narita, R. V. Davuluri, P. P. Pandolfi, G. Ferbeyre, and S. W. Lowe. 2004. PML is a direct p53 target that modulates p53 effector functions. Mol. Cell 13:523-535.
16. 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.
17. Dougherty, M. K., J. Muller, D. A. Ritt, M. Zhou, X. Z. Zhou, T. D. Copeland, T. P. Conrads, T. D. Veenstra, K. P. Lu, and D. K. Morrison. 2005. Regulation of Raf-1 by direct feedback phosphorylation. Mol. Cell 17:215-224.
18. el-Deiry, W. S., T. Tokino, V. E. Velculescu, D. B. Levy, R. Parsons, J. M. Trent, D. Lin, W. E. Mercer, K. W. Kinzler, and B. Vogelstein. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825.
19. Fantz, D. A., D. Jacobs, D. Glossip, and K. Kornfeld. 2001. Docking sites on substrate proteins direct extracellular signal-regulated kinase to phosphorylate specific residues. J. Biol. Chem. 276:27256-27265.
20. Ferbeyre, G., E. de Stanchina, A. W. Lin, E. Querido, M. E. McCurrach, G. J. Hannon, and S. W. Lowe. 2002. Oncogenic ras and p53 cooperate to induce cellular senescence. Mol. Cell. Biol. 22:3497-3508.
21. Ferbeyre, G., E. de Stanchina, E. Querido, N. Baptiste, C. Prives, and S. W. Lowe. 2000. PML is induced by oncogenic ras and promotes premature senescence. Genes Dev. 14:2015-2027.
22. Franza, B. R., Jr., K. Maruyama, J. I. Garrels, and H. E. Ruley. 1986. In vitro establishment is not a sufficient prerequisite for transformation by activated ras oncogenes. Cell 44:409-418.
23. 1 cell cycle progression. J. Biol. Chem. 274:22033-22040.
24. Hamad, N. M., J. H. Elconin, A. E. Karnoub, W. Bai, J. N. Rich, R. T. Abraham, C. J. Der, and C. M. Counter. 2002. Distinct requirements for Ras oncogenesis in human versus mouse cells. Genes Dev. 16:2045-2057.
25. Harvey, D. M., and A. J. Levine. 1991. p53 alteration is a common event in the spontaneous immortalization of primary BALB/c murine embryo fibroblasts. Genes Dev. 5:2375-2385.
26. Harvey, M., A. T. Sands, R. S. Weiss, M. E. Hegi, R. W. Wiseman, P. Pantazis, B. C. Giovanella, M. A. Tainsky, A. Bradley, and L. A. Donehower. 1993. In vitro growth characteristics of embryo fibroblasts isolated from p53-deficient mice. Oncogene 8:2457-2467.
27. Hayflick, L., and P. S. Moorhead. 1961. The serial cultivation of human diploid cell strains. Exp. Cell Res. 25:585-621.
28. INK4a confer resistance to Ras- and Ets-induced senescence in human diploid fibroblasts. Mol. Cell. Biol. 22:8135-8143.
29. INK4a and the control of cellular proliferative life span. Carcinogenesis 20:921-926.
30. Inoue, K., R. Wen, J. E. Rehg, M. Adachi, J. L. Cleveland, M. F. Roussel, and C. J. Sherr. 2000. Disruption of the ARF transcriptional activator DMP1 facilitates cell immortalization, Ras transformation, and tumorigenesis. Genes Dev. 14:1797-1809.
31. Jacobs, D., D. Glossip, H. Xing, A. J. Muslin, and K. Kornfeld. 1999. Multiple docking sites on substrate proteins form a modular system that mediates recognition by ERK MAP kinase. Genes Dev. 13:163-175.
32. Janssen, R. A., P. N. Kim, J. W. Mier, and D. K. Morrison. 2003. Overexpression of kinase suppressor of Ras upregulates the high-molecular-weight tropomyosin isoforms in ras-transformed NIH 3T3 fibroblasts. Mol. Cell. Biol. 23:1786-1797.
33. Joneson, T., J. A. Fulton, D. J. Volle, O. V. Chaika, D. Bar-Sagi, and R. E. Lewis. 1998. Kinase suppressor of Ras inhibits the activation of extracellular ligand-regulated (ERK) mitogen-activated protein (MAP) kinase by growth factors, activated Ras, and Ras effectors. J. Biol. Chem. 273:7743-7748.
34. Kamijo, T., F. Zindy, M. F. Roussel, D. E. Quelle, J. R. Downing, R. A. Ashmun, G. Grosveld, and C. J. Sherr. 1997. Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell 91:649-659.
35. Kolch, W. 2005. Coordinating ERK/MAPK signalling through scaffolds and inhibitors. Nat. Rev. Mol. Cell Biol. 6:827-837.
36. Kortum, R. L., D. L. Costanzo, J. Haferbier, S. J. Schreiner, G. L. Razidlo, M. H. Wu, D. J. Volle, T. Mori, H. Sakaue, N. V. Chaika, O. V. Chaika, and R. E. Lewis. 2005. The molecular scaffold kinase suppressor of Ras 1 (KSR1) regulates adipogenesis. Mol. Cell. Biol. 25:7592-7604.
37. Kortum, R. L., and R. E. Lewis. 2004. The molecular scaffold KSR1 regulates the proliferative and oncogenic potential of cells. Mol. Cell. Biol. 24:4407-4416.
38. Krtolica, A., S. Parrinello, S. Lockett, P. Y. Desprez, and J. Campisi. 2001. Senescent fibroblasts promote epithelial cell growth and tumorigenesis: a link between cancer and aging. Proc. Natl. Acad. Sci. USA 98:12072-12077.
39. Land, H., L. F. Parada, and R. A. Weinberg. 1983. Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature 304:596-602.
40. Latres, E., M. Malumbres, R. Sotillo, J. Martin, S. Ortega, J. Martin-Caballero, J. M. Flores, C. Cordon-Cardo, and M. Barbacid. 2000. Limited overlapping roles of P15(INK4b) and P18(INK4c) cell cycle inhibitors in proliferation and tumorigenesis. EMBO J. 19:3496-3506.
41. Lin, A. W., M. Barradas, J. C. Stone, L. van Aelst, M. Serrano, and S. W. Lowe. 1998. Premature senescence involving p53 and p16 is activated in response to constitutive MEK/MAPK mitogenic signaling. Genes Dev. 12: 3008-3019.
42. Lozano, J., R. Xing, Z. Cai, H. L. Jensen, C. Trempus, W. Mark, R. Cannon, and R. Kolesnick. 2003. Deficiency of kinase suppressor of Ras1 prevents oncogenic ras signaling in mice. Cancer Res. 63:4232-4238.
43. INK4b. Mol. Cell. Biol. 20:2915-2925.
44. Mansour, S. J., W. T. Matten, A. S. Hermann, J. M. Candia, S. Rong, K. Fukasawa, G. F. Vande Woude, and N. G. Ahn. 1994. Transformation of mammalian cells by constitutively active MAP kinase kinase. Science 265: 966-970.
45. Michaud, N. R., M. Therrien, A. Cacace, L. C. Edsall, S. Spiegel, G. M. Rubin, and D. K. Morrison. 1997. KSR stimulates Raf-1 activity in a kinase-independent manner. Proc. Natl. Acad. Sci. USA 94:12792-12796.
46. Morrison, D. K. 2001. KSR: a MAPK scaffold of the Ras pathway? J. Cell Sci. 114:1609-1612.
47. Muller, J., A. M. Cacace, W. E. Lyons, C. B. McGill, and D. K. Morrison. 2000. Identification of B-KSR1, a novel brain-specific isoform of KSR1 that functions in neuronal signaling. Mol. Cell. Biol. 20:5529-5539.
48. Muller, J., S. Ory, T. Copeland, H. Piwnica-Worms, and D. K. Morrison. 2001. C-TAK1 regulates Ras signaling by phosphorylating the MAPK scaffold, KSR1. Mol. Cell 8:983-993.
49. Nguyen, A., W. R. Burack, J. L. Stock, R. Kortum, O. V. Chaika, M. Afkarian, W. J. Muller, K. M. Murphy, D. K. Morrison, R. E. Lewis, J. McNeish, and A. S. Shaw. 2002. Kinase suppressor of Ras (KSR) is a scaffold which facilitates mitogen-activated protein kinase activation in vivo. Mol. Cell. Biol. 22:3035-3045.
50. Palmero, I., C. Pantoja, and M. Serrano. 1998. p19ARF links the tumour suppressor p53 to Ras. Nature 395:125-126.
51. Parada, L. F., C. J. Tabin, C. Shih, and R. A. Weinberg. 1982. Human EJ bladder carcinoma oncogene is homologue of Harvey sarcoma virus ras gene. Nature 297:474-478.
52. Peeper, D. S., J. H. Dannenberg, S. Douma, H. te Riele, and R. Bernards. 2001. Escape from premature senescence is not sufficient for oncogenic transformation by Ras. Nat. Cell Biol. 3:198-203.
53. Quelle, D. E., F. Zindy, R. A. Ashmun, and C. J. Sherr. 1995. Alternative reading frames of the INK4a tumor suppressor gene encode two unrelated proteins capable of inducing cell cycle arrest. Cell 83:993-1000.
54. Rapp, U. R., M. D. Goldsborough, G. E. Mark, T. I. Bonner, J. Groffen, F. H. Reynolds, Jr., and J. R. Stephenson. 1983. Structure and biological activity of v-raf, a unique oncogene transduced by a retrovirus. Proc. Natl. Acad. Sci. USA 80:4218-4222.
55. Razidlo, G. L., R. L. Kortum, J. L. Haferbier, and R. E. Lewis. 2004. Phosphorylation regulates KSR1 stability, ERK activation, and cell proliferation. J. Biol. Chem. 279:47808-47814.
56. Roy, F., G. Laberge, M. Douziech, D. Ferland-McCollough, and M. Therrien. 2002. KSR is a scaffold required for activation of the ERK/MAPK module. Genes Dev. 16:427-438.
57. 1 control and immortalization. Genes Dev. 14:3037-3050.
58. 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.
59. 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.
60. Cip1. Mol. Cell. Biol. 17:5588-5597.
61. Sharpless, N. E., N. Bardeesy, K. H. Lee, D. Carrasco, D. H. Castrillon, A. J. Aguirre, E. A. Wu, J. W. Homer, and R. A. DePinho. 2001. Loss of p16Ink4a with retention of p19Arf predisposes mice to tumorigenesis. Nature 413:86-91.
62. Sharpless, N. E., M. R. Ramsey, P. Balasubramanian, D. H. Castrillon, and R. A. DePinho. 2004. The differential impact of p16(INK4a) or p19(ARF) deficiency on cell growth and tumorigenesis. Oncogene 23:379-385.
63. Shih, T. Y., A. G. Papageorge, P. E. Stokes, M. O. Weeks, and E. M. Scolnick. 1980. Guanine nucleotide-binding and autophosphorylating activities associated with the p21src protein of Harvey murine sarcoma virus. Nature 287:686-691.
64. Sreeramaneni, R., A. Chaudhry, M. McMahon, C. J. Sherr, and K. Inoue. 2005. Ras-Raf-Arf signaling critically depends on the Dmp1 transcription factor. Mol. Cell. Biol. 25:220-232.
65. Stewart, S., M. Sundaram, Y. Zhang, J. Lee, M. Han, and K. L. Guan. 1999. Kinase suppressor of Ras forms a multiprotein signaling complex and modulates MEK localization. Mol. Cell. Biol. 19:5523-5534.
66. Sundaram, M., and M. Han. 1995. The C. elegans ksr-1 gene encodes a novel Raf-related kinase involved in Ras-mediated signal transduction. Cell 83: 889-901.
67. Todaro, G. J., and H. Green. 1963. Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J. Cell Biol. 17:299-313.
68. Webb, C. P., L. Van Aelst, M. H. Wigler, and G. F. Woude. 1998. Signaling pathways in Ras-mediated tumorigenicity and metastasis. Proc. Natl. Acad. Sci. USA 95:8773-8778.
69. ARF in replicative and induced senescence of human fibroblasts. Mol. Cell. Biol. 21: 6748-6757.
70. Wei, W., U. Herbig, S. Wei, A. Dutriaux, and J. M. Sedivy. 2003. Loss of retinoblastoma but not p16 function allows bypass of replicative senescence in human fibroblasts. EMBO Rep. 4:1061-1066.
71. White, M. A., C. Nicolette, A. Minden, A. Polverino, L. Van Aelst, M. Karin, and M. H. Wigler. 1995. Multiple Ras functions can contribute to mammalian cell transformation. Cell 80:533-541.
72. Cip1. Mol. Cell. Biol. 17:5598-5611.
73. Wu, X., J. H. Bayle, D. Olson, and A. J. Levine. 1993. The p53-mdm-2 autoregulatory feedback loop. Genes Dev. 7:1126-1132.
74. Xing, H. R., C. Cordon-Cardo, X. Deng, W. Tong, L. Campodonico, Z. Fuks, and R. Kolesnick. 2003. Pharmacologic inactivation of kinase suppressor of ras-1 abrogates Ras-mediated pancreatic cancer. Nat. Med. 9:1266-1268.
75. Yu, W., W. J. Fantl, G. Harrowe, and L. T. Williams. 1998. Regulation of the MAP kinase pathway by mammalian Ksr through direct interaction with MEK and ERK. Curr. Biol. 8:56-64.
76. Zhu, J., D. Woods, M. McMahon, and J. M. Bishop. 1998. Senescence of human fibroblasts induced by oncogenic Raf. Genes Dev. 12:2997-3007.