Identification of diverse full-length endogenous betaretroviruses in megabats and microbats

Retrovirology

Volumn 10, Issue 1, 2013, Pages

  Hayward, Joshua A ^a,b   Tachedjian, Mary ^c   Cui, Jie ^d   Field, Hume ^e   Holmes, Edward C ^d,f   Wang, Lin Fa ^c,g,h   Tachedjian, Gilda ^a,b,i  

^a BURNET INSTITUTE   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c CSIRO   (Australia)

^d UNIVERSITY OF SYDNEY   (Australia)

^e DEPARTMENT OF AGRICULTURE AND FISHERIES   (Australia)

^f NATIONAL INSTITUTES OF HEALTH   (United States)

^g DUKE NUS MEDICAL SCHOOL   (Singapore)

^h UNIVERSITY OF MELBOURNE   (Australia)

ⁱ MONASH UNIVERSITY   (Australia)

Author keywords

Bats; Betaretrovirus; Endogenous; Evolution; Myotis; Pteropus; Retrovirus; Rhinolophus

Indexed keywords

GAG PROTEIN; LYSINE; TRANSCRIPTOME; TRANSFER RNA;

ARTICLE; BETARETROVIRUS INFECTION; CLADISTICS; CONTROLLED STUDY; ENDOGENOUS RETROVIRUS; ENVELOPE GENE; GENETIC VARIABILITY; GROUP SPECIFIC ANTIGEN GENE; HOST RANGE; LONG TERMINAL REPEAT; MICROBIAL DIVERSITY; MOLECULAR CLOCK; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENETIC TREE; SEQUENCE ANALYSIS; STRUCTURAL GENE; VIRUS GENOME; VIRUS IDENTIFICATION; VIRUS TRANSMISSION;

ANIMALS; BETARETROVIRUS; CHIROPTERA; CLUSTER ANALYSIS; DNA, VIRAL; ENDOGENOUS RETROVIRUSES; EVOLUTION, MOLECULAR; PHYLOGENY; SEQUENCE ANALYSIS, DNA;

ANIMALIA; BETARETROVIRUS; GAMMARETROVIRUS; HUMAN ENDOGENOUS RETROVIRUS K; MAMMALIA; METATHERIA; MYOTIS; OVIS ARIES; PRIMATES; PTEROPUS; RHINOLOPHUS; RODENTIA;

EID: 84875297571     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-10-35     Document Type: Article

References (72)

1. Vogt VM. Historical introduction to the general properties of retroviruses. Retroviruses 1997, New York, USA: Cold Spring Harbor Laboratory Press, Coffin JM, Hughes SH, Varmus HE.
2. Stoye JP. Studies of endogenous retroviruses reveal a continuing evolutionary saga. Nat Rev Micro 2012, 10:395-406.
3. Kurth R, Bannert N. Retroviruses 2010, Berlin: Caister Academic Press.
4. Vogt VM. Retroviral virions and genomes. Retroviruses 1997, New York, USA: Cold Spring Harbor Laboratory Press, Coffin JM, Hughes SH, Varmus HE.
5. Cavallari I, Rende F, D'Agostino DM, Ciminale V. Converging strategies in expression of human complex retroviruses. Viruses 2011, 3:1395-1414. 10.3390/v3081395, 3185809, 21994786.
6. Gao F, Bailes E, Robertson DL, Chen Y, Rodenburg CM, Michael SF, Cummins LB, Arthur LO, Peeters MS, M G, Sharp PM, Hahn BH. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 1999, 397:436. 10.1038/17130, 9989410.
7. Callahan ME, Switzer WM, Matthews AL, Roberts BD, Heneine W, Folks TM, Sandstrom PA. Persistent zoonotic infection of a human with simian foamy virus in the absence of an intact orf-2 accessory gene. J Virol 1999, 73:9619-9624. 112999, 10516073.
8. Matsuoka M, Jeang KT. Human T-cell leukemia virus type 1 (HTLV-1) and leukemic transformation: viral infectivity, Tax, HBZ and therapy. Oncogene 2011, 30:1379-1389. 10.1038/onc.2010.537, 3413891, 21119600.
9. Subramanian RP, Wildschutte JH, Russon C, Coffin JM. Identification, characterization, and comparative genomic distribution of the HERV-K (HML-2) group of human endogenous retroviruses. Retrovirology 2011, 8:1. 10.1186/1742-4690-8-1, 3022809, 21210996.
10. Zhao J, Rycaj K, Geng S, Li M, Plummer JB, Yin B, Liu H, Xu X, Zhang Y, Yan Y. Expression of human endogenous retrovirus type K envelope protein is a novel candidate prognostic marker for human breast cancer 2012, Cancer: Genes.
11. Cadieux C, Kedinger V, Yao L, Vadnais C, Drossos M, Paquet M, Nepveu A. Mouse mammary tumor virus p75 and p110 CUX1 transgenic mice develop mammary tumors of various histologic types. Cancer Res 2009, 69:7188-7197. 10.1158/0008-5472.CAN-08-4899, 19738070.
12. Sonigo P, Barker C, Hunter E, Wain-Hobson S. Nucleotide sequence of Mason-Pfizer monkey virus: An immunosuppressive D-type retrovirus. Cell 1986, 45:375-385. 10.1016/0092-8674(86)90323-5, 2421920.
13. Wootton SK, Halbert CL, Miller AD. Sheep retrovirus structural protein induces lung tumours. Nature 2005, 434:904-907. 10.1038/nature03492, 1401489, 15829964.
14. Petropoulos C. Retroviral taxonomy, protein structures, sequences, and genetic maps. Retroviruses 1997, 757-806. New York, USA: Cold Spring Harbor Laboratory Press, Coffin JM, Hughes SH, Varmus HE.
15. Barabás O. dUTPase and nucleocapsid polypeptides of the Mason-Pfizer monkey virus form a fusion protein in the virion with homotrimeric organization and low catalytic efficiency. J Biol Chem 2003, 278:38803. 10.1074/jbc.M306967200, 12869552.
16. Németh-Pongrácz V, Barabás O, Fuxreiter M, Simon I, Pichová I, Rumlová M, Zábranská H, Svergun D, Petoukhov M, Harmat V. Flexible segments modulate co-folding of dUTPase and nucleocapsid proteins. Nuc Acid Res 2007, 35:495-505.
17. Mertz JA, Simper MS, Lozano MM, Payne SM, Dudley JP. Mouse mammary tumor virus encodes a self-regulatory RNA export protein and is a complex retrovirus. J Virol 2005, 79:14737-14747. 10.1128/JVI.79.23.14737-14747.2005, 1287593, 16282474.
18. Salmons B, Erfle V, Brem G, Günzburg WH. naf, a trans-regulating negative-acting factor encoded within the mouse mammary tumor virus open reading frame region. J Virol 1990, 64:6355-6359. 248820, 2173798.
19. Indik S, Günzburg WH, Salmons B, Rouault F. A novel, mouse mammary tumor virus encoded protein with Rev-like properties. Virology 2005, 337:1-6. 10.1016/j.virol.2005.03.040, 15914215.
20. Marrack P, Kushnir E, Kappler J. A maternally inherited superantigen encoded by a mammary tumour virus. Nature 1991, 349:524-526. 10.1038/349524a0, 1846947.
21. Nitta T, Hofacre A, Hull S, Fan H. Identification and mutational analysis of a Rej response element in Jaagsiekte sheep retrovirus RNA. J Virol 2009, 83:12499-12511. 10.1128/JVI.01754-08, 2786709, 19776134.
22. Bray M, Prasad S, Dubay JW, Hunter E, Jeang KT, Rekosh D, Hammarskjöld ML. A small element from the Mason-Pfizer monkey virus genome makes human immunodeficiency virus type 1 expression and replication Rev-independent. Proc Natl Acad Sci USA 1994, 91:1256-1260. 10.1073/pnas.91.4.1256, 43136, 8108397.
23. Zolotukhin AS, Michalowski D, Smulevitch S, Felber BK. Retroviral constitutive transport element evolved from cellular TAP(NXF1)-binding sequences. J Virol 2001, 75:5567-5575. 10.1128/JVI.75.12.5567-5575.2001, 114269, 11356964.
24. Feschotte C, Gilbert C. Endogenous viruses: insights into viral evolution and impact on host biology. Nat Rev Genet 2012, 13:283-296.
25. Baillie GJ, van-de-Lagemaat LN, Baust C, Mager DL. Multiple groups of endogenous betaretroviruses in mice, rats, and other mammals. J Virol 2004, 78:5784. 10.1128/JVI.78.11.5784-5798.2004, 415799, 15140976.
26. Baillie GJ, Wilkins RJ. Endogenous type D retrovirus in a marsupial, the common brushtail possum (Trichosurus vulpecula). J Virol 2001, 75:2499. 10.1128/JVI.75.5.2499-2507.2001, 114837, 11160757.
27. Van der Kuyl AC. Characterization of a full-length endogenous beta-retrovirus, EqERV-Beta1, in the genome of the horse (Equus caballus). Viruses 2011, 3:620. 10.3390/v3060620, 3185775, 21994749.
28. Teeling EC, Springer MS, Madsen O, Bates P, O'Brien SJ, Murphy WJ. A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 2005, 307:580-584. 10.1126/science.1105113, 15681385.
29. Zhang G, Cowled C, Shi Z, Huang Z, Bishop-Lilly KA, Fang X, Wynne JW, Xiong Z, Baker ML, Zhao W. Comparative analysis of bat genomes provides insight into the evolution of flight and immunity. Science 2013, 339:456-460. 10.1126/science.1230835, 23258410.
30. Calisher CH, Childs JE, Field HE, Holmes KV, Schountz T. Bats: Important reservoir hosts of emerging viruses. Clin Microbiol Rev 2006, 19:531-545. 10.1128/CMR.00017-06, 1539106, 16847084.
31. Baker ML, Schountz T, Wang LF. Antiviral immune responses of bats: A review. Zoonoses Public Health 2013, 60:104-116. 10.1111/j.1863-2378.2012.01528.x, 23302292.
32. Simmons NB, Seymour KL, Habersetzer J, Gunnell GF. Primitive early eocene bat from Wyoming and the evolution of flight and echolocation. Nature 2008, 451:818-821. 10.1038/nature06549, 18270539.
33. Eaton BT, Broder CC, Middleton D, Wang L-F. Hendra and nipah viruses: Different and dangerous. Nat Rev Micro 2006, 4:23-35.
34. Leroy EM, Kumulungui B, Pourrut X, Rouquet P, Hassanin A, Yaba P, Delicat A, Paweska JT, Gonzalez J-P, Swanepoel R. Fruit bats as reservoirs of ebola virus. Nature 2005, 438:575-576. 10.1038/438575a, 16319873.
35. Li W, Shi Z, Yu M, Ren W, Smith C, Epstein JH, Wang H, Crameri G, Hu Z, Zhang H. Bats are natural reservoirs of SARS-like coronaviruses. Science 2005, 310:676-679. 10.1126/science.1118391, 16195424.
36. Cui J, Tachedjian G, Tachedjian M, Holmes EC, Zhang S, Wang L-F. Identification of diverse groups of endogenous gammaretroviruses in mega and microbats. J Gen Virol 2012, 93:2037-2045. 10.1099/vir.0.043760-0, 22694899.
37. Cui J, Tachedjian M, Wang L, Tachedjian G, Wang L-F, Zhang S. Discovery of retroviral homologs in bats: implications for the origin of mammalian gammaretroviruses. J Virol 2012, 86:4288-4293. 10.1128/JVI.06624-11, 3318619, 22318134.
38. Sommerfelt MA, Weiss RA. Receptor interference groups of 20 retroviruses plating on human cells. Virology 1990, 176:58-69. 10.1016/0042-6822(90)90230-O, 1691887.
39. Edwards SA, Fan H. gag-Related polyproteins of Moloney murine leukemia virus: evidence for independent synthesis of glycosylated and unglycosylated forms. J Virol 1979, 30:551-563. 353359, 469993.
40. Nitta T. Moloney murine leukemia virus glyco-gag facilitates xenotropic murine leukemia virus-related virus replication through human APOBEC3-independent mechanisms. Retrovirology 2012, 9:58. 10.1186/1742-4690-9-58, 3423011, 22828015.
41. Kijima TE, Innan H. On the estimation of the insertion time of LTR retrotransposable elements. Mol Biol Evol 2010, 27:896-904. 10.1093/molbev/msp295, 19955475.
42. Armbruester V, Sauter M, Krautkraemer E, Meese E, Kleiman A, Best B, Roemer K, Mueller-Lantzsch N. A novel gene from the human endogenous retrovirus K expressed in transformed cells. Clin Cancer Res 2002, 8:1800-1807.
43. Galli UM, Sauter M, Lecher B, Maurer S, Herbst H, Roemer K, Mueller-Lantzsch N. Human endogenous retrovirus rec interferes with germ cell development in mice and may cause carcinoma in situ, the predecessor lesion of germ cell tumors. Oncogene 2005, 24:3223-3228. 10.1038/sj.onc.1208543, 15735668.
44. Shao W, Boltz V, Spindler J, Kearney M, Maldarelli F, Mellors J, Stewart C, Volfovsky N, Levitsky A, Stephens R, Coffin J. Analysis of 454 sequencing error rate, error sources, and artifact recombination for detection of Low-frequency drug resistance mutations in HIV-1 DNA. Retrovirology 2013, 10:18. 10.1186/1742-4690-10-18, 3599717, 23402264.
45. Rosati S, Pittau M, Alberti A, Pozzi S, York DF, Sharp JM, Palmarini M. An accessory open reading frame (orf-x) of jaagsiekte sheep retrovirus is conserved between different virus isolates. Virus Res 2000, 66:109-116. 10.1016/S0168-1702(99)00118-5, 10653922.
46. Lewinski MK, Yamashita M, Emerman M, Ciuffi A, Marshall H, Crawford G, Collins F, Shinn P, Leipzig J, Hannenhalli S. Retroviral DNA integration: viral and cellular determinants of target-site selection. PLoS Pathog 2006, 2:e60. 10.1371/journal.ppat.0020060, 1480600, 16789841.
47. Anai Y, Ochi H, Watanabe S, Nakagawa S, Kawamura M, Gojobori T, Nishigaki K. Infectious endogenous retroviruses in cats and emergence of recombinant viruses. J Virol 2012, 86:8634-8644. 10.1128/JVI.00280-12, 3421742, 22674983.
48. York DF, Vigne R, Verwoerd DW, Querat G. Nucleotide sequence of the jaagsiekte retrovirus, an exogenous and endogenous type D and B retrovirus of sheep and goats. J Virol 1992, 66:4930-4939. 241337, 1629959.
49. Tristem M. Identification and characterization of novel human endogenous retrovirus families by phylogenetic screening of the human genome mapping project database. J Virol 2000, 74:3715-3730. 10.1128/JVI.74.8.3715-3730.2000, 111881, 10729147.
50. Löwer R, Tönjes RR, Korbmacher C, Kurth R, Löwer J. Identification of a Rev-related protein by analysis of spliced transcripts of the human endogenous retroviruses HTDV/HERV-K. J Virol 1995, 69:141-149. 188557, 7983704.
51. Magin-Lachmann C, Hahn S, Strobel H, Held U, Löwer J, Löwer R. Rec (Formerly Corf) function requires interaction with a complex, folded RNA structure within its responsive element rather than binding to a discrete specific binding site. J Virol 2001, 75:10359-10371. 10.1128/JVI.75.21.10359-10371.2001, 114610, 11581404.
52. Müllner M, Salmons B, Günzburg WH, Indik S. Identification of the Rem-responsive element of mouse mammary tumor virus. Nuc Acid Res 2008, 36:6284.
53. Hofacre A, Nitta T, Fan H. Jaagsiekte sheep retrovirus encodes a regulatory factor, Rej, required for synthesis of gag protein. J Virol 2009, 83:12483-12498. 10.1128/JVI.01747-08, 2786725, 19776124.
54. Hatziioannou T, Bieniasz PD. Antiretroviral restriction factors. Curr Opin Virol 2011, 1:526-532. 10.1016/j.coviro.2011.10.007, 3263365, 22278313.
55. Churakov G, Sadasivuni MK, Rosenbloom KR, Huchon D, Brosius J, Schmitz J. Rodent evolution: Back to the root. Mol Biol Evol 2010, 27:1315-1326. 10.1093/molbev/msq019, 20100942.
56. Lawson JS, Glenn WK, Salmons B, Ye Y, Heng B, Moody P, Johal H, Rawlinson WD, Delprado W, Lutze-Mann L, Whitaker NJ. Mouse mammary tumor virus-like sequences in human breast cancer. Cancer Res 2010, 70:3576-3585. 10.1158/0008-5472.CAN-09-4160, 20388779.
57. Pogo BGT, Holland JF, Levine PH. Human mammary tumor virus in inflammatory breast cancer. Cancer 2010, 116:2741-2744. 10.1002/cncr.25179, 20503403.
58. Xu L, Sakalian M, Shen Z, Loss G, Neuberger J, Mason A. Cloning the human betaretrovirus proviral genome from patients with primary biliary cirrhosis. Hepatology 2004, 39:151-156. 10.1002/hep.20024, 14752833.
59. Johnson J, Gates J, Ford W. Distribution and activity of bats at local and landscape scales within a rural-urban gradient. Urban Ecosystems 2008, 11:227-242.
60. Mickleburgh S, Waylen K, Racey PA. Bats as bushmeat: a global review. Fauna & Flora International 2009, 43:217-234.
61. Papenfuss AT, Baker M, Feng Z-P, Tachedjian M, Crawmeri G, Cowled C, Ng J, Janardhana V, Field HE, Wang L-F. The immune gene repertoire of an important viral reservoir, the Australian black flying fox. BMC Genomics 2012, 13:261. 10.1186/1471-2164-13-261, 3436859, 22716473.
62. Reese MG. Application of a time-delay neural network to promoter annotation in the Drosophila melanogaster genome. Comput Chem 2001, 26:51-56. 10.1016/S0097-8485(01)00099-7, 11765852.
63. Milanesi L, Muselli M, Arrigo P. Hamming-Clustering method for signals prediction in 5′ and 3′ regions of eukaryotic genes. Comput Appl Biosci 1996, 12:399-404.
64. Jühling F, Mörl M, Hartmann RK, Sprinzl M, Stadler PF, Pütz J. tRNAdb 2009: compilation of tRNA sequences and tRNA genes. Nuc Acid Res 2009, 37:D159-D162.
65. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J. The Pfam protein families database. Nuc Acid Res 2012, 40:D290-D301.
66. Kosugi S, Hasebe M, Tomita M, Yanagawa H. Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc Natl Acad Sci USA 2009, 106:10171-10176. 10.1073/pnas.0900604106, 2695404, 19520826.
67. la Cour T, Kiemer L, Mølgaard A, Gupta R, Skriver K, Brunak S. Analysis and prediction of leucine-rich nuclear export signals. Protein Eng Des Sel 2004, 17:527-536. 10.1093/protein/gzh062, 15314210.
68. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nuc Acid Res 2004, 32:1792-1797.
69. Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 2007, 56:564-577. 10.1080/10635150701472164, 17654362.
70. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010, 59:307-321. 10.1093/sysbio/syq010, 20525638.
71. Abascal F, Zardoya R, Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005, 21:2104-2105. 10.1093/bioinformatics/bti263, 15647292.
72. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 2012, 29:1969-1973. 10.1093/molbev/mss075, 3408070, 22367748.