Is Hiv Short-Sighted? Insights From A Multistrain Nested Model

Evolution

Volumn 67, Issue 10, 2013, Pages 2769-2782

  Lythgoe, Katrina A ^a   Pellis, Lorenzo ^a,b   Fraser, Christophe ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

Epidemiology; Evolution; Nested model; Pathogen; Transmission virulence trade off; Virulence

Indexed keywords

EPIDEMIOLOGY; HOST-PATHOGEN INTERACTION; HUMAN IMMUNODEFICIENCY VIRUS; NUMERICAL MODEL; PATHOLOGY; TOPOLOGY; TRADE-OFF; VIRULENCE;

HUMAN IMMUNODEFICIENCY VIRUS;

ARTICLE; BIOLOGICAL MODEL; DISEASE TRANSMISSION; EPIDEMIOLOGY; EVOLUTION; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; NESTED MODEL; PATHOGENESIS; PATHOGENICITY; PHYSIOLOGY; SPECIES DIFFERENCE; TIME; TRANSMISSION-VIRULENCE TRADE-OFF; VIRULENCE; VIRUS REPLICATION;

EPIDEMIOLOGY; EVOLUTION; NESTED MODEL; PATHOGEN; TRANSMISSION-VIRULENCE TRADE-OFF; VIRULENCE;

BIOLOGICAL EVOLUTION; HIV; HIV INFECTIONS; HOST-PATHOGEN INTERACTIONS; HUMANS; MODELS, BIOLOGICAL; SPECIES SPECIFICITY; TIME FACTORS; VIRULENCE; VIRUS REPLICATION;

EID: 84885054606     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12166     Document Type: Article

References (48)

1. Alizon, S., and M. van Baalen 2008. Multiple infections, immune dynamics, and the evolution of virulence. Am. Nat. 172:E150-E168.
2. Alizon, S., V. von Wyl, T. Stadler, R. Kouyos, S. Yerly, B. Hirschel, J. Böni, C. Shah, T. Klimkait, H. Furrer, et al. 2010. Phylogenetic approach reveals that virus genotype largely determines HIV set-point viral load. PLoS Pathogens 6:e1001123.
3. André, J.-B., and S. Gandon 2006. Vaccination, within-host dynamics, and virulence evolution. Evolution 60:13-23.
4. Bar, K. J., C.-Y. Tsao, S. S. Iyer, J. M. Decker, Y. Yang, M. Bonsignori, X. Chen, K.-K. Hwang, D. C. Montefiori, H.-X. Liao, et al. 2012. Early low-titer neutralizing antibodies impede HIV-1 replication and select for virus escape. PLoS Pathogens 8:e1002721.
5. Coombs, D., M. A. Gilchrist, and C. L. Ball 2007. Evaluating the importance of within- and between-host selection pressures on the evolution of chronic pathogens. Theor. Popul. Biol. 72:576-591.
6. Daar, E. S., K. L. Kesler, T. Wrin, C. J. Petropoulo, M. Bates, A. Lail, N. S. Hellmann, E. Gomperts, and S. Donfield 2005. HIV-1 pol replication capacity predicts disease progression. AIDS 19:871-877.
7. De Wolf, F., I. Spijkerman, P. T. Schellekens, M. Langendam, C. Kuiken, M. Bakker, M. Roos, R. Coutinho, F. Miedema, and J. Goudsmit 1997. AIDS prognosis based on HIV-1 RNA, CD4+ T-cell count and function: markers with reciprocal predictive value over time after seroconversion. AIDS 11:1799-1806.
8. Diekmann, O., and J. A. P. Heesterbeek 2000. Mathematical epidemiology of infectious diseases: model building, analysis and interpretation. Wiley, Oxford, UK.
9. Domingo, E., C. R. Parrish, and J. J. Holland, eds. 2008. Origin and evolution of viruses. Academic Press, Cambridge, UK.
10. Fellay, J., D. Ge, K. V Shianna, S. Colombo, B. Ledergerber, E. T. Cirulli, T. J. Urban, K. Zhang, C. E. Gumbs, J. P. Smith, et al. 2009. Common genetic variation and the control of HIV-1 in humans. PLoS Genet. 5:e1000791.
11. Feng, Z., J. Velasco-Hernandez, B. Tapia-Santos, and M. C. a. Leite 2011. A model for coupling within-host and between-host dynamics in an infectious disease. Nonlinear Dynam. 68:401-411.
12. Frank, S. A. 2012. Natural selection. III. Selection versus transmission and the levels of selection. J. Evol. Biol. 25:227-243.
13. Fraser, C., T. D. Hollingsworth, R. Chapman, F. de Wolf, and W. P. Hanage 2007. Variation in HIV-1 set-point viral load: epidemiological analysis and an evolutionary hypothesis. Proc. Natl. Acad. Sci. USA 104:17441-17446.
14. Gao, F., Y. Chen, D. N. Levy, J. A. Conway, T. B. Kepler, and H. Hui 2004. Unselected mutations in the Human Immunodeficiency Virus Type 1 genome are mostly nonsynonymous and often deleterious. J. Virol. 78:2426-2433.
15. Gilchrist, M. A., and D. Coombs 2006. Evolution of virulence: interdependence, constraints, and selection using nested models. Theor. Popul. Biol. 69:145-153.
16. Gilchrist, M. A., A. Sasaki, and A. Sasakiz 2002. Modeling host-parasite coevolution: a nested approach based on mechanistic models. J. Theor. Biol. 218:289-308.
17. Gnanakaran, S., T. Bhattacharya, M. Daniels, B. F. Keele, P. T. Hraber, A. S. Lapedes, T. Shen, B. Gaschen, M. Krishnamoorthy, H. Li, et al. 2011. Recurrent signature patterns in HIV-1 B clade Envelope glycoproteins associated with either early or chronic infections. PLoS Pathogens 7:e1002209.
18. Go, E. P., G. Hewawasam, H.-X. Liao, H. Chen, L.-H. Ping, J. A. Anderson, D. C. Hua, B. F. Haynes, and H. Desaire 2011. Characterization of glycosylation profiles of HIV-1 transmitted/founder envelopes by mass spectrometry. J. Virol. 85:8270-8284.
19. Hecht, F. M., W. Hartogensis, L. Bragg, P. Bacchetti, R. Atchison, R. Grant, J. Barbour, and S. G. Deeks 2010. HIV RNA level in early infection is predicted by viral load in the transmission source. AIDS 24:941-945.
20. Herbeck, J. T., V. Müller, B. S. Maust, B. Ledergerber, C. Torti, S. Di Giambenedetto, L. Gras, H. F. Günthard, L. P. Jacobson, J. I. Mullins, et al. 2011. Is the virulence of HIV changing? A meta-analysis of trends in prognostic markers of HIV disease progression and transmission. AIDS 26:193-205.
21. Hollingsworth, T. D., O. Laeyendecker, G. Shirreff, C. A. Donnelly, D. Serwadda, M. J. Wawer, N. Kiwanuka, F. Nalugoda, A. Collinson-Streng, V. Ssempijja, et al. 2010. HIV-1 transmitting couples have similar viral load set-points in Rakai, Uganda. PLoS Pathogens 6:e1000876.
22. Joos, B., A. Trkola, M. Fischer, H. Kuster, P. Rusert, C. Leemann, J. Boni, A. Oxenius, D. A. Price, R. E. Phillips, et al. 2005. Low human immunodeficiency virus envelope diversity correlates with low In vitro replication capacity and predicts spontaneous control of plasma viremia after treatment interruptions. J. Virol. 79:9026-9037.
23. Keele, B. F., E. E. Giorgi, J. F. Salazar-Gonzalez, J. M. Decker, K. T. Pham, M. G. Salazar, C. Sun, T. Grayson, S. Wang, et al. 2008. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc. Natl. Acad. Sci. USA 105:7552-7557.
24. Korenromp, E. L., B. G. Williams, G. P. Schmid, and C. Dye 2009. Clinical prognostic value of RNA viral load and CD4 cell counts during untreated HIV-1 infection-a quantitative review. PLoS One 4:12.
25. Kouyos, R., G. E. Leventhal, T. Hinkley, M. Haddad, J. M. Whitcomb, C. J. Petropoulos, and S. Bonhoeffer 2012. Exploring the complexity of the HIV-1 fitness landscape. PLoS Genet. 8:e1002551.
26. Kouyos, R., V. von Wyl, T. Hinkley, C. J. Petropoulos, M. Haddad, J. M. Whitcomb, J. Böni, S. Yerly, C. Cellerai, T. Klimkait, et al. 2011. Assessing predicted HIV-1 replicative capacity in a clinical setting. PLoS Pathogens 7:e1002321.
27. Lemey, P., S. L. Kosakovsky Pond, A. J. Drummond, O. G. Pybus, B. Shapiro, H. Barroso, N. Taveira, and A. Rambaut 2007. Synonymous substitution rates predict HIV disease progression as a result of underlying replication dynamics. PLoS Comput. Biol. 3:e29.
28. Levin, B. R., and J. J. Bull 1994. Short-sighted evolution and the virulence of pathogenic microorganisms. Trends Microbiol. 2:76-81.
29. Luciani, F., and S. Alizon 2009. The evolutionary dynamics of a rapidly mutating virus within and between hosts: the case of hepatitis C virus. PLoS Comput. Biol. 5:e1000565.
30. Lythgoe, K. A., and C. Fraser 2012. New insights into the evolutionary rate of HIV-1 at the within-host and epidemiological levels. Proc. R. Soc. B: Biol. Sci. 279:3367-3375.
31. Mansky, L. M., and H. M. Temin 1995. Lower in vivo mutation rate of human immunodeficiency virus type 1 than that predicted from the fidelity of purified reverse transcriptase. Microbiology 69:5087-5094.
32. Mellors, J. W., C. R. Rinaldo, P. Gupta, R. M. White, J. A. Todd, and L. A. Kingsley 1996. Prognosis in HIV-1 infection predicted by the quantity of virus in plasma. Science 272:1167-1170.
33. Mollison, D. 1991. Dependence of epidemic and population velocities on basic parameters. Math. Biosci. 107:255-287.
34. Mostowy, R., R. Kouyos, I. Hoof, T. Hinkley, M. Haddad, J. M. Whitcomb, C. J. Petropoulos, C. Keşmir, and S. Bonhoeffer 2012. Estimating the fitness cost of escape from HLA presentation in HIV-1 protease and reverse transcriptase. PLoS Comput. Biol. 8:e1002525.
35. Müller, V., C. Fraser, and J. T. Herbeck 2011. A strong case for viral genetic factors in HIV virulence. Viruses 3:204-216.
36. Nowak, M. A. 2006. Evolutionary dynamics: exploring the equations of life. Belknap Press of Harvard University Press, Cambridge, USA.
37. Quiñones-Mateu, M. E., S. C. Ball, A. J. Marozsan, V. S. Torre, J. L. Albright, G. Vanham, G. Van Der Groen, R. L. Colebunders, and E. J. Arts 2000. A dual infection/competition assay shows a correlation between ex vivo human immunodeficiency virus type 1 fitness and disease progression. J. Virol. 74:9222-9233.
38. Rankin, D. J., K. Bargum, and H. Kokko 2007. The tragedy of the commons in evolutionary biology. Trends Ecol. Evol. 22:643-651.
39. Redd, A. D., A. N. Collinson-Streng, N. Chatziandreou, C. E. Mullis, O. Laeyendecker, C. Martens, S. Ricklefs, N. Kiwanuka, P. H. Nyein, T. Lutalo, et al. 2012a. Previously transmitted HIV-1 strains are preferentially selected during subsequent sexual transmissions. J. Infect. Dis. 206:1433-1442.
40. Redd, A. D., C. E. Mullis, D. Serwadda, X. Kong, C. Martens, S. M. Ricklefs, A. A. R. Tobian, C. Xiao, M. K. Grabowski, F. Nalugoda, et al. 2012b. The rates of HIV superinfection and primary HIV incidence in a general population in Rakai, Uganda. J. Infect. Dis. 206:267-274.
41. Saenz, R. A., and S. Bonhoeffer 2013. Nested model reveals potential amplification of an HIV epidemic due to drug resistance. Epidemics 5:34-43.
42. Sasaki, A., and Y. Iwasa 1991. Optimal growth schedule of pathogens within a host: switching between lytic and latent cycles. Theor. Popul. Biol. 239:201-239.
43. Shankarappa, R. A. J., J. B. Margolick, S. J. Gange, A. G. Rodrigo, D. Upchurch, H. Farzadegan, P. Gupta, C. R. Rinaldo, G. H. Learn, X. I. He, et al. 1999. Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection. J. Virol. 73:10489-10502.
44. Shirreff, G., L. Pellis, O. Laeyendecker, and C. Fraser 2011. Transmission selects for HIV-1 strains of intermediate virulence: a modelling approach. PLoS Comput. Biol. 7:e1002185.
45. Tang, J., S. Tang, E. Lobashevsky, I. Zulu, G. Aldrovandi, S. Allen, and R. A. Kaslow 2004. HLA allele sharing and HIV type 1 viremia in seroconverting Zambians with known transmitting partners. AIDS Res. Human Retroviruses 20:19-25.
46. Trkola, A., H. Kuster, C. Leemann, C. Ruprecht, B. Joos, A. Telenti, B. Hirschel, R. Weber, S. Bonhoeffer, and H. F. Günthard 2003. Human immunodeficiency virus type 1 fitness is a determining factor in viral rebound and set point in chronic infection. J. Virol. 77:13146-13155.
47. Troyer, R. M., K. R. Collins, A. Abraha, E. Fraundorf, D. M. Moore, R. W. Krizan, Z. Toossi, R. L. Colebunders, M. A. Jensen, J. I. Mullins, et al. 2005. Changes in human immunodeficiency virus type 1 fitness and genetic diversity during disease progression. J. Virol. 79:9006-9018.
48. Van der Kuyl, A. C., S. Jurriaans, G. Pollakis, M. Bakker, and M. Cornelissen 2010. HIV RNA levels in transmission sources only weakly predict plasma viral load in recipients. AIDS 24:1607-1608.