Regulation of neurogenesis: factors affecting of new neurons formation in adult mammals brain
Michalina Respondek 1 , Ewa Buszman 1Abstract
Neurogenesis is a complex and multi-step process of generating completely functional neurons. This process in adult brain is based on pluripotentional neuronal stem cells (NSC), which are able to proliferation and differentiation into mature neurons or glial cells. NSC are located in subgranular zone inside hippocampus and in subventricular zone. The new neurons formation depends on many endo- and exogenous factors which modulate each step of neurogenesis. This article describes the most important regulators of adult neurogenesis, mainly: neurotrophins, growth factors, hormones, neurotransmitters and microenvironment of NSC. Some drugs, especially antipsychotics, antidepressants and normothymics may affect the neurogenic properties of adult brain. Moreover pathological processes such as neuroinflammation, stroke or epilepsy are able to induce proliferation of NSC. The proneurogenic effects of psychotropic drugs and pathological processes are associated with their ability to increase some hormones and neurotrophins level, as well as with rising the expression of antiapoptotic Bcl-2 protein and metalloproteinase MMP-2. Additionaly, some drugs, for example haloperidol, are able to block prolactin and dopaminergic neuroblasts receptors. Down-regulation of adult neurogenesis is associated with alcohol abuse and high stress level. Negative effect of many drugs, such as cytostatics, COX-2 inhibitors and opioides was also observed. The proneurogenic effect of described factors suggest their broad therapeutic potential and gives a new perspective on an effective and modern treatment of many neuropsychiatric disorders. This effect can also help to clarify the pathogenesis of disorders associated with proliferation and degeneration of adult brain cells.
References
- 1. Abrous D.N., Koehl M., Le Moal M.: Adult neurogenesis: from precursorsto network and physiology. Physiol. Rev., 2005; 85: 523-569
Google Scholar - 2. Altman J., Das G.D.: Post-natal origin of microneurones in the ratbrain. Nature, 1965; 207: 953-956
Google Scholar - 3. Alvarez-Buylla A., Garcia-Verdugo J.M.: Neurogenesis in adultsubventricular zone. J. Neurosci., 2002; 22: 629-634
Google Scholar - 4. Balu D.T., Lucki I.: Adult hippocampal neurogenesis: regulation,functional implications, and contribution to disease pathology. Neurosci.Biobehav. Rev., 2009: 33: 232-252
Google Scholar - 5. Banasr M., Hery M., Printemps R., Daszuta A.: Serotonin-inducedincreases in adult cell proliferation and neurogenesis are mediatedthrough different and common 5-HT receptor subtypes in the dentategyrus and the subventricular zone. Neuropsychopharmacology,2004; 29: 450-460
Google Scholar - 6. Bauer S., Patterson P.H.: Leukemia inhibitory factor promotesneural stem cell self–renewal in the adult brain. J. Neurosci., 2006;26: 12089-12099
Google Scholar - 7. Belvindrah R., Hankel S., Walker J., Patton B.L., Müller U.: β1integrins control the formation of cell chains in the adult rostralmigratory stream. J. Neurosci., 2007; 27: 2704-2717
Google Scholar - 8. Bennett L., Yang M., Enikolopov G., Iacovitti L.: Circumventricularorgans: a novel site of neural stem cells in the adult brain. Mol. Cell.Neurosci., 2009; 41: 337-347
Google Scholar - 9. Berg D.A., Belnoue L., Song H., Simon A.: Neurotransmitter–mediatedcontrol of neurogenesis in the adult vertebrate brain. Development,2013; 140: 2548-2561
Google Scholar - 10. Bruno P., Carreira, A.I., Santos, Caetana M., Araújo C., AraújoI.M.: Neural stem cells – new perspectives. W: Bonfanti L. (red.),Neural Stem Cells – New Perspectives, Wyd. INTECH, 2013: 163-180
Google Scholar - 11. Cajal S.R.: Degeneration and regeneration of the nervous system.Haffner Publishing Co. New York, New York, USA, 1928: 750
Google Scholar - 12. Cameron H.A., Hazel T.G., McKay R.D.: Regulation of neurogenesisby growth factors and neurotransmitters. J. Neurobiol., 1998;36: 287-306
Google Scholar - 13. Chen J., Cai F., Cao J., Zhang X., Li S.: Long-term antiepilepticdrug administration during early life inhibits hippocampal neurogenesisin the developing brain. J. Neurosci. Res., 2009; 87: 2898-2907
Google Scholar - 14. Cohen P., Ocrant I., Fielder P.J., Neely E.K., Gargosky S.E., DealC.I., Ceda G.P., Youngman O., Pham H., Lamson G., Giudice L.C., RosenfeldR.G.: Insulin-like growth factors (IGFs): implications for aging.Psychoneuroendocrinology, 1992; 17: 335-342
Google Scholar - 15. Crews F.T., Nixon K.: Alcohol, neural stem cells, and adult neurogenesis.Alcohol Res. Health, 2003; 27: 197-204
Google Scholar - 16. Darsalia V., Heldmann U., Lindvall O., Kokaia Z.: Stroke-inducedneurogenesis in aged brain. Stroke, 2005; 36: 1790-1795
Google Scholar - 17. Dawirs R.R., Hildebrandt K., Teuchert-Noodt G.: Adult treatmentwith haloperidol increases dentate granule cell proliferation in thegerbil hippocampus. J. Neural Transm., 1998; 105: 317-327
Google Scholar - 18. Doetsch F., Caillé I., Lim D.A., García-Verdugo J.M., Alvarez-BuyllaA.: Subventricular zone astrocytes are neural stem cells in the adultmammalian brain. Cell, 1999; 97: 703-716
Google Scholar - 19. Doetsch F., Garcia-Verdugo J.M., Alvarez-Buylla A.: Cellular compositionand three-dimensional organization of the subventriculargerminal zone in the adult mammalian brain. J. Neurosci., 1997:17: 5046-5061
Google Scholar - 20. Duan X., Kang E., Liu C.Y., Ming G.L., Song H.: Development ofneural stem cell in the adult brain. Curr. Opin. Neurobiol., 2008;18: 108-115
Google Scholar - 21. Duman R.S., Malberg J., Nakagawa S.: Regulation of adult neurogenesisby psychotropic drugs and stress. J. Pharmacol. Exp. Ther.,2001; 299: 401-407
Google Scholar - 22. Duman R.S., Nakagawa S., Malberg J.: Regulation of adult neurogenesisby antidepressant treatment. Neuropsychopharmacology,2001; 25: 836-844
Google Scholar - 23. Eisch A.J., Barrot M., Schad C.A., Self D.W., Nestler E.J.: Opiatesinhibit neurogenesis in the adult rat hippocampus. Proc. Natl. Acad.Sci. USA, 2000; 97: 7579-7584
Google Scholar - 24. Eriksson P.S., Perfilieva E., Björk-Eriksson T., Alborn A.M., NordborgC., Peterson D.A., Gage F.H.: Neurogenesis in the adult humanhippocampus. Nat. Med., 1998; 4: 1313-1317
Google Scholar - 25. Fiorentini A., Rosi M.C., Grossi C., Luccarini I., Casamenti F.:Lithium improves hippocampal neurogenesis, neuropathology andcognitive functions in APP mutant mice. PLoS One, 2010; 5: e14382
Google Scholar - 26. Fuster-Matanzo A., Llorens-Martín M., Hernández F., Avila J.:Role of neuroinflammation in adult neurogenesis and Alzheimerdisease: therapeutic approaches. Mediators Inflamm., 2013; 2013:260925
Google Scholar - 27. Galea L.A., Spritzer M.D., Barker J.M., Pawluski J.L.: Gonadalhormone modulation of hippocampal neurogenesis in the adult.Hippocampus, 2006; 16: 225-232
Google Scholar - 28. Garcion E., Halilagic A., Faissner A., ffrench-Constant C.: Generationof an environmental niche for neural stem cell development bythe extracellular matrix molecule tenascin C. Development, 2004;131: 3423-3432
Google Scholar - 29. Gascon E., Vutskits L., Kiss J.Z.: The role of PSA-NCAM in adultneurogenesis. Adv. Exp. Med. Biol., 2010; 663: 127-136
Google Scholar - 30. Goncalves M.B., Williams E.J., Yip P., Yáñez-Muñoz R.J., WilliamsG., Doherty P.: The COX-2 inhibitors, meloxicam and nimesulide,suppress neurogenesis in the adult mouse brain. Br. J. Pharmacol.,2010; 159: 1118-1125
Google Scholar - 31. Gould E.: How widespread is adult neurogenesis in mammals?Nat. Rev. Neurosci., 2007; 8: 481-488
Google Scholar - 32. Gould E., Gross C.G.: Neurogenesis in adult mammals: someprogress and problems. J. Neurosci., 2002; 22: 619-623
Google Scholar - 33. Gójska A., Nyka W.M.: Komórki macierzyste w udarze mózgu.Choroby Serca Naczyń, 2010; 7: 23-31
Google Scholar - 34. Halim N.D., Weickert C.S., McClintock B.W., Weinberger D.R.,Lipska B.K.: Effects of chronic haloperidol and clozapine treatmenton neurogenesis in the adult rat hippocampus. Neuropsychopharmacology,2004; 29: 1063-1069
Google Scholar - 35. Hunsberger J., Austin D.R., Henter I.D., Chen G.: The neurotrophicand neuroprotective effects of psychotropic agents. Dialogues Clin.Neurosci., 2009; 11: 333-348
Google Scholar - 36. Jacobs B., Tanapat P., Reeves A., Gould E.: Serotonin stimulatesthe production of new hippocampal granule neurons via the 5HT1Areceptor in the adult rat. Soc. Neurosci. Abstr., 1998; 23: 1992
Google Scholar - 37. Jin K., Zhu Y., Sun Y., Mao X.O., Xie L., Greenberg D.A.: Vascularendothelial growth factor (VEGF) stimulates neurogenesis in vitroand in vivo. Proc. Natl. Acad. Sci. USA, 2002; 99: 11946-11950
Google Scholar - 38. Kaplan M.S., Hinds J.W.: Neurogenesis in the adult rat: electronmicroscopic analysis of light radioautographs. Science, 1977; 197:1092-1094
Google Scholar - 39. Keilhoff G., Grecksch G., Bernstein H.G., Roskoden T., BeckerA.: Risperidone and haloperidol promote survival of stem cells inthe rat hippocampus. Eur. Arch. Psychiatry Clin. Neurosci., 2010;260: 151-162
Google Scholar - 40. Kim H.M., Qu T., Kriho V., Lacor P., Smalheiser N., Pappas G.D.,Guidotti A., Costa E., Sugaya K.: Reelin function in neural stem cellbiology. Proc. Natl. Acad. Sci. USA, 2002; 99: 4020-4025
Google Scholar - 41. Kippin T.E., Kapur S., van der Kooy D.: Dopamine specificallyinhibits forebrain neural stem cell proliferation, suggesting a noveleffect of antipsychotic drugs. J. Neurosci., 2005; 25: 5815-5823
Google Scholar - 42. Kornack D.R., Rakic P.: The generation, migration, and differentiationof olfactory neurons in the adult primate brain. Proc. Natl.Acad. Sci. USA, 2001; 98: 4752-4757
Google Scholar - 43. Kuhn H.G., Winkler J., Kempermann G., Thal L.J., Gage F.H.: Epidermalgrowth factor and fibroblast growth factor-2 have differenteffects on neural progenitors in the adult rat brain. J. Neurosci.,1997; 17: 5820-5829
Google Scholar - 44. Lennington J.B., Yang Z., Conover J.C.: Neural stem cells and theregulation of adult neurogenesis. Reprod. Biol. Endocrinol., 2003; 1: 99
Google Scholar - 45. Lichtenwalner R.J., Parent J.M.: Adult neurogenesis and the ischemicforebrain. J. Cereb. Blood Flow Metab., 2006; 26: 1-20
Google Scholar - 46. Liu J., Solway K., Messing R.O., Sharp F.R.: Increased neurogenesisin the dentate gyrus after transient global ischemia in gerbils.J. Neurosci., 1998; 18: 7768-7778
Google Scholar - 47. Lucassen P.J., Meerlo P., Naylor A.S., van Dam A.M., Dayer A.G.,Fuchs E., Oomen C.A., Czéh B.: Regulation of adult neurogenesis bystress, sleep disruption, exercise and inflammation: Implicationsfor depression and antidepressant action. Eur. Neuropsychopharmacol.,2010; 20: 1-17
Google Scholar - 48. Malberg J.E., Eisch A.J., Nestler E.J., Duman R.S.: Chronic antidepressanttreatment increases neurogenesis in adult rat hippocampus.J. Neurosci., 2000; 20: 9104-9110
Google Scholar - 49. Manji H.K., Chen G.: PKC, MAP kinases and the bcl-2 family ofproteins as long-term targets for mood stabilizers. Mol. Psychiatry,2002; 7 (Suppl. 1): S46-S56
Google Scholar - 50. Mercier F., Hatton G.I.: Connexin 26 and basic fibroblast growthfactor are expressed primarily in the subpial and subependymallayers in adult brain parenchyma: roles in stem cell proliferationand morphological plasticity? J. Comp. Neurol., 2001: 431: 88-104
Google Scholar - 51. Ming G.L., Song H.: Adult neurogenesis in the mammalian brain:significant answers and significant questions. Neuron, 2011; 70:687-702
Google Scholar - 52. Mirzadech Z., Merkle T.F., Soriano-Navarro M., Garcia-VerdugoJ.M., Alvarez-Buylla A.: Neural stem cells confer unique pinwheelarchitecture to the ventricular surface in neurogenic regions of theadult brain. Cell Stem Cell, 2008; 3: 265-278
Google Scholar - 53. Mobley A.K., Tchaicha J.H., Shin J., Hossain M.G., McCarty J.H.:β8 integrin regulates neurogenesis and neurovascular homeostasisin the adult brain. J. Cell Sci., 2009; 122: 1842-1851
Google Scholar - 54. Nixon K., Crews F.T.: Binge ethanol exposure decreases neurogenesisin adult rat hippocampus. J. Neurochem., 2002; 83: 1087-1093
Google Scholar - 55. Okano H., Sakaguchi M., Ohki K., Suzuki N., Sawamoto K.: Regenerationof the central nervous system using endogenous repairmechanisms. J. Neurochem., 2007; 102: 1459-1465
Google Scholar - 56. Okano H., Sawamoto K.: Neural stem cells: involvement in adultneurogenesis and CNS repair. Philos.Trans. R. Soc. Lond. B Biol. Sci.,2008; 363: 2111-2122
Google Scholar - 57. Parent J.M., Jessberger S., Gage F.H., Gong C.: Is neurogenesis reparativeafter status epilepticus? Epilepsia, 2007; 48 (Suppl. 8): 69-71
Google Scholar - 58. Rice C.M., Halfpenny C.A., Scolding N.J.: Stem cells for the treatmentof neurological disease. Transfus. Med., 2003; 13: 351-361
Google Scholar - 59. Riquelme P.A., Drapeau E., Doetsch F.: Brain micro-ecologies:neural stem cell niches in the adult mammalian brain. Philos. Trans.R. Soc. Lond. B Biol. Sci., 2008; 363: 123-137
Google Scholar - 60. Schlett K.: Glutamate as a modulator of embryonic and adultneurogenesis. Curr. Top. Med. Chem., 2006; 6: 949-960
Google Scholar - 61. Schoenfeld T.J., Gould E.: Stress, stress hormones, and adultneurogenesis. Exp. Neurol., 2012; 233: 12-21
Google Scholar - 62. Seigers R., Schagen S.B., Beerling W., Boogerd W., van TellingenO., van Dam F.S., Koolhaas J.M., Buwalda B.: Long-lasting suppressionof hippocampal cell proliferation and impaired cognitiveperformance by methotrexate in the rat. Behav. Brain Res., 2008;186: 168-175
Google Scholar - 63. Seri B., García-Verdugo J.M., McEwen B.S., Alvarez-Buylla A.:Astrocytes give rise to new neurons in the adult mammalian hippocampus.J. Neurosci., 2001; 21: 7153-7160
Google Scholar - 64. Shingo T., Gregg C., Enwere E., Fujikawa H., Hassam R., Geary C.,Cross J.C., Weiss S.: Pregnancy-stimulated neurogenesis in the adultfemale forebrain mediated by prolactin. Science, 2003; 299: 117-120
Google Scholar - 65. Torner L., Karg S., Blume A., Kandasamy M., Kuhn H.G., WinklerJ., Aigner L., Neumann I.D.: Prolactin prevents chronic stress-induceddecrease of adult hippocampal neurogenesis and promotes neuronalfate. J. Neurosci., 2009; 29: 1826-1833
Google Scholar - 66. Tozuka Y., Fukuda S., Namba T., Seki T., Hisatsune T.: GABAergicexcitation promotes neuronal differentiation in adult hippocampalprogenitor cells. Neuron, 2005; 47: 803-815
Google Scholar - 67. Turlejski K., Djavadian R.: Life-long stability of neurons: a centuryof research on neurogenesis, neuronal death and neuron quantificationin adult CNS. Prog. Brain Res., 2002; 136: 39-65
Google Scholar - 68. Uchida N., Kiuchi Y., Miyamoto K., Uchida J., Tobe T., TomitaM., Shioda S., Nakai Y., Koide R., Oguchi K.: Glutamate-stimulatedproliferation of rat retinal pigment epithelial cells. Eur. J. Pharmacol.,1998; 343: 265-273
Google Scholar - 69. Valenzuela M., Sidhu K., Dean S., Sachdev P.: Neural stem celltherapy for neuropsychiatric disorders. Acta Neuropsychiatr., 2007;19: 11-26
Google Scholar - 70. Veena J., Rao B.S., Srikumar B.N.: Regulation of adult neurogenesisin the hippocampus by stress, acetylcholine and dopamine. J.Nat. Sci. Biol. Med., 2011; 2: 26-37
Google Scholar - 71. Vicini S.: The role of GABA and glutamate on adult neurogenesis.J. Physiol., 2008; 586: 3737-3738
Google Scholar - 72. Wada A.: Lithium and neuropsychiatric therapeutics: neuroplasticityvia glycogen synthase kinase-3β, β-catenin, and neurotrophincascades. J. Pharmacol. Sci., 2009; 110: 14-28
Google Scholar - 73. Wakade C.G., Mahadik S.P., Waller J.L., Chiu F.C.: Atypical neurolepticsstimulate neurogenesis in adult rat brain. J. Neurosci. Res.,2002; 69: 72-79
Google Scholar - 74. Wang H.D., Dunnavant F.D., Jarman T., Deutch A.Y.: Effects ofantipsychotic drugs on neurogenesis in the forebrain of the adultrat. Neuropsychopharmacology, 2004; 29: 1230-1238
Google Scholar - 75. Wang T.W., Zhang H., Gyetko M.R., Parent J.M.: Hepatocytegrowth factor acts as a mitogen and chemoattractant for postnatalsubventricular zone-olfactory bulb neurogenesis. Mol. Cell. Neurosci.,2011; 48: 38-50
Google Scholar - 76. Xu J.C., Xiao M.F., Jakovcevski I., Sivukhina E., Hargus G., Cui Y.F.,Irintchev A., Schachner M., Bernreuther C.: The extracellular matrixglycoprotein tenascin-R regulates neurogenesis during developmentand in the adult dentate gyrus of mice. J. Cell Sci., 2014; 127: 641-652
Google Scholar - 77. Yang M., Kim J.S., Song M.S., Kim S.H., Kang S.S., Bae C.S., KimJ.C., Wang H., Shin T., Moon C.: Cyclophosphamide impairs hippocampus-dependentlearning and memory in adult mice: Possible involvementof hippocampal neurogenesis in chemotherapy-inducedmemory deficits. Neurobiol. Learn. Mem., 2010; 93: 487-494
Google Scholar - 78. Zafra F., Castrén E., Thoenen H., Lindholm D.: Interplay betweenglutamate and g-aminobutyric acid transmitter systems in the physiologicalregulation of brain-derived neurotrophic factor and nervegrowth factor synthesis in hippocampal neurons. Proc. Natl. Acad.Sci. USA, 1991; 88: 10037-10041
Google Scholar - 79. Zhao C., Deng W., Gage F.H.: Mechanisms and functional implicationsof adult neurogenesis. Cell, 2008; 132: 645-660
Google Scholar