Resistance to UV-induced apoptosis by β-HPV5 E6 involves targeting of activated BAK for proteolysis by recruitment of the HERC1 ubiquitin ligase

International Journal of Cancer

Volumn 136, Issue 12, 2015, Pages 2831-2843

  Holloway, Amy ^a   Simmonds, Mark ^b   Azad, Abul ^a   Fox, Joanna L ^a   Storey, Alan ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

apoptosis; BAK; HERC1; HPV

Indexed keywords

LYSINE; PROTEIN BAK; PROTEIN E6; PROTEIN HERC1; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; E6 PROTEIN, HUMAN PAPILLOMAVIRUS TYPE 5; GUANINE NUCLEOTIDE EXCHANGE FACTOR; HERC1 PROTEIN, HUMAN; ONCOPROTEIN; PROTEIN BINDING;

AMINO ACID SEQUENCE; APOPTOSIS; ARTICLE; BETA HUMAN PAPILLOMAVIRUS TYPE 5; CONTROLLED STUDY; HYDROPHOBICITY; MUTATIONAL ANALYSIS; NON MELANOMA SKIN CANCER; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; SKIN CARCINOGENESIS; ULTRAVIOLET RADIATION; WART VIRUS; FLOW CYTOMETRY; GENETICS; HCT116 CELL LINE; HUMAN; METABOLISM; MUTATION; PHOSPHORYLATION; RADIATION RESPONSE; RNA INTERFERENCE; TUMOR CELL LINE; WESTERN BLOTTING;

APOPTOSIS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BLOTTING, WESTERN; CELL LINE, TUMOR; FLOW CYTOMETRY; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HCT116 CELLS; HUMANS; LYSINE; MUTATION; ONCOGENE PROTEINS, VIRAL; PHOSPHORYLATION; PROTEIN BINDING; PROTEOLYSIS; RNA INTERFERENCE; ULTRAVIOLET RAYS;

EID: 84927578274     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.29350     Document Type: Article

References (48)

1. Pfister H,. Human papillomavirus and skin cancer. J Natl Cancer Inst Monogr 2003; 31: 52-56.
2. Orth G,. Epidermodysplasia verruciformis: a model for understanding the oncogenicity of human papillomaviruses. Ciba Found Symp 1986; 120: 157-174.
3. Asgari MM, Kiviat NB, Critchlow CW, et al. Detection of human papillomavirus DNA in cutaneous squamous cell carcinoma among immunocompetent individuals. J Invest Dermatol 2008; 128: 1409-1417.
4. Harwood CA, Surentheran T, Sasieni P, et al. Increased risk of skin cancer associated with the presence of epidermodysplasia verruciformis human papillomavirus types in normal skin. Br J Dermatol 2004; 150: 949-957.
5. Harwood CA, Surentheran T, McGregor JM, et al. Human papillomavirus infection and non-melanoma skin cancer in immunosuppressed and immunocompetent individuals. J Med Virol 2000; 61: 289-297.
6. Weissenborn S, Neale RE, Waterboer T, et al. Beta-papillomavirus DNA loads in hair follicles of immunocompetent people and organ transplant recipients. Med Microbiol Immunol 2012; 201: 117-125.
7. Neale RE, Weissenborn S, Abeni D, et al. Human papillomavirus load in eyebrow hair follicles and risk of cutaneous squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev 2013; 22: 719-727.
8. Akgul B, Cooke JC, Storey A,. HPV-associated skin disease. J Pathol 2006; 208: 165-175.
9. Marcuzzi GP, Hufbauer M, Kasper HU, et al. Spontaneous tumour development in human papillomavirus type 8 E6 transgenic mice and rapid induction by UV-light exposure and wounding. J Gen Virol 2009; 90: 2855-2864.
10. Storey A,. Papillomaviruses: death-defying acts in skin cancer. Trends Mol Med 2002; 8: 417-421.
11. Tomlins C, Storey A,. Cutaneous HPV5 E6 causes increased expression of Osteoprotegerin and Interleukin 6 which contribute to evasion of UV-induced apoptosis. Carcinogenesis 2010; 31: 2155-2164.
12. Filippova M, Parkhurst L, Duerksen-Hughes PJ,. The human papillomavirus 16 E6 protein binds to Fas-associated death domain and protects cells from Fas-triggered apoptosis. J Biol Chem 2004; 279: 25729-25744.
13. Garnett TO, Filippova M, Duerksen-Hughes PJ,. Accelerated degradation of FADD and procaspase 8 in cells expressing human papilloma virus 16 E6 impairs TRAIL-mediated apoptosis. Cell Death Differ 2006; 13: 1915-1926.
14. Jackson S, Ghali L, Harwood C, Storey A,. Reduced apoptotic levels in squamous but not basal cell carcinomas correlates with detection of cutaneous human papillomavirus. Br J Cancer 2002; 87: 319-323.
15. Youle RJ, Strasser A,. The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 2008; 9: 47-59.
16. Chipuk JE, Fisher JC, Dillon CP, et al. Mechanism of apoptosis induction by inhibition of the anti-apoptotic BCL-2 proteins. Proc Natl Acad Sci USA 2008; 105: 20327-20332.
17. Antonsson B, Montessuit S, Lauper S, et al. Bax oligomerization is required for channel-forming activity in liposomes and to trigger cytochrome c release from mitochondria. Biochem J 2000; 345 (Part 2): 271-278.
18. Wei MC, Lindsten T, Mootha VK, et al. tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 2000; 14: 2060-2071.
19. Underbrink MP, Howie HL, Bedard KM, et al. E6 proteins from multiple human betapapillomavirus types degrade Bak and protect keratinocytes from apoptosis after UVB irradiation. J Virol 2008; 82: 10408-10417.
20. Griffiths GJ, Corfe BM, Savory P, et al. Cellular damage signals promote sequential changes at the N-terminus and BH-1 domain of the pro-apoptotic protein Bak. Oncogene 2001; 20: 7668-7676.
21. Griffiths GJ, Dubrez L, Morgan CP, et al. Cell damage-induced conformational changes of the pro-apoptotic protein Bak in vivo precede the onset of apoptosis. J Cell Biol 1999; 144: 903-914.
22. Dewson G, Kratina T, Czabotar P, et al. Bak activation for apoptosis involves oligomerization of dimers via their alpha6 helices. Mol Cell 2009; 36: 696-703.
23. Dewson G, Kratina T, Sim HW, et al. To trigger apoptosis, Bak exposes its BH3 domain and homodimerizes via BH3:groove interactions. Mol Cell 2008; 30: 369-380.
24. Magal SS, Jackman A, Ish-Shalom S, et al. Downregulation of Bax mRNA expression and protein stability by the E6 protein of human papillomavirus 16. J Gen Virol 2005; 86: 611-621.
25. Jackson S, Harwood C, Thomas M, et al. Role of Bak in UV-induced apoptosis in skin cancer and abrogation by HPV E6 proteins. Genes Dev 2000; 14: 3065-3073.
26. Thomas M, Banks L,. Human papillomavirus (HPV) E6 interactions with Bak are conserved amongst E6 proteins from high and low risk HPV types. J Gen Virol 1999; 80 (Part 6): 1513-1517.
27. Leverrier S, Bergamaschi D, Ghali L, et al. Role of HPV E6 proteins in preventing UVB-induced release of pro-apoptotic factors from the mitochondria. Apoptosis 2007; 12: 549-560.
28. Huibregtse JM, Scheffner M, Howley PM,. Cloning and expression of the cDNA for E6-AP, a protein that mediates the interaction of the human papillomavirus E6 oncoprotein with p53. Mol Cell Biol 1993; 13: 775-784.
29. Thomas M, Pim D, Banks L,. The role of the E6-p53 interaction in the molecular pathogenesis of HPV. Oncogene 1999; 18: 7690-7700.
30. Bedard KM, Underbrink MP, Howie HL, Galloway DA,. The E6 oncoproteins from human betapapillomaviruses differentially activate telomerase through an E6AP-dependent mechanism and prolong the lifespan of primary keratinocytes. J Virol 2008; 82: 3894-3902.
31. Simmonds M, Storey A,. Identification of the regions of the HPV 5 E6 protein involved in Bak degradation and inhibition of apoptosis. Int J Cancer 2008; 123: 2260-2266.
32. Jackson S, Storey A,. E6 proteins from diverse cutaneous HPV types inhibit apoptosis in response to UV damage. Oncogene 2000; 19: 592-598.
33. Hobbs S, Jitrapakdee S, Wallace JC,. Development of a bicistronic vector driven by the human polypeptide chain elongation factor 1alpha promoter for creation of stable mammalian cell lines that express very high levels of recombinant proteins. Biochem Biophys Res Commun 1998; 252: 368-372.
34. Azad A, Fox J, Leverrier S, et al. Blockade of the BAK hydrophobic groove by inhibitory phosphorylation regulates commitment to apoptosis. PLoS One 2012; 7: e49601.
35. Fox JL, Ismail F, Azad A, et al. Tyrosine dephosphorylation is required for Bak activation in apoptosis. EMBO J 2010; 29: 3853-3868.
36. Waterhouse NJ, Trapani JA,. A new quantitative assay for cytochrome c release in apoptotic cells. Cell Death Differ 2003; 10: 853-855.
37. Jiang P, Du W, Heese K, et al. The Bad guy cooperates with good cop p53: bad is transcriptionally up-regulated by p53 and forms a Bad/p53 complex at the mitochondria to induce apoptosis. Mol Cell Biol 2006; 26: 9071-9082.
38. Azad A, Storey A,. BAK multimerization for apoptosis, but not bid binding, is inhibited by negatively charged residue in the BAK hydrophobic groove. Mol Cancer 2013; 12: 65.
39. Gallenne T, Gautier F, Oliver L, et al. Bax activation by the BH3-only protein Puma promotes cell dependence on antiapoptotic Bcl-2 family members. J Cell Biol 2009; 185: 279-290.
40. Pietsch EC, Perchiniak E, Canutescu AA, et al. Oligomerization of BAK by p53 utilizes conserved residues of the p53 DNA binding domain. J Biol Chem 2008; 283: 21294-21304.
41. Tomaic V, Pim D, Thomas M, et al. Regulation of the human papillomavirus type 18 E6/E6AP ubiquitin ligase complex by the HECT domain-containing protein EDD. J Virol 2011; 85: 3120-3127.
42. Kuhnle S, Kogel U, Glockzin S, et al. Physical and functional interaction of the HECT ubiquitin-protein ligases E6AP and HERC2. J Biol Chem 2011; 286: 19410-19416.
43. Warr MR, Acoca S, Liu Z, et al. BH3-ligand regulates access of MCL-1 to its E3 ligase. FEBS Lett 2005; 579: 5603-5608.
44. Zhong Q, Gao W, Du F, et al. Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell 2005; 121: 1085-1095.
45. Kim H, Rafiuddin-Shah M, Tu HC, et al. Hierarchical regulation of mitochondrion-dependent apoptosis by BCL-2 subfamilies. Nat Cell Biol 2006; 8: 1348-1358.
46. Sattler M, Liang H, Nettesheim D, et al. Structure of Bcl-xL-Bak peptide complex: recognition between regulators of apoptosis. Science 1997; 275: 983-986.
47. Cleland MM, Norris KL, Karbowski M, et al. Bcl-2 family interaction with the mitochondrial morphogenesis machinery. Cell Death Differ 2011; 18: 235-247.
48. Chong-Kopera H, Inoki K, Li Y, et al. TSC1 stabilizes TSC2 by inhibiting the interaction between TSC2 and the HERC1 ubiquitin ligase. J Biol Chem 2006; 281: 8313-8316.