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Journal of Virology, November 2005, p. 14253-14260, Vol. 79, No. 22
0022-538X/05/$08.00+0     doi:10.1128/JVI.79.22.14253-14260.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Effect of Alternating Passage on Adaptation of Sindbis Virus to Vertebrate and Invertebrate Cells

Ivorlyne P. Greene,1,{dagger} Eryu Wang,1 Eleanor R. Deardorff,1 Rania Milleron,1,{ddagger} Esteban Domingo,2 and Scott C. Weaver1*

Center for Biodefense and Emerging Infectious Diseases and Department of Pathology, University of Texas Medical Branch, Galveston, Texas 77555-0609,1 Centro de Biologia Molecular "Severo Ochoa," Consejo Superior de Investigaciones Cientificas, Universidad Autonoma de Madrid, Cantoblanco, 28049 Madrid, Spain2

Received 8 April 2005/ Accepted 6 August 2005

Mosquito-borne alphaviruses, which replicate alternately and obligately in mosquitoes and vertebrates, appear to experience lower rates of evolution than do many RNA viruses that replicate solely in vertebrates. This genetic stability is hypothesized to result from the alternating host cycle, which constrains evolution by imposing compromise fitness solutions in each host. To test this hypothesis, Sindbis virus was passaged serially, either in one cell type to eliminate host alteration or alternately between vertebrate (BHK) and mosquito (C6/36) cells. Following 20 to 50 serial passages, mutations were identified and changes in fitness were assessed using competition assays against genetically marked, surrogate parent viruses. Specialized viruses passaged in a single cell exhibited more mutations and amino acid changes per passage than those passaged alternately. Single host-adapted viruses exhibited fitness gains in the cells in which they specialized but fitness losses in the bypassed cell type. Most but not all viruses passaged alternately experienced lesser fitness gains than specialized viruses, with fewer mutations per passage. Clonal populations derived from alternately passaged viruses also exhibited adaptation to both cell lines, indicating that polymorphic populations are not required for simultaneous fitness gains in vertebrate and mosquito cells. Nearly all passaged viruses acquired Arg or Lys substitutions in the E2 envelope glycoprotein, but enhanced binding was only detected for BHK cells. These results support the hypothesis that arbovirus evolution may be constrained by alternating host transmission cycles, but they indicate a surprising ability for simultaneous adaptation to highly divergent cell types by combinations of mutations in single genomes.

* Corresponding author. Mailing address: Department of Pathology, University of Texas Medical Branch, Galveston, Texas 77555-0609. Phone: (409) 747-0758. Fax: (409) 747-2415. E-mail: sweaver{at}utmb.edu.

{dagger} Present address: W. Harry Feinstone Department of Molecular Microbiology and Immunology, Johns Hopkins Bloomberg School of Public Health, 615 North Wolfe St., Baltimore, MD 21205.

{ddagger} Present address: Center for Molecular and Cellular Toxicology, College of Pharmacy, University of Texas, 1 University Station, A1915, Austin, TX 78712-0125.

Journal of Virology, November 2005, p. 14253-14260, Vol. 79, No. 22
0022-538X/05/$08.00+0     doi:10.1128/JVI.79.22.14253-14260.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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