Functional interactions between polydnavirus and host cellular innexins

Journal of Virology

Volumn 85, Issue 19, 2011, Pages 10222-10229

  Marziano, N K ^a,c   Hasegawa, D K ^b   Phelan, P ^a   Turnbull, M W ^b  

^a UNIVERSITY OF KENT   (United Kingdom)

^b CLEMSON UNIVERSITY   (United States)

^c UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GAP JUNCTION PROTEIN; INNEXIN; INNEXIN 2; UNCLASSIFIED DRUG; VINNEXIN D; VINNEXIN G; VINNEXIN Q1; VINNEXIN Q2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CAMPOLETIS SONORENSIS ICHNOVIRUS; CELL JUNCTION; CONTROLLED STUDY; HOST CELL; INSECT CELL; LEPIDOPTERA; NONHUMAN; OOCYTE; POLYDNAVIRIDAE; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS CELL INTERACTION;

ANIMALS; CONNEXINS; HOST-PATHOGEN INTERACTIONS; INTERCELLULAR JUNCTIONS; OOCYTES; POLYDNAVIRIDAE; SPODOPTERA; VIRAL PROTEINS; XENOPUS;

CAMPOLETIS SONORENSIS ICHNOVIRUS; DNA VIRUSES; HEXAPODA; ICHNEUMONOIDEA; ICHNOVIRUS; SPODOPTERA FRUGIPERDA;

EID: 80053933421     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00691-11     Document Type: Article

References (68)

1. Ayad, W. A., D. Locke, I. V. Koreen, and A. L. Harris. 2006. Heteromeric, but not homomeric, connexin channels are selectively permeable to inositol phosphates. J. Biol. Chem. 281:16727-16739.
2. Baerwald, R. J. 1975. Inverted gap and other cell junctions in cockroach hemocyte capsules: a thin section and freeze-fracture study. Tissue Cell 7:575-585.
3. Baldwin, K. M., R. S. Hakim, and G. B. Stanton. 1993. Cell-cell communication correlates with pattern formation in molting Manduca midgut epithelium. Dev. Dyn. 197:239-243.
4. Bauer, R., C. Lehmann, and M. Hoch. 2001. Gastrointestinal development in the Drosophila embryo requires the activity of innexin gap junction channel proteins. Cell Commun. Adhes. 8:307-310.
5. Beckage, N. E. 1998. Modulation of immune responses to parasitoids by polydnaviruses. Parasitology 116:S57-S64.
6. Bezier, A., et al. 2009. Polydnaviruses of braconid wasps derive from an ancestral nudivirus. Science 323:926-930.
7. Bruzzone, R., S. G. Hormuzdi, M. T. Barbe, A. Herb, and H. Monyer. 2003. Pannexins, a family of gap junction proteins expressed in brain. Proc. Natl. Acad. Sci. U. S. A. 100:13644-13649.
8. Caveney, S., and R. Berdan. 1982. Selectivity in junctional coupling between cells of insect tissues, p. 434-465. In R. C. King and H. Akai (ed.), Insect ultrastructure, vol. 1. Plenum Press, New York, NY.
9. Churchill, D., S. Coodin, R. R. Shivers, and S. Caveney. 1993. Rapid de novo formation of gap junctions between insect hemocytes in vitro: a freezefracture, dye-transfer and patch-clamp study. J. Cell Sci. 104:763-772.
10. Colman, A. 1984. Translation of eukaryotic mRNA in Xenopus oocytes, p. 271-302. In B. D. Hames and S. J. Higgins (ed.), Transcription and translation-a practical approach. IRL, Oxford, United Kingdom.
11. Cottrell, G. T., and J. M. Burt. 2005. Functional consequences of heterogeneous gap junction channel formation and its influence in health and disease. Biochim. Biophys. Acta 1711:126-141.
12. Cui, L., A. I. Soldevila, and B. A. Webb. 2000. Relationships between polydnavirus gene expression and host range of the parasitoid wasp Campoletis sonorensis. J. Insect Physiol. 46:1397-1407.
13. Curtin, K., Z. Zhang, and R. Wyman. 2002. Gap junction proteins are not interchangeable in development of neural function in the Drosophila visual system. J. Cell Sci. 115:3379-3388.
14. Dai, J., M. J. Costello, and L. E. Gilbert. 1994. The prothoracic glands of Manduca sexta: a microscopic analysis of gap junctions and intercellular bridges. Invertebr. Reprod. Dev. 25:93-110.
15. Davies, D. H., and S. B. Vinson. 1988. Interference with function of plasmatocytes of Heliothis virescens in vivo by calyx fluid of the parasitoid Campoletis sonorensis. Cell Tissue Res. 251:467-475.
16. Desjardins, C. A., et al. 2008. Comparative genomics of mutualistic viruses of Glyptapanteles parasitic wasps. Genome Biol. 9:R183.
17. Dover, B. A., D. H. Davies, and S. B. Vinson. 1988. Degeneration of last instar Heliothis virescens prothoracic glands by Campoletis sonorensis polydnavirus. J. Invertebr. Pathol. 51:80-91.
18. Dover, B. A., D. H. Davies, and S. B. Vinson. 1988. Dose-dependent influence of Campoletis sonorensis polydnavirus on the development and ecdysteroid titers of last-instar Heliothis virescens larvae. Arch. Insect Biochem. Physiol. 8:113-126.
19. Dover, B. A., T. Tanaka, and S. B. Vinson. 1995. Stadium-specific degeneration of host prothoracic glands by Campoletis sonorensis calyx fluid and its association with host ecdysteroid titers. J. Insect Physiol. 41:947-955.
20. Duchi, S., et al. 2010. The impact on microtubule network of a bracovirus I B-like protein. Cell. Mol. Life Sci. 67:1699-1712.
21. Dupuy, C., E. Huguet, and J. M. Drezen. 2006. Unfolding the evolutionary story of polydnaviruses. Virus Res. 117:81-89.
22. Dykes, I. M., F. M. Freeman, J. P. Bacon, and J. A. Davies. 2004. Molecular basis of gap junctional communication in the CNS of the leech Hirudo medicinalis. J. Neurosci. 24:886-894.
23. Frank, M., et al. 2010. Neuronal connexin-36 can functionally replace connexin-45 in mouse retina but not in the developing heart. J. Cell Sci. 123: 3605-3615.
24. Fushiki, D., Y. Hamada, R. Yoshimura, and Y. Endo. 2010. Phylogenetic and bioinformatic analysis of gap junction-related proteins, innexins, pannexins and connexins. Biomed. Res. 31:133-142.
25. Glatz, R. V., S. Asgari, and O. Schmidt. 2004. Evolution of polydnaviruses as insect immune suppressors. Trends Microbiol. 12:545-554.
26. Gupta, A. P. 1991. Gap cell junctions, cell adhesion molecules, and molecular basis of encapsulation, p. 133-167. In A. P. Gupta (ed.), Immunology of insects and other arthropods. CRC Press, Boca Raton, FL.
27. Han, S. S., and A. P. Gupta. 1989. Arthropod immune system. II. Encapsulation of implanted nerve cord and "plain gut" surgical suture by granulocytes of Blattella germanica (L.) (Dictyoptera: Blattellidae). Zoolog. Sci. (Tokyo) 6:303-320.
28. He, D. S., J. X. Jiang, S. M. Taffet, and J. M. Burt. 1999. Formation of heteromeric gap junction channels by connexins 40 and 43 in vascular smooth muscle cells. Proc. Natl. Acad. Sci. U. S. A. 96:6495-6500.
29. Hong, S. M., et al. 2008. Two gap junction (innexin) genes of the Bombyx mori and their expression. J. Insect Physiol. 54:180-191.
30. Irving, P., et al. 2005. New insights into Drosophila larval haemocyte functions through genome-wide analysis. Cell. Microbiol. 7:335-350.
31. Kroemer, J. A., and B. A. Webb. 2006. Divergences in protein activity and cellular localization within the Campoletis sonorensis ichnovirus vankyrin family. J. Virol. 80:12219-12228.
32. Kroemer, J. A., and B. A. Webb. 2005. I B-related vankyrin genes in the Campoletis sonorensis ichnovirus: temporal and tissue-specific patterns of expression in parasitized Heliothis virescens lepidopteran hosts. J. Virol. 79:7617-7628.
33. Lapointe, R., et al. 2007. Genomic and morphological features of a banchine polydnavirus: a comparison with bracoviruses and ichnoviruses. J. Virol. 81:6491-6501.
34. Lehmann, C., et al. 2006. Heteromerization of innexin gap junction proteins regulates epithelial tissue organization in Drosophila. Mol. Biol. Cell 17: 1676-1685.
35. Li, S., J. A. Dent, and R. Roy. 2003. Regulation of intermuscular electrical coupling by the Caenorhabditis elegans innexin inx-6. Mol. Biol. Cell 14:2630-2644.
36. Li, X., and B. A. Webb. 1994. Apparent functional role for a cysteine-rich polydnavirus protein in suppression of the insect cellular immune response. J. Virol. 68:7482-7489.
37. Lococo, D. J., C. S. Thompson, and S. S. Tobe. 1986. Intercellular communication in an insect endocrine gland. J. Exp. Biol. 121:407-419.
38. Luo, K., and M. W. Turnbull. 2008. Manipulations of host cell physiology by polydnaviruses, p. 93-115. In N. Liu (ed.), Recent advances in insect physiology, toxicology, and molecular biology. Research Signpost, Kerala, India.
39. Pech, L. L., and M. R. Strand. 1996. Granular cells are required for encapsulation of foreign targets by insect haemocytes. J. Cell Sci. 109:2053-2060.
40. Phelan, P. 2005. Innexins: members of an evolutionarily conserved family of gap-junction proteins. Biochim. Biophys. Acta 1711:225-245.
41. Phelan, P., et al. 2008. Molecular mechanism of rectification at identified electrical synapses in the Drosophila giant fiber system. Curr. Biol. 18:1955-1960.
42. Phelan, P., et al. 1998. Drosophila Shaking-B protein forms gap junctions in paired Xenopus oocytes. Nature 391:181-184.
43. Pow, D. V., and D. W. Golding. 1989. Intercellular junctions in the corpora cardiaca of locusts. Cell Tissue Res. 258:585-591.
44. Shelby, K. S., and H. J. Popham. 2009. Analysis of ESTs generated from immune-stimulated hemocytes of larval Heliothis virescens. J. Invertebr. Pathol. 101:86-95.
45. Shelby, K. S., and B. A. Webb. 1994. Polydnavirus infection inhibits synthesis of an insect plasma protein, arylphorin. J. Gen. Virol. 75:2285-2292.
46. Shelby, K. S., and B. A. Webb. 1997. Polydnavirus infection inhibits translation of specific growth-associated host proteins. Insect Biochem. Mol. Biol. 27:263-270.
47. Shelby, K. S., and B. A. Webb. 1999. Polydnavirus-mediated suppression of insect immunity. J. Insect Physiol. 45:507-514.
48. Spray, D. C., A. L. Harris, and M. V. Bennett. 1981. Equilibrium properties of a voltage-dependent junctional conductance. J. Gen. Physiol. 77:77-93.
49. Starich, T. A., J. Xu, I. M. Skerrett, B. J. Nicholson, and J. E. Shaw. 2009. Interactions between innexins UNC-7 and UNC-9 mediate electrical synapse specificity in the Caenorhabditis elegans locomotory nervous system. Neural Dev. 4:16.
50. Stebbings, L. A., M. G. Todman, P. Phelan, J. P. Bacon, and J. A. Davies. 2000. Two Drosophila innexins are expressed in overlapping domains and cooperate to form gap-junction channels. Mol. Biol. Cell 11:2459-2470.
51. Stebbings, L. A., et al. 2002. Gap junctions in Drosophila: developmental expression of the entire innexin gene family. Mech. Dev. 113:197-205.
52. Swenson, K. I., J. R. Jordan, E. C. Beyer, and D. L. Paul. 1989. Formation of gap junctions by expression of connexins in Xenopus oocyte pairs. Cell 57:145-155.
53. Tanaka, K., et al. 2007. Shared and species-specific features among ichnovirus genomes. Virology 363:26-35.
54. Turnbull, M. W., A.-N. Volkoff, B. A. Webb, and P. Phelan. 2005. Functional gap-junction genes are encoded by insect viruses. Curr. Biol. 15:R491-R492.
55. Turnbull, M. W., and B. A. Webb. 2002. Perspectives on polydnavirus origins and evolution. Adv. Virus Res. 58:203-254.
56. Verselis, V. K., M. V. Bennett, and T. A. Bargiello. 1991. A voltage-dependent gap junction in Drosophila melanogaster. Biophys. J. 59:114-126.
57. Vinson, S. B. 1990. Physiological interactions between the host genus Heliothis and its guild of parasitoids. Arch. Insect Biochem. Physiol. 13:63-81.
58. Volkoff, A. N., et al. 2010. Analysis of virion structural components reveals vestiges of the ancestral ichnovirus genome. PLoS Pathog. 6:e1000923.
59. Webb, B. A., and M. R. Strand. 2005. The biology and genomics of polydnaviruses, p. 260-323. In L. I. Gilbert, K. Iatrou, and S. S. Gill (ed.), Comprehensive molecular insect science, vol. 5. Elsevier Press, San Diego, CA.
60. Webb, B. A., et al. 2006. Polydnavirus genomes reflect their dual roles as mutualists and pathogens. Virology 347:160-174.
61. Weng, X. H., et al. 2008. Gap junctions in Malpighian tubules of Aedes aegypti. J. Exp. Biol. 211:409-422.
62. White, T. W. 2002. Unique and redundant connexin contributions to lens development. Science 295:319-320.
63. White, T. W., R. Bruzzone, S. Wolfram, D. L. Paul, and D. A. Goodenough. 1994. Selective interactions among the multiple connexin proteins expressed in the vertebrate lens: the second extracellular domain is a determinant of compatibility between connexins. J. Cell Biol. 125:879-892.
64. White, T. W., and D. L. Paul. 1999. Genetic diseases and gene knockouts reveal diverse connexin functions. Annu. Rev. Physiol. 61:283-310.
65. Wolfle, S. E., et al. 2007. Connexin45 cannot replace the function of connexin40 in conducting endothelium-dependent dilations along arterioles. Circ. Res. 101:1292-1299.
66. Yen, M. R., and M. H. Saier, Jr. 2007. Gap junctional proteins of animals: the innexin/pannexin superfamily. Prog. Biophys. Mol. Biol. 94:5-14.
67. Yum, S. W., et al. 2007. Human connexin26 and connexin30 form functional heteromeric and heterotypic channels. Am. J. Physiol. Cell Physiol. 293: C1032-C1048.
68. Zheng-Fischhofer, Q., et al. 2006. Connexin31 cannot functionally replace connexin43 during cardiac morphogenesis in mice. J. Cell Sci. 119:693-701.