Postnatal neurogenesis in the human brain

Abstract

Recently, a lot of data has been gathered which demonstrates neurogenesis in the brain of adult humans. In genetics, findings have been obtained that not only prove, but also elucidate the molecular mechanisms of neurogenesis. In some publications, however, morphology disputes neuronal renewal in adulthood. Therefore, this review presents the modern achievements of epigenetics, morphology, and physiology, which confirm and characterize postnatal neurogenesis in detail. We suggest that the introduction of molecular genetic technologies into morphological studies will be the starting point for the integration of these areas, complementing each other for the introduction of targeted therapy in clinical practice. Numerous evidence has been obtained of the presence of postnatal neurogenesis in adult humans in studies using bromodeoxyuridine, a carbon isotope of ¹⁴C, and ³H-thymidine, in comparative analyses of experimental data from animals. Neuronal stem cells, represented by radial glia present in the subventricular and subgranular zones of the human brain, are morphologically similar to neuroepithelial cells. They express marker proteins for astrocytes, which suggests that the proliferation of neuroglia found in adults can also indicate the regeneration of neurons. To prove this, further studies are required, with the exact identification of newly-formed cells, using specific molecular markers, and data from modern epigenetics. The integration of molecular genetic methods into morphology will facilitate not only the accurate determination of the classification of cells to a specific subpopulation but also to study the effects of various agents on the proliferation of neurons in the adult brain.

Keywords

hippocampus / brain / differentiation / neuronal stem cells

References

[1] Pereira Fernandes DP, Bitar M, Jacobs FM, Barry G. Long Non-Coding RNAs in Neuronal Aging. Noncoding RNA. 2018;4:E12.

[2] Pereira Fernandes D.P., Bitar M., Jacobs F.M., Barry G. Long Non-Coding RNAs in Neuronal Aging // Noncoding RNA. 2018. Vol. 4. pii: E12.

[3] Gomzakov OA. The aging of brain and neurotrophic therapy. M. 2011. 92 p. (In Russ).

[4] Гомзаков О.А. Старение мозга и нейротрофическая терапия. М. 2011. 92 с.

[5] Altman J, Das GD. Auroradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 1965;124:319–335.

[6] Altman J., Das G.D. Auroradiographic and histological evidence of postnatal hippocampal neurogenesis in rats // J. Comp. Neurol. 1965. Vol. 124. P. 319–335.

[7] Sorrells SF, Paredes MF, Cebrian-Silla A, et al. Human hippocampal neurogenesis drops sharply in children to undetectable levels in adults. Nature. 2018;555:377–381. doi: 10.1038/nature25975

[8] Sorrells S.F., Paredes M.F., Cebrian-Silla A., et al. Human hippocampal neurogenesis drops sharply in children to undetectable levels in adults // Nature. 2018. Vol. 555. V. 377–381. doi: 10.1038/nature25975

[9] Dennis CV, Suh LS, Rodriguez ML, et al. Human adult neurogenesis across the ages: An immunohistochemical study. Neuropathol. Appl. Neurobiol. 2016;42:621–638. doi: 10.1111/nan.12337

[10] Dennis C.V., Suh L.S., Rodriguez M.L., et al. Human adult neurogenesis across the ages: An immunohistochemical study // Neuropathol. Appl. Neurobiol. 2016. Vol. 42. P. 621–638. doi: 10.1111/nan.12337

[11] Polenov AL. Morphologic nature of the nerve cell nucleus mammilloinfundibularis of the hypothalamus in man. Dokl. Akad. Nauk SSSR. 1951;80(6):945–948. (In Russ).

[12] Поленов А.Л. Особенности морфологии нервных клеток гипоталамуса человека // Докл. АН СССР. 1951. Т. 80. № 6. С. 945–948.

[13] Polenov AL. Physiologic degeneration and restoration of neurosecretory cells of the nucleus praeopticus in carp and Cyprinus carpio. Dokl. Akad. Nauk SSSR. 1954;99(4):625–628. (In Russ).

[14] Поленов А.Л. О физиологической дегенерации и восстановлении нейросекреторных клеток у сазана и зеркального карпа // Докл. АН СССР. 1954. Т. 99. № 14. С. 625–628.

[15] Chetverukhin VK. Role of the preoptic recess ependyma in the formation and physiologic regeneration of the nucleus praeopticus in Amphibians. Materialy 1-y Vsesoyuznoy konferentsii po neyroendokrinologii. 1974;186–189. (In Russ).

[16] Четверухин В.К. К вопросу о роли эпендимы преоптической бухты в формировании и физиологической регенерации преоптического ядра у амфибий // Материалы 1-й Всесоюзной конференции по нейроэндокринологии. 1974. С. 186–189.

[17] Knoth R, Singec I, Ditter M, et al. Murine features of neurogenesis in the human hippocampus across the lifespan from 0 to 100 years. PLoS One. 2010;5. e8809. doi: 10.1371/journal.pone.0008809

[18] Knoth R., Singec I., Ditter M., et al. Murine features of neurogenesis in the human hippocampus across the lifespan from 0 to 100 years // PLoS One. 2010. Vol. 5. e8809. doi: 10.1371/journal.pone.0008809

[19] Eriksson PS, Perfilieva E, Bjork-Eriksson T, et al. Neurogenesis in the adult human hippocampus. Nat. Med. 1998;4:1313–17. doi: 10.1038/3305

[20] Eriksson P.S., Perfilieva E., Bjork-Eriksson T., et al. Neurogenesis in the adult human hippocampus // Nat. Med. 1998. Vol. 4. P. 1313–17. doi: 10.1038/3305

[21] Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 1992;255:1707–10.

[22] Reynolds B.A., Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system // Science. 1992. V. 255. P. 1707–10.

[23] Aleksandrova MA, Marey MV. Stem Cells in the Brain of Mammals and Human: Fundamental and Applied Aspects. Zhurnal vysshey nervnoy deyatelnosti. 2015;65(3):271–305. (In Russ).

[24] Александрова М.А., Марей М.В. Стволовые клетки в мозгу млекопитающих и человека: фундаментальные и прикладные аспекты // Журнал высшей нервной деятельности. 2015. Т. 65. № 3. С. 271–305.

[25] Hansen DV, Lui JH, Parker PR, Kriegstein AR. Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature. 2010;464:554–561. doi: 10.1038/nature08845

[26] Hansen D.V., Lui J.H., Parker P.R., Kriegstein A.R. Neurogenic radial glia in the outer subventricular zone of human neocortex // Nature. 2010. Vol. 464. P. 554–561. doi: 10.1038/nature08845

[27] Lie DC, Dziewczapolski G, Willhoite AR, et al. The adult substantia nigra contains progenitor cells with neurogenic potential. J. Neurosci. 2002;22:6639–49. doi: 10.1523/JNEUROSCI.22-15-06639.2002

[28] Lie D.C., Dziewczapolski G., Willhoite A.R., et al. The adult substantia nigra contains progenitor cells with neurogenic potential // J. Neurosci. 2002. Vol. 22. P. 6639–49. doi: 10.1523/JNEUROSCI.22-15-06639.2002

[29] Rojczyk-Golebieska E, Pflasz A, Wiaderkiewicz R. Hypothalamic subependymal niche: a novel site of the adult neurogenesis. Cellular and molecular neurobiology. 2014;34:631–642. doi: 10.1007/s10571-014-0058-5

[30] Rojczyk-Golebieska E., Pflasz A., Wiaderkiewicz R. Hypothalamic subependymal niche: a novel site of the adult neurogenesis // Cellular and molecular neurobiology. 2014. V. 34. P. 631–642. doi: 10.1007/s10571-014-0058-5

[31] Ming G, Song H. Adult Neurogenesis in the Mammalian Brain: Significant Answers and Significant Questions. Neuron. 2011;70:687–702. doi: 10.1016/j.neuron.2011.05.001

[32] Ming G., Song H. Adult Neurogenesis in the Mammalian Brain: Significant Answers and Significant Questions // Neuron. 2011. Vol. 70. P. 687–702. doi: 10.1016/j.neuron.2011.05.001

[33] Katsimpardi L, Lledo PM. Regulation of neurogenesis in the adult and aging brain. Curr. Opin. Neurobiol. 2018;53:131–138. doi: 10.1016/j.conb.2018.07.006

[34] Katsimpardi L., Lledo P.M. Regulation of neurogenesis in the adult and aging brain // Curr. Opin. Neurobiol. 2018. V. 53. P. 131–138. doi: 10.1016/j.conb.2018.07.006

[35] Obukhov DK, Pushchina EV, Varaksin AA. The structure of proliferative zones in the central nervous system of adult vertebrates. Voprosy morfologii XXI veka. 4:43–51. (In Russ).

[36] Обухов Д.К., Пущина Е.В., Вараксин А.А. Структура пролиферативных зон в ЦНС взрослых позвоночных животных // Вопросы морфологии XXI века. Выпуск 4. С. 43–51.

[37] Gomzakov OA. Neurogenesis as an Adaptive Function of Brain. M. 2014. 85 p. (In Russ).

[38] Гомзаков О.А. Нейрогенез как адаптивная функция мозга. М. 2014. 85 с.

[39] Luo Y, Coskun V, Liang A, et al. Single-cell transcriptome analyses reveal signals to activate dormant neural stem cells. Cell. 2015;161:1175–86. doi: 10.1016/j.cell.2015.04.001

[40] Luo Y., Coskun V., Liang A., et al. Single-cell transcriptome analyses reveal signals to activate dormant neural stem cells // Cell. 2015. V. 161. P. 1175–86. doi: 10.1016/j.cell.2015.04.001

[41] Amrein I, Dechmann DK, Winter Y, Lipp HP. Absent or low rate of adult neurogenesis in the hippocampus of bats (Chiroptera). PLoS One. 2007;2:e455. doi: 10.1371/journal.pone.0000455

[42] Amrein I., Dechmann D.K., Winter Y., Lipp H.P. Absent or low rate of adult neurogenesis in the hippocampus of bats (Chiroptera) // PLoS One. 2007. Vol. 2. e455. doi: 10.1371/journal.pone.0000455

[43] Polezhayev LV. Transplantaion of brain tissue and function recovery. Uspekhi Sovremennoy Biologii. 1985;99(1):123–140. (In Russ).

[44] Полежаев Л.В. Трансплантация ткани мозга и проблема восстановления функций // Усп. совр. биол. 1985. Т. 99. № 1. С. 123–140.

[45] Chapouton P, Jagasia R, Bally-Cuif L. Adult neurogenesis in non-mammalian vertebrates. Bioessays. 2007;29:745–757. doi: 10.1002/bies.20615

[46] Chapouton P., Jagasia R., Bally-Cuif L. Adult neurogenesis in non-mammalian vertebrates // Bioessays. 2007. V. 29. P. 745–757. doi: 10.1002/bies.20615

[47] Barbosa JS, Sanchez-Gonzalez R, Di Giaimo R, et al. Neurodevelopment. Live imaging of adult neural stem cell behavior in the intact and injured zebrafish brain. Science. 2015; 348(6236):789–793. doi: 10.1126/science.aaa2729

[48] Barbosa J.S., Sanchez-Gonzalez R., Di Giaimo R., et al. Neurodevelopment. Live imaging of adult neural stem cell behavior in the intact and injured zebrafish brain // Science. 2015. Vol. 348. № 6236. P. 789–793. doi: 10.1126/science.aaa2729

[49] Cameron HA, McKay RD. Restoring production of hippocampal neurons in old age. Nat. Neurosci. 1999;2:894–897. doi: 10.1038/13197

[50] Cameron H.A., McKay R.D. Restoring production of hippocampal neurons in old age // Nat. Neurosci. 1999. Vol. 2. P. 894–897. doi: 10.1038/13197

[51] Encians JM, Vaahtokari A, Enikolopov G. Fluoxetine targets early progenitor cells in the adult brain. Proc. Natl. Acad. Sci. USA. 2006;103:8233–38. doi: 10.1073/pnas.0601992103

[52] Encians J.M., Vaahtokari A., Enikolopov G. Fluoxetine targets early progenitor cells in the adult brain // Proc. Natl. Acad. Sci. USA. 2006. Vol. 103. P. 8233–38. doi: 10.1073/pnas.0601992103

[53] Fares J, Bou Diab Z, Nabha S, Fares Y. Neurogenesis in the adult hippocampus: history, regulation, and prospective roles. Int. J. Neurosci. 2019;129:598–611. doi: 10.1080/00207454.2018.1545771

[54] Fares J., Bou Diab Z., Nabha S., Fares Y. Neurogenesis in the adult hippocampus: history, regulation, and prospective roles // Int. J. Neurosci. 2019. V. 129. P. 598–611. doi: 10.1080/00207454.2018.1545771

[55] Engler A, Zhang R, Taylor V. Notch and Neurogenesis. Adv. Exp. Biol. 2018;1066:223–234. doi: 10.1007/978-3-319-89512-3_11

[56] Engler A., Zhang R., Taylor V. Notch and Neurogenesis // Adv. Exp. Biol. 2018. Vol. 1066. P. 223–234. doi: 10.1007/978-3-319-89512-3_11

[57] Zhang R, Engler A, Taylor V. Notch: an interactive player in neurogenesis and disease. Cell. Tissue Res. 2018;371:73–89. doi: 10.1007/s00441-017-2641-9

[58] Zhang R., Engler A., Taylor V. Notch: an interactive player in neurogenesis and disease // Cell. Tissue Res. 2018. V. 371. P. 73–89. doi: 10.1007/s00441-017-2641-9

[59] Zwamborn RAJ, Snijders C, An N, et al. Wnt Signaling in the Hippocampus in Relation to Neurogenesis, Neuroplasticity, Stress and Epigenetics. Prog. Mol. Biol. Transl. Sci. 2018;158:129–157. doi: 10.1016/bs.pmbts.2018.04.005

[60] Zwamborn R.A.J., Snijders C., An N., et al. Wnt Signaling in the Hippocampus in Relation to Neurogenesis, Neuroplasticity, Stress and Epigenetics // Prog. Mol. Biol. Transl. Sci. 2018. V. 158. P. 129–157. doi: 10.1016/bs.pmbts.2018.04.005

[61] de Miranda AS, Zhang CJ, Katsumoto A, Teixeira AL. Hippocampal adult neurogenesis: Does the immune system matter. J. Neurol. Sci. 2017;372:482–495. doi: 10.1016/j.jns.2016.10.052

[62] de Miranda A.S., Zhang C.J., Katsumoto A., Teixeira A.L. Hippocampal adult neurogenesis: Does the immune system matter // J. Neurol. Sci. 2017. Vol. 372. P. 482–495. doi: 10.1016/j.jns.2016.10.052

[63] Butovsky O, Ziv Y, Schwartz A, et al. Microglia activated by IL-4 of IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol. Cell. Neurosci. 2006;31:149–160. doi: 10.1016/j.mcn.2005.10.006

[64] Butovsky O., Ziv Y., Schwartz A., et al. Microglia activated by IL-4 of IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells // Mol. Cell. Neurosci. 2006. V. 31. P. 149–160. doi: 10.1016/j.mcn.2005.10.006

[65] Ziv Y, Ron N, Butovsky O, et al. Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat. Neurosci. 2006;9:268–275. doi: 10.1038/nn1629

[66] Ziv Y., Ron N., Butovsky O., et al. Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood // Nat. Neurosci. 2006. V. 9. P. 268–275. doi: 10.1038/nn1629

[67] Briggs JA, Wolvetang EJ, Mattick JS, et al. Mechanisms of Long Non-coding RNAs in Mammalian Nervous System Development, Plasticity, Desease, and Evolution. Neuron. 2015;88:861–877. doi: 10.1016/j.neuron.2015.09.045

[68] Briggs J.A., Wolvetang E.J., Mattick J.S., et al. Mechanisms of Long Non-coding RNAs in Mammalian Nervous System Development, Plasticity, Desease, and Evolution // Neuron. 2015. Vol. 88. P. 861–877. doi: 10.1016/j.neuron.2015.09.045

[69] Barry G, Guennewig B, Fung S, et al. Long Non-Coding RNA Expression during Aging in the Human Subependymal Zone. Front. Neurol. 2015;6:45. doi: 10.3389/fneur.2015.00045

[70] Barry G., Guennewig B., Fung S., et al. Long Non-Coding RNA Expression during Aging in the Human Subependymal Zone // Front. Neurol. 2015. Vol. 6. P. 45. doi: 10.3389/fneur.2015.00045

[71] Ramos AD, Diaz A, Nellore A, et al. Integration of genome-wide approaches identifies lncRNAs of adult neural stem cells and their progeny in vivo. Cell. Stem Cell. 2013;12:616–628. doi: 10.1016/j.stem.2013.03.003

[72] Ramos A.D., Diaz A., Nellore A., et al. Integration of genome-wide approaches identifies lncRNAs of adult neural stem cells and their progeny in vivo // Cell. Stem Cell. 2013. Vol. 12. P. 616–628. doi: 10.1016/j.stem.2013.03.003

[73] Ramos AD, Andersen RE, Liu SJ, et al. The long noncoding RNA Pnky regulates neuronal differentiation of embryonic and postnatal neural stem cells. Cell. Stem Cell. 2015;16:439–447. doi: 10.1016/j.stem.2015.02.007

[74] Ramos A.D., Andersen R.E., Liu S.J., et al. The long noncoding RNA Pnky regulates neuronal differentiation of embryonic and postnatal neural stem cells // Cell. Stem Cell. 2015. Vol. 16. P. 439–447. doi: 10.1016/j.stem.2015.02.007

[75] Dong X, Chen K, Cuevas-Diaz Duran R, et al. Comprehensive Identification of Long Non-coding RNAs in Purified Cell Types from the Brain Reveals Functional LncRNA in OPC Fate Determination. PLoS Genet. 2015;11:e1005669. doi: 10.1371/journal.pgen.1005669

[76] Dong X., Chen K., Cuevas-Diaz Duran R., et al. Comprehensive Identification of Long Non-coding RNAs in Purified Cell Types from the Brain Reveals Functional LncRNA in OPC Fate Determination // PLoS Genet. 2015. Vol. 11. e1005669. doi: 10.1371/journal.pgen.1005669

[77] Lois С, Alvarez-Buylla A. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl. Acad. Sci. USA. 1993;90:2074–77. doi: 10.1073/pnas.90.5.2074

[78] Lois С., Alvarez-Buylla A. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia // Proc. Natl. Acad. Sci. USA. 1993. Vol. 90. P. 2074–77. doi: 10.1073/pnas.90.5.2074

[79] Roy NS, Wang S, Jiang L, et al. In vitro neurogenesis by progenitor cells isolated from the adult human hippocampus. Nat. Med. 2000;6:271–277. doi: 10.1038/73119

[80] Roy N.S., Wang S., Jiang L., et al. In vitro neurogenesis by progenitor cells isolated from the adult human hippocampus // Nat. Med. 2000. Vol. 6. P. 271–277. doi: 10.1038/73119

[81] Spalding KL, Bergmann O, Alkass K, et al. Dynamics of hippoсampal neurogenesis in adult humans. Cell. 2013;153:1219–27. doi: 10.1016/j.cell.2013.05.002

[82] Spalding K.L., Bergmann O., Alkass K., et al. Dynamics of hippoсampal neurogenesis in adult humans // Cell. 2013. Vol. 153. P. 1219–27. doi: 10.1016/j.cell.2013.05.002

[83] Boldrini M, Fulmore CA, Tartt AN, et al. Human Hippocampal Neurogenesis Persists throughout Aging. Cell. Stem Cell. 2018;22:589–599. doi: 10.1016/j.stem.2018.03.015

[84] Boldrini M., Fulmore C.A., Tartt A.N., et al. Human Hippocampal Neurogenesis Persists throughout Aging // Cell. Stem Cell. 2018. V. 22. P. 589–599. doi: 10.1016/j.stem.2018.03.015

[85] Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buyalla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J. Neurosci. 2001;21:7153–60. doi: 10.1523/JNEUROSCI.21-18-07153.2001

[86] Seri B., Garcia-Verdugo J.M., McEwen B.S., Alvarez-Buyalla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus // J. Neurosci. 2001. Vol. 21. P. 7153–60. doi: 10.1523/JNEUROSCI.21-18-07153.2001

[87] Kriegstein A, Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells. Annu. Rev. Neurosci. 2009;32:149–184. doi: 10.1146/annurev.neuro.051508.135600

[88] Kriegstein A., Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells // Annu. Rev. Neurosci. 2009. Vol. 32. P. 149–184. doi: 10.1146/annurev.neuro.051508.135600

[89] Carlen M, Meletis K, Goritz C, et al. Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke. Nat. Neurosci. 2009;12:259–267. doi: 10.1038/nn.2268

[90] Carlen M., Meletis K., Goritz C., et al. Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke // Nat. Neurosci. 2009. Vol. 12. P. 259–267. doi: 10.1038/nn.2268

[91] van Praag H, Schinder AF, Christie BR, et al. Functional neurogenesis in the adult hippocampus. Nature. 2002;415:1030–34. doi: 10.1038/4151030a

[92] van Praag H., Schinder A.F., Christie B.R., et al. Functional neurogenesis in the adult hippocampus // Nature. 2002. Vol. 415. P. 1030–34. doi: 10.1038/4151030a

[93] Skala AM. Retroviral DNA Transposition: Themes and Variations. Microbiol. Sperctr. 2014;2. doi: 10.1128/microbiolspec.MDNA3-0005-2014.

[94] Skala A.M. Retroviral DNA Transposition: Themes and Variations // Microbiol. Sperctr. 2014. Vol. 2. doi: 10.1128/microbiolspec.MDNA3-0005-2014

[95] Notwell JH, Chung T, Heavner W, Bejerano G. A family of transposable elements co-opted into developmental enhancers in the mouse neocortex. Nat. Commun. 2015;6:6644. doi: 10.1038/ncomms7644

[96] Notwell J.H., Chung T., Heavner W., Bejerano G. A family of transposable elements co-opted into developmental enhancers in the mouse neocortex // Nat. Commun. 2015. Vol. 6. P. 6644. doi: 10.1038/ncomms7644

[97] Pastuzyn ED, Day CE, Kearns RB, et al. 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

[98] Pastuzyn E.D., Day C.E., Kearns R.B., et al. The Neuronal Gene Arc Encodes a Repurposed Retrotransposon Gag Protein that Mediates Intercellular RNA Transfer // Cell. 2018. Vol. 172. P. 275–288. doi: 10.1016/j.cell.2017.12.024

[99] Suarez NA, Macia A, Muotri AR. LINE-1 retrotransposons in healthy and diseased human brain. Dev. Neurobiol. 2018;78:434–455. doi: 10.1002/dneu.22567

[100] Suarez N.A., Macia A., Muotri A.R. LINE-1 retrotransposons in healthy and diseased human brain // Dev. Neurobiol. 2018. Vol. 78. P. 434–455. doi: 10.1002/dneu.22567

[101] Mustafin RN, Khusnutdinova EK. Non-coding parts of genomes as the basis of epigenetic heredity. Vavilov Journal of Genetics and Breeding. 2017;21(6):742–749. doi: 10.18699/10.18699/VJ17.30-o

[102] Mustafin R.N., Khusnutdinova E.K. Non-coding parts of genomes as the basis of epigenetic heredity // Vavilov Journal of Genetics and Breeding. 2017. Vol. 21. № 6. P. 742–749. doi: 10.18699/10.18699/VJ17.30-o

[103] Lapp HE, Hunter RG. The dynamic genome: transposons and environmental adaptation in the nervous system. Epigenomics. 2016;8:237. doi: 10.2217/epi.15.107

[104] Lapp H.E., Hunter R.G. The dynamic genome: transposons and environmental adaptation in the nervous system // Epigenomics. 2016. Vol. 8. P. 237. doi: 10.2217/epi.15.107

[105] Johnson R, Guigo R. The RIDL hypothesis: transposable elements as functional domains of long noncoding RNAs. RNA. 2014;20:959–976. doi: 10.1261/rna.044560.114

[106] Johnson R., Guigo R. The RIDL hypothesis: transposable elements as functional domains of long noncoding RNAs // RNA. 2014. Vol. 20. P. 959–976. doi: 10.1261/rna.044560.114

[107] Kapusta A, Feschotte C. Volatile evolution of long noncoding RNA repertoires: mechanisms and biological implications. Trends Genet. 2014;30:439–452. doi: 10.1016/j.tig.2014.08.004

[108] Kapusta A., Feschotte C. Volatile evolution of long noncoding RNA repertoires: mechanisms and biological implications // Trends Genet. 2014. Vol. 30. P. 439–452. doi: 10.1016/j.tig.2014.08.004

[109] Honson DD, Macfarlan TS. A lncRNA-like Role for LINE1s in Development. Dev. Cell. 2018;46:132–134. doi: 10.1016/j.devcel.2018.06.022

[110] Honson D.D., Macfarlan T.S. A lncRNA-like Role for LINE1s in Development // Dev. Cell. 2018. Vol. 46. P. 132–134. doi: 10.1016/j.devcel.2018.06.022

[111] Lu X, Sachs F, Ramsay L, et al. The retrovirus HERVH is a long noncoding RNA required for human embryonic stem cell identity. Nat. Struct. Mol. Biol. 2014;21:423–425. doi: 10.1038/nsmb.2799

[112] Lu X., Sachs F., Ramsay L., et al. The retrovirus HERVH is a long noncoding RNA required for human embryonic stem cell identity // Nat. Struct. Mol. Biol. 2014. Vol. 21. P. 423–425. doi: 10.1038/nsmb.2799

[113] Faulkner GJ. Retrotransposons: mobile and mutagenic from conception to death. FEBS Let. 2011;585:1589–94. doi: 10.1016/j.febslet.2011.03.061

[114] Faulkner G.J. Retrotransposons: mobile and mutagenic from conception to death // FEBS Let. 2011. Vol. 585. P. 1589–1594. doi: 10.1016/j.febslet.2011.03.061

[115] Kurnosov AA, Ustyugova SV, Nazarov V, et al. The evidence for increased L1 activity in the site of human adult brain neurogenesis. PLoS One. 2015;10.(2):e0117854. doi: 10.1371/journal.pone.0117854

[116] Kurnosov A.A., Ustyugova S.V., Nazarov V., et al. The evidence for increased L1 activity in the site of human adult brain neurogenesis // PLoS One. 2015. Vol. 10. № 2. e0117854. doi: 10.1371/journal.pone.0117854

[117] Upton KR, Gerhardt DJ, Jesuadian JS, et al. Ubiquitous L1 mosaicism in hippocampal neurons. Cell. 2015;161(2):228–239. doi: 10.1016/j.cell.2015.03.026

[118] Upton K.R., Gerhardt D.J., Jesuadian J.S., et al. Ubiquitous L1 mosaicism in hippocampal neurons // Cell. 2015. Vol. 161. № 2. P. 228–239. doi: 10.1016/j.cell.2015.03.026

[119] Gerdes P, Richardson SR, Mager DL, Faulkner GJ. Transposable elements in the mammalian embryo: pioneers surviving through stealth and service. Genome Biology. 2016;17:100. doi: 10.1186/s13059-016-0965-5

[120] Gerdes P., Richardson S.R., Mager D.L., Faulkner G.J. Transposable elements in the mammalian embryo: pioneers surviving through stealth and service // Genome Biology. 2016. Vol. 17. P. 100. doi: 10.1186/s13059-016-0965-5

[121] Macfarlan TS, Gifford WD, Driscoll S, et al. ES cell potency fluctuates with endogenous retrovirus activity. Nature. 2012;487:57–63. doi: 10.1038/nature11244

[122] Macfarlan T.S., Gifford W.D., Driscoll S., et al. ES cell potency fluctuates with endogenous retrovirus activity // Nature. 2012. Vol. 487. P. 57–63. doi: 10.1038/nature11244

RIGHTS & PERMISSIONS

Mustafin R.N., Khusnutdinova E.K.