Loss of Expression and Function of SOCS3 Is an Early Event in HNSCC: Altered Subcellular Localization as a Possible Mechanism Involved in Proliferation, Migration and Invasion

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Rossa, Carlos ^a   Sommer, Gunhild ^b   Spolidorio, Luis C ^a   Rosenzweig, Steven A ^b   Watson, Dennis K ^b   Kirkwood, Keith L ^c  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SMALL INTERFERING RNA; SUPPRESSOR OF CYTOKINE SIGNALING 3;

ARTICLE; CANCER CELL CULTURE; CANCER GRADING; CANCER GROWTH; CANCER INVASION; CANCER SIZE; CARCINOGENESIS; CELL MIGRATION; CELL NUCLEUS; CELL PROLIFERATION; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOMEGALOVIRUS; CYTOPLASM; DYSPLASIA; EPIGENETICS; GENE SILENCING; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; PLASMID; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SUPPRESSOR OF CYTOKINE SIGNALING 3 GENE; TISSUE MICROARRAY; TUMOR SUPPRESSOR GENE; WESTERN BLOTTING;

EID: 84866517656     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0045197     Document Type: Article

References (36)

1. Flowers LO, Johnson HM, Mujtaba MG, Ellis MR, Haider SM, et al. (2004) Characterization of a peptide inhibitor of Janus kinase 2 that mimics suppressor of cytokine signaling 1 function. J Immunol 172: 7510-7518.
2. Waiboci LW, Ahmed CM, Mujtaba MG, Flowers LO, Martin JP, et al. (2007) Both the suppressor of cytokine signaling 1 (SOCS-1) kinase inhibitory region and SOCS-1 mimetic bind to JAK2 autophosphorylation site: implications for the development of a SOCS-1 antagonist. J Immunol 178: 5058-5068.
3. Nicholson SE, De Souza D, Fabri LJ, Corbin J, Willson TA, et al. (2000) Suppressor of cytokine signaling-3 preferentially binds to the SHP-2-binding site on the shared cytokine receptor subunit gp130. Proc Natl Acad Sci U S A 97: 6493-6498.
4. Babon JJ, McManus EJ, Yao S, DeSouza DP, Mielke LA, et al. (2006) The structure of SOCS3 reveals the basis of the extended SH2 domain function and identifies an unstructured insertion that regulates stability. Mol Cell 22: 205-216.
5. Ueki K, Kondo T, Kahn CR, (2004) Suppressor of cytokine signaling 1 (SOCS-1) and SOCS-3 cause insulin resistance through inhibition of tyrosine phosphorylation of insulin receptor substrate proteins by discrete mechanisms. Mol Cell Biol 24: 5434-5446.
6. Kamura T, Sato S, Haque D, Liu L, Kaelin WG Jr, et al. (1998) The Elongin BC complex interacts with the conserved SOCS-box motif present in members of the SOCS, ras, WD-40 repeat, and ankyrin repeat families. Genes Dev 12: 3872-3881.
7. Weber A, Hengge UR, Bardenheuer W, Tischoff I, Sommerer F, et al. (2005) SOCS-3 is frequently methylated in head and neck squamous cell carcinoma and its precursor lesions and causes growth inhibition. Oncogene 24: 6699-6708.
8. Brender C, Lovato P, Sommer VH, Woetmann A, Mathiesen AM, et al. (2005) Constitutive SOCS-3 expression protects T-cell lymphoma against growth inhibition by IFNalpha. Leukemia 19: 209-213.
9. Brender C, Nielsen M, Kaltoft K, Mikkelsen G, Zhang Q, et al. (2001) STAT3-mediated constitutive expression of SOCS-3 in cutaneous T-cell lymphoma. Blood 97: 1056-1062.
10. Sakai I, Takeuchi K, Yamauchi H, Narumi H, Fujita S, (2002) Constitutive expression of SOCS3 confers resistance to IFN-alpha in chronic myelogenous leukemia cells. Blood 100: 2926-2931.
11. Yang SF, Yeh YT, Wang SN, Hung SC, Chen WT, et al. (2008) SOCS-3 is associated with vascular invasion and overall survival in hepatocellular carcinoma. Pathology 40: 558-563.
12. Croker BA, Kiu H, Nicholson SE, (2008) SOCS regulation of the JAK/STAT signalling pathway. Semin Cell Dev Biol 19: 414-422.
13. Schmitz J, Weissenbach M, Haan S, Heinrich PC, Schaper F, (2000) SOCS3 exerts its inhibitory function on interleukin-6 signal transduction through the SHP2 recruitment site of gp130. J Biol Chem 275: 12848-12856.
14. Liang CC, Park AY, Guan JL, (2007) In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nat Protoc 2: 329-333.
15. Sasi W, Jiang WG, Sharma A, Mokbel K, (2010) Higher expression levels of SOCS 1,3,4,7 are associated with earlier tumour stage and better clinical outcome in human breast cancer. BMC Cancer 10: 178.
16. Evans MK, Yu CR, Lohani A, Mahdi RM, Liu X, et al. (2007) Expression of SOCS1 and SOCS3 genes is differentially regulated in breast cancer cells in response to proinflammatory cytokine and growth factor signals. Oncogene 26: 1941-1948.
17. Pierconti F, Martini M, Pinto F, Cenci T, Capodimonti S, et al. (2011) Epigenetic silencing of SOCS3 identifies a subset of prostate cancer with an aggressive behavior. Prostate 71: 318-25.
18. Neuwirt H, Puhr M, Cavarretta IT, Mitterberger M, Hobisch A, et al. (2007) Suppressor of cytokine signalling-3 is up-regulated by androgen in prostate cancer cell lines and inhibits androgen-mediated proliferation and secretion. Endocr Relat Cancer 14: 1007-1019.
19. Tokita T, Maesawa C, Kimura T, Kotani K, Takahashi K, et al. (2007) Methylation status of the SOCS3 gene in human malignant melanomas. Int J Oncol 30: 689-694.
20. He B, You L, Uematsu K, Zang K, Xu Z, et al. (2003) SOCS-3 is frequently silenced by hypermethylation and suppresses cell growth in human lung cancer. Proc Natl Acad Sci U S A 100: 14133-14138.
21. Ogata H, Kobayashi T, Chinen T, Takaki H, Sanada T, et al. (2006) Deletion of the SOCS3 gene in liver parenchymal cells promotes hepatitis-induced hepatocarcinogenesis. Gastroenterology 131: 179-193.
22. Ying M, Li D, Yang L, Wang M, Wang N, et al. (2010) Loss of SOCS3 expression is associated with an increased risk of recurrent disease in breast carcinoma. J Cancer Res Clin Oncol 136: 1617-1626.
23. Baetz A, Koelsche C, Strebovsky J, Heeg K, Dalpke AH, (2008) Identification of a nuclear localization signal in suppressor of cytokine signaling 1. FASEB J 22: 4296-4305.
24. Zou T, Ouyang L, Chen L, Dong W, Qiao H, et al. (2008) The role of microtubule-associated protein 1S in SOCS3 regulation of IL-6 signaling. FEBS Lett 582: 4015-4022.
25. Wang Y, Wen J, Zhang W, (2011) MIIP, a cytoskeleton regulator that blocks cell migration and invasion, delays mitosis, and suppresses tumorogenesis. Curr Protein Pept Sci 12: 68-73.
26. Kuppens IE, (2006) Current state of the art of new tubulin inhibitors in the clinic. Curr Clin Pharmacol 1: 57-70.
27. Chen JY, Chang YL, Yu YC, Chao CC, Kao HW, et al. (2004) Specific induction of the high-molecular-weight microtubule-associated protein 2 (hmw-MAP2) by betel quid extract in cultured oral keratinocytes: clinical implications in betel quid-associated oral squamous cell carcinoma (OSCC). Carcinogenesis 25: 269-276.
28. Liu SY, Chen YT, Tseng MY, Hung CC, Chiang WF, et al. (2008) Involvement of microtubule-associated protein 2 (MAP2) in oral cancer cell motility: a novel biological function of MAP2 in non-neuronal cells. Biochem Biophys Res Commun 366: 520-525.
29. Lee KH, Moon KJ, Kim HS, Yoo BC, Park S, et al. (2008) Increased cytoplasmic levels of CIS, SOCS1, SOCS2, or SOCS3 are required for nuclear translocation. FEBS Lett 582: 2319-2324.
30. Maine GN, Mao X, Komarck CM, Burstein E, (2007) COMMD1 promotes the ubiquitination of NF-kappaB subunits through a cullin-containing ubiquitin ligase. EMBO J 26: 436-447.
31. Ryo A, Suizu F, Yoshida Y, Perrem K, Liou YC, et al. (2003) Regulation of NF-kappaB signaling by Pin1-dependent prolyl isomerization and ubiquitin-mediated proteolysis of p65/RelA. Mol Cell 12: 1413-1426.
32. Meng F, Henson R, Wehbe-Janek H, Smith H, Ueno Y, et al. (2007) The MicroRNA let-7a modulates interleukin-6-dependent STAT-3 survival signaling in malignant human cholangiocytes. J Biol Chem 282: 8256-8264.
33. Aoki Y, Feldman GM, Tosato G, (2003) Inhibition of STAT3 signaling induces apoptosis and decreases survivin expression in primary effusion lymphoma. Blood 101: 1535-1542.
34. Dechow TN, Pedranzini L, Leitch A, Leslie K, Gerald WL, et al. (2004) Requirement of matrix metalloproteinase-9 for the transformation of human mammary epithelial cells by Stat3-C. Proc Natl Acad Sci U S A 101: 10602-10607.
35. Masuda M, Suzui M, Yasumatu R, Nakashima T, Kuratomi Y, et al. (2002) Constitutive activation of signal transducers and activators of transcription 3 correlates with cyclin D1 overexpression and may provide a novel prognostic marker in head and neck squamous cell carcinoma. Cancer Res 62: 3351-3355.
36. Frobose H, Ronn SG, Heding PE, Mendoza H, Cohen P, et al. (2006) Suppressor of cytokine Signaling-3 inhibits interleukin-1 signaling by targeting the TRAF-6/TAK1 complex. Mol Endocrinol 20: 1587-1596.