Identification of a Src tyrosine kinase/SIAH2 E3 ubiquitin ligase pathway that regulates C/EBPδ expression and contributes to transformation of breast tumor cells

Molecular and Cellular Biology

Volumn 32, Issue 2, 2012, Pages 320-332

  Sarkar, Tapasree Roy ^a   Sharan, Shikha ^a   Wang, Jun ^a,c   Pawara, Snehalata A ^a,d   Cantwell, Carrie A ^a   Johnson, Peter F ^a   Morrison, Deborah K ^a   Wang, Ju Ming ^b   Sterneck, Esta ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^c NEBRASKA MEDICAL CENTER   (United States)

^d UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BOSUTINIB; CCAAT ENHANCER BINDING PROTEIN BETA; CCAAT ENHANCER BINDING PROTEIN DELTA; CYCLIN D1; PROTEIN TYROSINE KINASE; RETINOBLASTOMA PROTEIN; SIAH2 E3 UBIQUITIN LIGASE; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; BREAST CANCER; CELL INVASION; CELL MOTILITY; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSFORMATION; DOWN REGULATION; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SUMOYLATION; UBIQUITINATION;

BREAST; BREAST NEOPLASMS; CCAAT-ENHANCER-BINDING PROTEIN-DELTA; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; CYCLIN D1; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NUCLEAR PROTEINS; RNA, MESSENGER; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84863025642     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.05790-11     Document Type: Article

References (74)

1. Abram CL, Courtneidge SA. 2000. Src family tyrosine kinases and growth factor signaling. Exp. Cell Res. 254:1-13.
2. Adams PD. 2001. Regulation of the retinoblastoma tumor suppressor protein by cyclin/cdks. Biochim. Biophys. Acta 1471:M123-M133.
3. Agrawal S, et al. 2007. The C/EBPδ tumor suppressor is silenced by hypermethylation in acute myeloid leukemia. Blood 109:3895-3905.
4. Ahmed AU, et al. 2008. Effect of disrupting seven-in-absentia homolog 2 function on lung cancer cell growth. J. Natl. Cancer Inst. 100:1606-1629.
5. Albanese C, et al. 1995. Transforming p21ras mutants and c-Ets-2 activate the cyclin D1 promoter through distinguishable regions. J. Biol. Chem. 270:23589-23597.
6. Arias-Romero LE, et al. 2009. Activation of Src by protein tyrosine phosphatase 1B is required for ErbB2 transformation of human breast epithelial cells. Cancer Res. 69:4582-4588.
7. Balamurugan K, et al. 2010. The tumour suppressor C/EBPdelta inhibits FBXW7 expression and promotes mammary tumour metastasis.EMBO J. 29:4106-4117.
8. Barresi V, Vitarelli E, Cerasoli S, Barresi G. 2010. The cell growth inhibitory transcription factor C/EBPδ is expressed in human meningiomas in association with low histological grade and proliferation index. J. Neurooncol. 97:233-240.
9. Bengoechea-Alonso MT, Ericsson J. 2010. The ubiquitin ligase Fbxw7 controls adipocyte differentiation by targeting C/EBPα for degradation. Proc. Natl. Acad. Sci. U. S. A. 107:11817-11822.
10. Bennett HL, Brummer T, Jeanes A, Yap AS, Daly RJ. 2008. Gab2 and Src co-operate in human mammary epithelial cells to promote growth factor independence and disruption of acinar morphogenesis. Oncogene 27: 2693-2704.
11. Bromann PA, Korkaya H, Courtneidge SA. 2004. The interplay between Src family kinases and receptor tyrosine kinases. Oncogene 23:7957-7968.
12. Campone M, et al. 23 June 2011, posting date. Phase II study of singleagent bosutinib, a Src/Abl tyrosine kinase inhibitor, in patients with locally advanced or metastatic breast cancer pretreated with chemotherapy. Ann. Oncol. doi:10.1093/annonc/mdr261.
13. Cantwell CA, Sterneck E, Johnson PF. 1998. Interleukin-6-specific activation of the C/EBPδ gene in hepatocytes is mediated by Stat3 and Sp1. Mol. Cell. Biol. 18:2108-2117.
14. Chan P, et al. 2011. The expression of the ubiquitin ligase SIAH (seven in absentia homolog) 2 is mediated through gene copy number in breast cancer and is associated with a basal-like phenotype and p53 expression. Breast Cancer Res. 13:R19.
15. Coluccia AM, et al. 2006. SKI-606 decreases growth and motility of colorectal cancer cells by preventing pp60(c-Src)-dependent tyrosine phosphorylation of beta-catenin and its nuclear signaling. Cancer Res. 66:2279-2286.
16. Debnath J, Muthuswamy SK, Brugge JS. 2003. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in threedimensional basement membrane cultures. Methods 30:256-268.
17. Denuc A, Marfany G. 2010. SUMO and ubiquitin paths converge. Biochem. Soc. Trans. 38:34-39.
18. Fang S, Weissman AM. 2004. A field guide to ubiquitylation. Cell. Mol. Life Sci. 61:1546-1561.
19. Finn RS. 2008. Targeting Src in breast cancer. Ann. Oncol. 19:1379-1386.
20. Gery S, Tanosaki S, Hofmann WK, Koppel A, Koeffler HP. 2005. C/EBPδ expression in a BCR-ABL-positive cell line induces growth arrest and myeloid differentiation. Oncogene 24:1589-1597.
21. Giunciuglio D, et al. 1995. Invasive phenotype of MCF10A cells overexpressing c-Ha-ras and c-erbB-2 oncogenes. Int. J. Cancer 63:815-822.
22. Golas JM, et al. 2003. SKI-606, a 4-anilino-3-quinolinecarbonitrile dual inhibitor of Src and Abl kinases, is a potent antiproliferative agent against chronic myelogenous leukemia cells in culture and causes regression of K562 xenografts in nude mice. Cancer Res. 63:375-381.
23. Guarino M. 2010. Src signaling in cancer invasion. J. Cell. Physiol. 223: 14-26.
24. Hebbard L, et al. 2011. Control of mammary tumor differentiation by SKI-606 (bosutinib). Oncogene 30:301-312.
25. House CM, et al. 2003. A binding motif for SIAH ubiquitin ligase. Proc. Natl. Acad. Sci. U. S. A. 100:3101-3106.
26. House CM, et al. 2006. Elucidation of the substrate binding site of SIAH ubiquitin ligase. Structure 14:695-701.
27. House CM, Moller A, Bowtell DD. 2009. SIAH proteins: novel drug targets in the Ras and hypoxia pathways. Cancer Res. 69:8835-8838.
28. Huang AM, et al. 2004. Loss of CCAAT/enhancer binding protein delta promotes chromosomal instability. Oncogene 23:1549-1557.
29. Ikezoe T, et al. 2005. CCAAT/enhancer-binding protein delta: a molecular target of 1,25-dihydroxyvitamin D3 in androgen-responsive prostate cancer LNCaP cells. Cancer Res. 65:4762-4768.
30. Irby RB, et al. 1999. Activating SRC mutation in a subset of advanced human colon cancers. Nat. Genet. 21:187-190.
31. Jakobovits EB, Majors JE, Varmus HE. 1984. Hormonal regulation of the Rous sarcoma virus src gene via a heterologous promoter defines a threshold dose for cellular transformation. Cell 38:757-765.
32. Jallal H, et al. 2007. A Src/Abl kinase inhibitor, SKI-606, blocks breast cancer invasion, growth, and metastasis in vitro and in vivo. Cancer Res. 67:1580-1588.
33. Kaplan KB, et al. 1994. Association of the amino-terminal half of c-Src with focal adhesions alters their properties and is regulated by phosphorylation of tyrosine 527. EMBO J. 13:4745-4756.
34. Khurana A, et al. 2006. Regulation of the ring finger E3 ligase SIAH2 by p38 MAPK. J. Biol. Chem. 281:35316-35326.
35. Kim JK, Diehl JA. 2009. Nuclear cyclin D1: an oncogenic driver in human cancer. J. Cell. Physiol. 220:292-296.
36. Kim LC, Song L, Haura EB. 2009. Src kinases as therapeutic targets for cancer. Nat. Rev. Clin. Oncol. 6:587-595.
37. Kitagawa M, et al. 1996. The consensus motif for phosphorylation by cyclin D1-Cdk4 is different from that for phosphorylation by cyclin A/ECdk2. EMBO J. 15:7060-7069.
38. Ko CY, Hsu HC, Shen MR, Chang WC, Wang JM. 2008. Epigenetic silencing of CCAAT/enhancer-binding protein δ activity by YY1/ polycomb group/DNA methyltransferase complex. J. Biol. Chem. 283: 30919-30932.
39. Lehn S, et al. 2010. Down-regulation of the oncogene cyclin D1 increases migratory capacity in breast cancer and is linked to unfavorable prognostic features. Am. J. Pathol. 177:2886-2897.
40. Li Z, et al. 2008. Alternate cyclin D1 mRNA splicing modulates p27KIP1 binding and cell migration. J. Biol. Chem. 283:7007-7015.
41. Li Z, Wang C, Prendergast GC, Pestell RG. 2006. Cyclin D1 functions in cell migration. Cell Cycle 5:2440-2442.
42. Morrison DK, Heidecker G, Rapp UR, Copeland TD. 1993. Identification of the major phosphorylation sites of the Raf-1 kinase. J. Biol. Chem. 268:17309-17316.
43. Naderi A, et al. 2007. A gene-expression signature to predict survival in breast cancer across independent data sets. Oncogene 26:1507-1516.
44. Neve RM, et al. 2006. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 10:515-527.
45. O'Rourke JP, Newbound GC, Hutt JA, DeWille J. 1999. CCAAT/enhancer-binding protein delta regulates mammary epithelial cell G0 growth arrest and apoptosis. J. Biol. Chem. 274:16582-16589.
46. Palmieri D, et al. 2005. Medroxyprogesterone acetate elevation of Nm23-H1 metastasis suppressor expression in hormone receptornegative breast cancer. J. Natl. Cancer Inst. 97:632-642.
47. Pawar SA, et al. 2010. C/EBPδ targets cyclin D1 for proteasome-mediated degradation via induction of CDC27/APC3 expression. Proc. Natl. Acad. Sci. U. S. A. 107:9210-9215.
48. Porter D, et al. 2003. Molecular markers in ductal carcinoma in situ of the breast. Mol. Cancer Res. 1:362-375.
49. Porter DA, et al. 2001. A sage (serial analysis of gene expression) view of breast tumor progression. Cancer Res. 61:5697-5702.
50. Qi J, et al. 2008. The ubiquitin ligase SIAH2 regulates tumorigenesis and metastasis by HIF-dependent and -independent pathways. Proc. Natl. Acad. Sci. U. S. A. 105:16713-16718.
51. Ramji DP, Foka P. 2002. CCAAT/enhancer-binding proteins: structure, function and regulation. Biochem. J. 365:561-575.
52. Reissig D, et al. 2001. Elevated activity and expression of Src-family kinases in human breast carcinoma tissue versus matched non-tumor tissue. J. Cancer Res. Clin. Oncol. 127:226-230.
53. Riley D, Carragher NO, Frame MC, Wyke JA. 2001. The mechanism of cell cycle regulation by v-Src. Oncogene 20:5941-5950.
54. Saad F, Lipton A. 2010. SRC kinase inhibition: targeting bone metastases and tumor growth in prostate and breast cancer. Cancer Treat. Rev. 36: 177-184.
55. Santelli E, et al. 2005. Structural analysis of SIAH1-SIAH-interacting protein interactions and insights into the assembly of an E3 ligase multiprotein complex. J. Biol. Chem. 280:34278-34287.
56. Schmidt RL, et al. 2007. Inhibition of RAS-mediated transformation and tumorigenesis by targeting the downstream E3 ubiquitin ligase seven in absentia homologue. Cancer Res. 67:11798-11810.
57. Shim M, Smart RC. 2003. Lithium stabilizes the CCAAT/enhancerbinding protein alpha (C/EBPα) through a glycogen synthase kinase 3 (GSK3)-independent pathway involving direct inhibition of proteasomal activity. J. Biol. Chem. 278:19674-19681.
58. Silva CM. 2004. Role of STATs as downstream signal transducers in Src family kinase-mediated tumorigenesis. Oncogene 23:8017-8023.
59. Sullivan R, Graham CH. 2007. Hypoxia-driven selection of the metastatic phenotype. Cancer Metastasis Rev. 26:319-331.
60. Tang B, Sivko GS, DeWille J. 2006. Promoter methylation reduces C/EBPδ gene expression in the SUM-52PE human breast cancer cell line and in primary breast tumors. Breast Cancer Res. Treat. 95:161-170.
61. Thangaraju M, et al. 2005. C/EBP delta is a critical regulator of proapoptotic gene expression during mammary gland involution. Development 132:4675-4685.
62. Thomas SM, Brugge JS. 1997. Cellular functions regulated by Src family kinases. Annu. Rev. Cell Dev. Biol. 13:513-609.
63. Vultur A, et al. 2008. SKI-606 (bosutinib), a novel Src kinase inhibitor, suppresses migration and invasion of human breast cancer cells. Mol. Cancer Ther. 7:1185-1194.
64. Wang J, et al. 2010. CCAAT/enhancer binding protein delta (C/EBPδβ, CEBPD)-mediated nuclear import ofFANCD2by IPO4 augments cellular response toDNAdamage. Proc. Natl. Acad. Sci. U. S. A. 107:16131-16136.
65. Wang JM, Ko CY, Chen LC, Wang WL, Chang WC. 2006. Functional role of NF-IL6β and its sumoylation and acetylation modifications in promoter activation of cyclooxygenase 2 gene. Nucleic Acids Res. 34: 217-231.
66. Wheeler DL, Iida M, Dunn EF. 2009. The role of Src in solid tumors. Oncologist 14:667-678.
67. Williams SC, Baer M, Dillner AJ, Johnson PF. 1995. CRP2 (C/EBPβ) contains a bipartite regulatory domain that controls transcriptional activation, DNA binding and cell specificity. EMBO J. 14:3170-3183.
68. Xu Z, Sproul A, Wang W, Kukekov N, Greene LA. 2006. SIAH1 interacts with the scaffold protein POSH to promote JNK activation and apoptosis. J. Biol. Chem. 281:303-312.
69. Yasmeen A, Alachkar A, Dekhil H, Gambacorti-Passerini C, Al Moustafa AE. 2010. Locking Src/Abl tyrosine kinase activities regulate cell differentiation and invasion of human cervical cancer cells expressing E6/E7 oncoproteins of high-risk HPV. J. Oncol. 2010:530130.
70. Yun S, et al. 2008. SIAH proteins induce the epidermal growth factordependent degradation of phospholipase Cepsilon. J. Biol. Chem. 283: 1034-1042.
71. Zhang S, et al. 2011. Combating trastuzumab resistance by targeting SRC, a common node downstream of multiple resistance pathways. Nat. Med. 17:461-469.
72. Zhang Y, Sif S, DeWille J. 2007. The mouse C/EBPdelta gene promoter is regulated by STAT3 and Sp1 transcriptional activators, chromatin remodeling and c-Myc repression. J. Cell Biochem. 102:1256-1270.
73. Zhong Z, et al. 2010. Cyclin D1/cyclin-dependent kinase 4 interacts with filamin A and affects the migration and invasion potential of breast cancer cells. Cancer Res. 70:2105-2114.
74. Zhou S, Dewille JW. 2007. Proteasome-mediated CCAAT/enhancerbinding protein delta (C/EBPδ) degradation is ubiquitin-independent. Biochem. J. 405:341-349.