The protein kinase activity of the large subunit of herpes simplex virus type 2 ribonucleotide reductase (ICP10) fused to the extracellular domain of the epidermal growth factor receptor is ligand-inducible

Virology

Volumn 217, Issue 2, 1996, Pages 425-434

  Smith, C C ^a,b   Luo, J H ^c   Aurelian, L ^a,b  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b DEPARTMENT OF PATHOLOGY   (United States)

^c Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; PROTEIN KINASE; RIBONUCLEOTIDE REDUCTASE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME ACTIVITY; HERPES SIMPLEX VIRUS 2; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; VIROGENESIS;

3T3 CELLS; ANIMALS; CELL COMPARTMENTATION; CELL MEMBRANE; ENZYME ACTIVATION; EPIDERMAL GROWTH FACTOR; GTPASE-ACTIVATING PROTEINS; HERPESVIRUS 2, HUMAN; MICE; PROTEIN-SERINE-THREONINE KINASES; PROTEINS; RAS GTPASE-ACTIVATING PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECOMBINANT FUSION PROTEINS; RECOMBINANT PROTEINS; RIBONUCLEOTIDE REDUCTASES; SIGNAL TRANSDUCTION;

EID: 0029876531     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1006/viro.1996.0136     Document Type: Article

References (65)

1. Ali, M., McWheeney, D., Milosavljevic., A., Jurka, J., and Jariwalla, R. J. (1991). Enhanced malignant transformation induced by expression of a distinct protein domain of ribonucleotide reductase large subunit from herpes simplex virus type 2. Proc. Natl. Acad. Sci. USA 88, 8257-8261.
2. Ali, M. A. (1995). The 140-kDa RR1 protein from both HSV-1 and HSV-2 contains an intrinsic protein kinase activity capable of autophosphorylation but it is transphosphorylation defective. Virology 207, 409-416.
3. Anderson, K. P., Frink, R. J., Devi, G. B., Gaylord, B. H., Costa, R. H., and Wagner, E. K. (1981). Detailed characterization of the mRNA mapping in the HindIII fragment K region of the herpes simplex virus type 1 genome. J. Virol. 37, 1011-1027.
4. Averett, D. R., Lubbers, C., Elion, G. B., and Spector, T. (1983). Ribonucleotide reductase induced by herpes simplex virus type 1 virus. J. Biol. Chem. 258, 9831-9838.
5. Aurelian, L., Terzano, P., Smith, C. C., Chung, T. C., Shamsuddin, A., Costa, S., and Orlandi, C. (1989). Amino terminal epitope of herpes simplex virus type 2 ICP10 protein as a molecular diagnostic marker for cervical intraepithelial neoplasia. In "Cancer Cells," Vol. 7, "Molecular Diagnostics of Human Cancer," pp. 187-191. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
6. Chardin, P., Carnonis, J. H., Gale, N. W., Van Aelst, L., Schlesinger, J., Wilier, M. H., Bar-Sagi, D. (1993). Human Sos1 - A guanine nucleotide exchange factor for ras that binds to Grb2. Science 260, 1338-1343.
7. Chung, T. C., Luo, J. H., Wymer, J. P., Smith, C. C., and Aurelian, L. (1991). Leucine repeats in the large subunit of herpes simplex virus type 2 (HSV-2) ribonucleotide reductase (ICP10) are involved in RR activity and subunit complex formation. J. Gen. Virol. 72, 1139-1144.
8. Chung, T. D., Wymer, J. P., Kulka, M., Smith, C. C., and Aurelian, L. (1989). Protein kinase activity associated with the large subunit of the herpes simplex virus type 2 ribonucleotide reductase (ICP1). J. Virol. 63, 3389-3398.
9. Chung, T. D., Wymer, J. P., Kulka, M., Smith, C. C., and Aurelian, L. (1990). Myristylation and polylysine-mediated activation of the protein kinase domain of the large subunit of herpes simplex virus type 2 ribonucleotide reductase (ICP10). Virology 179, 168-178.
10. Cohen, J. C., Henry, B. E., Randall, C. C., and O'Callaghan, D. (1977). Ribonucleotide reductase activity in hydroxyurea-resistant herpesvirus replication. Proc. Soc. Exp. Biol. Med. 155, 395-399.
11. 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.
12. 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.
13. Davison, A. J., and Scott, J. E. (1986). The complete DNA sequence of varicella-zoster virus. J. Gen. Virol. 67, 1759-1816.
14. Di Fiore, P. P., Segato, O., Taylor, W. G., Aaronson, S. A., and Pierce, J. H. (1990). EGF receptor and erbB-2 tyrosine kinase domains confer cell specificity for mitogenic signaling. Science 248, 79-83.
15. Dutia, B. M. (1983). Ribonucleotide reductase induced by herpes simplex virus has a virus-specified constituent. J. Gen. Virol. 64, 513-521.
16. Ellis, L., Morgan, D. O., Jong, S. M., Wang, L. H., Roth, R. A., and Rutter, W. J. (1987). Heterologous transmembrane signaling by a human insulin receptor v-ros hybrid in Chinese hamster ovary cells. Proc. Natl. Acad. Sci. USA 84, 5101-5105.
17. Gatica, M., Hinrichs, M. V., Jedlicki, A., Allende, C. C., and Allende, J. E. (1993). Effect of metal ions on the activity of casein kinase II from Xenopus laevis. Fed. Eur. Biochem. Soc. 315, 173-177.
18. Gibbs, C. S., and Zoller, M. J. (1991). Rational scanning mutagenesis of a protein kinase identifies functional regions involved in catalysis and substrate interactions. J. Biol. Chem. 266, 8923-8931.
19. Goldstein, D. J., and Weller, S. K. (1988a). Factor(s) present in herpes simplex virus type 1-infected cells can compensate for the loss of the large subunit of the viral ribonucleotide reductase: Characterization of an ICP6 deletion mutant. Virology 166, 41-51.
20. Goldstein, D. J., and Weller, S. K. (1988b). Herpes simplex virus type 1-induced ribonucleotide reductase activity is dispensable for virus growth and DNA synthesis: Isolation and characterization of an ICP6 lacZ insertion mutant. J. Virol. 62, 196-205.
21. Haigler, H., Ash, J. F., Singer, S. J., and Cohen, S. (1978). Visualization by fluorescence of the binding and internalization of epidermal growth factor in human carcinoma cells A-431. Proc. Natl. Acad. Sci. USA 75, 3317-3321.
22. Hayashi, Y., Iwasaka, T., Smith, C. C., Aurelian, L., Lewis, G. K., and Ts'o, P. O. P. (1985). Multistep transformation by defined fragments of herpes simplex virus type 2 DNA: Oncogenic region and its gene product. Proc. Natl. Acad. Sci. USA 82, 8493-8497.
23. Henry, B. E., Glaser, R., Hewetson, J., and O'Callaghan, D. J. (1978). Expression of altered ribonucleotide reductase activity associated with the replication of Epstein-Barr virus. Virology 89, 262-271.
24. Hunter, J. C. R., Smith, C. C., Bose, D., Kulka, M., Broderick, R., and Aurelian, L. (1995a). Intracellular internalization and signaling pathways triggered by the large subunit of HSV-2 ribonucleotide reductase (ICP10). Virology 210, 345-360.
25. Hunter, J. C. R., Smith, C. C., and Aurelian, L. (1995b). The HSV-2 LA-1 oncogene is a member of a novel family of serine/threonine receptor kinases. Int. J. Oncol. 7, 515-522.
26. Iwasaka, T., Smith, C., Aurelian, L., and Ts'o, P. O. P. (1985). The cervical tumor-associated antigen (ICP10/AG-4) is encoded by the transforming region of the genome of herpes simplex virus type 2. Jpn. J. Cancer Res. 76, 946-958.
27. Jariwalla, R. J., Aurelian, L., and Ts'o, P. O. P. (1980). Tumorigenic transformation induced by a specific fragment of DNA from herpes simplex virus type 2. Proc. Natl. Acad. Sci. USA 77, 2279-2283.
28. Jacobson, J. G., Leib, D. A., Goldstein, D. J., Bogard, C. L., Schaffer, P. A., Weller, S. K., and Coen, D. M. (1989). A herpes simplex virus ribonucleotide reductase deletion mutant is defective for productive acute and reactivatable latent infections of mice and for replication in mouse cells. Virology 173, 276-283.
29. Kraus, M. H., Fedi, P., Starks, V., Muraro, R., and Aaronson, S. A. (1993). Demonstration of ligand-dependent signaling by the erbB3 tyrosine kinase and its constitutive activation in human breast tumor cells. Proc. Natl. Acad. Sci. USA 90, 2900-2904.
30. Langelier, Y., and Buttin, G. (1981). Characterization of ribonucleotide reductase induction in BHK-21/C13 Syrian hamster cell line upon infection by herpes simplex virus (HSV). J. Gen. Virol. 57, 21-31.
31. Lankinen, H., Graslund, A., and Thelander, L. (1982). Induction of a new ribonucleotide reductase after infection of mouse L cells with pseudorabies virus. J. Virol. 41, 893-900.
32. Lax, I., Bellor, F., Howk, R., Ullrich, A., Givol, D., and Schlessinger, J. (1989). Functional analysis of the ligand binding site of EGF-receptor utilizing chimeric chicken/human receptor molecules. EMBO J. 8, 421-427.
33. Lee, J., Dull, T. J., Lax, I., Schlessinger, J., and Ullrich, A. (1989). HER cytoplasmic domain generates normal mitogenic and transforming signals in a chimeric receptor. EMBO J. 8, 167-173.
34. Lehvaslaiho, H., Lehtola, L., Sistonen, L., and Alitalo, K. (1989). A chimeric EGF-R-neu proto-oncogene allows EGF to regulate neu tyrosine kinase and cell transformation. EMBO J. 8, 159-166.
35. Lhotak, V., and Pawson, T. (1993). Biological and biochemical activities of a chimeric epidermal growth factor-ELK receptor tyrosine kinase. Mol. Cell. Biol. 13, 7071-7079.
36. Li, N., Batzer, A., Daly, R., Yajnik, V., Skolnik, E., Chardin, P., Bar-Sagi, D., Margolis, B., and Schlessinger, J. (1993). Guanine-nucleotide-releasing factor hSos1 binds to Grb2 and links receptor tyrosine kinases to Ras signalling. Nature 363, 85-88.
37. Lowenstein, E. J., Daly, R. J., Batzer, A. G., Li, W., Margolis, B., Lammers, R., Ullrich, A., Scholnick, E., Bar-Sagi, D., and Schlessinger, J. (1992). The SH2 and SH3 domain containing protein Grb2 links receptor tyrosine kinases to ras signaling. Cell 70, 431-442.
38. Luo, J. H., and Aurelian, L. (1992). The transmembrane helical segment but not the invariant lysine is required for the kinase activity of the large subunit of herpes simplex virus type 2 ribonucleotide reductase. J. Biol. Chem. 267, 9645-9653.
39. Luo, J. H., Smith, C. C., Kulka, M., and Aurelian, L. (1991). A truncated protein kinase domain of the large subunit of the herpes simplex type 2 ribonucleotide reductase (ICP10) expressed in Escherichia coli. J. Biol. Chem. 266, 20976-20983.
40. Margolis, B., Bellot, F., Honegger, A. M., Ullrich, A., Schlessinger, J., and Zilberstein, A. (1990). Tyrosine kinase activity is essential for the association of phospholipase C γ with the epidermal growth factor receptor. Mol. Cell. Biol. 10, 435-441.
41. McCormick, F. (1989). ras GTPase activating protein: Signal transmitter and signal terminator. Cell 56, 5-8.
42. McLauchlan, J., and Clements, J. B. (1983). DNA sequence homology between two co-linear loci on the HSV genome which have different transforming abilities. EMBO J. 2, 1953-1961.
43. Molloy, C. J., Fleming, T. P., Bottaro, D. P., Cuadrado, A., and Aaronson, S. A. (1992). Platelet-derived growth factor stimulation of GTPase-activating protein tyrosine phosphorylation in control and c-H-ras-expressing NIH 3T3 cells correlates with p21 ras activation. Mol. Cell. Biol. 12, 3903-3909.
44. Nikas, I., McLauchlan, J., Davison, A. J., Taylor, W. R., and Clements, J. B. (1986). Structural features of ribonucleotide reductase. Proteins: Struct. Funct. Genet. 1, 376-384.
45. Osherov, N., Gazit, A., Gilon, C., and Levitzki, A. (1993). Selective inhibition of the epidermal growth factor and HER/neu receptors by tyrphostins. J. Biol. Chem. 268, 11134-11142.
46. 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 function. J. Biol. Chem. 266, 9647-9651.
47. Pawson, T. (1995). Protein modules and signaling networks. Nature 373, 573-580.
48. Peng, T., Colin-Hunter, J. R., and Nelson, J. (1996). The novel protein kinase of the RR1 subunit of herpes simplex virus has autophosphorylation and transphosphorylation activity that differs in its ATP requirements for HSV-1 and HSV-2. Virology 216, 184-196.
49. Preston, V. G., Darling, A. A., and McDougall, I. M. (1988). The herpes simplex virus type 1 temperature-sensitive mutant ts 1222 has a single base pair deletion in the small subunit of ribonucleotide reductase. Virology 167, 458-467.
50. Redel, H. (1994). Epidermal growth factor (EGF) modulation of feline sarcoma virus fms tyrosine kinase activity, internalization, degradation, and transforming potential in an EGF receptor/vfms chimera. J. Virol. 68, 411-424.
51. Redel, H., Dull, T. M., Honegger, A. M., Schlessinger, J., and Ullrich, A. (1989). Cytoplasmic domains determine signal specificity, cellular routing characteristics and influence ligand binding of epidermal growth factor and insulin receptors. EMBO J. 8, 2943-2954.
52. Redel, H., Schlessinger, J., and Ullrich, A. (1987). A chimeric, ligand-binding v-erbB/EGF receptor retains transforming potential. Science 236, 197-200.
53. Santoro, M., Wong, W. T., Aroca, P., Santos, E., Matoskova, B., Grieco, M., Fusco, A., and Di Fiore, P. P. (1994). An epidermal growth factor receptor/ret chimera generates mitogenic and transforming signals: Evidence for a ref-specific signaling pathway. Mol. Cell. Biol. 14, 663-675.
54. Satoh, T., Endo, M., Nakafuku, M., Akiyama, T., Yamamoto, T., and Kaziro, Y. (1990a). Accumulation of p21 ras GTP in response to stimulation with epidermal growth factor and oncogene products with tyrosine kinase activity. Proc. Natl. Acad. Sci. USA 87, 7926-7929.
55. Satoh, T., Endo, M., Nakafuku, M., Nakamura, S., and Kaziro, Y. (1990b). Platelet-derived growth factor stimulates formation of active p21ras GTP complex in Swiss mouse 3T3 cells. Proc. Natl. Acad. Sci. USA 87, 5993-5997.
56. Seedorf, K., Felder, S., Millauer, B., Schlessinger, J., and Ullrich, A. (1991). Analysis of platelet-derived growth factor receptor domain function using a novel chimeric receptor approach. J. Biol. Chem. 266, 12424-12431.
57. Smith, C. C., Kulka, M., Wymer, J. P., Chung, T. D., and Aurelian, L. (1992). Expression of the large subunit of herpes simplex virus type 2 ribonucleotide reductase (ICP10) is required for virus growth and neoplastic transformation. J. Gen. Virol. 73, 1417-1428.
58. Smith, C. C., Luo, J. H., Hunter, J. C. R., Ordonez, J. V., and Aurelian, L. (1994). The transmembrane domain of the large subunit of HSV-2 ribonucleotide reductase (ICP10) is required for protein kinase activity and transformation-related signaling pathways that result in ras activation. Virology 200, 598-612.
59. Strnad, B., and Aurelian, L. (1978). Proteins of herpesvirus type 2. III. Isolation and immunologic characterization of a large molecular weight viral protein. Virology 87, 401-415.
60. Swain, M., and Galloway, D. A. (1986). Herpes simplex virus specifies two subunits of ribonucleotide reductase encoded by 3′-coterminal transcripts. J. Virol. 57, 802-808.
61. Taylor, S. S., Knighton, D. R., Zheng, J., Ten Eyck, L. F., and Sowadski, J. M. (1992). Structural framework for the protein kinase family. Annu. Rev. Cell Biol. 8, 429-462.
62. Thelander, L., and Reichard, P. (1979). Reduction of ribonucleotides. Annu. Rev. Biochem. 48, 133-158.
63. Trahey, M., and McCormick, G. (1987). Acytoplasmic protein stimulates normal N-ras p21 GTPase, but does not affect oncogenic mutants. Science 238, 542-545.
64. van der Geer, P., Hunter, T., and Lindberg, R. A. (1994). Receptor protein-tyrosine kinases and their signal transduction pathways. Annu. Rev. Cell Biol. 10, 251-337.
65. Wymer, J. P., Chung, T. C., Chang, Y. N., Hayward, G. S., and Aurelian, L. (1989). Identification of immediate-early-type cis-response elements in the promotor for the ribonucleotide reductase large subunit form herpes simplex virus type 2. J. Virol. 63, 2773-2784.