A short polypeptide from the herpes simplex virus type 2 ICP10 gene can induce antigen aggregation and autophagosomal degradation for enhanced immune presentation

Human Gene Therapy

Volumn 21, Issue 12, 2010, Pages 1687-1696

  Fu, Xinping ^a   Tao, Lihua ^a   Zhang, Xiaoliu ^a,b  

^a University of Houston   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; IMMUNOLOGICAL ADJUVANT; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; OVALBUMIN; POLYPEPTIDE; SIGNAL PEPTIDE; TUMOR ANTIGEN; UNCLASSIFIED DRUG; VIRAL INDUCER OF PROTEIN AGGREGATION;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ANTINEOPLASTIC ACTIVITY; ARTICLE; AUTOPHAGOSOME; CANCER IMMUNIZATION; CARBOXY TERMINAL SEQUENCE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOPLASM; FEMALE; HERPES SIMPLEX VIRUS 2; HUMAN; HUMAN CELL; ICP10 GENE; LYSOSOME; MOUSE; NONHUMAN; PHAGOSOME; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; VIRUS GENE;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, NEOPLASM; AUTOPHAGY; CANCER VACCINES; CERCOPITHECUS AETHIOPS; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HERPESVIRUS 2, HUMAN; HUMANS; LYSOSOMES; MICE; MICE, INBRED C57BL; NEOPLASM TRANSPLANTATION; OVALBUMIN; PEPTIDES; PHAGOSOMES; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT FUSION PROTEINS; RIBONUCLEOTIDE REDUCTASES; TRANSFECTION; TUMOR CELLS, CULTURED; VERO CELLS;

ANIMALIA; HUMAN HERPESVIRUS 2;

EID: 78650155907     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/hum.2010.080     Document Type: Article

References (33)

1. Aurelian, L., Kokuba, H., and Smith, C.C. (1999). Vaccine potential of a herpes simplex virus type 2 mutant deleted in the PK domain of the large subunit of ribonucleotide reductase (ICP10). Vaccine 17, 1951-1963. (Pubitemid 29172365)
2. Bence, N.F., Sampat, R.M., and Kopito, R.R. (2001). Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292, 1552-1555. (Pubitemid 32493425)
3. Carbone, F.R., and Bevan, M.J. (1989). Induction of ovalbumin-specific cytotoxic T cells by in vivo peptide immunization. J. Exp. Med. 169, 603-612. (Pubitemid 19085807)
4. Casanova, G.,Cancela,R.,Alonzo,L.,Benuto, R., Magana Mdel, C., Hurley, D.R., Fishbein, E., Lara, C., Gonzalez, T., Ponce, R., Burnett, J.W., and Calton, G.J. (2002). A double-blind study of the efficacy and safety of the ICP10DPK vaccine against recurrent genital HSV-2 infections. Cutis 70, 235-239. (Pubitemid 41757449)
5. Chabaud, S., Lambert, H., Sasseville, A.M., Lavoie, H., Guilbault, C., Massie, B., Landry, J., and Langelier, Y. (2003). The R1 subunit of herpes simplex virus ribonucleotide reductase has chaperone-like activity similar to Hsp27. FEBS Lett. 545, 213-218. (Pubitemid 36694704)
6. Chabaud, S., Sasseville, A.M., Elahi, S.M., Caron, A., Dufour, F., Massie, B., and Langelier, Y. (2007). The ribonucleotide re-ductase domain of the R1 subunit of herpes simplex virus type 2 ribonucleotide reductase is essential for R1 antiapoptotic function. J. Gen. Virol. 88, 384-394. (Pubitemid 46210875)
7. Chung, T.D., Wymer, J.P., Smith, C.C., Kulka, M., and Aurelian, L. (1989). Protein kinase activity associated with the large subunit of herpes simplex virus type 2 ribonucleotide reduc-tase (ICP10). J. Virol. 63, 3389-3398. (Pubitemid 19181399)
8. Conner, J. (1999). The unique N terminus of herpes simplex virus type 1 ribonucleotide reductase large subunit is phosphory-lated by casein kinase 2, which may have a homologue in Escherichia coli. J. Gen. Virol. 80, 1471-1476. (Pubitemid 29261478)
9. Conner, J., Cooper, J., Furlong, J., and Clements, J.B. (1992). An autophosphorylating but not transphosphorylating activity is associated with the unique N terminus of the herpes simplex virus type 1 ribonucleotide reductase large subunit. J. Virol. 66, 7511-7516.
10. Cooper, J., Conner, J., and Clements, J.B. (1995). Characterization of the novel protein kinase activity present in the R1 subunit of herpes simplex virus ribonucleotide reductase. J. Virol. 69, 4979-4985.
11. Fu, L., Gao, Y.S., and Sztul, E. (2005). Transcriptional repression and cell death induced by nuclear aggregates of non-polyglutamine protein. Neurobiol. Dis. 20, 656-665. (Pubitemid 41619342)
12. Fu, X., Tao, L., Cai, R., Prigge, J., and Zhang, X. (2006). A mutant type 2 herpes simplex virus deleted for the protein kinase domain of the ICP10 gene is a potent oncolytic virus. Mol. Ther. 13, 882-890.
13. Fu, X., Tao, L., and Zhang, X. (2007). An HSV-2-based oncolytic virus deleted in the PK domain of the ICP10 gene is a potent inducer of apoptotic death in tumor cells. Gene Ther. 14, 1218-1225. (Pubitemid 47224553)
14. Gannage, M., and Munz, C. (2009). Autophagy in MHC class II presentation of endogenous antigens. Curr. Top. Microbiol. Immunol. 335, 123-140.
15. Garcia-Mata, R., Bebok, Z., Sorscher, E.J., and Sztul, E.S. (1999). Characterization and dynamics of aggresome formation by a cytosolic GFP-chimera. J. Cell Biol. 146, 1239-1254. (Pubitemid 29477692)
16. Hornung, R.L., Longo, D.L., Bowersox, O.C., and Kwak, L.W. (1995). Tumor antigen-specific immunization of bone marrow transplantation donors as adoptive therapy against established tumor. J. Natl. Cancer Inst. 87, 1289-1296.
17. Johnston, J.A., Ward, C.L., and Kopito, R.R. (1998). Aggresomes: A cellular response to misfolded proteins. J. Cell Biol. 143, 1883-1898. (Pubitemid 29022611)
18. Langelier, Y., Champoux, L., Hamel, M., Guilbault, C., La-marche, N., Gaudreau, P., and Massie, B. (1998). The R1 subunit of herpes simplex virus ribonucleotide reductase is a good substrate for host cell protein kinases but is not itself a protein kinase. J. Biol. Chem. 273, 1435-1443. (Pubitemid 28133664)
19. Langelier, Y., Bergeron, S., Chabaud, S., Lippens, J., Guilbault, C., Sasseville, A.M., Denis, S., Mosser, D.D., and Massie, B. (2002). The R1 subunit of herpes simplex virus ribonucleotide reductase protects cells against apoptosis at, or upstream of, caspase-8 activation. J. Gen. Virol. 83, 2779-2789. (Pubitemid 35276978)
20. Lansbury, P.T., and Lashuel, H.A. (2006). A century-old debate on protein aggregation and neurodegeneration enters the clinic. Nature 443, 774-779. (Pubitemid 44622681)
21. Li, H., Dutuor, A., Fu, X., and Zhang, X. (2007a). Induction of strong antitumor immunity by an HSV-2-based oncolytic virus in a murine mammary tumor model. J. Gene Med. 9, 161-169. (Pubitemid 46523534)
22. Li, H., Dutuor, A., Tao, L., Fu, X., and Zhang, X. (2007b). Virotherapy with a type 2 herpes simplex virus-derived oncolytic virus induces potent antitumor immunity against neuroblastoma. Clin. Cancer Res. 13, 316-322. (Pubitemid 46121885)
23. Link, C.D., Fonte, V., Hiester, B., Yerg, J., Ferguson, J., Csontos, S., Silverman, M.A., and Stein, G.H. (2006). Conversion of green fluorescent protein into a toxic, aggregation-prone protein by C-terminal addition of a short peptide. J. Biol. Chem. 281, 1808-1816.
24. Massie, B., Dionne, J., Lamarche, N., Fleurent, J., and Langelier, Y. (1995). Improved adenovirus vector provides herpes simplex virus ribonucleotide reductase R1 and R2 subunits very efficiently. Biotechnology 13, 602-608.
25. Mizushima, N., and Klionsky, D.J. (2007). Protein turnover via autophagy: Implications for metabolism. Annu. Rev. Nutr. 27, 19-40. (Pubitemid 351373346)
26. Paradis, H., Gaudreau, P., Massie, B., Lamarche, N., Guilbault, C., Gravel, S., and Langelier, Y. (1991). Affinity purification of active subunit 1 of herpes simplex virus type 1 ribonucleotide reductase exhibiting a protein kinase activity. J. Biol. Chem. 266, 9647-9651. (Pubitemid 21906705)
27. Perkins, D., Pereira, E.F., Gober, M., Yarowsky, P.J., and Aur-elian, L. (2002). The herpes simplex virus type 2 R1 protein kinase (ICP10 PK) blocks apoptosis in hippocampal neurons, involving activation of the MEK/MAPK survival pathway. J. Virol. 76, 1435-1449. (Pubitemid 34066444)
28. Schmid, D., Pypaert, M., and Munz, C. (2007). Antigen-loading compartments for major histocompatibility complex class II molecules continuously receive input from autophagosomes. Immunity 26, 79-92. (Pubitemid 46109341)
29. Smith, C.C., Peng, T., Kulka, M., and Aurelian, L. (1998). The PK domain of the large subunit of herpes simplex virus type 2 ribonucleotide reductase (ICP10) is required for immediate-early gene expression and virus growth. J. Virol. 72, 9131-9141. (Pubitemid 28471858)
30. Smith, C.C., Nelson, J., Aurelian, L., Gober, M., and Goswami, B.B. (2000). Ras-GAP binding and phosphorylation by herpes simplex virus type 2 RR1 PK (ICP10) and activation of the Ras/MEK/MAPK mitogenic pathway are required for timely onset of virus growth. J. Virol. 74, 10417-10429.
31. Tanida, I., Ueno, T., and Kominami, E. (2004). LC3 conjugation system in mammalian autophagy. Int. J. Biochem. Cell Biol. 36, 2503-2518. (Pubitemid 39119762)
32. \+ T cell-dependent antitumor immunity by TAT-mediated tumor antigen delivery into dendritic cells. J. Clin. Invest. 109, 1463-1470. (Pubitemid 34596172)
33. You, Z., Hester, J., Rollins, L., Spagnoli, G.C., van der Bruggen, P., and Chen, S.Y. (2001). A retrogen strategy for presentation of an intracellular tumor antigen as an exogenous antigen by dendritic cells induces potent antitumor T helper and CTL responses. Cancer Res. 61, 197-205. (Pubitemid 32095718)