CYLD: A deubiquitination enzyme with multiple roles in cancer

Future Oncology

Volumn 7, Issue 2, 2011, Pages 285-297

  Massoumi, Ramin ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

breast cancer; cervical cancer; colon cancer; CYLD; deubiquitination; head and neck cancer; multiple myeloma; NF B; prostate cancer; renal cell carcinoma; salivary gland tumor; skin cancer

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL;

BREAST CANCER; BROOKE SYNDROME; CANCER GROWTH; CANCER THERAPY; COLON CARCINOMA; CYLINDROMA; CYLINDROMATOSIS GENE; DEUBIQUITINATION; DNA REPAIR; ENDOCYTOSIS; ENZYME ACTIVITY; HEAD AND NECK CANCER; HUMAN; KIDNEY CARCINOMA; LIVER CELL CARCINOMA; LUNG CANCER; MELANOMA; MULTIPLE MYELOMA; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; REVIEW; SALIVARY GLAND TUMOR; SKIN CANCER; TRICHOEPITHELIOMA; TUMOR GENE; UBIQUITINATION; UTERINE CERVIX CANCER; VIRUS RELEASE;

ANIMALS; HUMANS; NEOPLASMS; NF-KAPPA B; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS; UBIQUITINATION;

EID: 79952152655     PISSN: 14796694     EISSN: 17448301     Source Type: Journal    
DOI: 10.2217/fon.10.187     Document Type: Review

References (84)

1. Pickart CM: Mechanisms underlying ubiquitination. Ann. Rev. Biochem. 70, 503-533 (2001).
2. Weissman AM: Themes and variations on ubiquitylation. Nat. Rev. Mol. Cell Biol. 2, 169-178 (2001).
3. Nijman SMB, Luna-Vargas MPA, Velds A et al.: A genomic and functional inventory of deubiquitinating enzymes. Cell 123, 773-786 (2005).
4. Puente XS, Lopez-Otin C: A genomic analysis of rat proteases and protease inhibitors. Genome Res. 14, 609-622 (2004).
5. Reyes-Turcu FE, Ventii KH, Wilkinson KD: Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Ann. Rev. Biochem. 78, 363-397 (2009).
6. Nanao MH, Tcherniuk SO, Chroboczek J, Dideberg O, Dessen A, Balakirev MY: Crystal structure of human otubain 2. EMBO Rep. 5, 783-788 (2004).
7. Malynn BA, Ma A: A20 takes on tumors: tumor suppression by an ubiquitin-editing enzyme. J. Exp. Med. 206, 977-980 (2009).
8. Hymowitz SG, Wertz IE: A20: from ubiquitin editing to tumor suppression. Nat. Rev. Cancer 10, 332-340 (2010).
9. Amerik AY, Hochstrasser M: Mechanism and function of deubiquitinating enzymes. Biochim. Biophys. Acta 1695, 189-207 (2004).
10. Ventii KH, Wilkinson KD: Protein partners of deubiquitinating enzymes. Biochem. J. 414, 161-175 (2008).
11. Komander D, Reyes-Turcu F, Licchesi JDF, Odenwaelder P, Wilkinson KD, Barford D: Molecular discrimination of structurally equivalent Lys 63-linked and linear polyubiquitin chains. EMBO Rep. 10, 466-473 (2009). •• Crystallization of Lys-63 and linear polyubiquitin chains.
12. Komander D, Lord CJ, Scheel H et al.: The structure of the CYLD USP domain explains its specificity for Lys63-linked polyubiquitin and reveals a B-box module. Mol. Cell 29, 451-464 (2008). • Crystallization of the CYLD ubiquitin-specific protease domain.
13. Trompouki E, Hatzivassiliou E, Tsichritzis T, Farmer H, Ashworth A, Mosialos G: CYLD is a deubiquitinating enzyme that negatively regulates NF-κB activation by TNFR family members. Nature 424, 793-796 (2003).
14. Kovalenko A, Chable-Bessia C, Cantarella G, Israël A, Wallach D, Courtois G: The tumor suppressor CYLD negatively regulates NF-κB signaling by deubiquitination. Nature 424, 801-805 (2003). • One of the first studies demonstrating the inhibition of NF-κB signaling by CYLD.
15. Brummelkamp TR, Nijman SM, Dirac AM, Bernards R: Loss of the cylindromatosis tumor suppressor inhibits apoptosis by activating NF-κB. Nature 424, 797-801 (2003).
16. Sun SC: CYLD: a tumor suppressor deubiquitinase regulating NF-κB activation and diverse biological processes. Cell Death Diff. 17, 25-34 (2010).
17. Courtois G: Tumor suppressor CYLD: negative regulation of NF-κB signaling and more. Cell. Mol. Life Sci. 65, 1123-1132 (2008).
18. Massoumi R: Ubiquitin chain cleavage: CYLD at work. Trends Biochem. Sci. 35, 392-399 (2010).
19. Sönnichsen B, Koski LB, Walsh A et al.: Full-genome RNAi profiling of early embryogenesis in Caenorhabditis elegans. Nature 434, 462-469 (2005).
20. Kamath RS, Fraser AG, Dong Y et al.: Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421, 231-237 (2003).
21. Tsichritzis T, Gaentzsch PC, Kosmidis S et al.: A Drosophila ortholog of the human cylindromatosis tumor suppressor gene regulates triglyceride content and antibacterial defense. Development 134, 2605-2614 (2007).
22. Xue L, Igaki T, Kuranaga E, Kanda H, Miura M, Xu T: Tumor suppressor CYLD regulates JNK-induced cell death in Drosophila. Dev. Cell 13, 446-454 (2007).
23. Hövelmeyer N, Wunderlich FT, Massoumi R et al.: Regulation of B-cell homeostasis and activation by the tumor suppressor gene CYLD. J. Exp. Med. 204, 2615-2627 (2007).
24. Trompouki E, Tsagaratou A, Kosmidis SK et al.: Truncation of the catalytic domain of the cylindromatosis tumor suppressor impairs lung maturation. Neoplasia 11, 469-476 (2009).
25. Gao J, Huo L, Sun X et al.: The tumor suppressor CYLD regulates microtubule dynamics and plays a role in cell migration. J. Biol. Chem. 283, 8802-8809 (2008).
26. Wickström SA, Masoumi KC, Khochbin S, Fässler R, Massoumi R: CYLD negatively regulates cell-cycle progression by inactivating HDAC6 and increasing the levels of acetylated tubulin. EMBO J. 29, 131-144 (2010).
27. Sun L, Gao J, Huo L et al.: Tumor suppressor CYLD is a negative regulator of the mitotic kinase Aurora-B. J. Pathol. 221, 425-432 (2010).
28. Regamey A, Hohl D, Liu JW et al.: The tumor suppressor CYLD interacts with TRIP and regulates negatively nuclear factor κB activation by tumor necrosis factor. J. Exp. Med. 198, 1959-1964 (2003).
29. Reiley W, Zhang M, Sun W: Negative regulation of JNK signaling by the tumor suppressor CYLD. J. Biol. Chem. 279, 55161-55167 (2004). • One of the first studies demonstrating the inhibition of JNK signaling by CYLD.
30. Xue L, Igaki T, Kuranaga E, Kanda H, Miura M, Xu T: Tumor suppressor CYLD regulates JNK-Induced cell death in Drosophila. Dev. Cell 13, 446-454 (2007).
31. Koga T, Lim JH, Jono H et al.: Tumor suppressor cylindromatosis acts as a negative regulator for Streptococcus pneumoniae-induced NFAT signaling. J. Biol. Chem. 283, 12546-12554 (2008).
32. Lim JH, Stirling B, Derry J et al.: Tumor suppressor CYLD regulates acute lung injury in lethal Streptococcus pneumoniae infections. Immunity 27, 349-360 (2007).
33. Zhang M, Wu X, Lee AJ et al.: Regulation of IκB kinase-related kinases and antiviral responses by tumor suppressor CYLD. J. Biol. Chem. 283, 18621-18626 (2008).
34. Friedman CS, O'Donnell MA, Legarda-Addison D et al.: The tumor suppressor CYLD is a negative regulator of RIG-I-mediated antiviral response. EMBO Rep. 9, 930-936 (2008).
35. Stegmeier F, Sowa ME, Nalepa G, Gygi SP, Harper JW, Elledge SJ: The tumor suppressor CYLD regulates entry into mitosis. Proc. Natl Acad. Sci. USA 104, 8869-8874 (2007).
36. Bignell GR, Warren W, Seal S et al.: Identification of the familial cylindromatosis tumor-suppressor gene. Nat. Genet. 25, 160-165 (2000). •• Identification of CYLD mutations in familial cylindromatosis.
37. Nakayama K: Growth and progression of melanoma and non-melanoma skin cancers regulated by ubiquitination. Pigment Cell Melanoma Res. 23, 338-351 (2010).
38. Young AL, Kellermayer R, Szigeti R, Tészás A, Azmi S, Celebi JT: CYLD mutations underlie Brooke-Spiegler, familial cylindromatosis, and multiple familial trichoepithelioma syndromes. Clin. Genet. 70, 246-249 (2006).
39. Lee DA, Grossman ME, Schneiderman P, Celebi JT: Genetics of skin appendage neoplasms and related syndromes. J. Med. Genet. 42, 811-819 (2005).
40. Salhi A, Bornholdt D, Oeffner F et al.: Multiple familial trichoepithelioma caused by mutations in the cylindromatosis tumor suppressor gene. Cancer Res. 64, 5113-5117 (2004).
41. Zhang G, Huang Y, Yan K et al.: Diverse phenotype of Brooke-Spiegler syndrome associated with a nonsense mutation in the CYLD tumor suppressor gene. Exp. Dermatol. 15, 966-970 (2006).
42. Massoumi R, PM Fässler R, Paus R: Cylindroma as tumor of hair follicle origin. J. Invest. Dermatol. 126, 1182-1184 (2006).
43. Massoumi R, Chmielarska K, Hennecke K, Pfeifer A, Fässler R: CYLD inhibits tumor cell proliferation by blocking Bcl-3-dependent NF-κB signaling. Cell 125, 665-677 (2006). • Highlights the relevance of Bcl-3 activation in CYLD-knockout papilloma and human cylindroma.
44. Tauriello DV, Haegebarth A, Kuper I et al.: Loss of the tumor suppressor CYLD enhances Wnt/β-catenin signaling through K63-linked ubiquitination of Dvl. Mol. Cell 37, 607-619 (2010). • Highlights the relevance of β-catenin and Wnt signaling in human cylindroma.
45. MacDonald BT, Tamai K, He X: Wnt/β-catenin signaling: components, mechanisms, and diseases. Dev. Cell 17, 9-26 (2009).
46. Chin L: The genetics of malignant melanoma: lessons from mouse and man. Nat. Rev. Cancer 3, 559-570 (2003).
47. Massoumi R, Kuphal S, Hellerbrand C et al.: Downregulation of CYLD expression by Snail promotes tumor progression in malignant melanoma. J. Exp. Med. 206, 221-232 (2009).
48. Salama AR, Ord RA: Clinical implications of the neck in salivary gland disease. Oral Maxillofac. Surg. Clin. North Am. 20, 445-458 (2008).
49. Choi HR, Batsakis JG, Callender DL et al.: Molecular analysis of chromosome 16q regions in dermal analogue tumors of salivary glands: a genetic link to dermal cylindroma? Am. J. Surg. Pathol. 26, 778-783 (2002).
50. Fukuda M, Fukuda F, Horiuchi Y et al.: Expression of CYLD, NF-κB and NF-κB-related factors in salivary gland tumors. In Vivo 20, 467-472 (2006).
51. Fukuda M, Hiroi M, Suzuki S, Ohmori Y, Sakashita H: Loss of CYLD might be associated with development of salivary gland tumors. Oncol. Rep. 19, 1421-1427 (2008).
52. Vu HL, Sikora AG, Fu S, Kao J: HPV-induced oropharyngeal cancer, immune response and response to therapy. Cancer Lett. 288, 149-155 (2009).
53. An J, Mo D, Liu H et al.: Inactivation of the CYLD deubiquitinase by HPV E6 mediates hypoxia-induced NF-κB activation. Cancer Cell 14, 394-407 (2008). • Proteasomal-mediated ubiquitination of CYLD by human papillomavirus under hypoxia.
54. Parkin DM, Bray F: Chapter 2: the burden of HPV-related cancers. Vaccine 24(Suppl. 3), S3/11-S25 (2006).
55. Woodman CBJ, Collins SI, Young LS: The natural history of cervical HPV infection: unresolved issues. Nat. Rev. Cancer 7, 11-22 (2007).
56. Hirai Y, Kawamata Y, Takeshima N et al.: Conventional and array-based comparative genomic hybridization analyses of novel cell lines harboring HPV18 from glassy cell carcinoma of the uterine cervix. Int. J. Oncol. 24, 977-986 (2004).
57. Arsura M, Cavin LG: Nuclear factor-κB and liver carcinogenesis. Cancer Lett. 229, 157-169 (2005).
58. Lind DS, Hochwald SN, Malaty J et al.: Nuclear factor-κB is upregulated in colorectal cancer. Surgery 130, 363-369 (2001).
59. Hellerbrand C, Bumes E, Bataille F, Dietmaier W, Massoumi R, Bosserhoff AK: Reduced expression of CYLD in human colon and hepatocellular carcinomas. Carcinogenesis 28, 21-27 (2007).
60. Chu L, Gu J, He Z, Xiao T, Liu X: Adenoviral vector expressing CYLD augments antitumor activity of TRAIL by suppression of NF-κB survival signaling in hepatocellular carcinoma. Cancer Biol. Ther. 5, 615-622 (2006).
61. Zhang J, Stirling B, Temmerman ST et al.: Impaired regulation of NF-κB and increased susceptibility to colitis-associated tumorigenesis in CYLD-deficient mice. J. Clin. Invest. 116, 3042-3049 (2006). • Development of colon cancer in CYLD-deficient animals.
62. Hideshima T, Mitsiades C, Tonon G, Richardson PG, Anderson KC: Understanding multiple myeloma pathogenesis in the bone marrow to identify new therapeutic targets. Nat. Rev. Cancer 7, 585-598 (2007).
63. Neri A, Chang CC, Lombardi L et al.: B-cell lymphoma-associated chromosomal translocation involves candidate oncogene lyt-10, homologous to NF-κB p50. Cell 67, 1075-1087 (1991).
64. Neri A, Fracchiolla NS, Roscetti E et al.: Molecular analysis of cutaneous B- and T-cell lymphomas. Blood 86, 3160-3172 (1995).
65. Migliazza A, Lombardi L, Rocchi M et al.: Heterogeneous chromosomal aberrations generate 3′ truncations of the NFKB2/lyt-10 gene in lymphoid malignancies. Blood 84, 3850-3860 (1994).
66. Annunziata CM, Davis RE, Demchenko Y et al.: Frequent engagement of the classical and alternative NF-κB pathways by diverse genetic abnormalities in multiple myeloma. Cancer Cell 12, 115-130 (2007).
67. Keats JJ, Fonseca R, Chesi M et al.: Promiscuous mutations activate the noncanonical NF-κB pathway in multiple myeloma. Cancer Cell 12, 131-144 (2007).
68. Sun S, Schiller JH, Gazdar AF: Lung cancer in never smokers - a different disease. Nat. Rev. Cancer 7, 778-790 (2007).
69. Zhong S, Fields CR, Su N, Pan YX, Robertson KD: Pharmacologic inhibition of epigenetic modifications, coupled with gene expression profiling, reveals novel targets of aberrant DNA methylation and histone deacetylation in lung cancer. Oncogene 26, 2621-2634 (2007).
70. Weigelt B, Peterse JL, van't Veer LJ: Breast cancer metastasis: markers and models. Nat. Rev. Cancer 5, 591-602 (2005).
71. Wang L, Baiocchi RA, Pal S, Mosialos G, Caligiuri M, Sif S: The BRG1-and hBRM-associated factor BAF57 induces apoptosis by stimulating expression of the cylindromatosis tumor suppressor gene. Mol. Cell. Biol. 25, 7953-7965 (2005).
72. Reiley W, Zhang M, Wu X, Granger E, Sun S-C: Regulation of the deubiquitinating enzyme CYLD by IκB kinase γ-dependent phosphorylation. Mol. Cell. Biol. 25, 3886-3895 (2005). • Phosphorylation of CYLD by IKK, which causes dissociation from the TNF receptor-associated factor 2 and NF-κB essential modifier complexes.
73. Hutti JE, Shen RR, Abbott DW et al.: Phosphorylation of the tumor suppressor CYLD by the breast cancer oncogene IKK-e promotes cell transformation. Mol. Cell 34, 461-472 (2009). • IKK-ε-induced tumorigenesis through phosphorylation and inactivation of CYLD.
74. Boehm JS, Zhao JJ, Yao J et al.: Integrative genomic approaches identify IKBKE as a breast cancer oncogene. Cell 129, 1065-1079 (2007).
75. Cohen HT, McGovern FJ: Renal-cell carcinoma. N. Engl. J. Med. 353, 2477-2490 (2005).
76. Strobel P, Zettl A, Ren Z et al.: Spiradenocylindroma of the kidney: clinical and genetic findings suggesting a role of somatic mutation of the CYLD1 gene in the oncogenesis of an unusual renal neoplasm. Am. J. Surg. Pathol. 26, 119-124 (2002).
77. Long RJ, Roberts KP, Wilson MJ, Ercole CJ, Pryor JL Long RJ: Prostate cancer: a clinical and basic science review. J. Androl. 18, 15-20 (1997).
78. Robertson KD: DNA methylation and chromatin - unraveling the tangled web. Oncogene 21, 5361-5379 (2002).
79. Bird A: DNA methylation patterns and epigenetic memory. Genes Dev. 16, 6-21 (2002).
80. Ullrich A, Schlessinger J: Signal transduction by receptors with tyrosine kinase-activity. Cell 61, 203-212 (1990).
81. Smirnoff P, Liel Y, Gnainsky J, Shany S, Schwartz B: The protective effect of estrogen against chemically induced murine colon carcinogenesis is associated with decreased CpG island methylation and increased mRNA and protein expression of the colonic vitamin D receptor. Oncol. Res. 11, 255-264 (1999).
82. Badia E, Duchesne M-J, Semlali A et al.: Long-term hydroxytamoxifen treatment of an MCF-7-derived breast cancer cell line irreversibly inhibits the expression of estrogenic genes through chromatin remodeling. Cancer Res. 60, 4130-4138 (2000).
83. Kikuno N, Shiina H, Urakami S et al.: Genistein mediated histone acetylation and demethylation activates tumor suppressor genes in prostate cancer cells. Int. J. Cancer 123, 552-560 (2008).
84. STRING - known and predicted protein-protein interactions http://string.embl.de