Dual Host-Virus Arms Races Shape an Essential Housekeeping Protein

PLoS Biology

Volumn 11, Issue 5, 2013, Pages

  Demogines, Ann ^a   Abraham, Jonathan ^b   Choe, Hyeryun ^b   Farzan, Michael ^c   Sawyer, Sara L ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CD71 ANTIGEN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CELL FUNCTION; CLADISTICS; GENE LOCUS; GENETIC CONSERVATION; GENETIC VARIABILITY; HOUSEKEEPING GENE; HUMAN; HUMAN CELL; IRON TRANSPORT; MOLECULAR EVOLUTION; MOUSE; MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN FUNCTION; RAT; RECEPTOR BINDING; TFR1 GENE; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS TRANSMISSION; ZOONOSIS;

AMINO ACID SEQUENCE; ANIMALS; ARENAVIRUSES, NEW WORLD; CELL LINE; DOGS; GENES, ESSENTIAL; HUMANS; IRON; MICE; MOLECULAR SEQUENCE DATA; MUTATION; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, TRANSFERRIN; RECEPTORS, VIRUS; VIRAL PROTEINS; VIRUS INTERNALIZATION; ZOONOSES;

MAMMALIA; RODENTIA;

EID: 84878323925     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001571     Document Type: Article

References (95)

1. Aisen P, (2004) Transferrin receptor 1. Int J Biochem Cell Biol 36: 2137-2143.
2. Bennett MJ, Lebrón JA, Bjorkman PJ, (2000) Crystal structure of the hereditary haemochromatosis protein HFE complexed with transferrin receptor. Nature 403: 46-53.
3. Eckenroth BE, Steere AN, Chasteen ND, Everse SJ, Mason AB, (2011) How the binding of human transferrin primes the transferrin receptor potentiating iron release at endosomal pH. Proc Natl Acad Sci USA 108: 13089-13094.
4. Cheng Y, Zak O, Aisen P, Harrison SC, Walz T, (2004) Structure of the human transferrin receptor-transferrin complex. Cell 116: 565-576.
5. Abraham J, Corbett KD, Farzan M, Choe H, Harrison SC, (2010) Structural basis for receptor recognition by New World hemorrhagic fever arenaviruses. Nat Struct Mol Biol 17: 438-444.
6. Radoshitzky SR, Abraham J, Spiropoulou CF, Kuhn JH, Nguyen D, et al. (2007) Transferrin receptor 1 is a cellular receptor for New World haemorrhagic fever arenaviruses. Nature 446: 92-96.
7. Radoshitzky SR, Kuhn JH, Spiropoulou CF, Albariño CG, Nguyen DP, et al. (2008) Receptor determinants of zoonotic transmission of New World hemorrhagic fever arenaviruses. Proc Natl Acad Sci USA 105: 2664-2669.
8. Abraham J, Kwong JA, Albariño CG, Lu JG, Radoshitzky SR, et al. (2009) Host-species Transferrin Receptor 1 orthologs are cellular receptors for nonpathogenic New World clade B arenaviruses. PLoS Pathog 5: e1000358 doi:10.1371/journal.ppat.1000358.
9. Flanagan ML, Oldenburg J, Reignier T, Holt N, Hamilton GA, et al. (2008) New world clade B arenaviruses can use transferrin receptor 1 (TfR1)-dependent and-independent entry pathways, and glycoproteins from human pathogenic strains are associated with the use of TfR1. J Virology 82: 938-948.
10. Choe H, Jemielity S, Abraham J, Radoshitzky SR, Farzan M, (2011) Transferrin receptor 1 in the zoonosis and pathogenesis of New World hemorrhagic fever arenaviruses. Curr Opin Microbiol 14: 476-482.
11. Charrel RN, de Lamballerie X, (2003) Arenaviruses other than Lassa virus. Antiviral Res 57: 89-100.
12. Ross SR, Schofield JJ, Farr CJ, Bucan M, (2002) Mouse transferrin receptor 1 is the cell entry receptor for mouse mammary tumor virus. Proc Natl Acad Sci USA 99: 12386-12390.
13. Wang E, Albritton L, Ross SR, (2006) Identification of the segments of the mouse transferrin receptor 1 required for mouse mammary tumor virus infection. J Biol Chem 281: 10243-10249.
14. Wang E, Obeng-Adjei N, Ying Q, Meertens L, Dragic T, et al. (2008) Mouse mammary tumor virus uses mouse but not human transferrin receptor 1 to reach a low pH compartment and infect cells. Virology 381: 230-240.
15. Bhadra S, Lozano MM, Dudley JP, (2005) Conversion of mouse mammary tumor virus to a lymphomagenic virus. J Virology 79: 12592-12596.
16. Parker JS, Murphy WJ, Wang D, O'Brien SJ, Parrish CR, (2001) Canine and feline parvoviruses can use human or feline transferrin receptors to bind, enter, and infect cells. J Virology 75: 3896-3902.
17. Allison AB, Harbison CE, Pagan I, Stucker KM, Kaelber JT, et al. (2011) Role of multiple hosts in the cross-species transmission and emergence of a pandemic parvovirus. J Virology 86: 865-872.
18. Parrish CR, Kawaoka Y, (2005) The origins of new pandemic viruses: the acquisition of new host ranges by canine parvovirus and influenza A viruses. Annu Rev Microbiol 59: 553-586.
19. Stucker KM, Pagan I, Cifuente JO, Kaelber JT, Lillie TD, et al. (2012) The role of evolutionary intermediates in the host adaptation of canine parvovirus. J Virology 86: 1514-1521.
20. Friedel CC, Haas J, (2011) Virus-host interactomes and global models of virus-infected cells. Trends Microbiol 19: 501-508.
21. Riddick NE, Hermann EA, Loftin LM, Elliott ST, Wey WC, et al. (2010) A novel CCR5 mutation common in sooty mangabeys reveals SIVsmm infection of CCR5-null natural hosts and efficient alternative coreceptor use in vivo. PLoS Pathog 6: e1001064 doi:10.1371/journal.ppat.1001064.
22. Galvani AP, Novembre J, (2005) The evolutionary history of the CCR5-Delta32 HIV-resistance mutation. Microbes Infect 7: 302-309.
23. Chen Z, Kwon D, Jin Z, Monard S, Telfer P, et al. (1998) Natural infection of a homozygous delta24 CCR5 red-capped mangabey with an R2b-tropic simian immunodeficiency virus. J Exp Med 188: 2057-2065.
24. Zimmerman PA, Woolley I, Masinde GL, Miller SM, McNamara DT, et al. (1999) Emergence of FY*A(null) in a Plasmodium vivax-endemic region of Papua New Guinea. Proc Natl Acad Sci USA 96: 13973-13977.
25. Tournamille C, Colin Y, Cartron J-P, Le Van Kim C, (1995) Disruption of a GATA motif in the Duffy gene promoter abolishes erythroid gene expression in Duffy-negative individuals. Nat Genet 10: 224-228.
26. Tung J, Primus A, Bouley AJ, Severson TF, Alberts SC, et al. (2009) Evolution of a malaria resistance gene in wild primates. Nature 460: 388-391.
27. Clifford HD, Hayden CM, Khoo SK, Zhang G, Le Souef PN, et al. (2012) CD46 measles virus receptor polymorphisms influence receptor protein expression and primary measles vaccine responses in naive Australian children. Clinical and Vaccine Immunology 19: 704-710.
28. Jern P, Coffin JM, (2008) Effects of retroviruses on host genome function. Annu Rev Genet 42: 709-732.
29. Stoye JP, (2012) Studies of endogenous retroviruses reveal a continuing evolutionary saga. Nat Rev Micro 10: 395-406.
30. Kozak CA, Gromet NJ, Ikeda H, Buckler CE, (1984) A unique sequence related to the ecotropic murine leukemia virus is associated with the Fv-4 resistance gene. Proc Natl Acad Sci USA 81: 834-837.
31. Ikeda H, Sugimura H, (1989) Fv-4 resistance gene: a truncated endogenous murine leukemia virus with ecotropic interference properties. J Virology 63: 5405-5412.
32. Limjoco TI, Dickie P, Ikeda H, Silver J, (1993) Transgenic Fv-4 mice resistant to Friend virus. J Virology 67: 4163-4168.
33. Spencer TE, Mura M, Gray CA, Griebel PJ, Palmarini M, (2003) Receptor usage and fetal expression of ovine endogenous betaretroviruses: implications for coevolution of endogenous and exogenous retroviruses. J Virology 77: 749-753.
34. Robinson HL, Astrin SM, Senior AM, Salazar FH, (1981) Host susceptibility to endogenous viruses: defective, glycoprotein-expressing proviruses interfere with infections. J Virology 40: 745-751.
35. McDougall AS, Terry A, Tzavaras T, Cheney C, Rojko J, et al. (1994) Defective endogenous proviruses are expressed in feline lymphoid cells: evidence for a role in natural resistance to subgroup B feline leukemia viruses. J Virology 68: 2151-2160.
36. Aswad A, Katzourakis A, (2012) Paleovirology and virally derived immunity. Trends Ecol Evol (Amst) 27: 627-636.
37. Wilkins C, Gale M, (2010) Recognition of viruses by cytoplasmic sensors. Curr Opin Immunol 22: 41-47.
38. Malim MH, Bieniasz PD, (2012) HIV restriction factors and mechanisms of evasion. Cold Spring Harb Perspect Med 2: a006940.
39. Bowie AG, Unterholzner L, (2008) Viral evasion and subversion of pattern-recognition receptor signalling. Nat Rev Immunol 8: 911-922.
40. Malim MH, Emerman M, (2008) HIV-1 accessory proteins-ensuring viral survival in a hostile environment. Cell Host Microbe 3: 388-398.
41. Sawyer SL, Wu LI, Emerman M, Malik HS, (2005) Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc Natl Acad Sci USA 102: 2832-2837.
42. Lim ES, Fregoso OI, McCoy CO, Matsen FA, Malik HS, et al. (2012) The ability of primate lentiviruses to degrade the monocyte restriction factor SAMHD1 preceded the birth of the viral accessory protein Vpx. Cell Host Microbe 11: 194-204.
43. Compton AA, Hirsch VM, Emerman M, (2012) The host restriction factor APOBEC3G and retroviral vif protein coevolve due to ongoing genetic conflict. Cell Host Microbe 11: 91-98.
44. Lim ES, Malik HS, Emerman M, (2010) Ancient adaptive evolution of tetherin shaped the functions of Vpu and Nef in human immunodeficiency virus and primate lentiviruses. J Virology 84: 7124-7134.
45. McNatt MW, Zang T, Hatziioannou T, Bartlett M, Fofana IB, et al. (2009) Species-specific activity of HIV-1 Vpu and positive selection of tetherin transmembrane domain variants. PLoS Pathog 5: e1000300 doi: 10.1371/journal.ppat.1000300.
46. Laguette N, Rahm N, Sobhian B, Chable-Bessia C, Munch J, et al. (2012) Evolutionary and functional analyses of the interaction between the myeloid restriction factor SAMHD1 and the lentiviral Vpx protein. Cell Host Microbe 11: 205-217.
47. Gupta RK, Hué S, Schaller T, Verschoor E, Pillay D, et al. (2009) Mutation of a single residue renders human tetherin resistant to HIV-1 Vpu-mediated depletion. PLoS Pathog 5: e1000443 doi: 10.1371/journal.ppat.1000443.
48. Elde NC, Child SJ, Geballe AP, Malik HS, (2009) Protein kinase R reveals an evolutionary model for defeating viral mimicry. Nature 457: 485-489.
49. Patel MR, Loo Y-M, Horner SM, Gale M, Malik HS, (2012) Convergent evolution of escape from hepaciviral antagonism in primates. PLoS Biol 10: e1001282 doi: 10.1371/journal.pbio.1001282.
50. Rothenburg S, Seo EJ, Gibbs JS, Dever TE, Dittmar K, (2008) Rapid evolution of protein kinase PKR alters sensitivity to viral inhibitors. Nat Struct Mol Biol 16: 63-70.
51. Meyerson NR, Sawyer SL, (2011) Two-stepping through time: mammals and viruses. Trends Microbiol 19: 286-294.
52. Daugherty MD, Malik HS, (2012) Rules of engagement: molecular insights from host-virus arms races. Annu Rev Genet 46: 677-700.
53. Duggal NK, Emerman M, (2012) Evolutionary conflicts between viruses and restriction factors shape immunity. Nat Rev Immunol 12: 687-695.
54. Trowsdale J, Parham P, (2004) Mini-review: defense strategies and immunity-related genes. Eur J Immunol 34: 7-17.
55. Worobey M, Bjork A, Wertheim J, (2007) Point, counterpoint: the evolution of pathogenic viruses and their human hosts. Annu Rev Ecol Evol Syst pp. 1-29.
56. Johnson WE, Sawyer SL, (2009) Molecular evolution of the antiretroviral TRIM5 gene. Immunogenetics 61: 163-176.
57. Han K, Lou DI, Sawyer SL, (2011) Identification of a genomic reservoir for new TRIM genes in primate genomes. PLoS Genet 7: e1002388 doi:10.1371/journal.pgen.1002388.
58. Sawyer SL, Emerman M, Malik HS, (2004) Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS Biol 2: e275 doi: 10.1371/journal.pbio.0020275.
59. Sawyer SL, Elde NC, (2012) A cross-species view on viruses. Current Opinion in Virology 2: 561-568.
60. Kirmaier A, Wu F, Newman RM, Hall LR, Morgan JS, et al. (2010) TRIM5 suppresses cross-species transmission of a primate immunodeficiency virus and selects for emergence of resistant variants in the new species. PLoS Biol 8: e1000462 doi:10.1371/journal.pbio.1000462.
61. Götz N, Sauter D, Usmani SM, Fritz JV, Goffinet C, et al. (2012) Reacquisition of nef-mediated tetherin antagonism in a single in vivo passage of HIV-1 through its original chimpanzee host. Cell Host Microbe 12: 373-380.
62. Holmes EC, (2004) Adaptation and immunity. PLoS Biol 2: e307 doi:10.1371/journal.pbio.0020307.
63. Yang Z, Bielawski J, (2000) Statistical methods for detecting molecular adaptation. Trends Ecol Evol 15: 496-503.
64. Yang Z, (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13: 555-556.
65. Lawrence CM, Ray S, Babyonyshev M, Galluser R, Borhani DW, et al. (1999) Crystal structure of the ectodomain of human transferrin receptor. Science 286: 779-782.
66. Bowden TA, Crispin M, Graham SC, Harvey DJ, Grimes JM, et al. (2009) Unusual molecular architecture of the machupo virus attachment glycoprotein. J Virology 83: 8259-8265.
67. Baillie GJ, van de Lagemaat LN, Baust C, Mager DL, (2004) Multiple groups of endogenous betaretroviruses in mice, rats, and other mammals. J Virology 78: 5784-5798.
68. Phan TG, Kapusinszky B, Wang C, Rose RK, Lipton HL, et al. (2011) The fecal viral flora of wild rodents. PLoS Pathog 7: e1002218 doi:10.1371/journal.ppat.1002218.
69. Zhang Y, Rassa JC, deObaldia ME, Albritton LM, Ross SR, (2003) Identification of the receptor binding domain of the mouse mammary tumor virus envelope protein. J Virology 77: 10468-10478.
70. Giannetti AM, Snow PM, Zak O, Bjorkman PJ, (2003) Mechanism for multiple ligand recognition by the human transferrin receptor. PLoS Biol 1: e51 doi:10.1371/journal.pbio.0000051.
71. Borio L, Inglesby T, Peters CJ, Schmaljohn AL, Hughes JM, et al. (2002) Hemorrhagic fever viruses as biological weapons: medical and public health management. JAMA 287: 2391-2405.
72. Kaelber JT, Demogines A, Harbison CE, Allison AB, Goodman LB, et al. (2012) Evolutionary reconstructions of the transferrin receptor of Caniforms supports canine parvovirus being a re-emerged and not a novel pathogen in dogs. PLoS Pathog 8: e1002666 doi:10.1371/journal.ppat.1002666.
73. O'Brien SJ, Nelson GW, (2004) Human genes that limit AIDS. Nat Genet 36: 565-574.
74. Kozak CA, (2010) The mouse "xenotropic" gammaretroviruses and their XPR1 receptor. Retrovirology 7: 101.
75. Rainey GJA, Natonson A, Maxfield LF, Coffin JM, (2003) Mechanisms of avian retroviral host range extension. J Virology 77: 6709-6719.
76. Demogines A, Farzan M, Sawyer SL, (2012) Evidence for ACE2-utilizing coronaviruses (CoVs) related to severe acute respiratory syndrome CoV in bats. J Virology 86: 6350-6353.
77. Parrish CR, Holmes EC, Morens DM, Park E-C, Burke DS, et al. (2008) Cross-species virus transmission and the emergence of new epidemic diseases. Microbiol Mol Biol Rev 72: 457-470.
78. Stehle T, Casasnovas JM, (2009) Specificity switching in virus-receptor complexes. Curr Opin Struct Biol 19: 181-188.
79. Baranowski E, Ruiz-Jarabo CM, Domingo E, (2001) Evolution of cell recognition by viruses. Science 292: 1102-1105.
80. Demogines A, Truong KA, Sawyer SL, (2012) Species-specific features of DARC, the primate receptor for Plasmodium vivax and Plasmodium knowlesi. Mol Biol Evol 29: 445-449.
81. Demogines A, East AM, Lee J-H, Grossman SR, Sabeti PC, et al. (2010) Ancient and recent adaptive evolution of primate non-homologous end joining genes. PLoS Genet 6: e1001169 doi: 10.1371/journal.pgen.1001169.
82. Sawyer SL, Malik HS, (2006) Positive selection of yeast nonhomologous end-joining genes and a retrotransposon conflict hypothesis. Proc Natl Acad Sci USA 103: 17614-17619.
83. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG, (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
84. Darriba D, Taboada GL, Doallo R, Posada D, (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Meth 9: 772.
85. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
86. D'Elía G, Luna L, González EM, Patterson BD, (2006) On the Sigmodontinae radiation (Rodentia, Cricetidae): an appraisal of the phylogenetic position of Rhagomys. Mol Phylogenet Evol 38: 558-564.
87. Pond S, Posada D, Gravenor MB, Woelk CH, Frost SDW, (2006) GARD: a genetic algorithm for recombination detection. Bioinformatics 22: 3096-3098.
88. Goldman N, Yang Z, (1994) A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol 11: 725-736.
89. Kent WJ, (2002) BLAT-The BLAST-like alignment tool. Genome Res 12: 656-664.
90. Mouse Genome Sequencing Consortium (2002) Waterston RH, Lindblad-Toh K, Birney E, Rogers J, et al. (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420: 520-562.
91. Gibbs RA, Weinstock GM, Metzker ML, Muzny DM, Sodergren EJ, et al. (2004) Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 428: 493-521.
92. Fujita PA, Rhead B, Zweig AS, Hinrichs AS, Karolchik D, et al. (2011) The UCSC Genome Browser database: update 2011. Nucleic Acids Res 39: D876-D882.
93. Gifford R, Kabat P, Martin J, Lynch C, Tristem M, (2005) Evolution and distribution of class II-related endogenous retroviruses. J Virology 79: 6478-6486.
94. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
95. Yamashita M, Emerman M, (2004) Capsid is a dominant determinant of retrovirus infectivity in nondividing cells. J Virology 78: 5670-5678.