A 19S proteasomal subunit cooperates with an ERK MAPK-regulated degron to regulate accumulation of Fra-1 in tumour cells

Oncogene

Volumn 31, Issue 14, 2012, Pages 1817-1824

  Pakay, J L ^a   Diesch, J ^a,e   Gilan, O ^a,e   Yip, Y Y ^a   Sayan, E ^b   Kolch, W ^c   Mariadason, J M ^d   Hannan, R D ^a,e,f   Tulchinsky, E ^b   Dhillon, A S ^e  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

^c UNIVERSITY COLLEGE DUBLIN   (Ireland)

^d LUDWIG INSTITUTE FOR CANCER RESEARCH   (Australia)

^e PETER MACCALLUM CANCER CENTRE   (Australia)

^f MONASH UNIVERSITY   (Australia)

Author keywords

cancer; ERK; Fra 1; RAS; TBP 1; turnover

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; PROTEASOME; TRANSCRIPTION FACTOR FRA 1;

ARTICLE; CANCER GENETICS; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GENE LOSS; GENETIC CORRELATION; GENETIC REGULATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; TRANSCRIPTION INITIATION;

CELL LINE, TUMOR; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MAP KINASE SIGNALING SYSTEM; NEOPLASMS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTO-ONCOGENE PROTEINS C-FOS; RAS PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR AP-1;

EID: 84859611380     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.375     Document Type: Article

References (50)

1. Acquaviva C, Brockly F, Ferrara P, Bossis G, Salvat C, Jariel- Encontre I et al. (2001). Identification of a C-terminal tripeptide motif involved in the control of rapid proteasomal degradation of c-Fos proto-oncoprotein during the G(0)-to-S phase transition. Oncogene 20: 7563-7572. (Pubitemid 33086916)
2. Adiseshaiah P, Lindner DJ, Kalvakolanu DV, Reddy SP. (2007). FRA-1 proto-oncogene induces lung epithelial cell invasion and anchorage-independent growth in vitro, but is insufficient to promote tumor growth in vivo. Cancer Res 67: 6204-6211. (Pubitemid 47037501)
3. Andreolas C, Kalogeropoulou M, Voulgari A, Pintzas A. (2008). Fra-1 regulates vimentin during Ha-RAS-induced epithelial mesenchymal transition in human colon carcinoma cells. Int J Cancer 122: 1745-1756. (Pubitemid 351413420)
4. Asher G, Tsvetkov P, Kahana C, Shaul Y. (2005). A mechanism of ubiquitin-independent proteasomal degradation of the tumor suppressors p53 and p73. Genes Dev 19: 316-321. (Pubitemid 40189294)
5. Basbous J, Chalbos D, Hipskind R, Jariel-Encontre I, Piechaczyk M. (2007). Ubiquitin-independent proteasomal degradation of Fra-1 is antagonized by Erk1/2 pathway-mediated phosphorylation of a unique C-terminal destabilizer. Mol Cell Biol 27: 3936-3950. (Pubitemid 47010992)
6. Basbous J, Jariel-Encontre I, Gomard T, Bossis G, Piechaczyk M. (2008). Ubiquitin-independent- versus ubiquitin-dependent proteasomal degradation of the c-Fos and Fra-1 transcription factors: is there a unique answer? Biochimie 90: 296-305. (Pubitemid 351181245)
7. Baugh JM, Viktorova EG, Pilipenko EV. (2009). Proteasomes can degrade a significant proportion of cellular proteins independent of ubiquitination. J Mol Biol 386: 814-827.
8. Belguise K, Kersual N, Galtier F, Chalbos D. (2005). FRA-1 expression level regulates proliferation and invasiveness of breast cancer cells. Oncogene 24: 1434-1444. (Pubitemid 40343123)
9. Burch PM, Yuan Z, Loonen A, Heintz NH. (2004). An extracellular signal-regulated kinase 1- and 2-dependent program of chromatin trafficking of c-Fos and Fra-1 is required for cyclin D1 expression during cell cycle reentry. Mol Cell Biol 24: 4696-4709. (Pubitemid 38668037)
10. Casalino L, Bakiri L, Talotta F, Weitzman JB, Fusco A, Yaniv M et al. (2007). Fra-1 promotes growth and survival in RAS-transformed thyroid cells by controlling cyclin A transcription. EMBO J 26: 1878-1890. (Pubitemid 46624039)
11. Casalino L, De Cesare D, Verde P. (2003). Accumulation of Fra-1 in ras-transformed cells depends on both transcriptional autoregulation and MEK-dependent posttranslational stabilization. Mol Cell Biol 23: 4401-4415. (Pubitemid 36666439)
12. Chen C, Zhou Z, Guo P, Dong JT. (2007a). Proteasomal degradation of the KLF5 transcription factor through a ubiquitin-independent pathway. FEBS Lett 581: 1124-1130. (Pubitemid 46394549)
13. Chen X, Barton LF, Chi Y, Clurman BE, Roberts JM. (2007b). Ubiquitin-independent degradation of cell-cycle inhibitors by the REGgamma proteasome. Mol Cell 26: 843-852. (Pubitemid 46921008)
14. Chinenov Y, Kerppola TK. (2001). Close encounters of many kinds: Fos-Jun interactions that mediate transcription regulatory specificity. Oncogene 20: 2438-2452. (Pubitemid 32531301)
15. Cohn MA, Hjelmso I, Wu LC, Guldberg P, Lukanidin EM, Tulchinsky EM. (2001). Characterization of Sp1, AP-1, CBF and KRC binding sites and minisatellite DNA as functional elements of the metastasis-associated mts1/S100A4 gene intronic enhancer. Nucleic Acids Res 29: 3335-3346. (Pubitemid 32799106)
16. Corn PG, McDonald III ER, Herman JG, El-Deiry WS. (2003). Tat-binding protein-1, a component of the 26S proteasome, contributes to the E3 ubiquitin ligase function of the von Hippel-Lindau protein. Nat Genet 35: 229-237. (Pubitemid 37363176)
17. Debinski W, Gibo DM. (2005). Fos-related antigen 1 modulates malignant features of glioma cells. Mol Cancer Res 3: 237-249. (Pubitemid 40525334)
18. Doehn U, Hauge C, Frank SR, Jensen CJ, Duda K, Nielsen JV et al. (2009). RSK is a principal effector of the RAS-ERK pathway for eliciting a coordinate promotile/invasive gene program and phenotype in epithelial cells. Mol Cell 35: 511-522.
19. Dong Z, Xu RH, Kim J, Zhan SN, Ma WY, Colburn NH et al. (1996). AP-1/jun is required for early Xenopus development and mediates mesoderm induction by fibroblast growth factor but not by activin. J Biol Chem 271: 9942-9946. (Pubitemid 26131547)
20. Finley D. (2009). Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu Rev Biochem 78: 477-513.
21. Gallastegui N, Groll M. (2010). The 26S proteasome: assembly and function of a destructive machine. Trends Biochem Sci 35: 634-642.
22. Gomard T, Jariel-Encontre I, Basbous J, Bossis G, Mocquet-Torcy G, Piechaczyk M. (2008). Fos family protein degradation by the proteasome. Biochem Soc Trans 36: 858-863.
23. Higashitsuji H, Itoh K, Nagao T, Dawson S, Nonoguchi K, Kido T et al. (2000). Reduced stability of retinoblastoma protein by gankyrin, an oncogenic ankyrin-repeat protein overexpressed in hepatomas. Nat Med 6: 96-99. (Pubitemid 30048534)
24. Hoyt MA, Coffino P. (2004). Ubiquitin-free routes into the proteasome. Cell Mol Life Sci 61: 1596-1600. (Pubitemid 38962042)
25. Ishizuka T, Satoh T, Monden T, Shibusawa N, Hashida T, Yamada M et al. (2001). Human immunodeficiency virus type 1 Tat binding protein-1 is a transcriptional coactivator specific for TR. Mol Endocrinol 15: 1329-1343. (Pubitemid 32703481)
26. Jariel-Encontre I, Bossis G, Piechaczyk M. (2008). Ubiquitin-independent degradation of proteins by the proteasome. Biochim Biophys Acta 1786: 153-177.
27. Kakumoto K, Sasai K, Sukezane T, Oneyama C, Ishimaru S, Shibutani K et al. (2006). FRA1 is a determinant for the difference in RAS-induced transformation between human and rat fibroblasts. Proc Natl Acad Sci USA 103: 5490-5495.
28. Kalejta RF, Shenk T. (2003). Proteasome-dependent, ubiquitin-independent degradation of the Rb family of tumor suppressors by the human cytomegalovirus pp71 protein. Proc Natl Acad Sci USA 100: 3263-3268. (Pubitemid 36356571)
29. Karin M, Liu Z, Zandi E. (1997). AP-1 function and regulation. Curr Opin Cell Biol 9: 240-246. (Pubitemid 27135992)
30. Kustikova O, Kramerov D, Grigorian M, Berezin V, Bock E, Lukanidin E et al. (1998). Fra-1 induces morphological transformation and increases in vitro invasiveness and motility of epithelioid adenocarcinoma cells. Mol Cell Biol 18: 7095-7105. (Pubitemid 28533029)
31. Lam YA, Lawson TG, Velayutham M, Zweier JL, Pickart CM. (2002). A proteasomal ATPase subunit recognizes the polyubiquitin degradation signal. Nature 416: 763-767. (Pubitemid 34429155)
32. Luo YP, Zhou H, Krueger J, Kaplan C, Liao D, Markowitz D et al. (2010). The role of proto-oncogene Fra-1 in remodeling the tumor microenvironment in support of breast tumor cell invasion and progression. Oncogene 29: 662-673.
33. Park BW, O'Rourke DM, Wang Q, Davis JG, Post A, Qian X et al. (1999). Induction of the Tat-binding protein 1 gene accompanies the disabling of oncogenic erbB receptor tyrosine kinases. Proc Natl Acad Sci USA 96: 6434-6438. (Pubitemid 29256683)
34. Pollice A, Sepe M, Villella VR, Tolino F, Vivo M, Calabro V et al. (2007). TBP-1 protects the human oncosuppressor p14ARF from proteasomal degradation. Oncogene 26: 5154-5162. (Pubitemid 47206945)
35. Pollock CB, Shirasawa S, Sasazuki T, Kolch W, Dhillon AS. (2005). Oncogenic K-RAS is required to maintain changes in cytoskeletal organization, adhesion, and motility in colon cancer cells. Cancer Res 65: 1244-1250. (Pubitemid 40270149)
36. Prakash S, Tian L, Ratliff KS, Lehotzky RE, Matouschek A. (2004). An unstructured initiation site is required for efficient proteasome-mediated degradation. Nat Struct Mol Biol 11: 830-837. (Pubitemid 39128798)
37. Ramos-Nino ME, Scapoli L, Martinelli M, Land S, Mossman BT. (2003). Microarray analysis and RNA silencing link fra-1 to cd44 and c-met expression in mesothelioma. Cancer Res 63: 3539-3545. (Pubitemid 36793033)
38. Saksela K, Baltimore D. (1993). Negative regulation of immunoglobulin kappa light-chain gene transcription by a short sequence homologous to the murine B1 repetitive element. Mol Cell Biol 13: 3698-3705. (Pubitemid 23157306)
39. Satoh T, Ishizuka T, Tomaru T, Yoshino S, Nakajima Y, Hashimoto K et al. (2009). Tat-binding protein-1 (TBP-1), an ATPase of 19S regulatory particles of the 26S proteasome, enhances androgen receptor function in cooperation with TBP-1-interacting protein/ Hop2. Endocrinology 150: 3283-3290.
40. Shin S, Dimitri CA, Yoon SO, Dowdle W, Blenis J. (2010). but not ERK1 induces epithelial-to-mesenchymal transformation via DEF motif-dependent signaling events. Mol Cell 38: 114-127.
41. Takeuchi J, Chen H, Coffino P. (2007). Proteasome substrate degradation requires association plus extended peptide. EMBO J 26: 123-131. (Pubitemid 46094705)
42. Talotta F, Mega T, Bossis G, Casalino L, Basbous J, Jariel-Encontre I et al. (2003). Heterodimerization with Fra-1 cooperates with the ERK pathway to stabilize c-Jun in response to the RAS oncoprotein. Oncogene 29: 4732-4740.
43. Terasawa K, Okazaki K, Nishida E. (2003). Regulation of c-Fos and Fra-1 by the MEK5-ERK5 pathway. Genes Cells 8: 263-273. (Pubitemid 36511707)
44. Vial E, Marshall CJ. (2003). Elevated ERK-MAP kinase activity protects the FOS family member FRA-1 against proteasomal degradation in colon carcinoma cells. J Cell Sci 116: 4957-4963. (Pubitemid 38016702)
45. Vial E, Sahai E, Marshall CJ. (2003). ERK-MAPK signaling coordinately regulates activity of Rac1 and RhoA for tumor cell motility. Cancer Cell 4: 67-79. (Pubitemid 36904162)
46. Vikhanskaya F, Toh WH, Dulloo I, Wu Q, Boominathan L, Ng HH et al. (2007). p73 supports cellular growth through c-Jun-dependent AP-1 transactivation. Nat Cell Biol 9: 698-705.
47. von Kriegsheim A, Pitt A, Grindlay GJ, Kolch W, Dhillon AS. (2006). Regulation of the Raf-MEK-ERK pathway by protein phosphatase 5. Nat Cell Biol 8: 1011-1016. (Pubitemid 44314733)
48. Young MR, Colburn NH. (2006). Fra-1 a target for cancer prevention or intervention. Gene 379: 1-11. (Pubitemid 44247331)
49. Young MR, Nair R, Bucheimer N, Tulsian P, Brown N, Chapp C et al. (2002). Transactivation of Fra-1 and consequent activation of AP-1 occur extracellular signal-regulated kinase dependently. Mol Cell Biol 22: 587-598. (Pubitemid 34027503)
50. Zhang M, Pickart CM, Coffino P. (2003). Determinants of proteasome recognition of ornithine decarboxylase, a ubiquitin-independent substrate. Embo J 22: 1488-1496. (Pubitemid 36417398)