Patterns of epistasis in RNA viruses: A review of the evidence from vaccine design

Journal of Evolutionary Biology

Volumn 16, Issue 6, 2003, Pages 1223-1235

  Burch, C L ^a   Turner, P E ^b   Hanley, K A ^c  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

Attenuation; Epistasis; Evolution; Mutation; RNA virus; Vaccine

Indexed keywords

VIRUS VACCINE;

DRUG DEVELOPMENT; EPISTASIS; VACCINATION; VIRUS;

DRUG DESIGN; GENETIC EPISTASIS; GENETICS; MUTATION; PATHOGENICITY; REVIEW; RNA VIRUS; RNA VIRUS INFECTION;

DRUG DESIGN; EPISTASIS, GENETIC; MUTATION; RNA VIRUS INFECTIONS; RNA VIRUSES; VIRAL VACCINES;

RNA VIRUSES;

EID: 0242542705     PISSN: 1010061X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1420-9101.2003.00632.x     Document Type: Review

References (66)

1. Agrawal, A.F. 2001. Sexual selection and the maintenance of sexual reproduction. Nature 411: 692-695.
2. Barton, N.H. & Charlesworth, B. 1998. Why sex and recombination? Science 281: 1986-1990.
3. Basler, C.F., Garcia-Sastre, A. & Palese, P. 1999. Mutation of neuraminidase cysteine residues yields temperature-sensitive influenza viruses. J. Virol. 73: 8095-8103.
4. Blaney, J.E. Jr, Johnson, D.H., Firestone, C.Y., Hanson, C.T., Murphy, B.R. & Whitehead, S.S. 2001. Chemical mutagenesis of dengue virus type 4 yields mutant viruses which are temperature sensitive in vero cells or human liver cells and attenuated in mice. J. Virol. 75: 9731-9740.
5. Boot, H.J., ter Huurne, A.A., Vastenhouw, S.A., Kant, A., Peeters, B.P. & Gielkens, A.L. 2001. Rescue of infectious bursal disease virus from mosaic full-length clones composed of serotype I and II cDNA. Arch. Virol. 146: 1991-2007.
6. Brown, H.E., Chen, H. & Engelman, A. 1999. Structure-based mutagenesis of the human immunodeficiency virus type 1 DNA attachment site: effects on integration and cDNA synthesis. J. Virol. 73: 9011-9020.
7. Butrapet, S., Huang, C.Y., Pierro, D.J., Bhamarapravati, N., Gubler, D.J. & Kinney, R.M. 2000. Attenuation markers of a candidate dengue type 2 vaccine virus, strain 16681 (PDK-53), are defined by mutations in the 5′ noncoding region and nonstructural proteins 1 and 3. J. Virol. 74: 3011-3019.
8. CDC 2000. Outbreak of poliomyelitis - Dominican Republic and Haiti, 2000. MMWR Morb. Mortal. Wkly. Rep. 49: 1094-1103.
9. Charlesworth, B. 1990. Mutation-selection balance and the evolutionary advantage of sex and recombination. Genet. Res. 55: 199-221.
10. Cheng, X., Zhou, H., Tang, R.S., Munoz, M.G. & Jin, H. 2001. Chimeric subgroup A respiratory syncytial virus with the glycoproteins substituted by those of subgroup B and RSV without the M2-2 gene are attenuated in African green monkeys. Virology 283: 59-68.
11. Crotty, S., Cameron, C.E. & Andino, R. 2001. RNA virus error catastrophe: direct molecular test by using ribavirin. Proc. Natl Acad. Sci. USA 98: 6895-6900.
12. de Visser, J.A.G.M., Hoekstra, R.F. & van den Ende, H. 1997. Test of interaction between genetic markers that affect fitness in Aspergillus niger. Evolution 51: 1499-1505.
13. Ebihara, H., Yoshimatsu, K., Ogino, M., Araki, K., Ami, Y., Kariwa, H., Takashima, I., Li, D. & Arikawa, J. 2000. Pathogenicity of Hantaan virus in newborn mice: genetic reassortant study demonstrating that a single amino acid change in glycoprotein Gl is related to virulence. J. Virol. 74: 9245-9255.
14. Elena, S.F. 1999. Little evidence for synergism among deleterious mutations in a nonsegmented RNA virus. J. Mol. Evol. 49: 703-707.
15. Elena, S.F. & Lenski, R.E. 1997. Test of synergistic interactions among deleterious mutations in bacteria. Nature 390: 395-398.
16. Fenster, C.B., Galloway, L.F. & Chao, L. 1997. Epistasis and its consquences for the evolution of natural populations. Trends Ecol. Evol. 12: 282-287.
17. Fodor, E., Palese, P., Brownlee, G.G. & Garcia-Sastre, A. 1998. Attenuation of influenza A virus mRNA levels by promoter mutations. J. Virol. 72: 6283-6290.
18. Gritsun, T.S., Desai, A. & Gould, E.A. 2001. The degree of attenuation of tick-borne encephalitis virus depends on the cumulative effects of point mutations. J. Gen. Virol. 82: 1667-1675.
19. Hanley, K.A., Lee, J.J., Blaney, J.E.J., Murphy, B.R. & Whitehead, S.S. 2002. Paired charge-to-alanine mutagenesis of dengue virus type 4 NS5 generates mutants with temperature-sensitive, host-range and mouse-attenuation phenotypes. J. Virol. 76: 525-531.
20. Hazelton, P.R. & Coombs, K.M. 1995. The reovirus mutant tsA279 has temperature-sensitive lesions in the M2 and L2 genes: the M2 gene is associated with decreased viral protein production and blockade in transmembrane transport. Virology 207: 46-58.
21. Kanno, T., Mackay, D., Wilsden, G. & Kitching, P. 2001. Virulence of swine vesicular disease virus is determined at two amino acids in capsid protein VP1 and 2A protease Virus Res. 80: 101-107.
22. Keightley, P.D. 1996. Nature of deleterious mutation load in Drosophila. Genetics 144: 1993-1999.
23. Kinney, R.M., Chang, G.-J., Tsuchiya, K.R., Sneider, J.M., Roehrig, J.T., Woodward, T.M. & Trent, D.W. 1993. Attenuation of Venezuelan equine encephalitis virus strain TC-83 is encoded by the 5′-noncoding region and the E2 envelope glycoprotein. J. Virol. 67: 1269-1277.
24. Kondrashov, A.S. 1988. Deleterious mutations and the evolution of sexual reproduction. Nature 336: 435-440.
25. Kondrashov, A.S. 1993. Classification of hypotheses on the advantage of amphimixis. J. Hered. 84: 372-387.
26. Kondrashov, A.S. 1994. Muller's ratchet under epistatic selection. Genetics 136: 1469-1473.
27. Kondrashov, A.S. & Crow, J.F. 1991. Haploidy or diploidy: which is better? Nature 351: 314-315.
28. Kondrashov, F.A. & Kondrashov, A.S. 2001. Multidimensional epistasis and the disadvantage of sex. Proc. Natl Acad. Sci. USA 98: 12089-12092.
29. Latorre, P., Cadd, T., Itoh, M., Curran, J. & Kolakofsky, D. 1998. The various sendai virus C proteins are not functionally equivalent and exert both positive and negative effects on viral RNA accumulation during the course of infection. J. Virol. 72: 5984-5993.
30. Lynch, M. & Gabriel, W. 1990. Mutation load and the survival of small populations. Evolution 44: 1725-1737.
31. Mandl, C.M., Allison, S.L., Holzmann, H., Meixner, T. & Heinz, F.X. 2000. Attenuation of tick-borne encephalitis virus by structure-based site-specific mutagenesis of a putative flavivirus receptor site. J. Virol. 74: 9601-9609.
32. Maynard Smith, J. 1978. The Evolution of Sex. Cambridge University Press, Cambridge.
33. McGoldrick, A., Macadam, A.J., Dunn, G., Rowe, A., Burlison, J., Minor, P.D., Meredith, J., Evans, D.J. & Almond, J.W. 1995. Role of mutations G-480 and C-6203 in the attenuation phenotype of Sabin type 1 poliovirus. J. Virol. 69: 7601-7605.
34. Men, R., Bray, M., Clark, D., Chanock, R.M. & Lai, C.-J. 1996. Dengue type 4 virus mutants containing deletions in the 3′ noncoding region of the RNA genome: analysis of growth restriction in cell culture and altered viremia pattern and immunogenicity in rhesus monkeys. J. Virol. 70: 3930-3937.
35. Moore, F.B., Rozen, D.E. & Lenski, R.E. 2000. Pervasive compensatory adaptation in Escherichia coli. Proc. Natl Acad. Sci. USA 267: 515-522.
36. Morse, S.S., ed. 1994. The Evolutionary Biology of Viruses. Raven Press Ltd, New York, NY.
37. Mukai, T. 1969. The genetic structure of natural populations of D. melanogaster. VIII. Synergistic interactions of spontaneous mutant polygenes controlling viability. Genetics 61: 749-761.
38. Murphy, B.R. & Chanock, R.M. (2001). Immunization against viral diseases. In: Fields Virology (P. M. Howley, ed.), pp. 435-467. Lippincott Williams and Wilkins, Philadelphia, PA.
39. Nuzhdin, S.V., Pasyukova, E.G. & Mackay, T.F. 1996. Positive association between copia transposition rate and copy number in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 263: 823-831.
40. Omata, T., Kohara, M., Kuge, S., Komatsu, T., Abe, S., Semler, B., Kameda, A., Itoh, H., Arita, M., Wimmer, E. & Nomoto, A. 1986. Genetic analysis of the attenuation of phenotype of poliovirus type 1 J. Virol. 58: 348-358.
41. Otto, S.P. 1997. Unravelling gene interactions. Nature 390: 343.
42. Parkin, N.T., Chiu, P. & Coelingh, K. 1997. Genetically engineered live attenuated influenza A virus vaccine candidates. J. Virol. 71: 2772-2778.
43. Partridge, L. & Barton, N.H. 1993. Optimality, mutation and the evolution of ageing. Nature 362: 305-311.
44. Peck, J.R., Barreau, G. & Heath, S.C. 1997. Imperfect genes, Fisherian mutation and the evolution of sex. Genetics 145: 1171-1199.
45. Peck, J.R. & Waxman, D. 2000. Mutation and sex in a competitive world. Nature 406: 399-404.
46. Peters, A.D. & Keightley, P.D. 2000. A test for epistasis among induced mutations in Caenorhabdities elegans. Genetics 156: 1635-1647.
47. Roner, M.R., Neplouev, I., Sherry, B. & Joklik, W.K. 1997. Construction and characterization of a reovirus double temperature-sensitive mutant. Proc. Natl Acad. Sci. USA 94: 6826-6830.
48. Schmidt, A.C., Wenzke, D.R., McAuliffe, J.M., St Claire, M., Elkins, W.R., Murphy, B.R. & Collins, P.L. 2002. Mucosal immunization of rhesus monkeys against respiratory syncytial virus subgroups A and B and human parainfluenza virus type 3 by using a live cDNA-derived vaccine based on a host range-attenuated bovine parainfluenza virus type 3 vector backbone. J. Virol. 76: 1089-1099.
49. Schultz, S.T. & Lynch, M. 1997. Mutation and extinction: the role of variable mutational effects, synergistic epistasis, beneficial mutations, and degree of outcrossing. Evolution 51: 1363-1371.
50. Siller, S. 2001. Sexual selection and the maintenance of sex. Nature 411: 689-692.
51. Skiadopoulos, M.H., Durbin, A.P., Tatem, J.M., Wu, S.-L., Paschalis, M., Tao, T., Collins, P.R. & Murphy, B.R. 1998. Three amino acid substitutions in the L protein of the human parainfluenza virus type 3 cp45 live attenuated vaccine candidate contribute to its temperature-sensitive and attenuation phenotypes. J. Virol. 72: 1762-1768.
52. Skiadopoulos, M.H., Surman, S., Tatem, J.M., Paschalis, M., Wu, S.-L., Udem, S.A., Durbin, A.P., Collins, P.L. & Murphy, B.R. 1999. Identification of mutations contributing to the temperature-sensitive, cold-adapted, and attenuation phenotypes of the live-attenuated, cold-passage 45 (cp 45) human parainfluenza virus 3 candidate vaccine. J. Virol. 73: 1374-1381.
53. Sokal, R.R. & Rohlf, F.J. 1995. Biometry. W. H. Freeman and Company, New York, NY.
54. Subbarao, E.K., Park, E.J., Lawson, C.M., Chen, A.Y. & Murphy, B.R. 1995. Sequential addition of temperature-sensitive missense mutations into the PB2 gene of influenza A transfectant viruses can effect an increase in temperature sensitivity and attenuation and permits the rational design of a genetically engineered live influenza A virus vaccine. J. Virol. 69: 5969-5977.
55. Szathmary, E. 1993. Do deleterious mutations act synergistically? Metabolic control theory provides a partial answer. Genetics 133: 127-132.
56. Tang, R.S., Nguyen, N., Zhou, H. & Jin, H. 2002. Clustered charge-to-alanine mutagenesis of human respiratory syncytial virus L polymerase generates temperature-sensitive viruses. Virology 302: 207-216.
57. Tao, T., Skiadopoulos, M.H., Davoodi, F., Riggs, J.M., Collins, P.L. & Murphy, B.R. 2000. Replacement of the ectodomains of the hemagglutinin-neuraminidase and fusion glycoproteins of recombinant parainfluenza virus type 3 (PIV3) with their counterparts from PIV2 yields attenuated PIV2 vaccine candidates. J. Virol. 74: 6448-6458.
58. Turner, P.E. 2003. Searching for the advantages of virus sex. Orig. Life Evol. Biosph 33: 95-108.
59. Wade, M.J., Winther, R.G., Agrawal, A.F. & Goodnight, C.J. 2001. Alternative definitions of epistasis: dependence and interaction. Trends Ecol. Evol. 16: 498-504.
60. Waxman, D. & Peck, J.R. 1999. Sex and adaptation in a changing environment. Genetics 153: 1041-1053.
61. West, S.A., Lively, C.M. & Read, A.F. 1999. A pluralistic approach to sex and recombination. J. Evol. Biol. 12: 1003-1012.
62. Whitehead, S.S., Firestone, C.-Y., Collins, P.L. & Murphy, B.R. 1998. A single nucleotide substitution in the transcription start signal of the M2 gene of respiratory syncytial virus vaccine candidate cpts 248/404 is the major determinant of the temperature-sensitive and attenuation phenotypes. Virology 247: 232-239.
63. Whitehead, S.S., Firestone, C.-Y., Karron, R.A., Crowe, J.E., Elkins, W.R., Collins, P.L. & Murphy, B.R. 1999. Addition of a missense mutation present in the L gene of respiratory syncytial virus (RSV) cpts 530/1030 to RSV vaccine candidate cpts 248/404 increases its attenuation and temperature sensitivity. J. Virol. 73: 871-877.
64. Whitlock, M.C. & Bourguet, D. 2000. Factors affecting the genetic load in Drosophila: synergistic epistasis and correlations among fitness components. Evolution 54: 1654-1660.
65. Wolf, J.D., Brodie, E.D. & Wade, M.J., eds. 2000. Epistasis and the Evolutionary Process. Oxford University Press, Oxford.
66. Zhang, L., Marriott, K.A., Harnish, D.G. & Aronson, J.F. 2001. Reassortant analysis of guinea-pig virulence of Pichinde virus variants. Virology 290: 30-38.