Elevated Rate of Fixation of Endogenous Retroviral Elements in Haplorhini TRIM5 and TRIM22 Genomic Sequences: Impact on Transcriptional Regulation

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2013 Mar 22

PMID 23516500

Citations 4

Authors

William E Diehl

Welkin E Johnson

Eric Hunter

Affiliations

Soon will be listed here.

Abstract

All genes in the TRIM6/TRIM34/TRIM5/TRIM22 locus are type I interferon inducible, with TRIM5 and TRIM22 possessing antiviral properties. Evolutionary studies involving the TRIM6/34/5/22 locus have predominantly focused on the coding sequence of the genes, finding that TRIM5 and TRIM22 have undergone high rates of both non-synonymous nucleotide replacements and in-frame insertions and deletions. We sought to understand if divergent evolutionary pressures on TRIM6/34/5/22 coding regions have selected for modifications in the non-coding regions of these genes and explore whether such non-coding changes may influence the biological function of these genes. The transcribed genomic regions, including the introns, of TRIM6, TRIM34, TRIM5, and TRIM22 from ten Haplorhini primates and one prosimian species were analyzed for transposable element content. In Haplorhini species, TRIM5 displayed an exaggerated interspecies variability, predominantly resulting from changes in the composition of transposable elements in the large first and fourth introns. Multiple lineage-specific endogenous retroviral long terminal repeats (LTRs) were identified in the first intron of TRIM5 and TRIM22. In the prosimian genome, we identified a duplication of TRIM5 with a concomitant loss of TRIM22. The transposable element content of the prosimian TRIM5 genes appears to largely represent the shared Haplorhini/prosimian ancestral state for this gene. Furthermore, we demonstrated that one such differentially fixed LTR provides for species-specific transcriptional regulation of TRIM22 in response to p53 activation. Our results identify a previously unrecognized source of species-specific variation in the antiviral TRIM genes, which can lead to alterations in their transcriptional regulation. These observations suggest that there has existed long-term pressure for exaptation of retroviral LTRs in the non-coding regions of these genes. This likely resulted from serial viral challenges and provided a mechanism for rapid alteration of transcriptional regulation. To our knowledge, this represents the first report of persistent evolutionary pressure for the capture of retroviral LTR insertions.

Citing Articles

Human endogenous retroviruses and exogenous viral infections.

Bao C, Gao Q, Xiang H, Shen Y, Chen Q, Gao Q Front Cell Infect Microbiol. 2024; 14:1439292.

PMID: 39397863 PMC: 11466896. DOI: 10.3389/fcimb.2024.1439292.

TRIM family contribute to tumorigenesis, cancer development, and drug resistance.

Huang N, Sun X, Li P, Liu X, Zhang X, Chen Q Exp Hematol Oncol. 2022; 11(1):75.

PMID: 36261847 PMC: 9583506. DOI: 10.1186/s40164-022-00322-w.

To TRIM the Immunity: From Innate to Adaptive Immunity.

Yang W, Gu Z, Zhang H, Hu H Front Immunol. 2020; 11:02157.

PMID: 33117334 PMC: 7578260. DOI: 10.3389/fimmu.2020.02157.

Not so unique to Primates: The independent adaptive evolution of TRIM5 in Lagomorpha lineage.

Agueda-Pinto A, de Matos A, Pinheiro A, Neves F, de Sousa-Pereira P, Esteves P PLoS One. 2019; 14(12):e0226202.

PMID: 31830084 PMC: 6907815. DOI: 10.1371/journal.pone.0226202.

References

Samuelson L, Phillips R, Swanberg L . Amylase gene structures in primates: retroposon insertions and promoter evolution. Mol Biol Evol. 1996; 13(6):767-79. DOI: 10.1093/oxfordjournals.molbev.a025637. View

Stoye J, Fenner S, Greenoak G, Moran C, Coffin J . Role of endogenous retroviruses as mutagens: the hairless mutation of mice. Cell. 1988; 54(3):383-91. DOI: 10.1016/0092-8674(88)90201-2. View

Owens C, Song B, Perron M, Yang P, Stremlau M, Sodroski J . Binding and susceptibility to postentry restriction factors in monkey cells are specified by distinct regions of the human immunodeficiency virus type 1 capsid. J Virol. 2004; 78(10):5423-37. PMC: 400345. DOI: 10.1128/jvi.78.10.5423-5437.2004. View

Virgen C, Kratovac Z, Bieniasz P, Hatziioannou T . Independent genesis of chimeric TRIM5-cyclophilin proteins in two primate species. Proc Natl Acad Sci U S A. 2008; 105(9):3563-8. PMC: 2265128. DOI: 10.1073/pnas.0709258105. View

Sawyer S, Wu L, Emerman M, Malik H . Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc Natl Acad Sci U S A. 2005; 102(8):2832-7. PMC: 549489. DOI: 10.1073/pnas.0409853102. View

Wang T, Zeng J, Lowe C, Sellers R, Salama S, Yang M . Species-specific endogenous retroviruses shape the transcriptional network of the human tumor suppressor protein p53. Proc Natl Acad Sci U S A. 2007; 104(47):18613-8. PMC: 2141825. DOI: 10.1073/pnas.0703637104. View

Javanbakht H, Yuan W, Yeung D, Song B, Diaz-Griffero F, Li Y . Characterization of TRIM5alpha trimerization and its contribution to human immunodeficiency virus capsid binding. Virology. 2006; 353(1):234-46. DOI: 10.1016/j.virol.2006.05.017. View

Kohany O, Gentles A, Hankus L, Jurka J . Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinformatics. 2006; 7:474. PMC: 1634758. DOI: 10.1186/1471-2105-7-474. View

Perry M, Piette J, Zawadzki J, Harvey D, Levine A . The mdm-2 gene is induced in response to UV light in a p53-dependent manner. Proc Natl Acad Sci U S A. 1993; 90(24):11623-7. PMC: 48036. DOI: 10.1073/pnas.90.24.11623. View

10.

Li X, Gold B, OhUigin C, Diaz-Griffero F, Song B, Si Z . Unique features of TRIM5alpha among closely related human TRIM family members. Virology. 2006; 360(2):419-33. DOI: 10.1016/j.virol.2006.10.035. View

11.

Hasler J, Strub K . Alu elements as regulators of gene expression. Nucleic Acids Res. 2006; 34(19):5491-7. PMC: 1636486. DOI: 10.1093/nar/gkl706. View

12.

Rahm N, Yap M, Snoeck J, Zoete V, Munoz M, Radespiel U . Unique spectrum of activity of prosimian TRIM5alpha against exogenous and endogenous retroviruses. J Virol. 2011; 85(9):4173-83. PMC: 3126249. DOI: 10.1128/JVI.00075-11. View

13.

Ylinen L, Keckesova Z, Wilson S, Ranasinghe S, Towers G . Differential restriction of human immunodeficiency virus type 2 and simian immunodeficiency virus SIVmac by TRIM5alpha alleles. J Virol. 2005; 79(18):11580-7. PMC: 1212619. DOI: 10.1128/JVI.79.18.11580-11587.2005. View

14.

Hatziioannou T, Cowan S, Bieniasz P . Capsid-dependent and -independent postentry restriction of primate lentivirus tropism in rodent cells. J Virol. 2003; 78(2):1006-11. PMC: 368775. DOI: 10.1128/jvi.78.2.1006-1011.2004. View

15.

Sayah D, Sokolskaja E, Berthoux L, Luban J . Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature. 2004; 430(6999):569-73. DOI: 10.1038/nature02777. View

16.

Tissot C, Mechti N . Molecular cloning of a new interferon-induced factor that represses human immunodeficiency virus type 1 long terminal repeat expression. J Biol Chem. 1995; 270(25):14891-8. DOI: 10.1074/jbc.270.25.14891. View

17.

Tareen S, Sawyer S, Malik H, Emerman M . An expanded clade of rodent Trim5 genes. Virology. 2009; 385(2):473-83. PMC: 2692226. DOI: 10.1016/j.virol.2008.12.018. View

18.

Sardiello M, Cairo S, Fontanella B, Ballabio A, Meroni G . Genomic analysis of the TRIM family reveals two groups of genes with distinct evolutionary properties. BMC Evol Biol. 2008; 8:225. PMC: 2533329. DOI: 10.1186/1471-2148-8-225. View

19.

Kaneshiro K, Tsutsumi S, Tsuji S, Shirahige K, Aburatani H . An integrated map of p53-binding sites and histone modification in the human ENCODE regions. Genomics. 2006; 89(2):178-88. DOI: 10.1016/j.ygeno.2006.09.001. View

20.

Yap M, Lindemann D, Stanke N, Reh J, Westphal D, Hanenberg H . Restriction of foamy viruses by primate Trim5alpha. J Virol. 2008; 82(11):5429-39. PMC: 2395188. DOI: 10.1128/JVI.02462-07. View