Transglutaminase 2 inhibits Rb binding of human papillomavirus E7 by incorporating polyamine

EMBO Journal

Volumn 22, Issue 19, 2003, Pages 5273-5282

  Jeon, Ju Hong ^a   Choi, Kyung Ho ^a   Cho, Sung Yup ^a   Kim, Chai Wan ^a   Shin, Dong Myung ^a   Kwon, Joon Cheol ^a   Song, Kye Yong ^a,b   Park, Sang Chul ^a   Kim, In Gyu ^a  

^a Seoul National University College of Medicine   (South Korea)

^b Chung Ang University College of Medicine   (South Korea)

Author keywords

Host virus interaction; Human papillomavirus E7 oncoprotein; Polyamination; Transglutaminase 2

Indexed keywords

ONCOPROTEIN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; RETINOBLASTOMA PROTEIN; VIRUS PROTEIN;

AMINATION; ANIMAL CELL; ARTICLE; CELL STRAIN 3T3; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; VIRUS CELL INTERACTION; VIRUS INHIBITION; WART VIRUS;

DNA-BINDING PROTEINS; GTP-BINDING PROTEINS; HUMANS; ONCOGENE PROTEINS, VIRAL; POLYAMINES; RETINOBLASTOMA PROTEIN; TRANSGLUTAMINASES;

ANIMALIA; HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPE 18; HUMAN PAPILLOMAVIRUS TYPES; PAPILLOMAVIRUS;

EID: 0141864664     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg495     Document Type: Article

References (41)

1. Amendola, A., Gougeon, M.L., Poccia, F., Bondurand, A., Fesus, L. and Piacentini, M. (1996) Induction of 'tissue' transglutaminase in HIV-pathogenesis: evidence for high rate of apoptosis of CD4+ T lymphocytes and accessory cells in lymphoid tissues. Proc. Natl Acad. Sci. USA, 93, 11057-11062.
2. Baek, K.J., Kang, S., Damron, D. and Im, M. (2001) Phospholipase Cdelta1 is a guanine nucleotide exchanging factor for transglutaminase II (Galpha h) and promotes alpha 1B-adrenoreceptor-mediated GTP binding and intracellular calcium release. J. Biol. Chem., 276, 5591-5597.
3. Ballestar, E., Abad, C. and Franco, L. (1996) Core histones are glutaminyl substrates for tissue transglutaminase. J. Biol. Chem., 271, 18817-18824.
4. Boehm, J.E., Singh, U., Combs, C., Antonyak, M.A. and Cerione, R.A. (2002) Tissue transglutaminase protects against apoptosis by modifying the tumor suppressor protein p110 Rb. J. Biol. Chem., 277, 20127-20130.
5. Brehm, A., Nielsen, S.J., Miska, E.A., McCance, D.J., Reid, J.L., Bannister, A.J. and Kouzarides, T. (1999) The E7 oncoprotein associates with Mi2 and histone deacetylase activity to promote cell growth. EMBO J., 18, 2449-2458.
6. Clifford, G.M., Smith, J.S., Plummer, M., Munoz, N. and Franceschi, S. (2003) Human papillomavirus types in invasive cervical cancer worldwide: a meta-analysis. Br. J. Cancer, 88, 63-73.
7. Cordella-Miele, E., Miele, L., Beninati, S. and Mukherjee, A.B. (1993) Transglutaminase-catalyzed incorporation of polyamines into phospholipase A2. J. Biochem., 113, 164-173.
8. De Laurenzi, V. and Melino, G. (2001) Gene disruption of tissue transglutaminase. Mol. Cell. Biol., 21, 148-155.
9. Feng, J.F., Rhee, S.G. and Im, M.J. (1996) Evidence that phospholipase deltal is the effector in the Gh (transglutaminase II)-mediated signaling. J. Biol. Chem., 271, 16451-16454.
10. Fesus, L. and Piacentini, M. (2002) Transglutaminase 2: an enigmatic enzyme with diverse functions. Trends Biochem. Sci., 27, 534-539.
11. Folk, J.E. (1980) Transglutaminases. Annu. Rev. Biochem., 49, 517-531.
12. Fujikawa, K., Furuse, M., Uwabe, K., Maki, H. and Yoshie, O. (1994) Nuclear localization and transforming activity of human papillomavirus type 16 E7-beta-galactosidase fusion protein: characterization of the nuclear localization sequence. Virology, 204, 789-793.
13. Grenard, P., Bates, M.K. and Aeschlimann, D. (2001) Evolution of transglutaminase genes: identification of a transglutaminase gene cluster on human chromosome 15q15. Structure of the gene encoding transglutaminase X and a novel gene family member, transglutaminase Z. J. Biol. Chem., 276, 33066-33078.
14. Grootjans, J.J., Groenen, P.J. and de Jong, W.W. (1995) Substrate requirements for transglutaminases. Influence of the amino acid residue preceding the amine donor lysine in a native protein. J. Biol. Chem., 270, 22855-22858.
15. Hammad, S.M., Ranganathan, S., Loukinova, E., Twal, W.O. and Argraves, W.S. (1997) Interaction of apolipoprotein J-amyloid beta-peptide complex with low density lipoprotein receptor-related protein-2/megalin. J. Biol. Chem., 272, 18644-18649.
16. Heck, D.V., Yee, C.L., Howley, P.M. and Munger, K. (1992) Efficiency of binding the retinoblastoma protein correlates with the transforming capacity of the E7 oncoproteins of the human papillomaviruses. Proc. Natl Acad. Sci. USA, 89, 4442-4446.
17. Huang, P.S., Patrick, D.R., Edwards, G., Goodhart, P.J., Huber, H.E., Miles, L., Garsky, V.M., Oliff, A. and Heimbrook, D.C. (1993) Protein domains governing interactions between E2F, the retinoblastoma gene product, and human papillomavirus type 16 E7 protein. Mol. Cell. Biol., 13, 953-960.
18. Jeon, J.H., Cho, S.Y., Kim, C.W., Shin, D.M., Kweon, J.C., Choi, K.H., Park, S.C. and Kim, I.G. (2002a) GTP is required to stabilize and display transamidation activity of transglutaminase 2. Biochem. Biophys. Res. Commun., 294, 818-822.
19. Jeon, J.H., Cho, S.Y., Kim, C.W., Shin, D.M., Kwon, J.C., Choi, K.H. and Kim, I.G. (2002b) Improved immunodetection of human papillomavirus E7, Exp. Mol. Med., 34, 481-484.
20. Jeon, J.H., Kim, C.W., Shin, D.M., Kim, K.I., Cho, S.Y., Kwon, J.C., Choi, K.H., Kang, H.S. and Kim, I.G. (2003) Differential incorporation of biotinylated polyamines by transglutaminase 2. FEBS Lett., 534, 180-184.
21. Lam, E.W., Morris, J.D., Davies, R., Crook, T., Watson, R.J. and Vousden, K.H. (1994) HPV16 E7 oncoprotein deregulates B-myb expression: correlation with targeting of p107/E2F complexes. EMBO J., 13, 871-878.
22. Lee, J.O., Russo, A.A. and Pavletich, N.P. (1998) Structure of the retinoblastoma tumour-suppressor pocket domain bound to a peptide from HPV E7. Nature, 391, 859-865.
23. Lesort, M., Attanavanich, K., Zhang, J. and Johnson, G.V. (1998) Distinct nuclear localization and activity of tissue transglutaminase. J. Biol. Chem., 273, 11991-11994.
24. Liu, S., Cerione, R.A. and Clardy, J. (2002) Structural basis for the guanine nucleotide-binding activity of tissue transglutaminase and its regulation of transamidation activity. Proc. Natl Acad. Sci. USA, 99, 2743-2747.
25. Lorand, L. and Graham, R.M. (2003) Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat. Rev. Mol. Cell Biol., 4, 140-156.
26. Lu, W., Strohecker, A. and Ou, J.H. (2001) Post-translational modification of the hepatitis C virus core protein by tissue transglutaminase. J. Biol. Chem., 276, 47993-47999.
27. Massimi, P., Pim, D. and Banks, L. (1997) Human papillomavirus type 16 E7 binds to the conserved carboxy-terminal region of the TATA box binding protein and this contributes to E7 transforming activity. J. Gen. Virol., 78, 2607-2613.
28. Munger, K. and Halpern, A.L. (1997) HPV16 E7: primary structure and biological properties. In Human Papillomaviruses 1997 Compendium, Part III, pp. 17-36. [Online]. The human papillomaviruses compendium on line: http://hpv-web.lan1.gov
29. Munger, K. and Howley, P.M. (2002) Human papillomavirus immortalization and transformation functions. Virus Res., 89, 213-228.
30. Munger, K., Basile, J.R., Duensing, S., Eichten, A., Gonzalez, S.L., Grace, M. and Zacny, V.L. (2001) Biological activities and molecular targets of the human papillomavirus E7 oncoprotein. Oncogene, 20, 7888-7898.
31. Nanda, N., Iismaa, S.E., Owens, W.A., Husain, A., Mackay, F. and Graham, R.M. (2001) Targeted inactivation of Gh/tissue transglutaminase II. J. Biol. Chem., 276, 20673-20678.
32. Park, J.S., Kim, E.J., Kwon, H.J., Hwang, E.S., Namkoong, S.E. and Um, S.J. (2000) Inactivation of interferon regulatory factor-1 tumor suppressor protein by HPV E7 oncoprotein. Implication for the E7-mediated immune evasion mechanism in cervical carcinogenesis. J. Biol. Chem., 275, 6764-6769.
33. Pastor, M.T., Diez, A., Perez-Paya, E. and Abad, C. (1999) Addressing substrate glutamine requirements for tissue transglutaminase using substance P analogues. FEBS Lett., 451, 231-234.
34. Peng, X., Zhang, Y., Zhang, H., Graner, S., Williams, J.F., Levitt, M.L. and Lokshin, A. (1999) Interaction of tissue transglutaminase with nuclear transport protein importin-alpha3. FEBS Lett., 446, 35-39.
35. Romanczuk, H. and Howley, P.M. (1992) Disruption of either the E1 or the E2 regulatory gene of human papillomavirus type 16 increases viral immortalization capacity. Proc. Natl Acad. Sci. USA, 89, 3159-3163.
36. Sang, B.C. and Barbosa, M.S. (1992) Single amino acid substitutions in 'low-risk' human papillomavirus (HPV) type 6 E7 protein enhance features characteristic of the 'high-risk' HPV E7 oncoproteins. Proc. Natl Acad. Sci. USA, 89, 8063-8067.
37. Tucholski, J., Kuret, J. and Johnson, G.V. (1999) Tau is modified by tissue transglutaminase in situ: possible functional and metabolic effects of polyamination. J. Neurochem., 73, 1871-1880.
38. Woodman, C.B., Collins, S., Winter, H., Bailey, A., Ellis, J., Prior, P., Yates, M., Rollason, T.P. and Young, L.S. (2001) Natural history of cervical human papillomavirus infection in young women: a longitudinal cohort study. Lancet, 357, 1831-1836.
39. Zhang, J., Kang, D.E., Xia, W., Okochi, M., Mori, H., Selkoe, D.J. and Koo, E.H. (1998) Subcellular distribution and turnover of presenilins in transfected cells. J. Biol. Chem., 273, 12436-12442.
40. Zwerschke, W., Mazurek, S., Massimi, P., Banks, L., Eigenbrodt, E. and Jansen-Durr, P. (1999) Modulation of type M2 pyruvate kinase activity by the human papillomavirus type 16 E7 oncoprotein. Proc. Natl Acad. Sci. USA., 96, 1291-1296.
41. Zwerschke, W., Mannhardt, B., Massimi, P., Nauenburg, S., Pim, D., Nickel, W., Banks, L., Reuser, A.J. and Jansen-Durr, P. (2000) Allosteric activation of acid alpha-glucosidase by the human papillomavirus E7 protein. J. Biol. Chem., 275, 9534-9541.