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Spontaneous Recovery Mechanisms-Brain Reorganization

  • Sonia-Luz Albarracin
  • Jhon-Jairo Sutachan
Chapter

Abstract

Traumatic brain injury (TBI) is one of the major causes of death and disability. TBI is initially characterized by the activation of a group of mechanisms that induces spontaneous recovery and brain reorganization. It has been suggested that processes such as neurogenesis, synaptogenesis and plasticity (reorganization of connectivity), and angiogenesis play a role in spontaneous recovery after TBI. Adult neurogenesis has been described in the subventricular zone of the lateral ventricle and in the subgranular zone of the hippocampus. TBI is characterized by the activation of neurogenesis that is important for the recovery of cognitive and learning skills. Although the exact mechanisms by which TBI can induce spontaneous recovery and brain reorganization have not been fully established, it is thought that activation of several signaling pathways by growth factors, signaling molecules, and cytokines that are produced after TBI play a role. This chapter will focus on reviewing how these molecules affect cell proliferation, viability, commitment, guidance, and location of neural stem cells in the two most characterized neurogenic niches (subventricular and subgranular zones). Additionally other mechanisms of brain reorganization will be reviewed.

Keywords

Traumatic brain injury TBI Spontaneous recovery Brain reorganization Neurogenesis Neural stem cells Neural progenitors cells Granular neurons Subventricular zone Subgranular zone Notch Wnt Sonic hedgehog Ephrins Neurotrophins BDNF IL-1β IL-6 TNFα IL-10 TGF-β1 Slit DISC1 

Notes

Acknowledgments

This chapter was funded by Grant 4800 “BDNF-TrkB signaling regulation of GABAergic neurotransmission” from Vicerrectoria de Investigaciones at Pontificia Universidad Javeriana.

References

  1. 1.
    Hyder AA, Wunderlich CA, Puvanachandra P, Gururaj G, Kobusingye OC. The impact of traumatic brain injuries: a global perspective. NeuroRehabilitation. 2007;22(5):341–53.PubMedGoogle Scholar
  2. 2.
    Langlois JA, Sattin RW. Traumatic brain injury in the United States: research and programs of the Centers for Disease Control and Prevention (CDC). J Head Trauma Rehabil. 2005;20(3):187–8.CrossRefGoogle Scholar
  3. 3.
    Roozenbeek B, Maas AI, Menon DK. Changing patterns in the epidemiology of traumatic brain injury. Nat Rev Neurol. 2013;9(4):231–6.CrossRefGoogle Scholar
  4. 4.
    Tagliaferri F, Compagnone C, Korsic M, Servadei F, Kraus J. A systematic review of brain injury epidemiology in Europe. Acta Neurochir. 2006;148(3):255–68; discussion 68.CrossRefGoogle Scholar
  5. 5.
    Ray SK, Dixon CE, Banik NL. Molecular mechanisms in the pathogenesis of traumatic brain injury. Histol Histopathol. 2002;17(4):1137–52.PubMedGoogle Scholar
  6. 6.
    Yu TS, Washington PM, Kernie SG. Injury-induced neurogenesis: mechanisms and relevance. Neuroscientist. 2016;22(1):61–71.CrossRefGoogle Scholar
  7. 7.
    Jin K, Wang X, Xie L, Mao XO, Zhu W, Wang Y, et al. Evidence for stroke-induced neurogenesis in the human brain. Proc Natl Acad Sci U S A. 2006;103(35):13198–202.CrossRefGoogle Scholar
  8. 8.
    Li D, Ma S, Guo D, Cheng T, Li H, Tian Y, et al. Environmental circadian disruption worsens neurologic impairment and inhibits hippocampal neurogenesis in adult rats after traumatic brain injury. Cell Mol Neurobiol. 2016;36:1045.CrossRefGoogle Scholar
  9. 9.
    Sun D, Daniels TE, Rolfe A, Waters M, Hamm R. Inhibition of injury-induced cell proliferation in the dentate gyrus of the hippocampus impairs spontaneous cognitive recovery after traumatic brain injury. J Neurotrauma. 2015;32(7):495–505.CrossRefGoogle Scholar
  10. 10.
    Doetsch F, García-Verdugo JM, Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci. 1997;17(13):5046–61.CrossRefGoogle Scholar
  11. 11.
    Reznikov KI. Local proliferation of cells of the granular layer of the dentate gyrus of the mouse hippocampus during postnatal ontogenesis and following brain injury. Ontogenez. 1975;6(3):242–50.PubMedGoogle Scholar
  12. 12.
    García-Verdugo JM, Doetsch F, Wichterle H, Lim DA, Alvarez-Buylla A. Architecture and cell types of the adult subventricular zone: in search of the stem cells. J Neurobiol. 1998;36(2):234–48.CrossRefGoogle Scholar
  13. 13.
    Kleindienst A, McGinn MJ, Harvey HB, Colello RJ, Hamm RJ, Bullock MR. Enhanced hippocampal neurogenesis by intraventricular S100B infusion is associated with improved cognitive recovery after traumatic brain injury. J Neurotrauma. 2005;22(6):645–55.CrossRefGoogle Scholar
  14. 14.
    Song H, Stevens CF, Gage FH. Astroglia induce neurogenesis from adult neural stem cells. Nature. 2002;417(6884):39–44.CrossRefGoogle Scholar
  15. 15.
    Oh J, McCloskey MA, Blong CC, Bendickson L, Nilsen-Hamilton M, Sakaguchi DS. Astrocyte-derived interleukin-6 promotes specific neuronal differentiation of neural progenitor cells from adult hippocampus. J Neurosci Res. 2010;88(13):2798–809.PubMedPubMedCentralGoogle Scholar
  16. 16.
    Tao Y, Ma L, Liao Z, Le Q, Yu J, Liu X, et al. Astroglial β-Arrestin1-mediated nuclear signaling regulates the expansion of neural precursor cells in adult hippocampus. Sci Rep. 2015;5:15506.CrossRefGoogle Scholar
  17. 17.
    Horgusluoglu E, Nudelman K, Nho K, Saykin AJ. Adult neurogenesis and neurodegenerative diseases: a systems biology perspective. Am J Med Genet B Neuropsychiatr Genet. 2016;174(1):93–112.CrossRefGoogle Scholar
  18. 18.
    Kopan R, Ilagan MX. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell. 2009;137(2):216–33.CrossRefGoogle Scholar
  19. 19.
    Ables JL, Decarolis NA, Johnson MA, Rivera PD, Gao Z, Cooper DC, et al. Notch1 is required for maintenance of the reservoir of adult hippocampal stem cells. J Neurosci. 2010;30(31):10484–92.CrossRefGoogle Scholar
  20. 20.
    Imayoshi I, Sakamoto M, Yamaguchi M, Mori K, Kageyama R. Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. J Neurosci. 2010;30(9):3489–98.CrossRefGoogle Scholar
  21. 21.
    Givogri MI, de Planell M, Galbiati F, Superchi D, Gritti A, Vescovi A, et al. Notch signaling in astrocytes and neuroblasts of the adult subventricular zone in health and after cortical injury. Dev Neurosci. 2006;28(1–2):81–91.CrossRefGoogle Scholar
  22. 22.
    Chambers CB, Peng Y, Nguyen H, Gaiano N, Fishell G, Nye JS. Spatiotemporal selectivity of response to Notch1 signals in mammalian forebrain precursors. Development. 2001;128(5):689–702.PubMedGoogle Scholar
  23. 23.
    Lebkuechner I, Wilhelmsson U, Möllerström E, Pekna M, Pekny M. Heterogeneity of Notch signaling in astrocytes and the effects of GFAP and vimentin deficiency. J Neurochem. 2015;135(2):234–48.CrossRefGoogle Scholar
  24. 24.
    Zhao Y, Gibb SL, Zhao J, Moore AN, Hylin MJ, Menge T, et al. Wnt3a, a protein secreted by mesenchymal stem cells is neuroprotective and promotes neurocognitive recovery following traumatic brain injury. Stem Cells. 2016;34(5):1263–72.CrossRefGoogle Scholar
  25. 25.
    Gao Z, Ure K, Ables JL, Lagace DC, Nave KA, Goebbels S, et al. Neurod1 is essential for the survival and maturation of adult-born neurons. Nat Neurosci. 2009;12(9):1090–2.CrossRefGoogle Scholar
  26. 26.
    Kuwabara T, Hsieh J, Muotri A, Yeo G, Warashina M, Lie DC, et al. Wnt-mediated activation of NeuroD1 and retro-elements during adult neurogenesis. Nat Neurosci. 2009;12(9):1097–105.CrossRefGoogle Scholar
  27. 27.
    Pataskar A, Jung J, Smialowski P, Noack F, Calegari F, Straub T, et al. NeuroD1 reprograms chromatin and transcription factor landscapes to induce the neuronal program. EMBO J. 2016;35(1):24–45.CrossRefGoogle Scholar
  28. 28.
    Araújo GL, Araújo JA, Schroeder T, Tort AB, Costa MR. Sonic hedgehog signaling regulates mode of cell division of early cerebral cortex progenitors and increases astrogliogenesis. Front Cell Neurosci. 2014;8:77.PubMedPubMedCentralGoogle Scholar
  29. 29.
    Mierzwa AJ, Sullivan GM, Beer LA, Ahn S, Armstrong RC. Comparison of cortical and white matter traumatic brain injury models reveals differential effects in the subventricular zone and divergent Sonic hedgehog signaling pathways in neuroblasts and oligodendrocyte progenitors. ASN Neuro. 2014;6(5):175909141455178.CrossRefGoogle Scholar
  30. 30.
    Palma V, Lim DA, Dahmane N, Sánchez P, Brionne TC, Herzberg CD, et al. Sonic hedgehog controls stem cell behavior in the postnatal and adult brain. Development. 2005;132(2):335–44.CrossRefGoogle Scholar
  31. 31.
    Depaepe V, Suarez-Gonzalez N, Dufour A, Passante L, Gorski JA, Jones KR, et al. Ephrin signalling controls brain size by regulating apoptosis of neural progenitors. Nature. 2005;435(7046):1244–50.CrossRefGoogle Scholar
  32. 32.
    Jiao JW, Feldheim DA, Chen DF. Ephrins as negative regulators of adult neurogenesis in diverse regions of the central nervous system. Proc Natl Acad Sci U S A. 2008;105(25):8778–83.CrossRefGoogle Scholar
  33. 33.
    Ashton RS, Conway A, Pangarkar C, Bergen J, Lim KI, Shah P, et al. Astrocytes regulate adult hippocampal neurogenesis through ephrin-B signaling. Nat Neurosci. 2012;15(10):1399–406.CrossRefGoogle Scholar
  34. 34.
    Reichardt LF. Neurotrophin-regulated signalling pathways. Philos Trans R Soc Lond Ser B Biol Sci. 2006;361(1473):1545–64.CrossRefGoogle Scholar
  35. 35.
    Chao MV. Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci. 2003;4(4):299–309.CrossRefGoogle Scholar
  36. 36.
    Vilar M, Mira H. Regulation of neurogenesis by neurotrophins during adulthood: expected and unexpected roles. Front Neurosci. 2016;10:26.CrossRefGoogle Scholar
  37. 37.
    Bagley JA, Belluscio L. Dynamic imaging reveals that brain-derived neurotrophic factor can independently regulate motility and direction of neuroblasts within the rostral migratory stream. Neuroscience. 2010;169(3):1449–61.CrossRefGoogle Scholar
  38. 38.
    Snapyan M, Lemasson M, Brill MS, Blais M, Massouh M, Ninkovic J, et al. Vasculature guides migrating neuronal precursors in the adult mammalian forebrain via brain-derived neurotrophic factor signaling. J Neurosci. 2009;29(13):4172–88.CrossRefGoogle Scholar
  39. 39.
    Bergami M, Vignoli B, Motori E, Pifferi S, Zuccaro E, Menini A, et al. TrkB signaling directs the incorporation of newly generated periglomerular cells in the adult olfactory bulb. J Neurosci. 2013;33(28):11464–78.CrossRefGoogle Scholar
  40. 40.
    Galvão RP, Garcia-Verdugo JM, Alvarez-Buylla A. Brain-derived neurotrophic factor signaling does not stimulate subventricular zone neurogenesis in adult mice and rats. J Neurosci. 2008;28(50):13368–83.CrossRefGoogle Scholar
  41. 41.
    Delgado AC, Ferrón SR, Vicente D, Porlan E, Perez-Villalba A, Trujillo CM, et al. Endothelial NT-3 delivered by vasculature and CSF promotes quiescence of subependymal neural stem cells through nitric oxide induction. Neuron. 2014;83(3):572–85.CrossRefGoogle Scholar
  42. 42.
    Chiaramello S, Dalmasso G, Bezin L, Marcel D, Jourdan F, Peretto P, et al. BDNF/ TrkB interaction regulates migration of SVZ precursor cells via PI3-K and MAP-K signalling pathways. Eur J Neurosci. 2007;26(7):1780–90.CrossRefGoogle Scholar
  43. 43.
    Bath KG, Mandairon N, Jing D, Rajagopal R, Kapoor R, Chen ZY, et al. Variant brain-derived neurotrophic factor (Val66Met) alters adult olfactory bulb neurogenesis and spontaneous olfactory discrimination. J Neurosci. 2008;28(10):2383–93.CrossRefGoogle Scholar
  44. 44.
    Taliaz D, Stall N, Dar DE, Zangen A. Knockdown of brain-derived neurotrophic factor in specific brain sites precipitates behaviors associated with depression and reduces neurogenesis. Mol Psychiatry. 2010;15(1):80–92.CrossRefGoogle Scholar
  45. 45.
    Scharfman H, Goodman J, Macleod A, Phani S, Antonelli C, Croll S. Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp Neurol. 2005;192(2):348–56.CrossRefGoogle Scholar
  46. 46.
    Lee J, Seroogy KB, Mattson MP. Dietary restriction enhances neurotrophin expression and neurogenesis in the hippocampus of adult mice. J Neurochem. 2002;80(3):539–47.CrossRefGoogle Scholar
  47. 47.
    Catts VS, Al-Menhali N, Burne TH, Colditz MJ, Coulson EJ. The p75 neurotrophin receptor regulates hippocampal neurogenesis and related behaviours. Eur J Neurosci. 2008;28(5):883–92.CrossRefGoogle Scholar
  48. 48.
    Shimazu K, Zhao M, Sakata K, Akbarian S, Bates B, Jaenisch R, et al. NT-3 facilitates hippocampal plasticity and learning and memory by regulating neurogenesis. Learn Mem. 2006;13(3):307–15.CrossRefGoogle Scholar
  49. 49.
    Guadagno J, Swan P, Shaikh R, Cregan SP. Microglia-derived IL-1β triggers p53-mediated cell cycle arrest and apoptosis in neural precursor cells. Cell Death Dis. 2015;6:e1779.CrossRefGoogle Scholar
  50. 50.
    Ryan SM, O'Keeffe GW, O'Connor C, Keeshan K, Nolan YM. Negative regulation of TLX by IL-1β correlates with an inhibition of adult hippocampal neural precursor cell proliferation. Brain Behav Immun. 2013;33:7–13.CrossRefGoogle Scholar
  51. 51.
    Green HF, Treacy E, Keohane AK, Sullivan AM, O'Keeffe GW, Nolan YM. A role for interleukin-1β in determining the lineage fate of embryonic rat hippocampal neural precursor cells. Mol Cell Neurosci. 2012;49(3):311–21.CrossRefGoogle Scholar
  52. 52.
    Woodcock T, Morganti-Kossmann MC. The role of markers of inflammation in traumatic brain injury. Front Neurol. 2013;4:18.CrossRefGoogle Scholar
  53. 53.
    Campbell IL, Erta M, Lim SL, Frausto R, May U, Rose-John S, et al. Trans-signaling is a dominant mechanism for the pathogenic actions of interleukin-6 in the brain. J Neurosci. 2014;34(7):2503–13.CrossRefGoogle Scholar
  54. 54.
    Vallières L, Campbell IL, Gage FH, Sawchenko PE. Reduced hippocampal neurogenesis in adult transgenic mice with chronic astrocytic production of interleukin-6. J Neurosci. 2002;22(2):486–92.CrossRefGoogle Scholar
  55. 55.
    Nakanishi M, Niidome T, Matsuda S, Akaike A, Kihara T, Sugimoto H. Microglia-derived interleukin-6 and leukaemia inhibitory factor promote astrocytic differentiation of neural stem/progenitor cells. Eur J Neurosci. 2007;25(3):649–58.CrossRefGoogle Scholar
  56. 56.
    Islam O, Gong X, Rose-John S, Heese K. Interleukin-6 and neural stem cells: more than gliogenesis. Mol Biol Cell. 2009;20(1):188–99.CrossRefGoogle Scholar
  57. 57.
    Iosif RE, Ekdahl CT, Ahlenius H, Pronk CJ, Bonde S, Kokaia Z, et al. Tumor necrosis factor receptor 1 is a negative regulator of progenitor proliferation in adult hippocampal neurogenesis. J Neurosci. 2006;26(38):9703–12.CrossRefGoogle Scholar
  58. 58.
    Longhi L, Perego C, Ortolano F, Aresi S, Fumagalli S, Zanier ER, et al. Tumor necrosis factor in traumatic brain injury: effects of genetic deletion of p55 or p75 receptor. J Cereb Blood Flow Metab. 2013;33(8):1182–9.CrossRefGoogle Scholar
  59. 59.
    Scherbel U, Raghupathi R, Nakamura M, Saatman KE, Trojanowski JQ, Neugebauer E, et al. Differential acute and chronic responses of tumor necrosis factor-deficient mice to experimental brain injury. Proc Natl Acad Sci U S A. 1999;96(15):8721–6.CrossRefGoogle Scholar
  60. 60.
    Cacci E, Claasen JH, Kokaia Z. Microglia-derived tumor necrosis factor-alpha exaggerates death of newborn hippocampal progenitor cells in vitro. J Neurosci Res. 2005;80(6):789–97.CrossRefGoogle Scholar
  61. 61.
    Ben-Hur T, Ben-Menachem O, Furer V, Einstein O, Mizrachi-Kol R, Grigoriadis N. Effects of proinflammatory cytokines on the growth, fate, and motility of multipotential neural precursor cells. Mol Cell Neurosci. 2003;24(3):623–31.CrossRefGoogle Scholar
  62. 62.
    Heldmann U, Thored P, Claasen JH, Arvidsson A, Kokaia Z, Lindvall O. TNF-alpha antibody infusion impairs survival of stroke-generated neuroblasts in adult rat brain. Exp Neurol. 2005;196(1):204–8.CrossRefGoogle Scholar
  63. 63.
    Chen Z, Palmer TD. Differential roles of TNFR1 and TNFR2 signaling in adult hippocampal neurogenesis. Brain Behav Immun. 2013;30:45–53.CrossRefGoogle Scholar
  64. 64.
    Ouyang W, Rutz S, Crellin NK, Valdez PA, Hymowitz SG. Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annu Rev Immunol. 2011;29:71–109.CrossRefGoogle Scholar
  65. 65.
    Perez-Asensio FJ, Perpiñá U, Planas AM, Pozas E. Interleukin-10 regulates progenitor differentiation and modulates neurogenesis in adult brain. J Cell Sci. 2013;126(Pt 18):4208–19.CrossRefGoogle Scholar
  66. 66.
    Pereira L, Font-Nieves M, Van den Haute C, Baekelandt V, Planas AM, Pozas E. IL-10 regulates adult neurogenesis by modulating ERK and STAT3 activity. Front Cell Neurosci. 2015;9:57.PubMedPubMedCentralGoogle Scholar
  67. 67.
    Han G, Li F, Singh TP, Wolf P, Wang XJ. The pro-inflammatory role of TGFβ1: a paradox? Int J Biol Sci. 2012;8(2):228–35.CrossRefGoogle Scholar
  68. 68.
    Morganti-Kossmann MC, Hans VH, Lenzlinger PM, Dubs R, Ludwig E, Trentz O, et al. TGF-beta is elevated in the CSF of patients with severe traumatic brain injuries and parallels blood-brain barrier function. J Neurotrauma. 1999;16(7):617–28.CrossRefGoogle Scholar
  69. 69.
    Attisano L, Cárcamo J, Ventura F, Weis FM, Massagué J, Wrana JL. Identification of human activin and TGF beta type I receptors that form heteromeric kinase complexes with type II receptors. Cell. 1993;75(4):671–80.CrossRefGoogle Scholar
  70. 70.
    Wachs FP, Winner B, Couillard-Despres S, Schiller T, Aigner R, Winkler J, et al. Transforming growth factor-beta1 is a negative modulator of adult neurogenesis. J Neuropathol Exp Neurol. 2006;65(4):358–70.CrossRefGoogle Scholar
  71. 71.
    Ibrahim S, Hu W, Wang X, Gao X, He C, Chen J. Traumatic brain injury causes aberrant migration of adult-born neurons in the Hippocampus. Sci Rep. 2016;6:21793.CrossRefGoogle Scholar
  72. 72.
    Lighthall JW. Controlled cortical impact: a new experimental brain injury model. J Neurotrauma. 1988;5(1):1–15.CrossRefGoogle Scholar
  73. 73.
    Marín O, Rubenstein JL. Cell migration in the forebrain. Annu Rev Neurosci. 2003;26:441–83.CrossRefGoogle Scholar
  74. 74.
    Wu W, Wong K, Chen J, Jiang Z, Dupuis S, Wu JY, et al. Directional guidance of neuronal migration in the olfactory system by the protein Slit. Nature. 1999;400(6742):331–6.CrossRefGoogle Scholar
  75. 75.
    Duan X, Chang JH, Ge S, Faulkner RL, Kim JY, Kitabatake Y, et al. Disrupted-in-schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell. 2007;130(6):1146–58.CrossRefGoogle Scholar
  76. 76.
    Nudo RJ. Recovery after brain injury: mechanisms and principles. Front Hum Neurosci. 2013;7:887.CrossRefGoogle Scholar
  77. 77.
    Stroemer RP, Kent TA, Hulsebosch CE. Neocortical neural sprouting, synaptogenesis, and behavioral recovery after neocortical infarction in rats. Stroke. 1995;26(11):2135–44.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Sonia-Luz Albarracin
    • 1
  • Jhon-Jairo Sutachan
    • 1
  1. 1.Nutrition and Biochemistry Department – Pontifical Xavierian UniversityBogotáColombia

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