Syntenin-mediated regulation of Sox4 proteasomal degradation modulates transcriptional output

Oncogene

Volumn 31, Issue 21, 2012, Pages 2668-2679

  Beekman, J M ^a,b   Vervoort, S J ^a,b   Dekkers, F ^b   Van Vessem, M E ^a   Vendelbosch, S ^a   Brugulat Panes A ^a   Van Loosdregt, J ^a   Braat, A K ^a   Coffer, P J ^a,b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

metastasis; proteasomal degradation; Sox4; syntenin

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CYCLOHEXIMIDE; POLYUBIQUITIN; PROTEASOME; SYNTENIN; TRANSCRIPTION FACTOR SOX4;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CARCINOGENESIS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN SYNTHESIS; TUMOR CELL;

AMINO ACID MOTIFS; CELL LINE, TUMOR; CELL NUCLEUS; HALF-LIFE; HUMANS; PROTEASOME ENDOPEPTIDASE COMPLEX; RNA PROCESSING, POST-TRANSCRIPTIONAL; SOXC TRANSCRIPTION FACTORS; SYNTENINS; TRANSCRIPTIONAL ACTIVATION;

MURINAE;

EID: 84861526038     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.445     Document Type: Article

References (50)

1. Asher G, Reuven N, Shaul Y. (2006). 20S proteasomes and protein degradation "by default". Bioessays 28: 844-849. (Pubitemid 44433746)
2. Asher G, Shaul Y. (2006). Ubiquitin-independent degradation: lessons from the p53 model. Isr Med Assoc J 8: 229-232.
3. 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)
4. Beekman JM, Bakema JE, van de Winkel JGJ, Leusen JHW. (2004). Direct interaction between FcgammaRI (CD64) and periplakin controls receptor endocytosis and ligand binding capacity. Proc Natl Acad Sci USA 101: 10392-10397. (Pubitemid 38924936)
5. Beekman JM, Coffer PJ. (2008). The ins and outs of syntenin, a multifunctional intracellular adaptor protein. J Cell Sci 121: 1349-1355. (Pubitemid 351936299)
6. Beekman JM, Verhagen LP, Geijsen N, Coffer PJ. (2009). Regulation of myelopoiesis through syntenin-mediated modulation of IL-5 receptor output. Blood 114: 3917-3927.
7. Belizario JE, Alves J, Garay-Malpartida M, Occhiucci JM. (2008). Coupling caspase cleavage and proteasomal degradation of proteins carrying PEST motif. Curr Protein Pept Sci 9: 210-220. (Pubitemid 351997837)
8. Bergsland M, Werme M, Malewicz M, Perlmann T, Muhr J. (2006). The establishment of neuronal properties is controlled by Sox4 and Sox11. Genes Dev 20: 3475-3486. (Pubitemid 44969164)
9. Bhattaram P, Penzo-Mendez A, Sock E, Colmenares C, Kaneko KJ, Vassilev A. (2010). Organogenesis relies on SoxC transcription factors for the survival of neural and mesenchymal progenitors. Nat Commun 1: 9.
10. Boukerche H, Aissaoui H, Prévost C, Hirbec H, Das SK, Su ZZ. (2010). Mda-9/Syntenin promotes metastasis in human melanoma cells by activating c-Src. Oncogene 29: 3054-3066.
11. Boukerche H, Su ZZ, Prévot C, Sarkar D, Fisher PB. (2008). Src kinase activation is mandatory for MDA-9/syntenin-mediated activation of nuclear factor-kappaB. Proc Natl Acad Sci USA 105: 15914-15919.
12. Bowles J, Schepers G, Koopman P. (2000). Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev Biol 227: 239-255.
13. Dy P, Penzo-Mendez A, Wang H, Pedraza CE, Macklin WB, Lefebvre V. (2008). The three SoxC proteins-Sox4, Sox11 and Sox12-exhibit overlapping expression patterns and molecular properties. Nucleic Acids Res 36: 3101-3117. (Pubitemid 351737202)
14. Dyson HJ, Wright PE. (2005). Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 6: 197-208. (Pubitemid 40314921)
15. Elenbaas B, Spirio L, Koerner F, Fleming MD, Zimonjic DB, Donaher JL. (2001). Human breast cancer cells generated by oncogenic transformation of primary mammary epithelial cells. Genes Dev 15: 50-65. (Pubitemid 32060682)
16. Fietta P, Delsante G. (2010). Proteasomes and immunoproteasomes. Riv Biol 103: 29-50.
17. Geijsen N, Uings IJ, Pals C, Armstrong J, McKinnon M, Raaijmakers JA. (2001). Cytokine-specific transcriptional regulation through an IL-5Ralpha interacting protein. Science 293: 1136-1138. (Pubitemid 32758094)
18. Goldberg AL. (2003). Protein degradation and protection against misfolded or damaged proteins. Nature 426: 895-899. (Pubitemid 38056882)
19. Grootjans JJ, Zimmermann P, Reekmans G, Smets A, Degeest G, Dü rr J. (1997). Syntenin, a PDZ protein that binds syndecan cytoplasmic domains. Proc Natl Acad Sci USA 94: 13683-13688. (Pubitemid 28009643)
20. Hoser M, Potzner MR, Koch JM, Bosl MR, Wegner M, Sock E. (2008). Sox12 deletion in the mouse reveals nonreciprocal redundancy with the related Sox4 and Sox11 transcription factors. Mol Cell Biol 28: 4675-4687.
21. Hunt SM, Clarke CL. (1999). Expression and hormonal regulation of the Sox4 gene in mouse female reproductive tissues. Biol Reprod 61: 476-481. (Pubitemid 29344767)
22. Kerscher O, Felberbaum R, Hochstrasser M. (2006). Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 22: 159-180.
23. Krappmann D, Wulczyn FG, Scheidereit C. (1996). Different mechanisms control signal-induced degradation and basal turnover of the NF-kappaB inhibitor IkappaB alpha in vivo. EMBO J 15: 6716-6726. (Pubitemid 26413803)
24. Kruger E, Kloetzel PM, Enenkel C. (2001). 20S proteasome biogenesis. Biochimie 83: 289-293. (Pubitemid 32293648)
25. Kwak J, Workman JL, Lee D. (2010). The proteasome and its regulatory roles in gene expression. Biochim Biophys Acta 1809: 88-96.
26. Lambaerts K, Wilcox-Adelman SA, Zimmermann P. (2009). The signaling mechanisms of syndecan heparan sulfate proteoglycans. Curr Opin Cell Biol 21: 662-669.
27. Lin JJ, Jiang H, Fisher PB. (1998). Melanoma differentiation associated gene-9, mda-9, is a human gamma interferon responsive gene. Gene 207: 105-110. (Pubitemid 28085338)
28. Lund AH, Turner G, Trubetskoy A, Verhoeven E, Wientjens E, Hulsman D. (2002). Genome-wide retroviral insertional tagging of genes involved in cancer in Cdkn2a-deficient mice. Nat Genet 32: 160-165. (Pubitemid 34977212)
29. Malki S, Boizet-Bonhoure B, Poulat F. (2010). Shuttling of SOX proteins. Int J Biochem Cell Biol 42: 411-416.
30. Medina PP, Castillo SD, Blanco S, Sanz-Garcia M, Largo C, Alvarez S. (2009). The SRY-HMG box gene, SOX4, is a target of gene amplification at chromosome 6p in lung cancer. Hum Mol Genet 18: 1343-1352.
31. Nissen-Meyer LS, Jemtland R, Gautvik VT, Pedersen ME, Paro R, Fortunati D. (2007). Osteopenia, decreased bone formation and impaired osteoblast development in Sox4 heterozygous mice. J Cell Sci 120: 2785-2795. (Pubitemid 47394253)
32. Pan X, Zhao J, Zhang WN, Li HY, Mu R, Zhou T. (2009). Induction of SOX4 by DNA damage is critical for p53 stabilization and function. Proc Natl Acad Sci USA 106: 3788-3793.
33. Penzo-Mendez AI. (2010). Critical roles for SoxC transcription factors in development and cancer. Int J Biochem Cell Biol 42: 425-428.
34. Potzner MR, Tsarovina K, Binder E, Penzo-Mendez A, Lefebvre V, Rohrer H. (2010). Sequential requirement of Sox4 and Sox11 during development of the sympathetic nervous system. Development 137: 775-784.
35. Prakash S, Tian L, Ratliff KS, Lehotzky RE, Matouschek A. (2004). An unstructured initiation site is required for efficient proteasomemediated degradation. Nat Struct Mol Biol 11: 830-837. (Pubitemid 39128798)
36. Rechsteiner M, Rogers SW. (1996). PEST sequences and regulation by proteolysis. Trends Biochem Sci 21: 267-271. (Pubitemid 26228278)
37. Reits EA, Benham AM, Plougastel B, Neefjes J, Trowsdale J. (1997). Dynamics of proteasome distribution in living cells. EMBO J 16: 6087-6094. (Pubitemid 27458328)
38. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D. (2004). Large-scale meta-analysis of cancer microarray data identifies common transcriptional profiles of neoplastic transformation and progression. Proc Natl Acad Sci USA 101: 9309-9314. (Pubitemid 38812872)
39. Sarkar D, Boukerche H, Su ZZ, Fisher PB. (2004). Mda-9/syntenin: recent insights into a novel cell signaling and metastasis-associated gene. Pharmacol Ther 104: 101-115. (Pubitemid 39429466)
40. Sarkar D, Boukerche H, Su ZZ, Fisher PB. (2008). Mda-9/Syntenin: more than just a simple adapter protein when it comes to cancer metastasis. Cancer Res 68: 3087-3093.
41. Schilham MW, Moerer P, Cumano A, Clevers HC. (1997). Sox-4 facilitates thymocyte differentiation. Eur J Immunol 27: 1292-1295. (Pubitemid 27197236)
42. Schilham MW, Oosterwegel MA, Moerer P, Ya J, de Boer PA, van De WM. (1996). Defects in cardiac outflow tract formation and pro-B-lymphocyte expansion in mice lacking Sox-4. Nature 380: 711-714. (Pubitemid 26125470)
43. Shin MS, Fredrickson TN, Hartley JW, Suzuki T, Akagi K, Morse III HC. (2004). High-throughput retroviral tagging for identification of genes involved in initiation and progression of mouse splenic marginal zone lymphomas. Cancer Res 64: 4419-4427. (Pubitemid 38856912)
44. Sinner D, Kordich JJ, Spence JR, Opoka R, Rankin S, Lin SC. (2007). Sox17 and Sox4 differentially regulate beta-catenin/T-cell factor activity and proliferation of colon carcinoma cells. Mol Cell Biol 27: 7802-7815. (Pubitemid 350086414)
45. Suzuki T, Shen H, Akagi K, Morse HC, Malley JD, Naiman DQ. (2002). New genes involved in cancer identified by retroviral tagging. Nat Genet 32: 166-174. (Pubitemid 34977213)
46. Tavazoie SF, Alarcon C, Oskarsson T, Padua D, Wang Q, Bos PD. (2008). Endogenous human microRNAs that suppress breast cancer metastasis. Nature 451: 147-152.
47. Van de Wetering M, Oosterwegel M, van NK, Clevers H. (1993). Sox-4, an Sry-like HMG box protein, is a transcriptional activator in lymphocytes. EMBO J 12: 3847-3854. (Pubitemid 23282761)
48. Van Loosdregt J, Vercoulen Y, Guichelaar T, Gent YY, Beekman JM, van Beekum O. (2010). Regulation of Treg functionality by acetylation-mediated Foxp3 protein stabilization. Blood 115: 965-974.
49. Wilson ME, Yang KY, Kalousova A, Lau J, Kosaka Y, Lynn FC. (2005). The HMG box transcription factor Sox4 contributes to the development of the endocrine pancreas. Diabetes 54: 3402-3409. (Pubitemid 43334329)
50. Ziegler EC, Ghosh S. (2005). Regulating inducible transcription through controlled localization. Sci STKE 2005: 1-6.