Association of polymorphic variants of the gene BDNF in human adaptation to extreme environmental conditions and life expectancy
- Authors: Spivak I.M.1,2, Zhekalov A.N.1, Spivak D.L.3, Shapovalov P.A.1, Timoshenko R.V.1,2, Glushakov R.I.1, Golovko K.P.1
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Affiliations:
- Military Medical Academy
- Saint Petersburg State University
- N.P. Bechtereva Human Brain Institute, Russian Academy of Sciences
- Issue: Vol 42, No 3 (2023)
- Pages: 293-301
- Section: Reviews
- URL: https://journals.rcsi.science/RMMArep/article/view/264768
- DOI: https://doi.org/10.17816/rmmar303662
- ID: 264768
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Abstract
BDNF is a member of the neurotrophin protein family, which plays an important role in the development, maintenance and plasticity of the central and peripheral nervous system. BDNF is expressed in neurons of the developing and adult mammalian nervous system, where it is produced in relatively small amounts, but has high activity, causing biological reactions at picomolar concentrations. It promotes the differentiation of neurons from stem cells, enhances neurite growth and synaptogenesis, and can prevent programmed cell death (apoptosis). The role of BDNF in the regulation of energy homeostasis is also great: by stimulating glucose transport and mitochondrial biogenesis, BDNF enhances cell bioenergetics and protects neurons from damage and neurodegenerative diseases. It is BDNF that controls nutrition patterns (regulating appetite) and types of physical activity, modulates glucose metabolism in peripheral tissues and mediates the positive effect of exercise and fasting on cognitive functions, mood, cardiovascular function and peripheral metabolism. This article presents a mini-review of the data accumulated to date on the role of polymorphic variants of the BDNF gene in the processes of active physiological and psychological adaptation and their comparison with the data obtained by the authors in the study of psychological adaptation to working conditions in the Arctic region of the Russian Federation. The given materials allow us to conclude that optimal adaptation to extreme external conditions is most likely provided genetically by the presence of the Val/Val genotype of the BDNF gene (also associated, in turn, with the probable extension of the individual survival period), and psychologically by the increased use of creative ability.
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##article.viewOnOriginalSite##About the authors
Irina M. Spivak
Military Medical Academy; Saint Petersburg State University
Email: Irina_spivak@hotmail.com
ORCID iD: 0000-0003-1351-8696
SPIN-code: 6740-5392
senior researcher
Russian Federation, Saint Petersburg; Saint PetersburgAndrey N. Zhekalov
Military Medical Academy
Email: Jann1960@mail.ru
ORCID iD: 0000-0001-6580-4075
SPIN-code: 3154-9228
senior researcher
Russian Federation, Saint PetersburgDmitry L. Spivak
N.P. Bechtereva Human Brain Institute, Russian Academy of Sciences
Email: d.spivak@mail.ru
ORCID iD: 0000-0001-7276-5182
SPIN-code: 6764-3561
leading expert
Russian Federation, Saint PetersburgPavel A. Shapovalov
Military Medical Academy
Email: pavel.shapovalov.2001@mail.ru
ORCID iD: 0000-0003-0639-017X
SPIN-code: 2498-7308
5th year cadet
Russian Federation, Saint PetersburgRuslan V. Timoshenko
Military Medical Academy; Saint Petersburg State University
Email: rtimbio@yandex.ru
Bachelor of Biology Faculty
Russian Federation, Saint Petersburg; Saint PetersburgRuslan I. Glushakov
Military Medical Academy
Email: Glushakovruslan@gmail.com
ORCID iD: 0000-0002-0161-5977
SPIN-code: 6860-8990
M.D., D.Sc. (Medicine)
Russian Federation, Saint PetersburgKonstantin P. Golovko
Military Medical Academy
Author for correspondence.
Email: labws@mail.ru
ORCID iD: 0000-0002-1584-1748
SPIN-code: 2299-6153
M.D., D.Sc. (Medicine)
Russian Federation, Saint PetersburgReferences
- Lau H, Fitri A, Ludin M, Rajab NF, Shahar S. Identification of Neuroprotective Factors Associated with Successful Ageing and Risk of Cognitive Impairment among Malaysia Older Adults. Curr Gerontol Geriatr Res. 2017;2017:4218756. doi: 10.1155/2017/4218756
- Prabu P, Poongothai S, Shanthirani CS, et al. Altered circulatory levels of miR-128, BDNF, cortisol and shortened telomeres in patients with type 2 diabetes and depression. Acta Diabetol. 2020;57(7):799–807. doi: 10.1007/s00592-020-01486-9
- Vasconcelos-Moreno MP, Fries GR, Gubert C, et al. Telomere Length, Oxidative Stress, Inflammation and BDNF Levels in Siblings of Patients with Bipolar Disorder: Implications for Accelerated Cellular Aging. Int J Neuropsychopharmacol. 2017;20(6):445–454. doi: 10.1093/ijnp/pyx001
- Zhou JX, Li HC, Bai XJ, et al. Functional Val66Met polymorphism of Brain-derived neurotrophic factor in type 2 diabetes with depression in Han Chinese subjects. Behav Brain Funct. 2013;9:34. doi: 10.1186/1744-9081-9-34
- Chao MV, Rajagopal R, Lee FS. Neurotrophin signalling in health and disease. Clin Sci (Lond). 2006;110(2):167–173. doi: 10.1042/CS20050163
- Markham A, Cameron I, Bains R, et al. Brain-derived neurotrophic factor-mediated effects on mitochondrial respiratory coupling and neuroprotection share the same molecular signalling pathways. Eur J Neurosci. 2012;35(3):366–374. doi: 10.1111/j.1460-9568.2011.07965.x
- Marosi K, Mattson MP. BDNF mediates adaptive brain and body responses to energetic challenges. Trends Endocrinol Metab. 2014;25(2):89–98. doi: 10.1016/j.tem.2013.10.006
- Lebrun B, Bariohay B, Moyse E, Jean A. Brain-derived neurotrophic factor (BDNF) and food intake regulation: a minireview. Auton Neurosci. 2006;126–127:30–38. doi: 10.1016/j.autneu.2006.02.027
- Koppel I, Aid-Pavlidis T, Jaanson K, et al. Tissue-specific and neural activity-regulated expression of human BDNF gene in BAC transgenic mice. BMC Neurosci. 2009;10:68. doi: 10.1186/1471-2202-10-68
- Dean C, Liu H, Staudt T, et al. Distinct subsets of Syt-IV/BDNF vesicles are sorted to axons versus dendrites and recruited to synapses by activity. J Neurosci. 2012;32(16):5398–5413. doi: 10.1523/JNEUROSCI.4515-11.2012
- Totoson P, Santini C, Prigent-Tessier A, Marie C, Demougeot C. Endothelial TrkB receptor activation controls vascular tone of rat middle cerebral artery. Vascul Pharmacol. 2021;141:106930. doi: 10.1016/j.vph.2021.106930
- Cheng A, Wan R, Yang JL, et al. Involvement of PGC-1α in the formation and maintenance of neuronal dendritic spines. Nat Commun. 2012;3:1250. doi: 10.1038/ncomms2238
- Albrecht U. Timing to perfection: the biology of central and peripheral circadian clocks. Neuron. 2012;74(2):246–260. doi: 10.1016/j.neuron.2012.04.006
- Pollock GS, Vernon E, Forbes ME, et al. Effects of early visual experience and diurnal rhythms on BDNF mRNA and protein levels in the visual system, hippocampus, and cerebellum. J Neurosci. 2001;21(11):3923–3931. doi: 10.1523/JNEUROSCI.21-11-03923.2001
- Dolci C, Montaruli A, Roveda E, et al. Circadian variations in expression of the trkB receptor in adult rat hippocampus. Brain Res. 2003;994(1):67–72. doi: 10.1016/j.brainres.2003.09.018
- Mattson MP. Energy intake and exercise as determinants of brain health and vulnerability to injury and disease. Cell Metab. 2012;16(6):706–722. doi: 10.1016/j.cmet.2012.08.012
- Mattson MP. Evolutionary aspects of human exercise — born to run purposefully. Ageing Res Rev. 2012;11(3):347–352. doi: 10.1016/j.arr.2012.01.007
- Hopkins ME, Nitecki R, Bucci DJ. Physical exercise during adolescence versus adulthood: differential effects on object recognition memory and brain-derived neurotrophic factor levels. Neuroscience. 2011;194:84–94. doi: 10.1016/j.neuroscience.2011.07.071
- Molteni R, Wu A, Vaynman S, et al. Exercise reverses the harmful effects of consumption of a high-fat diet on synaptic and behavioral plasticity associated to the action of brain-derived neurotrophic factor. Neuroscience. 2001;23(2):429–404. doi: 10.1016/j.neuroscience.2003.09.020
- Vaynman S, Ying Z, Gomez-Pinilla F. Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci. 2004;20(10):2580–2590. doi: 10.1111/j.1460-9568.2004.03720.x
- Stranahan AM, Khalil D, Gould E. Running induces widespread structural alterations in the hippocampus and entorhinal cortex. Hippocampus. 2007;17(11):1017–1022. doi: 10.1002/hipo.20348
- Kobilo T, Liu QR, Gandhi K, et al. Running is the neurogenic and neurotrophic stimulus in environmental enrichment. Learn Mem. 2011;18(9):605–609. doi: 10.1101/lm.2283011
- Winter B, Breitenstein C, Mooren FC, et al. High impact running improves learning. Neurobiol Learn Mem. 2007;87(4):597–609. doi: 10.1016/j.nlm.2006.11.003
- Griffin EW, Mullally S, Foley C, et al. Aerobic exercise improves hippocampal function and increases BDNF in the serum of young adult males. Physiol Behav. 2011;104(5):934–941. doi: 10.1016/j.physbeh.2011.06.005
- Duman CH, Schlesinger L, Russell DS, Duman RS. Voluntary exercise produces antidepressant and anxiolytic behavioral effects in mice. Brain Res. 2008;1199:148–158. doi: 10.1016/j.brainres.2007.12.047
- Marais L, Stein DJ, Daniels WM. Exercise increases BDNF levels in the striatum and decreases depressive-like behavior in chronically stressed rats. Metab Brain Dis. 2009;24(4):587–597. doi: 10.1007/s11011-009-9157-2
- Sartori CR, Vieira AS, Ferrari EM, et al. The antidepressive effect of the physical exercise correlates with increased levels of mature BDNF, and proBDNF proteolytic cleavage-related genes, p11 and tPA. Neuroscience. 2011;180:9–18. doi: 10.1016/j.neuroscience.2011.02.055
- Levay EA, Govic A, Penman J, Paolini AG, Kent S. Effects of adult-onset calorie restriction on anxiety-like behavior in rats. Physiol Behav. 2007;92(5):889–896. doi: 10.1016/j.physbeh.2007.06.018
- Kashiwaya Y, Bergman C, Lee JH, et al. A ketone ester diet exhibits anxiolytic and cognition-sparing properties, and lessens amyloid and tau pathologies in a mouse model of Alzheimer’s disease. Neurobiol Aging. 2013;34(6):1530–1539. doi: 10.1016/j.neurobiolaging.2012.11.023
- Riddle MC, McKenna MC, Yoon YJ, et al. Caloric restriction enhances fear extinction learning in mice. Neuropsychopharmacology. 2013;38(6):930–937. doi: 10.1038/npp.2012.268
- Vaynman S, Ying Z, Gomez-Pinilla F. The select action of hippocampal calcium calmodulin protein kinase II in mediating exercise-enhanced cognitive function. Neuroscience. 2007;144(3):825–833. doi: 10.1016/j.neuroscience.2006.10.005
- Wrann CD, White JP, Salogiannnis J, et al. Exercise induces hippocampal BDNF through a PGC-1α/FNDC5 pathway. Cell Metab. 2013;18(5):649–659. doi: 10.1016/j.cmet.2013.09.008
- Chen MJ, Russo-Neustadt AA. Exercise activates the phosphatidylinositol 3-kinase pathway. Brain Res Mol Brain Res. 2005;135(1–2): 181–193. doi: 10.1016/j.molbrainres.2004.12.001
- Aguiar AS Jr, Castro AA, Moreira EL, et al. Short bouts of mild-intensity physical exercise improve spatial learning and memory in aging rats: involvement of hippocampal plasticity via AKT, CREB and BDNF signaling. Mech Ageing Dev. 2011;132(11–12):560–567. doi: 10.1016/j.mad.2011.09.005
- Stranahan AM, Mattson MP. Recruiting adaptive cellular stress responses for successful brain ageing. Nat Rev Neurosci. 2012;13(3):209–216. doi: 10.1038/nrn3151
- Yang B, Slonimsky JD, Birren SJ. A rapid switch in sympathetic neurotransmitter release properties mediated by the p75 receptor. Nat Neurosci. 2002;5(6):539–545. doi: 10.1038/nn0602-853
- Wan R, Weigand LA, Bateman R, et al. Evidence that BDNF regulates heart rate by a mechanism involving increased brainstem parasympathetic neuron excitability. J Neurochem. 2014;129(4):573–580. doi: 10.1111/jnc.12656
- Griffioen KJ, Wan R, Brown TR, et al. Aberrant heart rate and brainstem brain-derived neurotrophic factor (BDNF) signaling in a mouse model of Huntington’s disease. Neurobiol Aging. 2012;33(7):1481.e1–5. doi: 10.1016/j.neurobiolaging.2011.11.030
- Wan R, Camandola S, Mattson MP. Intermittent food deprivation improves cardiovascular and neuroendocrine responses to stress in rats. J Nutr. 2003;133(6):1921–1929. doi: 10.1093/jn/133.6.1921
- Zuccato C, Cattaneo E. Brain-derived neurotrophic factor in neurodegenerative diseases. Nat Rev Neurol. 2009;5(6):311–322. doi: 10.1038/nrneurol.2009.54
- Spivak IM, Lemeshchenko AV, Agafonov PV, et al. Relationship of creativity and genetic factors in military services in the conditions of the arctic region. Bulletin of the Russian Military Medical Academy. 2021;23(4):139–146. (In Russ.) doi: 10.17816/brmma84997
- Spivak DL, Shapovalov PA, Trandina AE, et al. Psychological resources of longevity and their genetic correlates. Science and world. 2022;(11 (111)):67–71. (In Russ.)
- Spivak I, Zhekalov A, Glushakov R, Nyrov V, Spivak D. Creativity and Life Expectancy in Strategies of Adaptation. In: Bylieva D., Nordmann A., eds. Technologies in a Multilingual Environment. XXII Professional Culture of the Specialist of the Future 2022. Lecture Notes in Networks and Systems, vol 636. Cham: Springer; 2022. P. 202–210. doi: 10.1007/978-3-031-26783-3_18
- De Sousa RAL, Improta-Caria AC, Aras-Júnior R, et al. Physical exercise effects on the brain during COVID-19 pandemic: links between mental and cardiovascular health. Neurol Sci. 2021;42(4): 1325–1334. doi: 10.1007/s10072-021-05082-9
- Shin CH, Kim KH, Jeeva S, Kang SM. Towards Goals to Refine Prophylactic and Therapeutic Strategies Against COVID-19 Linked to Aging and Metabolic Syndrome. Cells. 2021;10(6):1412. doi: 10.3390/cells10061412
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