Gene targeting of mouse Sushi-ichi-related retrotransposon homologue 11/Zinc finger CCHC domain-containing 16 (Sirh11/Zcchc16) causes abnormal behaviors related to cognition, including attention, impulsivity and working memory. Sirh11/Zcchc16 encodes a CCHC type of zinc-finger protein that exhibits high homology to an LTR retrotransposon Gag protein. Upon microdialysis analysis of the prefrontal cortex region, the recovery rate of noradrenaline (NA) was reduced compared with dopamine (DA) after perfusion of high potassium-containing artificial cerebrospinal fluid in knockout (KO) mice. These data indicate that Sirh11/Zcchc16 is involved in cognitive function in the brain, possibly via the noradrenergic system, in the contemporary mouse developmental systems. Interestingly, it is highly conserved in three out of the four major groups of the eutherians, euarchontoglires, laurasiatheria and afrotheria, but is heavily mutated in xenarthran species such as the sloth and armadillo, suggesting that it has contributed to brain evolution in the three major eutherian lineages, including humans and mice. Sirh11/Zcchc16 is the first SIRH gene to be involved in brain function, instead of just the placenta, as seen in the case of Peg10, Peg11/Rtl1 and Sirh7/Ldoc1.
References
[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. pmid:1279691 doi: 10.1073/pnas.89.22.10706
[2]
Smit AF. Interspersed repeats and other mementos of transposable elements in mammalian genomes. Curr Opin Genet Dev. 1999;9: 657–663. pmid:10607616 doi: 10.1016/s0959-437x(99)00031-3
[3]
Volff J, K？rting C, Schartl M. Ty3/Gypsy retrotransposon fossils in mammalian genomes: did they evolve into new cellular functions? Mol Biol Evol. 2001;18: 266–270. pmid:11158386 doi: 10.1093/oxfordjournals.molbev.a003801
[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. pmid:12956954 doi: 10.1016/s0960-9822(03)00618-3
[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. pmid:15716091 doi: 10.1016/j.gene.2004.11.022
[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. pmid:16155747 doi: 10.1007/s00239-004-0332-0
[7]
Campillos M, Doerks T, Shah PK, Bork P. Computational characterization of multiple Gag-like human proteins. Trends Genet. 2006;22: 585–589. pmid:16979784 doi: 10.1016/j.tig.2006.09.006
[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. pmid:16341224 doi: 10.1038/ng1699
[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. pmid: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. pmid: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. pmid:25468940
[12]
Nishihara H, Smit AF, Okada N. Functional noncoding sequences derived from SINEs in the mammalian genome. Genome Res. 2006; 16: 864–874. pmid:16717141 doi: 10.1101/gr.5255506
[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. pmid: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. pmid: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. pmid:21946353
[16]
Schmidt D, Schwalie PC, Wilson MD, Ballester B, Gonalves ？, 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. pmid: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. pmid: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. pmid: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. pmid:10362822 doi: 10.1056/nejm199906103402303
[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. pmid:11558790 doi: 10.1002/ana.1288
[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. pmid:16214224 doi: 10.1016/j.jneuroim.2005.08.019
[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. pmid: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. pmid:17432937 doi: 10.1371/journal.pgen.0030055
[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. doi: 10.1371/journal.pbio.0060135
[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. pmid:21636603
[26]
Aston-Jones G, Rajkowski J, Cohen J. Role of locus coeruleus in attention and behavioral flexibility. Biol Psychiatry. 1999;46: 1309–1320. pmid:10560036 doi: 10.1016/s0006-3223(99)00140-7
[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. pmid:12668290 doi: 10.1016/s0165-0173(03)00143-7
[28]
Bouret S, Sara SJ. Network reset: A simplified overarching theory of locus coeruleus noradrenaline function. Trends Neurosci. 2005;28: 574–582. pmid:16165227 doi: 10.1016/j.tins.2005.09.002
[29]
Sara SJ. The locus coeruleus and noradrenergic modulation of cognition. Nat Rev Neurosci. 2009;10: 211–223. doi: 10.1038/nrn2573. pmid: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. pmid:19286970
[31]
Yang Z. PAML 4: Phylogenetic Analysis by Maximum Likelihood. Mol Biol Evol. 2007;24: 1586–1591. pmid:17483113 doi: 10.1093/molbev/msm088
[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. pmid:8865189 doi: 10.1016/0306-4522(96)00161-3
[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. pmid:8986335 doi: 10.1037//0735-7044.110.6.1321
[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. pmid:15148402 doi: 10.1073/pnas.0401080101
[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. pmid: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. pmid:15745958 doi: 10.1523/jneurosci.3038-04.2005
[37]
Thomas SA, Matsumoto AM, Palmiter RD. Noradrenaline is essential for mouse fetal development. Nature. 1995;374: 643–646. pmid:7715704 doi: 10.1038/374643a0
[38]
Steward O, Worley PF. Selective targeting of newly synthesized Arc mRNA to active synapses requires NMDA receptor activation. Neuron. 2001;30: 227–240. pmid:11343657 doi: 10.1016/s0896-6273(01)00275-6
[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. pmid: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. pmid:24952431
[41]
Ropers HH. X-linked mental retardation: many genes for a complex disorder. Curr Opin Genet Dev. 2006;16: 260–269. pmid:16647850 doi: 10.1016/j.gde.2006.04.017
[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. pmid: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. doi: 10.1002/ajmg.a.32472
[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. pmid:18160706 doi: 10.1128/mcb.01038-07
[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. pmid:16845082 doi: 10.1093/nar/gkl315
[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. pmid:8250257 doi: 10.1006/abio.1993.1458
[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. pmid:10737965 doi: 10.1002/(sici)1098-2795(200005)56:1<34::aid-mrd5>3.0.co;2-m
