Regenerative potential of the brain: composition and forming of regulatory microenvironment in neurogenic niches

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Abstract

An important mechanism of neuronal plasticity is neurogenesis, which occurs during the embryonic period, forming the brain and its structure, and in the postnatal period, providing repair processes and participating in the mechanisms of memory consolidation. Adult neurogenesis in mammals, including humans, is limited in two specific brain areas, the lateral walls of the lateral ventricles (subventricular zone) and the granular layer of the dentate gyrus of the hippocampus (subgranular zone). Neural stem cells (NSC), self-renewing, multipotent progenitor cells, are formed in these zones. Neural stem cells are capable of differentiating into the basic cell types of the nervous system. In addition, NSC may have neurogenic features and non-specific non-neurogenic functions aimed at maintaining the homeostasis of the brain. The microenvironment formed in neurogenic niches has importance maintaining populations of NSC and regulating differentiation into neural or glial cells via cell-to-cell interactions and microenvironmental signals. The vascular microenvironment in neurogenic niches are integrated by signaling molecules secreted from endothelial cells in the blood vessels of the brain or by direct contact with these cells. Accumulation of astrocytes in neurogenic niches if also of importance and leads to activation of neurogenesis. Dysregulation of neurogenesis contributes to the formation of neurological deficits observed in neurodegenerative diseases. Targeting regulation of neurogenesis could be the basis of new protocols of neuroregeneration.

About the authors

Yuliya K. Komleva

Voyno-Yasenetsky Krasnoyarsk State Medical University

Author for correspondence.
Email: yuliakomleva@mail.ru
Russian Federation, Krasnoyarsk

N. V. Kuvacheva

Voyno-Yasenetsky Krasnoyarsk State Medical University

Email: yuliakomleva@mail.ru
Russian Federation, Krasnoyarsk

N. A. Malinovskaya

Voyno-Yasenetsky Krasnoyarsk State Medical University

Email: platonova@neurology.ru
Russian Federation, Krasnoyarsk

Yana V. Gorina

Voyno-Yasenetsky Krasnoyarsk State Medical University

Email: yuliakomleva@mail.ru
Russian Federation, Krasnoyarsk

Olga L. Lopatina

Voyno-Yasenetsky Krasnoyarsk State Medical University

Email: yuliakomleva@mail.ru
Russian Federation, Krasnoyarsk

E. A. Teplyashina

Voyno-Yasenetsky Krasnoyarsk State Medical University

Email: yuliakomleva@mail.ru
Russian Federation, Krasnoyarsk

E. A. Pozhilenkova

Voyno-Yasenetsky Krasnoyarsk State Medical University

Email: yuliakomleva@mail.ru
Russian Federation, Krasnoyarsk

A. S. Zamay

Voyno-Yasenetsky Krasnoyarsk State Medical University

Email: yuliakomleva@mail.ru
Russian Federation, Krasnoyarsk

A. V. Morgun


Voyno-Yasenetsky Krasnoyarsk State Medical University

Email: yuliakomleva@mail.ru
Russian Federation, Krasnoyarsk

Alla B. Salmina

Voyno-Yasenetsky Krasnoyarsk State Medical University

Email: yuliakomleva@mail.ru
Russian Federation, Krasnoyarsk

References

  1. Салмина А.Б., Малиновская Н.А., Кувачева Н.В. и др. Коннексиновые и паннексиновые транспортные системы в клетках нейроваскулярной единицы головного мозга. Нейрохимия 2014; 31: 122–133.
  2. Abbracchio M. P., Burnstock G., Verkhratsky A., Zimmermann H. Purinergic signalling in the nervous system: an overview. Trends Neurosci. 2009; 32: 19–29.
  3. Altman J., Das G. D. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 1965; 124: 319–335.
  4. Avarez-Buylla A., Lim D.A. For the long run: maintaining germinal niches in the adult brain. Neuron 2004; 41: 683–686.
  5. Belluzzi O., Benedusi M., Ackman J., Loturco J.J. Electrophysiological differentiation of new neurons in the olfactory bulb. J. Neurosci. 2003; 23: 10411–10418.
  6. Boekhoorn K., Joels M., Lucassen P. J. Increased proliferation reflects glial and vascular-associated changes, but not neurogenesis in the presenile Alzheimer hippocampus. Neurobiol. Dis. 2006; 24: 1–14.
  7. Bossers K., Wirz K. T., Meerhoff G. F. et al. Concerted changes in transcripts in the prefrontal cortex precede neuropathology in Alzheimer’s disease. Brain. 2010; 133: 3699–3723.
  8. Braak H., Del Tredici K., Rub U. et al. Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol. Aging 2003; 24: 197–211.
  9. Brinton R.D., Wang J.M. Therapeutic potential of neurogenesis for prevention and recovery from Alzheimer’s disease: allopregnanolone as a proof of concept neurogenic agent. Curr. Alzheimer Res. 2006; 3: 185–190.
  10. Butti E., Cusimano M., Bacigaluppi M., Martino G. Neurogenic and non-neurogenic functions of endogenous neural stem cells. Front. Neurosci. 2014; 8: 1–11.
  11. Carson M.J., Thrash J.C., Walter B. The cellular response in neuroinflammation: The role of leukocytes, microglia and astrocytes in neuronal death and survival. Clin. Neurosci. Res. 2006; 6: 237–245.
  12. Cheng A., Wang S., Cai J., Rao M.S. et al. Nitric oxide acts in a positive feedback loop with BDNF to regulate neural progenitor cell proliferation and differentiation in the mammalian brain. Dev. Biol. 2003; 258: 319–333.
  13. Choi S.H., Veeraraghavalu K., Lazarov O. et al. Non-cellautonomous effects of presenilin 1 variants on enrichment-mediate hippocampal progenitor cell proliferation and differentiation. Neuron 2008; 59: 568–580.
  14. Chugh D., Nilsson P., Afjei S.A. et al. Brain inflammation induces post-synaptic changes during early synapse formation in adult-born hippocampal neurons. Exp. Neurol. 2013; 250: 176–88.
  15. Conover J.C., Notti R.Q. The neural stem cell niche. Cell Tissue Res. 2008; 331: 211–224.
  16. Curtis M.A., Eriksson P.S., Faull R.L. Progenitor cells and adult neurogenesis in neurodegenerative diseases and injuries of the basal ganglia. Clin. Exp. Pharmacol. Physiol. 2007; 34: 528–532.
  17. da Silva P.G., Benton J.L., Beltz B.S., Allodi S. Adult neurogenesis: ultrastructure of a neurogenic niche and neurovascular relationships. PLoS One. 2012; 7(6): e39267.
  18. Doetsch F., Caille I., Lim D.A., Garcia-Verdugo J.M. et al. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999; 97: 703–716.
  19. Doetsch F., García-Verdugo J.M., Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosci. 1997; 17: 5046–5061.
  20. Doetsch F., Petreanu L., Caille I. et al. EGF converts transitamplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 2002; 36: 1021–1034.
  21. Donovan M.H., Yazdani U., Norris R.D. et al. Decreased adult hippocampal neurogenesis in the PDAPP mouse model of Alzheimer’s disease. J. Comp. Neurol. 2006; 495: 70–83.
  22. Doze V.A., Perez D.M. G-protein-coupled receptors in adult neurogenesis. Pharmacol Rev. 2012; 64: 645–675.
  23. Duan X., Kang E., Liu C.Y. et al. Development of neural stem cell in the adult brain. Curr. Opin. Neurobiol. 2008; 18: 108–115.
  24. Ehmsen J.T., Ma T.M., Sason H. et al. D-serine in glia and neurons derives from 3-phosphoglycerate dehydrogenase. J. Neurosci. 2013; 33: 12464–12469.
  25. Ernst A., Alkass K., Bernard S. et al. Neurogenesis in the striatum of the adult human brain. Cell 2014; 156: 1072–1083.
  26. Filippov V., Kronenberg G., Pivneva T. et al. Subpopulation of nestinexpressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol. Cell. Neurosci. 2003; 23: 373–382.
  27. Fuentealba L. C., Obernier K., Alvarez-Buylla A. Adult neural stem cells bridge their niche. Cell Stem Cell 2012; 10: 698–708.
  28. Fukuda S., Kato F., Tozuka Y. Two distinct subpopulations of nestinpositive cells in adult mouse dentate gyrus.et al. J. Neurosci. 2003; 23: 9357–9366.
  29. Ge S., Sailor K.A., Ming G.L. et al. Synaptic integration and plasticity of new neurons in the adult hippocampus. J. Physiol. 2008; 586: 3759–3765.
  30. Goldberg J.S., Hirschi K.K. Diverse roles of the vasculature within the neural stem cell niche. Regen Med. 2009; 4: 879–897.
  31. Han Y.G., Spassky N., Romaguera-Ros M. et al. Hedgehog signaling and primary cilia are required for the formation of adult neural stem cells. Nat. Neurosci. 2008; 11: 277–284.
  32. Haughey N.J., Liu D., Nath A. et al. Disruption of neurogenesis in the subventricular zone of adult mice, and in human cortical neuronal precursor cells in culture, by amyloid beta-peptide: implications for the pathogenesis of Alzheimer’s disease. Neuromol. Med. 2002; 1: 125–135.
  33. Horner P.J., Palmer T.D. New roles for astrocytes: the nightlife of an ‘astrocyte’. La vida loca! Trends Neurosci. 2003; 26: 597–603.
  34. Huang X., Kong H., Tang M. et al. D-Serine regulates proliferation and neuronal differentiation of neural stem cells from postnatal mouse forebrain. CNS Neurosci. Ther. 2012; 18: 4–13.
  35. Ihrie, R. A., Avarez-Buylla A. Lake-front property: A unique germinal niche by the lateral ventricles of the adult brain. Neuron 2011; 70: 674–686.
  36. Imayoshi I., Sakamoto M., Ohtsuka T. et al. Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat. Neurosci. 2008; 11: 1153–1161.
  37. Jablonska B., Aguirre A., Raymond M. et al. Chordin-induced lineage plasticity of adult SVZ neuroblasts after demyelination. Nat. Neurosci. 2010; 13: 541–550.
  38. Jin K., Galvan V., Xie L. et al. Enhanced neurogenesis in Alzheimer’s disease transgenic (PDGF-APPSw,Ind) mice. Proc. Natl. Acad. Sci. USA 2004; 101: 13363–13367.
  39. Johanson C.E., Duncan J.A., Klinge P.M. et al. Multiplicity of cerebrospinal fluid functions: New challenges in health and disease. Cerebrospinal Fluid Res. 2008; 5: 10.
  40. Kawakami Y., Yoshida K., Yang J.H. et al. Impaired neurogenesis in embryonic spinal cord of Phgdh knockout mice, a serine deficiency disorder model. Neurosci. Res. 2009; 63: 184–193.
  41. Kempermann G., Gast D., Gage F.H. Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann. Neurol. 2002; 52: 135–143.
  42. Kempermann G., Jessberger S., Steiner B. et al. Milestones of neuronal development in the adult hippocampus. Trends Neurosci. 2004; 27: 447–452.
  43. Kilpatrick T.J., Bartlett P.F. Cloned multipotential precursors from the mouse cerebrum require FGF-2, whereas glial restricted precursors are stimulated with either FGF-2 or EGF. J Neurosci. 1995; 15 (5 Pt1): 3653–3661.
  44. Kitamura T., Saitoh Y., Takashima N. et al. Adult neurogenesis modulates the hippocampus-dependent period of associative fear memory. Cell 2009; 139: 814–827.
  45. Koos T., Tepper J.M. Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat. Neurosci. 1999; 2: 467–472.
  46. Lazarini F., Mouthon M.A., Gheusi G. et al. Cellular and behavioral effects of cranial irradiation of the subventricular zone in adult mice. PLoS ONE 2009; 4: e7017.
  47. Lazarov O., Marr R.A. Neurogenesis and Alzheimer’s disease: at the crossroads. Exp. Neurol. 2010; 223: 267–281.
  48. Lee C., Hu J., Ralls S. et al. The molecular profiles of neural stem cell niche in the adult subventricular zone. PLoS One 2012; 7: e50501.
  49. Lee D.A., Bedont J.L., Pak T. et al. Tanycytes of the hypothalamic median eminence form a diet-responsive neurogenic niche. Nat. Neurosci. 2012; 15: 700–702.
  50. Li B., Yamamori H., Tatebayashi Y. et al. Failure of neuronal maturation in Alzheimer disease dentate gyrus. J. Neuropathol. Exp. Neurol. 2008; 67: 78–84.
  51. Lim D.A., Alvarez-Buylla A. Interaction between astrocytes and adult subventricular zone precursors stimulates neurogenesis. Proc. Natl. Acad. Sci. USA 1999; 96: 7526–7531.
  52. Lin J.H., Takano T., Arcuino G. et al. Purinergic signaling regulates neural progenitor cell expansion and neurogenesis. Dev. Biol. 2007; 302: 356–366.
  53. Lois C., Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science 1994; 264: 1145–1148.
  54. Lo‡pez-Toledano M.A., Shelanski M.L. Neurogenic effect of betaamyloid peptide in the development of neural stem cells. J. Neurosci. 2004; 24: 5439–5444.
  55. Lu Z., Elliott M. R., Chen Y. et al. Phagocytic activity of neuronal progenitors regulates adult neurogenesis. Nat. Cell Biol. 2011; 13:1076–1083.
  56. Ma D.K., Ming G.L., Song H. Glial influences on neural stem cell development: cellular niches for adult neurogenesis. Curr. Opin. Neurobiol. 2005; 15: 514–520.
  57. Mandairon N., Sacquet J., Garcia S. et al. Neurogenic correlates of an olfactory discrimination task in the adult olfactory bulb. Eur. J. Neurosci. 2006; 24: 3578–3588.
  58. Martino G., Pluchino S. The therapeutic potential of neural stem cells. Nat. Rev. Neurosci. 2006; 7: 395–406.
  59. Ming G.L., Song H. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 2011; 70: 687–702.
  60. Ming G.L., Song H. Adult neurogenesis in the mammalian central nervous system. Annu. Rev. Neurosci. 2005; 28: 223–250.
  61. Mirochnic S., Wolf S., Staufenbiel M. et al. Age effects on the regulation of adult hippocampal neurogenesis by physical activity and environmental enrichment in the APP23 mouse model of Alzheimer disease. Hippocampus 2009; 19: 1008–1018.
  62. Mirzadeh Z., Merkle F. T., Soriano-Navarro M. et al. Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 2008; 3: 265–278.
  63. Mongiat L.A., Schinder A.F. Adult neurogenesis and the plasticity of the dentate gyrus network. Eur. J. Neurosci. 2011; 33: 1055–1061.
  64. Moreno M.M., Linster C., Escanilla O. et al. Olfactory perceptual learning requires adult neurogenesis. Proc. Natl. Acad. Sci. USA. 2009;106: 17980–17985.
  65. Morrens J., Van Den Broeck W., Kempermann G. Glial cells in adult neurogenesis. Glia 2012; 60: 159–74.
  66. Mosher K. I., Andres R. H., Fukuhara T. et al. Neural progenitor cells regulate microglia functions and activity. Nat. Neurosci. 2012; 15: 1485–1487.
  67. Nissant A., Bardy C., Katagiri H. et al. Adult neurogenesis promotes synaptic plasticity in the olfactory bulb. Nat. Neurosci. 2009; 12: 728–730.
  68. Overstreet-Wadiche L.S., Bromberg D.A., Bensen A.L. et al. Seizures accelerate functional integration of adult-generated granule cells. J. Neurosci. 2006; 26: 4095–4103.
  69. Palmer T.D., Willhoite A.R., Gage F.H. Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol. 2000; 425: 479–494.
  70. Parent J.M. Adult neurogenesis in the intact and epileptic dentate gyrus. Prog. Brain Res. 2007; 163: 529–540.
  71. Pietropaolo S., Sun Y., Li R. et al. Limited impact of social isolation on Alzheimer-like symptoms in a triple transgenic mouse model. Behav. Neurosci. 2009; 123: 181–195.
  72. Plane J.M., Andjelkovic A.V., Keep R.F., Parent J.M. Intact and injured endothelial cells differentially modulate postnatal murine forebrain neural stem cells. Neurobiol Dis. 2010; 37: 218–227.
  73. Platel J.C., Dave K.A., Gordon V. et al. NMDA receptors activated by subventricular zone astrocytic glutamate are critical for neuroblast survival prior to entering a synaptic network. Neuron 2010; 65: 859–872.
  74. Porlan E., Perez-Villalba A., Delgado A.C., Ferroˆn S.R. Paracrine regulation of neural stem cells in the subependymal zone. Arch. Biochem. Biophys. 2013; 534: 11–19.
  75. Ramírez-Castillejo C., Saˆnchez-Saˆnchez F., Andreu-Agulloˆ C. et al. Pigment epithelium-derived factor is a niche signal for neural stem cell renewal. Nat. Neurosci. 2006; 9: 331–339.
  76. 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.
  77. Sahay A., Scobie K. N., Hill A.S. et al. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 2011; 472: 466–470.
  78. Sawamoto K., Wichterle H., Gonzalez-Perez O. et al. New neurons follow the flow of cerebrospinal fluid in the adult brain. Science 2006; 311: 629–632.
  79. Schlett K. Glutamate as a modulator of embryonic and adult neurogenesis. Curr. Top. Med. Chem. 2006; 6: 949–960.
  80. Schmidt-Hieber C., Jonas P., Bischofberger J. Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 2004; 429: 184–187.
  81. Shen Q., Goderie S.K., Jin L. et al. Endothelial cells stimulate selfrenewal and expand neurogenesis of neural stem cells. Science 2004;304: 1338–1340.
  82. Shors T. J., Townsend D. A., Zhao M. et al. Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 2002; 12: 578–584.
  83. Sierra A., Encinas J. M., Deudero J.J. et al. Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 2010; 7: 483–495.
  84. Singla V., Reiter J.F. The primary cilium as the cell’s antenna: signaling at a sensory organelle. Science 2006; 313: 629–633.
  85. Small S. A. Measuring correlates of brain metabolism with highresolution MRI: a promising approach for diagnosing Alzheimer disease and mapping its course. Alzheimer Dis. Assoc. Disord. 2003; 17: 154–161.
  86. Snyder J. S., Hong N. S., McDonald R. J., Wojtowicz J.M. A role for adult neurogenesis in spatial long-term memory. Neuroscience 2005; 130: 843–852.
  87. Snyder J. S., Soumier A., Brewer M. J. et al. Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature 2011; 476: 458–461.
  88. Steiner B., Klempin F., Wang L. et al. Type-2 cells as link between glial and neuronal lineage in adult hippocampal neurogenesis . Glia 2006; 54: 805–814.
  89. Sultan S., Gebara E.G., Moullec K., Toni N. D-serine increases adult hippocampal neurogenesis. Front Neurosci. 2013; 7: 155.
  90. Suzuki M., Nelson A.D., Eickstaedt J.B. et al. Glutamate enhances proliferation and neurogenesis in human neural progenitor cell cultures derived from the fetal cortex. Eur. J. Neurosci. 2006; 24: 645–653.
  91. Tashiro A., Sandler V.M., Toni N. et al. NMDA-receptor-mediated, cell-specifc integration of new neurons in adult dentate gyrus. Nature 2006; 442: 929–933.
  92. Tavazoie M., Van der Veken L., Silva-Vargas V. et al. A specialized vascular niche for adult neural stem cells. Cell Stem Cell 2008; 3: 279–288.
  93. Tong C.K., Chen J., Cebrian-Silla A. et al. Axonal control of the adult neural stem cell niche. Cell Stem Cell 2014; 14: 500–511.
  94. Toni N., Teng E.M., Bushong E.A. et al. Synapse formation on neurons born in the adult hippocampus. Nat. Neurosci. 2007; 10: 727–734.
  95. van Tijn P., Hobo B., Verhage M.C. et al. Alzheimer-associated mutant ubiquitin impairs spatial reference memory. Physiol. Behav. 2011; 102: 193–200.
  96. Varvel N.H., Bhaskar K., Kounnas M.Z. et al. NSAIDs prevent, but do not reverse, neuronal cell cycle reentry in a mouse model of Alzheimer disease. J. Clin. Invest. 2009; 119: 3692–3702.
  97. Weidenfeller C., Svendsen C.N., Shusta E.V. Differentiating embryonic neural progenitor cells induce blood-brain barrier properties. J. Neurochem. 2007; 101: 555–565.
  98. Wicki-Stordeur L.E., Swayne L.A. Large pore ion and metabolitepermeable channel regulation of postnatal ventricular zone neural stem and progenitor cells: interplay between aquaporins, connexins, and pannexins? Stem Cells Int. 2012; 2012: 454180.
  99. Willshaw D.J., Buckingham J.T. An assessment of Marr’s theory of the hippocampus as a temporary memory store. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1990; 329: 205–215.
  100. Yamashima T., Tonchev A.B., Yukie M. Adult hippocampal neurogenesis in rodents and primates: endogenous, enhanced, and engrafted. Rev. Neurosci. 2007; 18: 67–82.
  101. Young J.K., Heinbockel T., Gondreˆ-Lewis M.C. Astrocyte fatty acid binding protein-7 is a marker for neurogenic niches in the rat hippocampus. Hippocampus 2013; 23: 1476-1483.
  102. Young S.Z., Taylor M.M., Bordey A. Neurotransmitters couple brain activity to subventricular zone neurogenesis. Eur. J. Neurosci. 2011; 33:1123–1132.
  103. Zhao C., Deng W., Gage F.H. Mechanisms and functional implications of adult neurogenesis. Cell 2008; 132: 645–660.
  104. Zhao C., Teng E.M., Summers R.G. et al. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J. Neurosci. 2006; 26: 3–11.

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Copyright (c) 2014 Komleva Y.K., Kuvacheva N.V., Malinocskaya N.A., Gorina Y.V., Lopatina O.L., Teplyashina E.A., Pozhilenkova E.A., Zamay A.S., Morgun A.V., Salmina A.B.

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