#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Cognitive Function Related to the Gene Acquired from an LTR Retrotransposon in Eutherians


Retrotransposon-derived DNA sequences occupy approximately 40% of the mammalian genome, compared with only 1.5% of protein coding genes. They have been commonly considered “junk DNA” and even potentially harmful for host organisms. However, a series of knockout (KO) mouse analyses demonstrated that at least some of the LTR retrotransposon- and retrovirus-derived sequences play essential roles in the current mammalian developmental system as endogenous genes, such as Peg10, Peg11/Rtl1, Sirh7/Ldoc1, SYNCYTINs and FEMATRIN-1, which are active in multiple aspects of placental function. Here we demonstrate that another LTR retrotransposon-derived gene, Sirh11/Zcchc16, plays an important role in cognitive function in the brain. Sirh11/Zcchc16 KO mice exhibit abnormal behaviors related to cognition, including attention, impulsivity and working memory, possibly due to the locus coeruleus-noradrenaline (LC-NA) system, suggesting that human SIRH11/ZCCHC16 may be involved in X-linked intellectual disability and/or attention-deficit/hyperactivity disorder. Comparative genome analysis demonstrates that SIRH11/ZCCHC16 was acquired in a common eutherian ancestor, suggesting that it contributed to eutherian brain evolution because it confers a critically important advantage in the competition that occurs in daily life. This study provides further insight into the impact of LTR retrotransposon-derived genes on mammalian evolution.


Vyšlo v časopise: Cognitive Function Related to the Gene Acquired from an LTR Retrotransposon in Eutherians. PLoS Genet 11(9): e32767. doi:10.1371/journal.pgen.1005521
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005521

Souhrn

Retrotransposon-derived DNA sequences occupy approximately 40% of the mammalian genome, compared with only 1.5% of protein coding genes. They have been commonly considered “junk DNA” and even potentially harmful for host organisms. However, a series of knockout (KO) mouse analyses demonstrated that at least some of the LTR retrotransposon- and retrovirus-derived sequences play essential roles in the current mammalian developmental system as endogenous genes, such as Peg10, Peg11/Rtl1, Sirh7/Ldoc1, SYNCYTINs and FEMATRIN-1, which are active in multiple aspects of placental function. Here we demonstrate that another LTR retrotransposon-derived gene, Sirh11/Zcchc16, plays an important role in cognitive function in the brain. Sirh11/Zcchc16 KO mice exhibit abnormal behaviors related to cognition, including attention, impulsivity and working memory, possibly due to the locus coeruleus-noradrenaline (LC-NA) system, suggesting that human SIRH11/ZCCHC16 may be involved in X-linked intellectual disability and/or attention-deficit/hyperactivity disorder. Comparative genome analysis demonstrates that SIRH11/ZCCHC16 was acquired in a common eutherian ancestor, suggesting that it contributed to eutherian brain evolution because it confers a critically important advantage in the competition that occurs in daily life. This study provides further insight into the impact of LTR retrotransposon-derived genes on mammalian evolution.


Zdroje

1. Brosius J, Gould SJ. On “genomenclature”: a comprehensive (and respectful) taxonomy for pseudogenes and other “junk DNA”. Proc Natl Acad Sci U S A. 1992;89: 10706–10710. 1279691

2. Smit AF. Interspersed repeats and other mementos of transposable elements in mammalian genomes. Curr Opin Genet Dev. 1999;9: 657–663. 10607616

3. Volff J, Körting C, Schartl M. Ty3/Gypsy retrotransposon fossils in mammalian genomes: did they evolve into new cellular functions? Mol Biol Evol. 2001;18: 266–270. 11158386

4. Lynch C, Tristem M. A co-opted gypsy-type LTR-retrotransposon is conserved in the genomes of humans, sheep, mice, and rats. Curr Biol. 2003;13: 1518–1523. 12956954

5. Brandt J, Schrauth S, Veith AM, Froschauer A, Haneke T, Schultheis C, et al. Transposable elements as a source of genetic innovation: Expression and evolution of a family of retrotransposon-derived neogenes in mammals. Gene. 2005;345: 101–111. 15716091

6. Youngson NA, Kocialkowski S, Peel N, Ferguson-Smith AC. A small family of sushi-class retrotransposon-derived genes in mammals and their relation to genomic imprinting. J Mol Evol. 2005;61: 481–490. 16155747

7. Campillos M, Doerks T, Shah PK, Bork P. Computational characterization of multiple Gag-like human proteins. Trends Genet. 2006;22: 585–589. 16979784

8. Ono R, Nakamura K, Inoue K, Naruse M, Usami T, Wakisaka-Saito N, et al. Deletion of Peg10, an imprinted gene acquired from a retrotransposon, causes early embryonic lethality. Nat Genet. 2006;38: 101–106. 16341224

9. Sekita Y, Wagatsuma H, Nakamura K, Ono R, Kagami M, Wakisaka N, et al. Role of retrotransposon-derived imprinted gene, Rtl1, in the feto-maternal interface of mouse placenta. Nat Genet. 2008;40: 243–248. doi: 10.1038/ng.2007.51 18176565

10. Kaneko-Ishino T, Ishino F. The role of genes domesticated from LTR retrotransposons and retroviruses in mammals. Front Microbiol. 2012;3: 262. doi: 10.3389/fmicb.2012.00262 22866050

11. Naruse M, Ono R, Irie M, Nakamura K, Furuse T, Hino T, et al. Sirh7/Ldoc1 knockout mice exhibit placental P4 overproduction and delayed parturition. Development. 2014;141: 4763–4771. doi: 10.1242/dev.114520 25468940

12. Nishihara H, Smit AF, Okada N. Functional noncoding sequences derived from SINEs in the mammalian genome. Genome Res. 2006; 16: 864–874. 16717141

13. Kuwabara T, Hsieh J, Muotri A, Yeo G, Warashina M, Lie DC, et al. Wnt-mediated activation of NeuroD1 and retro-elements during adult neurogenesis. Nat Neurosci. 2009;12: 1097–1105. doi: 10.1038/nn.2360 19701198

14. Levin HL, Moran J V. Dynamic interactions between transposable elements and their hosts. Nat Rev Genet. 2011;12: 615–627. doi: 10.1038/nrg3030 21850042

15. Lynch VJ, Leclerc RD, May G, Wagner GP. Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat Genet. 2011;43: 1154–1159. doi: 10.1038/ng.917 21946353

16. Schmidt D, Schwalie PC, Wilson MD, Ballester B, Gonalves Â, Kutter C, et al. Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages. Cell. 2012;148: 335–348. doi: 10.1016/j.cell.2011.11.058 22244452

17. Kaneko-Ishino T, Ishino F. Retrotransposon silencing by DNA methylation contributed to the evolution of placentation and genomic imprinting in mammals. Dev Growth Differ. 2010;52: 533–543. doi: 10.1111/j.1440-169X.2010.01194.x 20646026

18. Renfree MB, Suzuki S, Kaneko-Ishino T. The origin and evolution of genomic imprinting and viviparity in mammals. Philos Trans R Soc Lond B Biol Sci. 2013;368: 20120151. doi: 10.1098/rstb.2012.0151 23166401

19. Voltz R, Gultekin SH, Rosenfeld MR, Gerstner E, Eichen J, Posner JB, et al. A serologic marker of paraneoplastic limbic and brain-stem encephalitis in patients with testicular cancer. N Engl J Med. 1999;340: 1788–1795. 10362822

20. Rosenfeld MR, Eichen JG, Wade DF, Posner JB, Dalmau J. Molecular and clinical diversity in paraneoplastic immunity to Ma proteins. Ann Neurol. 2001;50: 339–348. 11558790

21. Schüller M, Jenne D, Voltz R. The human PNMA family: Novel neuronal proteins implicated in paraneoplastic neurological disease. J Neuroimmunol. 2005;169: 172–176. 16214224

22. Iwasaki S, Suzuki S, Pelekanos M, Clark H, Ono R, Shaw G, et al. Identification of a novel PNMA-MS1 gene in marsupials suggests the LTR retrotransposon-derived PNMA genes evolved differently in marsupials and eutherians. DNA Res. 2013;20: 425–436. doi: 10.1093/dnares/dst020 23704700

23. Suzuki S, Ono R, Narita T, Pask AJ, Shaw G, Wang C, et al. Retrotransposon silencing by DNA methylation can drive mammalian genomic imprinting. PLoS Genet. 2007;3: e55. 17432937

24. Edwards CA, Mungall AJ, Matthews L, Ryder E, Gray DJ, Pask AJ, et al. The evolution of the DLK1-DIO3 imprinted domain in mammals. PLoS Biol. 2008;6: 1292–1305.

25. Ono R, Kuroki Y, Naruse M, Ishii M, Iwasaki S, Toyoda A, et al. Identification of tammar wallaby SIRH12, derived from a marsupial-specific retrotransposition event. DNA Res. 2011;18: 211–219. doi: 10.1093/dnares/dsr012 21636603

26. Aston-Jones G, Rajkowski J, Cohen J. Role of locus coeruleus in attention and behavioral flexibility. Biol Psychiatry. 1999;46: 1309–1320. 10560036

27. Berridge CW, Waterhouse BD. The locus coeruleus-noradrenergic system: Modulation of behavioral state and state-dependent cognitive processes. Brain Res Rev. 2003;42: 33–84. 12668290

28. Bouret S, Sara SJ. Network reset: A simplified overarching theory of locus coeruleus noradrenaline function. Trends Neurosci. 2005;28: 574–582. 16165227

29. Sara SJ. The locus coeruleus and noradrenergic modulation of cognition. Nat Rev Neurosci. 2009;10: 211–223. doi: 10.1038/nrn2573 19190638

30. Nishihara H, Maruyama S, Okada N. Retroposon analysis and recent geological data suggest near-simultaneous divergence of the three superorders of mammals. Proc Natl Acad Sci. 2009;106: 5235–5240. doi: 10.1073/pnas.0809297106 19286970

31. Yang Z. PAML 4: Phylogenetic Analysis by Maximum Likelihood. Mol Biol Evol. 2007;24: 1586–1591. 17483113

32. Yamada K, Hiramatsu M, Noda Y, Mamiya T, Murai M, Kameyama T, et al. Role of nitric oxide and cyclic GMP in the dizocilpine-induced impairment of spontaneous alternation behavior in mice. Neuroscience. 1996;74: 365–374. 8865189

33. Conrad CD, Galea LAM, Kuroda Y, McEwen BS. Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine treatment. Behav Neurosci. 1996;110: 1321–1334. 8986335

34. Cryan JF, O’Leary OF, Jin S-H, Friedland JC, Ouyang M, Hirsch BR, et al. Norepinephrine-deficient mice lack responses to antidepressant drugs, including selective serotonin reuptake inhibitors. Proc Natl Acad Sci U S A. 2004;101: 8186–8191. 15148402

35. Jaskiw GE, Newbould E, Bongiovanni R. Tyrosine availability modulates potassium-induced striatal catecholamine efflux in vivo. Brain Res. 2008;1209: 74–84. doi: 10.1016/j.brainres.2008.02.050 18400209

36. Rossetti ZL and Carboni S. Noradrenaline and dopamine elevations in the rat prefrontal cortex in spatial working memory. J. Neurosci. 2005;25: 2322–2329. 15745958

37. Thomas SA, Matsumoto AM, Palmiter RD. Noradrenaline is essential for mouse fetal development. Nature. 1995;374: 643–646. 7715704

38. Steward O, Worley PF. Selective targeting of newly synthesized Arc mRNA to active synapses requires NMDA receptor activation. Neuron. 2001;30: 227–240. 11343657

39. Gumy LF, Katrukha EA, Kapitein LC, Hoogenraad CC. New insights into mRNA trafficking in axons. Dev Neurobiol. 2014;74: 233–244. doi: 10.1002/dneu.22121 23959656

40. Smith R, Rathod RJ, Rajkumar S, Kennedy D. Nervous translation, do you get the message? A review of mRNPs, mRNA-protein interactions and translational control within cells of the nervous system. Cell Mol Life Sci. 2014;71: 3917–3937. doi: 10.1007/s00018-014-1660-x 24952431

41. Ropers HH. X-linked mental retardation: many genes for a complex disorder. Curr Opin Genet Dev. 2006;16: 260–269. 16647850

42. Lubs HA, Stevenson RE, Schwartz CE. Fragile X and X-linked intellectual disability: Four decades of discovery. Am J Hum Genet. 2012;90: 579–590. doi: 10.1016/j.ajhg.2012.02.018 22482801

43. Cho G, Bhat SS, Gao J, Collins JS, Rogers RC, Simensen RJ, et al. Evidence that SIZN1 is a candidate X-linked mental retardation gene. Am J Med Genet Part A. 2008;146: 2644–2650.

44. Cho G, Lim Y, Zand D, Golden JA. Sizn1 is a novel protein that functions as a transcriptional coactivator of bone morphogenic protein signaling. Mol Cell Biol. 2008;28: 1565–1572. 18160706

45. Suyama M, Torrents D, Bork P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 2006;34: W609–W612. 16845082

46. Yagi T, Tokunaga T, Furuta Y, Nada S, Yoshida M, Tsukada T, et al. A novel ES cell line, TT2, with high germline-differentiating potency. Anal Biochem. 1993;214: 70–76. 8250257

47. Sato M, Yasuoka Y, Kodama H, Watanabe T, Miyazaki JI, Kimura M. New approach to cell lineage analysis in mammals using the Cre-loxP system. Mol Reprod Dev. 2000;56: 34–44. 10737965

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2015 Číslo 9
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#