Neurogenesis in adult human brain. Substantiation of a therapeutic approach
Keywords:
neurogenesis in adult brain; hippocampus; neurons in human brain; targets of reparative therapy.
Abstract
Neurons of the adult brain formed in the course of neurogenesis are indispensable participants of important physiological processes. New cells play an important role in supporting cognitive functions, learning and memory. Endogenous activation of neural progenitor cells has been noted to respond to pathological changes, such as ischemia, neurodegenerative diseases, physical trauma, and mental disorders. However, despite a large number of experimental studies, understanding of the role of new cells in human brain remains a matter of great doubt. This review focuses on analyzing information about neurogenesis in the human brain, identifying steps of endogenous regulation, and outlining possible «targets» of reparative therapy.
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References
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14. Nierode G.J., Perea B.C., McFarland S.K., Pascoal J.F., Clark D.S., Schaffer D.V., Dordick J.S. High-Throughput Toxicity and Phenotypic Screening of 3D Human Neural Progenitor Cell Cultures on a Microarray Chip Platform. Stem Cell Reports. 2016; 7(5): 970-82.
15. Eriksson P.S., Perfilieva E., Bjоrk-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., Gage F.H. Neurogenesis in the human hippocampus. Nat. Med. 1998; 4(11): 1313-7.
16. Kukekov V.G., Laywell E.D., Suslov O., Davies K., Scheffler B., Thomas L.B. et al. Multipotent stem/progenitor cells with similar properties arise from two neurogenic regions of adult human brain. Exp. Neurol. 1999; 156(2): 333-44.
17. Weissleder C., Fung S.J., Wong M.W., Barry G., Double K.L., Halliday G.M. et al. Decline in Proliferation and Immature Neuron Markers in the Human Subependymal Zone during Aging: Relationship to EGF- and FGF-Related Transcripts. Front Aging Neurosci. 2016; 8; 274.
18. Alizadeh R., Hassanzadeh G., Joghataei M.T., Soleimani M., Moradi F., Mohammadpour S., et al. In vitro differentiation of neural stem cells derived from human olfactory bulb into dopaminergic-like neurons. Eur. J. Neurosci. 2016. doi:10.1111/ejn.13504.
19. Dennis C.V., Suh L.S., Rodriguez M.L., Kril J.J., Sutherland G.T. Human adult neurogenesis across the ages: An immunohistochemical study. Neuropathol. Appl. Neurobiol. 2016; 42(7): 621-38.
20. Marucci G. Commentary on Human adult neurogenesis across the ages: An immunohistochemical study. Neuropathol. Appl. Neurobiol. 2016. doi: 10.1111/nan.12377.
21. Cawsey T., Duflou J., Weickert C.S., Gorrie C.A. Nestin-Positive Ependymal Cells Are Increased in the Human Spinal Cord after Traumatic Central Nervous System Injury. J. Trauma. 2015; 32(18): 1393-402.
22. Jin K., Wang X., Xie L., Mao X.O., Zhu W., Wang Y. et al. Evidence for stroke-induced neurogenesis in the human brain. Proc. Natl. Acad. Sci. USA. 2006;103(35): 13198-202.
23. Nakayama D., Matsuyama T., Ishibashi-Ueda H., Nakagomi T., Kasahara Y., Hirose H. et al. Injury-induced neural stem/progenitor cells in post-stroke human cerebral cortex. Eur. J. Neurosci. 2010; 31(1): 90-8.
24. Minger S.L., Ekonomou A., Carta E.M., Chinoy A., Perry R.H., Ballard C.G. Endogenous neurogenesis in the human brain following cerebral infarction. Regen Med. 2007; 2(1): 69-74.
25. Jin K., Peel A.L, Mao X.O., Xie L., Cottrell B.A., Henshall D.C., Greenberg D.A. Increased hippocampal neurogenesis in Alzheimer’s disease. Proc. Natl. Acad. Sci. USA. 2004; 101(1): 343-7.
26. Mu Y., Gage F.H. Adult hippocampal neurogenesis and its role in Alzheimer’s disease. Mol. Neurodegener. 2011; 6: 85. doi: 10.1186/1750-1326-6-85.
27. Perry E.K., Johnson M., Ekonomou A., Perry R.H., Ballard C., Attems J. Neurogenic abnormalities in Alzheimer’s disease differ between stages of neurogenesis and are partly related to cholinergic pathology. Neurobiol. Dis. 2012; 47(2): 155-62.
28. Hoglinger G.U., Rizk P., Muriel M.P., Duyckaerts C., Oertel W.H., Caille I. et al. Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat. Neurosci. 2004; 7(7): 726-35.
29. Le Grand J.N., Gonzalez-Cano L., Pavlou M.A., Schwamborn J.C. Neural stem cells in Parkinson’s disease: a role for neurogenesis defects in onset and progression. Cell Mol. Life Sci. 2015; 72(4): 773-97.
30. Yang P., Arnold S.A., Habas A., Hetman M., Hagg T. Ciliary Neurotrophic Factor Mediates Dopamine D2 Receptor-Induced CNS Neurogenesis in Adult Mice. J. Neurosci. 2008; 28(9): 2231-41.
31. O’Keeffe G.C., Tyers P., Aarsland D., Dalley J.W., Barker R.A., Caldwell M.A. Dopamine-induced proliferation of adult neural precursor cells in the mammalian subventricular zone is mediated through EGF Proc. Natl. Acad. Sci. USA. 2009; 106: 8754-9.
32. Dranovsky A., Leonardo E.D. Is there a role for young hippocampal neurons in adaptation to stress? Behav. Brain. Res. 2012; 227(2): 371-5.
33. Drew L.J., Fusi S., Hen R. Adult neurogenesis in the mammalian hippocampus: why the dentate gyrus? Learn Mem. 2013; 20(12): 710-29.
34. Gusev E.I., Bogolepova A.N. The role of neuroplasticity in the development of depressive disorders. Trudnyy patsient. 2010; 10: 3-7.
35. Campbell St., Marriott M., Nahmias C.l., MacQueen G.M. Lower hippocampal volume in patients suffering from depression: a meta-analysis. Am. J. Psychiatry. 2004; 161(4): 598-607.
36. Boldrini M., Santiago A.N., Hen R., Dwork A.J., Rosoklija G.B., Tamir H. et al. Hippocampal granule neuron number and dentate gyrus volume in antidepressant-treated and untreated major depression. Neuropsychopharmacology. 2013; 38(6): 1068-77.
37. Malberg J.E., Eisch A.J., Nestler E.J., Duman R.S. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 2000; 20(24): 9104-10.
38. Brezun J.M., Daszuta A. Depletion in serotonin decreases neurogenesis in the dentate gyrus and the subventricular zone of adult rats. Neuroscience. 1999; 89(4): 999-1002.
39. Wang H.D., Dunnavant F.D., Jarman T., Deutch A.Y. Effects of antipsychotic drugs on neurogenesis in the forebrain of the adult rat. Neuropsychopharmacology. 2004; 29(7): 1230-8.
40. Perera T.D., Coplan J.D., Lisanby S.H., Lipira C.M., Arif M., Carpio C. et al. Antidepressant-Induced Neurogenesis in the Hippocampusof Adult Nonhuman Primates. J. Neurosci. 2007; 27(18): 4894-901.
41. Boldrini M., Underwood M.D., Hen R., Rosoklija G.B., Dwork A.J., John Mann J., Arango V. Antidepressants increase neural progenitor cells in the human hippocampus. Neuropsychopharmacology. 2009; 34(11): 2376-89.
42. David D.J., Samuels B.A., Rainer Q., Wang J.W., Marsteller D., Mendez I. et al. Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron. 2009; 62(4): 479-93.
43. Santarelli L., Saxe M., Gross C., Surget A., Battaglia F., Dulawa S., et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science. 2003; 301(5634): 805-9.
44. Lucassen P.J., Stumpel M.W., Wang Q., Aronica E. Decreased numbers of progenitor cells but no response to antidepressant drugs in the hippocampus of elderly depressed patients. Neuropharmacology. 2010; 58(6): 940-9.
45. Perera T.D., Park S., Nemirovskaya Y. Cognitive role of neurogenesis in depression and antidepressant treatment. Neuroscientis. 2010; 14(4): 326-38.
46. Avram S., Borcan F., Borcan L.C., Milac A.L., Mihailescu D. QSAR Approaches Applied to Antidepressants Induced Neurogenesis — in vivo and in silico Applications. Mini Rev. Med. Chem. 2015; 16(3): 230-40.
47. Tang S.W., Helmeste D., Leonard B. Is neurogenesis relevant in depression and in the mechanism of antidepressant drug action? A critical review. World J. Biol. Psychiatry. 2012; 13(6): 402-12.
48. Wang H., Zhang Y., Qiao M. Mechanisms of extracellular signal-regulated kinase/ cAMP response element-binding protein/ brain-derived neurotrophic factor signal transduction pathway in depressive disorder. Neural Regen. Res. 2013; 8(9): 843-52.
49. Musazzi L., Cattaneo A., Tardito D., Barbon A., Gennarelli M., Barlati S. et al. Early raise of BDNF in hippocampus suggests induction of posttranscriptional mechanisms by antidepressants. BMC Neurosci. 2009; 10: 48. doi: 10.1186/1471-2202-10-48.
50. Gomazkov O.A. Signaling Molecules and Disturbances of Cognitive Functions in Brain Diseases. Neyrokhimiya. 2015; 9(3):169-80. (in Russian)
51. Eisch A.J., Cameron H.A., Encinas J.M., Meltzer L.A., Ming G.L., Overstreet-Wadiche L.S. Adult neurogenesis, mental health, and mental illness: hope or hype? J. Neurosci. 2008; 28(46): 11785-91.
52. Cattaneo E., Bonfanti L. Therapeutic potential of neural stem cells: greater in people’s perception than in their brains? Front Neurosci., 2014; 8: 79. doi: 10.3389/fnins.2014.00079.
53. Ihunwo A.O., Tembo L.H., Dzamalala C. The dynamics of adult neurogenesis in human hippocampus. Neural Regen. Res. 2016; 11(12): 1869-1883. doi: 10.4103/1673-5374.195278.
54. Gomazkov O.A. Correction of Neurogenesis in the Adult Brain: Selection of Therapeutic Targets. Neyrokhimiya. 2017; 11(1):1-9. (in Russian)
55. Rhim J.H., Luo X., Xu X., Gao D., Zhou T., Li F. et al. A High-content screen identifies compounds promoting the neuronal differentiation and the midbrain dopamine neuron specification of human neural progenitor cells. Sci. Rep. 2015; 5: 16237. doi: 10.1038/srep16237.
56. Zhuang P., Zhang Y., Cui G., Bian Y., Zhang M., Zhang J., Liu Yet al. Direct stimulation of adult neural stem -progenitor cells in vitro and neurogenesis in vivo by salvianolic acid. PLoS One. 2012; 7(4):e35636. doi: 10.1371/journal.pone.0035636.
57. Kong S.Y., Park M.H., Lee M., Kim J.O., Lee H.R., Han B.W. et al. Kuwanon V inhibits proliferation, promotes cell survival and increases neurogenesis of neural stem cells. PLoS One. 2015; 10(2):e0118188. doi: 10.1371/journal.pone.0118188.
58. Liu A., Jain N., Vyas A., Lim L.M. Ventromedial prefrontal cortex stimulation enhances memory and hippocampal neurogenesis in the middle-aged rats. ELife. 2015; 4:e04803. doi: 10.7554/eLife.04803.
59. Paltsyn А.А., Komissarova S.V. Age changes in the brain. Patologicheskaya Fiziologiya I eksperimentalnaya Terapiya. 2015; 59(4):108-16. (in Russian)
2. Colucci-D’Amato L., Bonavita V., di Porzio U. The end of the central dogma of neurobiology: stem cells and neurogenesis in adult CNS. Neurol. Sci. 2006; 27(4): 266-70.
3. Gomazkov O.A. Why Does the Brain Needs New Nerve Cells? [Zashem vzroslomu mozgu novye nervnye kletki?] Moscow; IKAR, 2016. (in Russian)
4. Yamaguchi M., Mori K. Critical periods in adult neurogenesis and possible clinical utilization of new neurons. Front Neurosci. 2014; 8(2): 177-83.
5. Yarygin K.N. Yarygin V.N. Neurogenesis in the central nervous system and prospects of regenerative neurology. Zhurnal Neyropatol. Psikhiatr. im. S.S. Korsakova. 2012; 112(1): 4-13. (in Russian)
6. Gomazkov O.A. Transformation of neural stem cells and reparative processes in the brain. Zhurnal Neyropathol. Psikhiatr. im. S.S. Korsakova. 2014; 114(8): 4-12. (in Russian)
7. Enikolopov G., Guillermier C., Wang M., Trakimas L., Steinhauser M., Lechene C. Brain stem cell division and maintenance studied using multi-isotope imaging mass spectrometry (MIMS). Surf. Interface Anal. 2014; 46 (Suppl 1):140-3.
8. Sierra A., Encinas J.M., Maletic-Savatic M. Adult human neurogenesis: from microscopy to magnetic resonance imaging. Front Neurosci. 2011. doi: 10.3389/fnins.2011.00047.
9. Rueger M.A., Schroeter M. In vivo imaging of endogenous neural stem cells in the adult brain. World J. Stem Cells. 2015; 7(1): 75-83.
10. Zhong X.M., Zhang F, Yang M., Wen X.H., Zhang X., Duan X.H., Shen J. In Vivo Targeted Magnetic Resonance Imaging of Endogenous Neural Stem Cells in the Adult Rodent Brain. Biomed. Res. Int. 2015. doi: 10.1155/2015/131054.
11. Zhang F., Duan X., Lu L., Zhang X., Zhong X., Mao J., Chen M., Shen J. In Vivo Targeted MR Imaging of Endogenous Neural Stem Cells in Ischemic Stroke. Molecules. 2016. doi: 10.3390/molecules21091143.
12. Lee M.Y., Kumar R. A., Sukumaran S.M., Hogg M.G., Clark D.S., Dordick J.S. Three-dimensional cellular microarray for high-throughput toxicology assays. Proc. Natl. Acad. Sci. USA. 2008; 105(1): 59-63.
13. Meli L., Barbosa H.S.C., Hickey A.M., Gasimli L., Nierode G., Diogo M.M., et al. Stem Cell Research. 2014; 13(1): 36-47.
14. Nierode G.J., Perea B.C., McFarland S.K., Pascoal J.F., Clark D.S., Schaffer D.V., Dordick J.S. High-Throughput Toxicity and Phenotypic Screening of 3D Human Neural Progenitor Cell Cultures on a Microarray Chip Platform. Stem Cell Reports. 2016; 7(5): 970-82.
15. Eriksson P.S., Perfilieva E., Bjоrk-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., Gage F.H. Neurogenesis in the human hippocampus. Nat. Med. 1998; 4(11): 1313-7.
16. Kukekov V.G., Laywell E.D., Suslov O., Davies K., Scheffler B., Thomas L.B. et al. Multipotent stem/progenitor cells with similar properties arise from two neurogenic regions of adult human brain. Exp. Neurol. 1999; 156(2): 333-44.
17. Weissleder C., Fung S.J., Wong M.W., Barry G., Double K.L., Halliday G.M. et al. Decline in Proliferation and Immature Neuron Markers in the Human Subependymal Zone during Aging: Relationship to EGF- and FGF-Related Transcripts. Front Aging Neurosci. 2016; 8; 274.
18. Alizadeh R., Hassanzadeh G., Joghataei M.T., Soleimani M., Moradi F., Mohammadpour S., et al. In vitro differentiation of neural stem cells derived from human olfactory bulb into dopaminergic-like neurons. Eur. J. Neurosci. 2016. doi:10.1111/ejn.13504.
19. Dennis C.V., Suh L.S., Rodriguez M.L., Kril J.J., Sutherland G.T. Human adult neurogenesis across the ages: An immunohistochemical study. Neuropathol. Appl. Neurobiol. 2016; 42(7): 621-38.
20. Marucci G. Commentary on Human adult neurogenesis across the ages: An immunohistochemical study. Neuropathol. Appl. Neurobiol. 2016. doi: 10.1111/nan.12377.
21. Cawsey T., Duflou J., Weickert C.S., Gorrie C.A. Nestin-Positive Ependymal Cells Are Increased in the Human Spinal Cord after Traumatic Central Nervous System Injury. J. Trauma. 2015; 32(18): 1393-402.
22. Jin K., Wang X., Xie L., Mao X.O., Zhu W., Wang Y. et al. Evidence for stroke-induced neurogenesis in the human brain. Proc. Natl. Acad. Sci. USA. 2006;103(35): 13198-202.
23. Nakayama D., Matsuyama T., Ishibashi-Ueda H., Nakagomi T., Kasahara Y., Hirose H. et al. Injury-induced neural stem/progenitor cells in post-stroke human cerebral cortex. Eur. J. Neurosci. 2010; 31(1): 90-8.
24. Minger S.L., Ekonomou A., Carta E.M., Chinoy A., Perry R.H., Ballard C.G. Endogenous neurogenesis in the human brain following cerebral infarction. Regen Med. 2007; 2(1): 69-74.
25. Jin K., Peel A.L, Mao X.O., Xie L., Cottrell B.A., Henshall D.C., Greenberg D.A. Increased hippocampal neurogenesis in Alzheimer’s disease. Proc. Natl. Acad. Sci. USA. 2004; 101(1): 343-7.
26. Mu Y., Gage F.H. Adult hippocampal neurogenesis and its role in Alzheimer’s disease. Mol. Neurodegener. 2011; 6: 85. doi: 10.1186/1750-1326-6-85.
27. Perry E.K., Johnson M., Ekonomou A., Perry R.H., Ballard C., Attems J. Neurogenic abnormalities in Alzheimer’s disease differ between stages of neurogenesis and are partly related to cholinergic pathology. Neurobiol. Dis. 2012; 47(2): 155-62.
28. Hoglinger G.U., Rizk P., Muriel M.P., Duyckaerts C., Oertel W.H., Caille I. et al. Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat. Neurosci. 2004; 7(7): 726-35.
29. Le Grand J.N., Gonzalez-Cano L., Pavlou M.A., Schwamborn J.C. Neural stem cells in Parkinson’s disease: a role for neurogenesis defects in onset and progression. Cell Mol. Life Sci. 2015; 72(4): 773-97.
30. Yang P., Arnold S.A., Habas A., Hetman M., Hagg T. Ciliary Neurotrophic Factor Mediates Dopamine D2 Receptor-Induced CNS Neurogenesis in Adult Mice. J. Neurosci. 2008; 28(9): 2231-41.
31. O’Keeffe G.C., Tyers P., Aarsland D., Dalley J.W., Barker R.A., Caldwell M.A. Dopamine-induced proliferation of adult neural precursor cells in the mammalian subventricular zone is mediated through EGF Proc. Natl. Acad. Sci. USA. 2009; 106: 8754-9.
32. Dranovsky A., Leonardo E.D. Is there a role for young hippocampal neurons in adaptation to stress? Behav. Brain. Res. 2012; 227(2): 371-5.
33. Drew L.J., Fusi S., Hen R. Adult neurogenesis in the mammalian hippocampus: why the dentate gyrus? Learn Mem. 2013; 20(12): 710-29.
34. Gusev E.I., Bogolepova A.N. The role of neuroplasticity in the development of depressive disorders. Trudnyy patsient. 2010; 10: 3-7.
35. Campbell St., Marriott M., Nahmias C.l., MacQueen G.M. Lower hippocampal volume in patients suffering from depression: a meta-analysis. Am. J. Psychiatry. 2004; 161(4): 598-607.
36. Boldrini M., Santiago A.N., Hen R., Dwork A.J., Rosoklija G.B., Tamir H. et al. Hippocampal granule neuron number and dentate gyrus volume in antidepressant-treated and untreated major depression. Neuropsychopharmacology. 2013; 38(6): 1068-77.
37. Malberg J.E., Eisch A.J., Nestler E.J., Duman R.S. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 2000; 20(24): 9104-10.
38. Brezun J.M., Daszuta A. Depletion in serotonin decreases neurogenesis in the dentate gyrus and the subventricular zone of adult rats. Neuroscience. 1999; 89(4): 999-1002.
39. Wang H.D., Dunnavant F.D., Jarman T., Deutch A.Y. Effects of antipsychotic drugs on neurogenesis in the forebrain of the adult rat. Neuropsychopharmacology. 2004; 29(7): 1230-8.
40. Perera T.D., Coplan J.D., Lisanby S.H., Lipira C.M., Arif M., Carpio C. et al. Antidepressant-Induced Neurogenesis in the Hippocampusof Adult Nonhuman Primates. J. Neurosci. 2007; 27(18): 4894-901.
41. Boldrini M., Underwood M.D., Hen R., Rosoklija G.B., Dwork A.J., John Mann J., Arango V. Antidepressants increase neural progenitor cells in the human hippocampus. Neuropsychopharmacology. 2009; 34(11): 2376-89.
42. David D.J., Samuels B.A., Rainer Q., Wang J.W., Marsteller D., Mendez I. et al. Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron. 2009; 62(4): 479-93.
43. Santarelli L., Saxe M., Gross C., Surget A., Battaglia F., Dulawa S., et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science. 2003; 301(5634): 805-9.
44. Lucassen P.J., Stumpel M.W., Wang Q., Aronica E. Decreased numbers of progenitor cells but no response to antidepressant drugs in the hippocampus of elderly depressed patients. Neuropharmacology. 2010; 58(6): 940-9.
45. Perera T.D., Park S., Nemirovskaya Y. Cognitive role of neurogenesis in depression and antidepressant treatment. Neuroscientis. 2010; 14(4): 326-38.
46. Avram S., Borcan F., Borcan L.C., Milac A.L., Mihailescu D. QSAR Approaches Applied to Antidepressants Induced Neurogenesis — in vivo and in silico Applications. Mini Rev. Med. Chem. 2015; 16(3): 230-40.
47. Tang S.W., Helmeste D., Leonard B. Is neurogenesis relevant in depression and in the mechanism of antidepressant drug action? A critical review. World J. Biol. Psychiatry. 2012; 13(6): 402-12.
48. Wang H., Zhang Y., Qiao M. Mechanisms of extracellular signal-regulated kinase/ cAMP response element-binding protein/ brain-derived neurotrophic factor signal transduction pathway in depressive disorder. Neural Regen. Res. 2013; 8(9): 843-52.
49. Musazzi L., Cattaneo A., Tardito D., Barbon A., Gennarelli M., Barlati S. et al. Early raise of BDNF in hippocampus suggests induction of posttranscriptional mechanisms by antidepressants. BMC Neurosci. 2009; 10: 48. doi: 10.1186/1471-2202-10-48.
50. Gomazkov O.A. Signaling Molecules and Disturbances of Cognitive Functions in Brain Diseases. Neyrokhimiya. 2015; 9(3):169-80. (in Russian)
51. Eisch A.J., Cameron H.A., Encinas J.M., Meltzer L.A., Ming G.L., Overstreet-Wadiche L.S. Adult neurogenesis, mental health, and mental illness: hope or hype? J. Neurosci. 2008; 28(46): 11785-91.
52. Cattaneo E., Bonfanti L. Therapeutic potential of neural stem cells: greater in people’s perception than in their brains? Front Neurosci., 2014; 8: 79. doi: 10.3389/fnins.2014.00079.
53. Ihunwo A.O., Tembo L.H., Dzamalala C. The dynamics of adult neurogenesis in human hippocampus. Neural Regen. Res. 2016; 11(12): 1869-1883. doi: 10.4103/1673-5374.195278.
54. Gomazkov O.A. Correction of Neurogenesis in the Adult Brain: Selection of Therapeutic Targets. Neyrokhimiya. 2017; 11(1):1-9. (in Russian)
55. Rhim J.H., Luo X., Xu X., Gao D., Zhou T., Li F. et al. A High-content screen identifies compounds promoting the neuronal differentiation and the midbrain dopamine neuron specification of human neural progenitor cells. Sci. Rep. 2015; 5: 16237. doi: 10.1038/srep16237.
56. Zhuang P., Zhang Y., Cui G., Bian Y., Zhang M., Zhang J., Liu Yet al. Direct stimulation of adult neural stem -progenitor cells in vitro and neurogenesis in vivo by salvianolic acid. PLoS One. 2012; 7(4):e35636. doi: 10.1371/journal.pone.0035636.
57. Kong S.Y., Park M.H., Lee M., Kim J.O., Lee H.R., Han B.W. et al. Kuwanon V inhibits proliferation, promotes cell survival and increases neurogenesis of neural stem cells. PLoS One. 2015; 10(2):e0118188. doi: 10.1371/journal.pone.0118188.
58. Liu A., Jain N., Vyas A., Lim L.M. Ventromedial prefrontal cortex stimulation enhances memory and hippocampal neurogenesis in the middle-aged rats. ELife. 2015; 4:e04803. doi: 10.7554/eLife.04803.
59. Paltsyn А.А., Komissarova S.V. Age changes in the brain. Patologicheskaya Fiziologiya I eksperimentalnaya Terapiya. 2015; 59(4):108-16. (in Russian)
Published
2017-12-18
How to Cite
Gomazkov O. A. Neurogenesis in adult human brain. Substantiation of a therapeutic approach // Patologicheskaya Fiziologiya i Eksperimental’naya Terapiya (Pathological physiology and experimental therapy). 2017. VOL. 61. № 4. PP. 126–135.
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Reviews
