Identification of an overprinting gene in Merkel cell polyomavirus provides evolutionary insight into the birth of viral genes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 31, 2013, Pages 12744-12749

  Carter, Joseph J ^a   Daugherty, Matthew D ^c   Qi, Xiaojie ^a   Bheda Malge, Anjali ^a,e   Wipf, Gregory C ^a   Robinson, Kristin ^a   Roman, Ann ^a   Malik, Harmit S ^c,d   Galloway, Denise A ^a,b  

^a Division of Human Biology   (United States)

^b Division of Public Health Sciences   (United States)

^c Division of Basic Sciences   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^e INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

Author keywords

Disordered motifs; Gene evolution; Synonymous substitution

Indexed keywords

VIRUS DNA; VIRUS LARGE T ANTIGEN;

ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA REPLICATION; GENE EXPRESSION; HUMAN; HUMAN CELL; HYDROPHOBICITY; MERKEL CELL POLYOMAVIRUS; MERKEL CELL TUMOR; OPEN READING FRAME; PHYLOGENY; PRIORITY JOURNAL; PROTEIN MOTIF; STOP CODON; VIRUS GENE; VIRUS REPLICATION;

DISORDERED MOTIFS; GENE EVOLUTION; SYNONYMOUS SUBSTITUTION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANTIGENS, VIRAL, TUMOR; CODON, INITIATOR; EVOLUTION, MOLECULAR; EXONS; MERKEL CELL POLYOMAVIRUS; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES;

EID: 84881103245     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1303526110     Document Type: Article

References (40)

1. Keese PK, Gibbs A (1992) Origins of genes: "Big bang" or continuous creation? Proc Natl Acad Sci USA 89(20):9489-9493.
2. Chirico N, Vianelli A, Belshaw R (2010) Why genes overlap in viruses. Proc Biol Sci 277(1701):3809-3817.
3. Sabath N, Wagner A, Karlin D (2012) Evolution of viral proteins originated de novo by overprinting. Mol Biol Evol 29(12):3767-3780.
4. Rancurel C, Khosravi M, Dunker AK, Romero PR, Karlin D (2009) Overlapping genes produce proteins with unusual sequence properties and offer insight into de novo protein creation. J Virol 83(20):10719-10736.
5. Firth AE, Atkins JF (2010) Candidates in Astroviruses, Seadornaviruses, Cytorhabdoviruses and Coronaviruses for +1 frame overlapping genes accessed by leaky scanning. Virol J 7:17.
6. Pavesi A, De Iaco B, Granero MI, Porati A (1997) On the informational content of overlapping genes in prokaryotic and eukaryotic viruses. J Mol Evol 44(6):625-631.
7. Schowalter RM, Pastrana DV, Pumphrey KA, Moyer AL, Buck CB (2010) Merkel cell polyomavirus and two previously unknown polyomaviruses are chronically shed from human skin. Cell Host Microbe 7(6):509-515.
8. Cole CN, Conzen SD (2001) Fields Virology, Polyomaviridae: The Viruses and Their Replication, ed Knipe DM, Howley PM (Lippincott Williams & Wilkens, Philadelphia), pp 2141-2174.
9. Cheng J, DeCaprio JA, Fluck MM, Schaffhausen BS (2009) Cellular transformation by Simian Virus 40 and Murine Polyoma Virus T antigens. Semin Cancer Biol 19(4):218-228.
10. DeCaprio JA (2009) How the Rb tumor suppressor structure and function was revealed by the study of Adenovirus and SV40. Virology 384(2):274-284.
11. Ahuja D, Sáenz-Robles MT, Pipas JM (2005) SV40 large T antigen targets multiple cellular pathways to elicit cellular transformation. Oncogene 24(52):7729-7745.
12. Feng H, Shuda M, Chang Y, Moore PS (2008) Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science 319(5866):1096-1100.
13. Becker JC, et al. (2009) MC polyomavirus is frequently present in Merkel cell carcinoma of European patients. J Invest Dermatol 129(1):248-250.
14. Shuda M, et al. (2008) T antigen mutations are a human tumor-specific signature for Merkel cell polyomavirus. Proc Natl Acad Sci USA 105(42):16272-16277.
15. Jagger BW, et al. (2012) An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. Science 337(6091):199-204.
16. Lin MF, et al. (2011) Locating protein-coding sequences under selection for additional, overlapping functions in 29 mammalian genomes. Genome Res 21(11):1916-1928.
17. Firth AE, Brown CM (2006) Detecting overlapping coding sequences in virus genomes. BMC Bioinformatics 7:75.
18. Sabath N, Landan G, Graur D (2008) A method for the simultaneous estimation of selection intensities in overlapping genes. PLoS ONE 3(12):e3996.
19. Neumann F, et al. (2011) Replication, gene expression and particle production by a consensus Merkel Cell Polyomavirus (MCPyV) genome. PLoS ONE 6(12):e29112.
20. Schowalter RM, Pastrana DV, Buck CB (2011) Glycosaminoglycans and sialylated glycans sequentially facilitate Merkel cell polyomavirus infectious entry. PLoS Pathog 7(7):e1002161.
21. Altschul SF, et al. (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25(17):3389-3402.
22. Fluck MM, Schaffhausen BS (2009) Lessons in signaling and tumorigenesis from polyomavirus middle T antigen. Microbiol Mol Biol Rev 73(3):542-563.
23. Fagrouch Z, et al. (2012) Novel polyomaviruses in South American bats and their relationship to other members of the family Polyomaviridae. J Gen Virol 93(Pt 12): 2652-2657.
24. Lim ES, et al. (2013) Discovery of STL polyomavirus, a polyomavirus of ancestral recombinant origin that encodes a unique T antigen by alternative splicing. Virology 436(2):295-303.
25. Tao Y, et al. (2013) Discovery of diverse polyomaviruses in bats and the evolutionary history of the Polyomaviridae. J Gen Virol 94(Pt 4):738-748.
26. Lane DP, Crawford LV (1979) T antigen is bound to a host protein in SV40-transformed cells. Nature 278(5701):261-263.
27. Reich NC, Levine AJ (1982) Specific interaction of the SV40 T antigen-cellular p53 protein complex with SV40 DNA. Virology 117(1):286-290.
28. Kaessmann H (2010) Origins, evolution, and phenotypic impact of new genes. Genome Res 20(10):1313-1326.
29. Xie C, et al. (2012) Hominoid-specific de novo protein-coding genes originating from long non-coding RNAs. PLoS Genet 8(9):e1002942.
30. Liu X, et al. (2011) Merkel cell polyomavirus large T antigen disrupts lysosome clustering by translocating human Vam6p from the cytoplasm to the nucleus. J Biol Chem 286(19):17079-17090.
31. Kim HY, Ahn BY, Cho Y (2001) Structural basis for the inactivation of retinoblastoma tumor suppressor by SV40 large T antigen. EMBO J 20(1-2):295-304.
32. Zhou AY, et al. (2011) Polyomavirus middle T-antigen is a transmembrane protein that binds signaling proteins in discrete subcellular membrane sites. J Virol 85(7): 3046-3054.
33. Zádori Z, Szelei J, Tijssen P (2005) SAT: A late NS protein of porcine parvovirus. J Virol 79(20):13129-13138.
34. Dunker AK, Silman I, Uversky VN, Sussman JL (2008) Function and structure of inherently disordered proteins. Curr Opin Struct Biol 18(6):756-764.
35. Southern E (2006) Southern blotting. Nat Protoc 1(2):518-525.
36. Edgar RC (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792-1797.
37. Guindon S, et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of Phy ML 3.0. Syst Biol 59(3):307-321.
38. Dereeper A, et al. (2008) Phylogeny.fr: Robust phylogenetic analysis for the nonspecialist. Nucleic Acids Res 36(Web Server issue):W465-9.
39. Yang Z (2007) PAML 4: Phylogenetic analysis by maximum likelihood. Mol Biol Evol 24(8):1586-1591.
40. Drummond AJ, et al. (2010). Geneious version 5.0 created by Biomatters. Available at www.geneious.com.