Preview

Vavilov Journal of Genetics and Breeding

Advanced search

Longitudinal genetic studies of cognitive characteristics

https://doi.org/10.18699/VJ20.599

Abstract

The present review describes longitudinal studies of cognitive traits and functions determining the causes of their variations and their possible correction to prevent cognitive impairment. The present study reviews the involvement of such environmental factors as nutrition, prenatal maternal stress, social isolation and others in cognitive functioning. The role of epigenetic factors in the implementation of environmental effects in cognitive characteristics is revealed. Considering the epigenome significance, several studies were focused on the design of substances affecting methylation and histone modification, which can be used for the treatment of cognitive disorders. The appropriate correction of epigenetic factors related to environmental differences in cognitive abilities requires to determine the mechanisms of chromatin modifications and variations in DNA methylation. Transposons representing stress-sensitive DNA elements appeared to mediate the environmental influence on epigenetic modifications. They can explain the mechanism of transgenerational transfer of information on cognitive abilities. Recently, large-scale meta-analyses based on the results of studies, which identified genetic associations with various cognitive traits, were carried out. As a result, the role of genes actively expressed in the brain, such as BDNF, COMT, CADM2, CYP2D6, APBA1, CHRNA7, PDE1C, PDE4B, and PDE4D in cognitive abilities was revealed. The association between cognitive functioning and genes, which have been previously involved in developing psychiatric disorders (MEF2C, CYP2D6, FAM109B, SEPT3, NAGA, TCF20, NDUFA6 genes), was revealed, thus indicating the role of the similar mechanisms of genetic and neural networks in both normal cognition and cognitive impairment. An important role in both processes belongs to common epigenetic factors. The genes involved in DNA methylation (DNMT1, DNMT3B, and FTO), histone modifications (CREBBP, CUL4B, EHMT1, EP300, EZH2, HLCS, HUWE1, KAT6B, KMT2A, KMT2D, KMT2C, NSD1, WHSC1, and UBE2A) and chromatin remodeling (ACTB, ARID1A, ARID1B, ATRX, CHD2, CHD7, CHD8, SMARCA2, SMARCA4, SMARCB1, SMARCE1, SRCAP, and SS18L1) are associated with increased risk of psychiatric diseases with cognitive deficiency together with normal cognitive functioning. The data on the correlation between transgenerational epigenetic inheritance of cognitive abilities and the insert of transposable elements in intergenic regions is discussed. Transposons regulate genes functioning in the brain due to the processing of their transcripts into non-coding RNAs. The content, quantity and arrangement of transposable elements in human genome, which do not affect changes in nucleotide sequences of protein encoding genes, but affect their expression, can be transmitted to the next generation.

About the Authors

R. N. Mustafin
Bashkir State Medical University
Russian Federation

Ufa



A. V. Kazantseva
Institute of Biochemistry and Genetics - Subdivision of the Ufa Federal Research Centre, Russian Academy of Sciences
Russian Federation


R. F. Enikeeva
Institute of Biochemistry and Genetics - Subdivision of the Ufa Federal Research Centre, Russian Academy of Sciences
Russian Federation


S. B. Malykh
Psychological Institute of the Russian Academy of Education
Russian Federation

Moscow



E. K. Khusnutdinova
Institute of Biochemistry and Genetics - Subdivision of the Ufa Federal Research Centre, Russian Academy of Sciences; M.V. Lomonosov Moscow State University, Laboratory of psychology of professions and conflicts
Russian Federation


References

1. Abbott C.W., Rohac D.J., Bottom R.T., Patadia S., Huffman K.J. Prenatal ethanol exposure and neocortical development: a transgenerational model of FASD. Cereb. Cortex. 2018;28(8):2908-2921.

2. Aimone J.B., Li Y, Lee S.W., Clemenson G.D., Deng W., Gage F.H. Regulation and function of adult neurogenesis: from genes to cognition. Physiol. Rev. 2014;94(4):991-1026.

3. Andrews S.J., Das D., Anstey K.J., Easteal S. Association of AKAP6 and MIR2113 with cognitive performance in population-based sample of older adults. Genet. Brain Behav. 2017;16:472-478. DOI 10.1111/gbb.12368.

4. Barry G. Integrating the roles of long and small non-coding RNA in brain function and disease. Mol. Psychiatry. 2014;19:410-416. DOI 10.1038/mp.2013.196.

5. Barry G. Small RNAs and transposable elements are key components in the control of adaptive evolution in eukaryotes. Bioessays. 2018;40(8):e1800070.

6. Bayley N. Consistency and variability in the growth of intelligence from birth to 18 years. J. Genet. Psychol. 1949;75:165-196.

7. Bell J.T., Spector T.D. A twin approach to unraveling epigenetics. Trends Genet. 2011;27:116-125.

8. Bergen S.E., Gardner C.O., Kendler K.S. Agerelated changes in heritability of behavioral phenotypes over adolescence and young adulthood: a meta-analysis. Twin. Res. Hum. Genet. 2007;10(3):423-433.

9. Bohacek J., Mansuy I.M. Molecular insights into transgenerational non-genetic inheritance of acquired behaviours. Nat. Rev. Genet. 2015;16(11):641-652.

10. Braun K., Bock J., Wainstock T., Matas E., Gaisler-Salomon I., Fegert J., Ziegenhain U., Segal M. Experience-induced transgenerational (re-)programming of neuronal structure and functions: impact of stress prior and during pregnancy. Neuro-sci. Biobehav. Rev. 2017;pii:S0149-7634(16)30731-X. DOI 10.1016/j.neubiorev.2017.05.021.

11. Briggs J.A., Wolvetang E.J., Mattick J.S., Rinn J.L., Barry G. Mechanisms of long non-coding RNAs in mammalian nervous system development, plasticity, disease, and evolution. Neuron. 2015;88:861-877. DOI 10.1016/j.neuron.2015.09.045.

12. Briley D.A., Tucker-Drob E.M. Explaining the increasing heritabi-lity of cognitive ability across development: a meta-analysis of longitudinal twin and adoption studies. Psychol. Sci. 2013;24: 1704-1713.

13. Chow B.W., Ho C.S., Wong S.W., Waye M.M., Bishop D.V Generalist genes and cognitive abilities in Chinese twins. Dev. Sci. 2013;16:260-268.

14. Chuong E.B., Elde N.C., Feschotte C. Regulatory activities of transposable elements: from conflicts to benefits. Nat. Rev. Genet. 2017;18:71-86.

15. Claesdotter E., Cervin M., Akerlund S., Rastam M., Lindvall M. The effects of ADHD on cognitive performance. Nord. J. Psychiatry. 2018;72(3):158-163.

16. Crabtree G.R. Our fragile intellect. Part I. Trends Genet. 2013; 29(1):1-3.

17. Das D., Tan X., Bielak A.A., Cherbuin N., Easteal S., Anstey K.J. Cognitive ability, intraindividual variability, and common genetic variants of catechol-O-methyltransferase and brain-derived neurotorophic factor: a longitudinal study in a population-based sample of older adults. Psychol. Aging. 2014;29(2):393-403.

18. Dauncey M.J. Nutrition, the brain and cognitive decline: insights from epigenetics. Eur. J. Clin. Nutr. 2014;68:1179-1185.

19. Davies G., Marioni R.E., Liewald D.C., Hill W.D., Hagenaars S.P., Harris S.E., Ritchie S.J., Luciano M., Fawns-Ritchie C., Ly-all D., Cullen B., Cox S.R., Hayward C., Porteous D.J., Evans J., Mclntosh A.M., Gallacher J., Craddock N., Pell J.P., Smith D.J., Gale C.R., Deary I.J. Genome-wide association study of cognitive functions and educational attainment in UK Biobank (N = 112151). Mol. Psychiatry. 2016;21:758-767.

20. Davis E.P., Sandman C.A. The timing of prenatal exposure to maternal cortisol and psychosocial stress is associated with human infant cognitive development. Child. Dev. 2010;81:131-148.

21. Davis O.S., Band G., Pirinen M., Haworth C.M., Meaburn E.L., Kovas Y, Harlaar N., Docherty S.J., Hansocombe K.B., Trzaskowski M., Curtis C.J., Strange A., Wellcome Trust case Control Consortium, Donnelly P., Plomin R., Spencer C.C. The correlation between reading and mathematics ability at age twelve has a substantial genetic component. Nat. Commun. 2014;5:4204.

22. Daxinger L., Whitelaw E. Understanding transgenerational epigenetic inheritance via the gametes in mammals. Nat. Rev. Genet. 2012;13(3):153-162.

23. de Souza F.S., Franchini L.F., Rubinstein M. Exaptation of transposable elements into novel cis-regulatory elements: is the evidence always strong. Mol. Biol. Evol. 2013;30:1239-1251.

24. Doehner W., PraPe L., Wolpers J., Bruckner M.K., Ueberham U., Arendt T. Transgenerational transmission of an anticholinergic endophenotype with memory dysfunction. Neurobiol. Aging. 2017;51:19-30. DOI 10.1016/j.neurobiolaging.2016.11.016.

25. Faulkner G.J. Retrotransposons: mobile and mutagenic from conception to death. FEBS Lett. 2011;585:1589-1594.

26. Feng G., Leem YE., Levin H.L. Transposon integration enhances expression of stress response genes. Nucleic Acids Res. 2013; 41(2):775-789.

27. Fine J.G., Sung C. Neuroscience of child and adolescent health development. J. Couns. Psychol. 2014;61:521-527.

28. Franić S., Groen-Blokhuis M.M., Dolan C.V, Kattenberg M.V, Pool R., Xiao X., Scheet P.A., Ehli E.A., Davies G.E., van der Sluis S., Abdellaoui A., Hansell N.K., Martin N.G., Hudziak J.J., van Beijsterveldt C.E., Swagerman S.C., Hulshoff Pol H.E., de Geus E.J., Bartels M., Ropers H.H., Hottenga J.J., Boomsma D.I. Intelligence: shared genetic basis between Mendelian disorders and a polygenic trait. Eur. J. Hum. Genet. 2015;23: 1378-1383.

29. Fujiwara H. Site-specific non-LTR retrotransposons. Microbiol. Spectr. 2015;3(2):MDNA3-0001-2014. DOI 10.1128/microbiol spec.MDNA3-0001-2014.

30. Gao J., Wang W.Y, Mao Y.W., Graff J., Guan J.S., Pan L., Mak G., Kim D., Su S.C., Tsai L.H. A novel pathway regulates memory and plasticity via SIRT1 and miR-134. Nature. 2010;466:1105-1109. DOI 10.1038/nature09271.

31. Gerdes P., Richardson S.R., Mager D.L., Faulkner G.J. Transposable elements in the mammalian embryo: pioneers surviving through stealth and service. Genome Biol. 2016;17:100.

32. Gervin K., Nordeng H., Ystrom E., Reichborn-Kjennerud T., Lyle R. Long-term prenatal exposure to paracetamol is associated with DNA methylation differences in children diagnosed with ADHD. Clin. Epigenetics. 2017;9:77.

33. Goldberg T.E., Weinberger D.R. Genes and the parsing of cognitive processes. Trends Cogn. Sci. 2004;8(7):325-335.

34. Griggs E.M., Young E.J., Rumbaugh G., Miller C.A. Micro-RNA-182 regulates amygdale-dependent memory formation. J. Neurosci. 2013;33:1734-1740.

35. Gurney M.E. Genetic association of phosphodiesterases with human cognitive performance. Front. Mol. Neurosci. 2019;12:22.

36. Haworth C.M., Wright M.J., Luciano M., Martin N.G., de Geus E.J., van Beijsterveldt C.E., Bartels M., Posthuma D., Boomsma D.I., Davis O.S., Kovas Y, Corley R.P., Defries J.C., Hewitt J.K., Olson R.K., Rhea S.A., Wadsworth S.J., Iacono W.G., McGue M., Thompson L.A., Hart S.A., Petrill S.A., Lubinski D., Plomin R. The heritability of general cognitive ability increases linearly from childhood to young adulthood. Mol. Psychiatry. 2010;15: 1112-1120.

37. Hernandez D.G., Nalls M.A., Gibbs J.R., Arepalli S., van der Brug M., Chong S., Moore M., Longo D.L., Cookson M.R., Traynor B.J., Singleton A.B. Distinct DNA methylation changes highly correlated with chronological age in the human brain. Hum. Mol. Genet. 2011;20:1164-1172.

38. Hunter R.G., Murakami G., Dewell S., Seigsohn M., Baker M.E., Datson N.A., McEwen B.S., Pfaff D.W. Acute stress and hippocampal histone H3 lysine 9 trimethylation, a retrotransposon silencing response. Proc. Natl. Acad. Sci. USA. 2012;109:17657-17662.

39. Izquierdo V., Palomera-Avalos V., López-Ruiz S., Canudas A., Pallas M., Grinan-Ferre C. Maternal resveratrol supplementation prevents cognitive decline in senescent mice offspring. Int. J. Mol. Sci. 2019;20(5):1134. DOI 10.3390/ijms20051134.

40. Jacques P.E., Jeyakani J., Bourgue G. The majority of primate-specific regulatory sequences are derived from transposable elements. PLoS Genet. 2013;9(5):e1003504.

41. Junkiert-Czarnecka A., Haus O. Genetical background of intelligence. Postepy Hig. Med. Dosw. 2016;70:590-598. DOI 10.5604/17322693.1204943.

42. Kapusta A., Kronenberg Z., Lynch V.J., Zhuo X., Ramsay L., Bourque G., Yandell M., Feschotte C. Transposable elements are major contributors to the origin, diversification, and regulation of vertebrate long noncoding RNAs. PLoS Genet. 2013;9(4): e1003470.

43. Kleefstra T., Schenck A., Kramer J.M., van Bokhoven H. The genetics of cognitive epigenetics. Neuropharmacology. 2014;80: 83-94.

44. Kurnosov A.A., Ustyugova S.V, Nazarov V, Minervina A.A., Komkov A.Y., Shhugay M., Pogorelyy M.V., Khodosevich K.V., Mamedov I.Z., Lebedev Y.B. The evidence for increased L1 activity in the site of human adult brain neurogenesis. PLoS One. 2015;10(2):e0117854.

45. Li M., Du W., Shao F., Wang W. Cognitive dysfunction and epigenetic alterations of the BDNF gene are induced by social isolation during early adolescence. Behav. Brain Res. 2016;313: 177-183.

46. Lupu D.S., Tint D., Niculescu M.D. Perinatal epigenetic determinants of cognitive and metabolic disorders. Aging Dis. 2012;3: 444-453.

47. Mather K.A., Kwok J.B., Armstrong N., Sachdev P.S. The role of epigenetics in cognitive ageing. Int. J. Geriatr. Psychiatry. 2014; 29:1162-1171. DOI 10.1002/gps.4183.

48. Medaglia J.D., Lynall M.E., Bassett D.S. Cognitive network neuroscience. J. Cogn. Neurosci. 2015;27:1471-1491.

49. Mengel-From J., Feddersen S., Halekoh U., Heegaard N.H.H., McGue M., Christensen K., Tan Q., Christiansen L. Circulating microRNA disclose biology of normal cognitive function in healthy elderly people - a discovery twin study. Eur. J. Hum. Genet. 2018;26:378-1387.

50. Misra P, Ganesh S. Sex-biased transgenerational effect of maternal stress on neurodevelopment and cognitive functions. J. Genet. 2018;97(2):581-583.

51. Muotri A.R., Chu V.T., Marchetto M.C., Deng W., Moran J.V, Gage F.H. Somatic mosaicism in neuronal precursor cells mediated by L1 retrotransposition. Nature. 2005;435:903-910.

52. Mustafin R.N., Khusnutdinova E.K. Non-coding parts of genomes as the basis of epigenetic heredity. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov Journal of Genetics and Breeding. 2017;21(6):742-749. DOI 10.18699/VJ17.30-o. (in Russian)

53. Mustafin R.N., Khusnutdinova E.K. The role of transposable elements in the ecological morphogenesis under influence of stress. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov Journal of Genetics and Breeding. 2019;23(4):380-389. DOI 10.18699/VJ19.506. (in Russian)

54. Nygaard E., Moe V, Slinning K., Walhovd K.B. Longitudinal cognitive development of children born to mothers with opioid and polysubstance use. Pediatr. Res. 2015;78:330-335.

55. Owens M., Goodyer I.M., Wilkinson P 5-HTTLPR and early childhood adversities moderate cognitive and emotional processing in adolescence. PLoS One. 2012;7(11):e48482.

56. Pastuzyn E.D., Day C.E., Kearns R.B., Kyrke-Smith M., Taibi A.V, McCormick J., Yoder N., Belnap D.M., Erlendsson S., Mora-do D.R., Briggs J.A.G., Feschotte C., Shepherd J.D. The neuronal gene Arc encodes a repurposed retrotransposon Gag protein that mediates intercellular RNA transfer. Cell. 2018;172:275-288. DOI 10.1016/j.cell.2017.12.024.

57. Pereira Fernandes D., Bitar M., Jacobs F.M.J., Barry G. Long noncoding RNAs in neuronal aging. Noncoding RNA. 2018;4(2): E12. DOI 10.3390/ncrna4020012.

58. Plomin R., Deary I.J. Genetics and intelligence differences: five special findings. Mol. Psychiatry. 2015;20(1):98-108.

59. Plomin R., Kovas Y Generalist genes and learning disabilities. Psychol. Bull. 2005;131:592-617.

60. Qin S., Jin P, Zhou X., Chen L., Ma F. The role of transposable elements in the origin and evolution of microRNAs in human. PLoS One. 2015;10(6):e0131365.

61. Rudenko A., Tsai L.H. Epigenetic modifications in the nervous system and their impact upon cognitive impairments. Neuropharmacology. 2014;80:70-82.

62. Samantarrai D., Dash S., Chhetri B., Mallick B. Genomic and epigenomic cross-talks in the regulatory landscape of miRNAs in breast cancer. Mol. Cancer Res. 2013;11:315-328.

63. Savvateeva-Popova E.V, Nikitina E.A., Medvedeva A.V. Neurogenetics and neuroepigenetics. Russ. J. Genet. 2015;51 (5): 518528. DOI 10.1134/S1022795415050075.

64. Sengupta S.M., Smith A.K., Grizenko N., Joober R. Locus-specific DNA methylation changes and phenotypic variability in children with attention-deficit hyperactivity disorder. Psychiatry Res. 2017;256:298-304. DOI 10.1016/j.psychres.2017.06.048.

65. Shaltiel G., Hanan M., Wolf Y, Barbash S., Kovalev E., Shoham S., Soreq H. Hippocampal microRNA-132 mediates stress-inducible cognitive deficits through its acetylcholinesterase target. Brain Struct. Funct. 2013;218:59-72.

66. Singer T., McConnell M.J., Marchetto M.C., Coufal N.G., Gage F.H. LINE-1 retrotransposons: mediators of somatic variation in neuronal genomes. Trends Neurosci. 2010;33(8):345-354.

67. Smirnova L., Grafe A., Seiler A., Schumacher S., Nitsch R., Wul-czyn F.G. Regulation of miRNA expression during neural cell specification. Eur. J. Neurosci. 2005;21(6):1499-1477.

68. Sniekers S., Stringer S., Watanabe K., Jansen P.R., Coleman J.R.I., Krapohl E., Taskesen E., Hammerschlag A.R., Okbay A., Za-baneh D., Amin N., Breen G., Cesarini D., Chabris C.F., Iacono W.G., Ikram M.A., Johannesson M., Koellinger P., Lee J.J., Magnusson PK.E., McGue M., Miller M.B., Ollier W.E.R., Payton A., Penedleton N., Plomin R., Rietveld C.A., Tiemeier H., van Duijn C.M., Posthuma D. Genome-wide association metaanalysis of 78,308 individuals identifies new loci and genes influencing human intelligence. Nat. Genet. 2017;49:1107-1112.

69. Stappert L., Roese-Koerner B., Brustle O. The role of microRNAs in human neural stem cells, neuronal differentiation and subtype specification. Cell. Tissue. Res. 2015;359:47-64. DOI 10.1007/s00441-014-1981-y.

70. Sternberg R.J. Intelligence. Dialogues Clin. Neurosci. 2012;14(1): 19-27.

71. Tartaglione A.M., Cipriani C., Chiarotti F., Perrone B., Bales-trieri E., Matteucci C., Sinibaldi-Vallebona P., Calamandrei G., Ricceri L. Early behavioral alterations and increased expression of endogenous retrovireses are inherited across generations in mice prenatally exposed to valproic acid. Mol. Neurobiol. 2019; 56(5):3736-3750.

72. Trizzino M., Kapusta A., Brown C.D. Transposable elements generate regulatory novelty in a tissue-specific fashion. BMC Genomics. 2018;19(1):468.

73. Tucker-Drob E.M., Briley D.A. Continuity of genetic and environmental influences on cognition across the life span: a metaanalysis of longitudinal twin and adoption studies. Psychol. Bull. 2014;140:949-979.

74. Upton K.R., Gerhardt D.J., Jesuadian J.S., Richardson S.R., Sanchez-Luque F.J., Bodea G.O., Ewing A.D., Salvador-Paloeque C., van der Knaap M.S., Brennan P.M., Vanderver A., Faulkner G.J. Ubiquitous L1 mosaicism in hippocampal neurons. Cell. 2015;161(2):228-239. DOI 10.1016/j.cell.2015.03.026.

75. Woldemichael B.T., Mansuy I.M. Micro-RNAs in cognition and cognitive disorders: potential for novel biomarkers and therapeutics. Biochem. Pharmacol. 2016;104:1-7.

76. Wong C.C., Caspi A., Williams B., Craig I.W., Houts R., Ambler A., Moffitt T.E., Mill J. A longitudinal study of epigenetic variation in twins. Epigenetics. 2010;5:516-526.

77. Yang L., Zhang R., Li M., Wu X., Wang J., Huang L., Shi X., Li Q., Su B. A functional MiR-124 binding-site polymorphism in IQGAP1 affects human cognitive performance. PLoS One. 2014;9:e107065. DOI 10.1371/journal.pone.0107065.

78. Yuan Z., Sun X., Jianq D., Ding Y, Lu Z., Gong L., Liu H., Xie J. Origin and evolution of a placental-specific microRNA family in the human genome. BMC Evol. Biol. 2010;10:346-358.

79. Yuan Z., Sun X., Liu H., Xie J. MicroRNA genes derived from repetitive elements and expanded by segmental duplication events in mammalian genomes. PLoS One. 2011;6(3):e17666. DOI 10.1371/joumal.pone.0017666.

80. Zabaneh D., Krapohl E., Gaspar H.A., Curtis C., Lee S.H., Patel H., Newhouse S., Wu H.M., Simpson M.A., Putallaz M., Lubinski D., Plomin R., Breen G. A genome-wide association study for extremely high intelligence. Mol. Psychiatry. 2018;23:12261232.

81. Zhang G., Esteve P., Chin H.G., Terragni J., Dai N., Correa I.R., Pradhan S. Small RNA-mediated DNA (cytosine-5) methyltransferase 1 inhibition leads to aberrant DNA methylation. Nucleic Acids Res. 2015;43(12):6112-6124.


Review

Views: 2732


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 2500-3259 (Online)