Advertisement

Transcriptional and Genomic Advances on the Pathophysiology of Stem Cell Repairment After Intracerebral Hemorrhage

  • Sheng Zhang
  • Yongjie Zhou
  • Yujie ChenEmail author
Chapter
  • 774 Downloads
Part of the Springer Series in Translational Stroke Research book series (SSTSR)

Abstract

Intracerebral hemorrhage is a life-threatening disease characterized by a sudden rupture of cerebral blood vessels, and it is widely believed that neural cell death occurs after exposure to blood metabolites or subsequently damaged cells. Based on these disappointing results of 1026 neuroprotective agents, researchers turned their interests on neurogenesis, which is traditionally considered as an endogenous neuroprotective mechanism after acute central nervous system injuries. However, because of complexity in stem cell survival, migration, differentiation, and maturation, current strategies have either been proved unsatisfactory or resulted in serious side effects during clinical translation. It is well known that transcriptional and genomic pathways play important roles in ensuring the normal functions of stem cells, including proliferation, migration, differentiation and neural reconnection. And reprogramming technology and other non-invasive electromagnetic stimulation were recently employed and proved effective for the stem cell characteristics. Therefore, in the present chapter, we sought to summarize the advances in the pathophysiology and strategies of stem cell repairment after ICH at the level of transcription and genome, hoping to provide potential sparks for better stem cell repairment for ICH patients.

Keywords

Stem cell Intracerebral hemorrhage Transcriptome Genome Bioinformatics Reprogramming technology Neurological recovery 

Abbreviations

ICH

Intracerebral hemorrhage

LncRNA

Long non-coding RNA

miRNA

MicroRNA

NSC

Neural stem cell

SPIO

super-paramagnetic iron oxide

STICH

Surgical Trial in Intracerebral Hemorrhage

SVZ

subependymal ventricular zone

US FDA

United States Food and Drug Administration

Notes

Acknowledgements

This work was supported by Incubation Foundation of Interdisciplinary Laboratory of Physics and Biomedicine (Grant No. WSS-2015-08), Basic Science and Advanced Technology Research Project of Chongqing (Grant No. cstc2016jcyjA1730), National Natural Science Foundation of China (Grant No. 81501002, 81220108009) and National Basic Research Program of China (973 Program, Grant No. 2014CB541600).

Conflicts of Interest: The authors declared no potential conflicts of interest.

References

  1. 1.
    Keep RF, Hua Y, Xi G. Intracerebral haemorrhage: mechanisms of injury and therapeutic targets. Lancet Neurol. 2012;11(8):720–31.PubMedCrossRefGoogle Scholar
  2. 2.
    Macdonald RL, Schweizer TA. Spontaneous subarachnoid haemorrhage. Lancet. 2016;Google Scholar
  3. 3.
    Mendelow AD, Gregson BA, Fernandes HM, Murray GD, Teasdale GM, Hope DT, et al. Early surgery versus initial conservative treatment in patients with spontaneous supratentorial intracerebral haematomas in the International Surgical Trial in Intracerebral Haemorrhage (STICH): a randomised trial. Lancet. 2005;365(9457):387–97.PubMedCrossRefGoogle Scholar
  4. 4.
    Mendelow AD, Gregson BA, Rowan EN, Murray GD, Gholkar A, Mitchell PM, et al. Early surgery versus initial conservative treatment in patients with spontaneous supratentorial lobar intracerebral haematomas (STICH II): a randomised trial. Lancet. 2013;382(9890):397–408.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Mayer SA, Brun NC, Begtrup K, Broderick J, Davis S, Diringer MN, et al. Efficacy and safety of recombinant activated factor VII for acute intracerebral hemorrhage. N Engl J Med. 2008;358(20):2127–37.PubMedCrossRefGoogle Scholar
  6. 6.
    Adeoye O, Broderick JP. Advances in the management of intracerebral hemorrhage. Nat Rev Neurol. 2010;6(11):593–601.PubMedCrossRefGoogle Scholar
  7. 7.
    Morgenstern LB, Hemphill JC, 3rd, Anderson C, Becker K, Broderick JP, Connolly ES Jr., et al. Guidelines for the management of spontaneous intracerebral hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2010;41(9):2108-2129.Google Scholar
  8. 8.
    O’Collins VE, Macleod MR, Donnan GA, Horky LL, van der Worp BH, Howells DW. 1,026 experimental treatments in acute stroke. Ann Neurol. 2006;59(3):467–77.PubMedCrossRefGoogle Scholar
  9. 9.
    Aronowski J, Hall CE. New horizons for primary intracerebral hemorrhage treatment: experience from preclinical studies. Neurol Res. 2005;27(3):268–79.PubMedCrossRefGoogle Scholar
  10. 10.
    Shen J, Xie L, Mao X, Zhou Y, Zhan R, Greenberg DA, et al. Neurogenesis after primary intracerebral hemorrhage in adult human brain. J Cereb Blood Flow Metab. 2008;28(8):1460–8.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Sgubin D, Aztiria E, Perin A, Longatti P, Leanza G. Activation of endogenous neural stem cells in the adult human brain following subarachnoid hemorrhage. J Neurosci Res. 2007;85(8):1647–55.PubMedCrossRefGoogle Scholar
  12. 12.
    Masuda T, Isobe Y, Aihara N, Furuyama F, Misumi S, Kim TS, et al. Increase in neurogenesis and neuroblast migration after a small intracerebral hemorrhage in rats. Neurosci Lett. 2007;425(2):114–9.PubMedCrossRefGoogle Scholar
  13. 13.
    Bang OY. Clinical trials of adult stem cell therapy in patients with ischemic stroke. J Clin Neurol. 2016;12(1):14–20.PubMedCrossRefGoogle Scholar
  14. 14.
    Lin R, Iacovitti L. Classic and novel stem cell niches in brain homeostasis and repair. Brain Res. 2015;1628(Pt B):327–42.PubMedCrossRefGoogle Scholar
  15. 15.
    Kalladka D, Muir KW. Brain repair: cell therapy in stroke. Stem Cells Clon. 2014;7:31–44.Google Scholar
  16. 16.
    Lazarov O, Hollands C. Hippocampal neurogenesis: learning to remember. Prog Neurobiol. 2016;138-140:1–18.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, et al. Neurogenesis in the adult human hippocampus. Nat Med. 1998;4(11):1313–7.PubMedCrossRefGoogle Scholar
  18. 18.
    Spalding KL, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner HB, et al. Dynamics of hippocampal neurogenesis in adult humans. Cell. 2013;153(6):1219–27.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Tang T, Li XQ, Wu H, Luo JK, Zhang HX, Luo TL. Activation of endogenous neural stem cells in experimental intracerebral hemorrhagic rat brains. Chin Med J (Engl). 2004;117(9):1342–7.Google Scholar
  20. 20.
    Jeong SW, Chu K, Jung KH, Kim SU, Kim M, Roh JK. Human neural stem cell transplantation promotes functional recovery in rats with experimental intracerebral hemorrhage. Stroke. 2003;34(9):2258–63.PubMedCrossRefGoogle Scholar
  21. 21.
    Nonaka M, Yoshikawa M, Nishimura F, Yokota H, Kimura H, Hirabayashi H, et al. Intraventricular transplantation of embryonic stem cell-derived neural stem cells in intracerebral hemorrhage rats. Neurol Res. 2004;26(3):265–72.PubMedCrossRefGoogle Scholar
  22. 22.
    Chang NK, Jeong YY, Park JS, Jeong HS, Jang S, Jang MJ, et al. Tracking of neural stem cells in rats with intracerebral hemorrhage by the use of 3T MRI. Korean J Radiol. 2008;9(3):196–204.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Lee HJ, Kim KS, Kim EJ, Choi HB, Lee KH, Park IH, et al. Brain transplantation of immortalized human neural stem cells promotes functional recovery in mouse intracerebral hemorrhage stroke model. Stem Cells. 2007;25(5):1204–12.PubMedCrossRefGoogle Scholar
  24. 24.
    Liao W, Zhong J, Yu J, Xie J, Liu Y, Du L, et al. Therapeutic benefit of human umbilical cord derived mesenchymal stromal cells in intracerebral hemorrhage rat: implications of anti-inflammation and angiogenesis. Cell Physiol Biochem. 2009;24(3-4):307–16.PubMedCrossRefGoogle Scholar
  25. 25.
    Liu AM, Lu G, Tsang KS, Li G, Wu Y, Huang ZS, et al. Umbilical cord-derived mesenchymal stem cells with forced expression of hepatocyte growth factor enhance remyelination and functional recovery in a rat intracerebral hemorrhage model. Neurosurgery. 2010;67(2):357–65. discussion 65–6.PubMedCrossRefGoogle Scholar
  26. 26.
    Chen J, Tang YX, Liu YM, Chen J, XQ H, Liu N, et al. Transplantation of adipose-derived stem cells is associated with neural differentiation and functional improvement in a rat model of intracerebral hemorrhage. CNS Neurosci Ther. 2012;18(10):847–54.PubMedCrossRefGoogle Scholar
  27. 27.
    Liang H, Yin Y, Lin T, Guan D, Ma B, Li C, et al. Transplantation of bone marrow stromal cells enhances nerve regeneration of the corticospinal tract and improves recovery of neurological functions in a collagenase-induced rat model of intracerebral hemorrhage. Mol Cells. 2013;36(1):17–24.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Bao XJ, Liu FY, Lu S, Han Q, Feng M, Wei JJ, et al. Transplantation of Flk-1+ human bone marrow-derived mesenchymal stem cells promotes behavioral recovery and anti-inflammatory and angiogenesis effects in an intracerebral hemorrhage rat model. Int J Mol Med. 2013;31(5):1087–96.PubMedCrossRefGoogle Scholar
  29. 29.
    Ding R, Lin C, Wei S, Zhang N, Tang L, Lin Y, et al. Therapeutic benefits of mesenchymal stromal cells in a rat model of hemoglobin-induced hypertensive intracerebral hemorrhage. Mol Cells. 2017;40(2):133–42.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Zhang Q, Shang X, Hao M, Zheng M, Li Y, Liang Z, et al. Effects of human umbilical cord mesenchymal stem cell transplantation combined with minimally invasive hematoma aspiration on intracerebral hemorrhage in rats. Am J Transl Res. 2015;7(11):2176–86.PubMedPubMedCentralGoogle Scholar
  31. 31.
    Suda S, Yang B, Schaar K, Xi X, Pido J, Parsha K, et al. Autologous bone marrow mononuclear cells exert broad effects on short- and long-term biological and functional outcomes in rodents with intracerebral hemorrhage. Stem Cells Dev. 2015;24(23):2756–66.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Qin J, Ma X, Qi H, Song B, Wang Y, Wen X, et al. Transplantation of induced pluripotent stem cells alleviates cerebral inflammation and neural damage in hemorrhagic stroke. PLoS One. 2015;10(6):e0129881.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Qin J, Gong G, Sun S, Qi J, Zhang H, Wang Y, et al. Functional recovery after transplantation of induced pluripotent stem cells in a rat hemorrhagic stroke model. Neurosci Lett. 2013;554:70–5.PubMedCrossRefGoogle Scholar
  34. 34.
    Ma X, Qin J, Song B, Shi C, Zhang R, Liu X, et al. Stem cell-based therapies for intracerebral hemorrhage in animal model: a meta-analysis. Neurol Sci. 2015;36(8):1311–7.PubMedCrossRefGoogle Scholar
  35. 35.
    Horgusluoglu E, Nudelman K, Nho K, Saykin AJ. Adult neurogenesis and neurodegenerative diseases: a systems biology perspective. Am J Med Genet B Neuropsychiatr Genet. 2017;174:193.CrossRefGoogle Scholar
  36. 36.
    YH Y, Narayanan G, Sankaran S, Ramasamy S, Chan SY, Lin S, et al. Purification, visualization, and molecular signature of neural stem cells. Stem Cells Dev. 2016;25(2):189–201.CrossRefGoogle Scholar
  37. 37.
    Gao Y, Wang F, Eisinger BE, Kelnhofer LE, Jobe EM, Zhao X. Integrative single-cell transcriptomics reveals molecular networks defining neuronal maturation during postnatal neurogenesis. Cereb Cortex. 2017;27:2064.PubMedGoogle Scholar
  38. 38.
    Mateo JL, van den Berg DL, Haeussler M, Drechsel D, Gaber ZB, Castro DS, et al. Characterization of the neural stem cell gene regulatory network identifies OLIG2 as a multifunctional regulator of self-renewal. Genome Res. 2015;25(1):41–56.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Ertaylan G, Okawa S, Schwamborn JC, Del Sol A. Gene regulatory network analysis reveals differences in site-specific cell fate determination in mammalian brain. Front Cell Neurosci. 2014;8:437.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Karikari TK, Aleksic J. Neurogenomics: an opportunity to integrate neuroscience, genomics and bioinformatics research in Africa. Appl Transl Genom. 2015;5:3–10.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Qureshi IA, Mehler MF. Understanding neurological disease mechanisms in the era of epigenetics. JAMA Neurol. 2013;70(6):703–10.PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Zhang JH, Badaut J, Tang J, Obenaus A, Hartman R, Pearce WJ. The vascular neural network--a new paradigm in stroke pathophysiology. Nat Rev Neurol. 2012;8(12):711–6.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Yan Y, Martin LM, Bosco DB, Bundy JL, Nowakowski RS, Sang QX, et al. Differential effects of acellular embryonic matrices on pluripotent stem cell expansion and neural differentiation. Biomaterials. 2015;73:231–42.PubMedCrossRefGoogle Scholar
  44. 44.
    Gomez-Gaviro MV, Scott CE, Sesay AK, Matheu A, Booth S, Galichet C, et al. Betacellulin promotes cell proliferation in the neural stem cell niche and stimulates neurogenesis. Proc Natl Acad Sci U S A. 2012;109(4):1317–22.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Ramirez-Castillejo C, Sanchez-Sanchez F, Andreu-Agullo C, Ferron SR, Aroca-Aguilar JD, Sanchez P, et al. Pigment epithelium-derived factor is a niche signal for neural stem cell renewal. Nat Neurosci. 2006;9(3):331–9.PubMedCrossRefGoogle Scholar
  46. 46.
    Andreu-Agullo C, Morante-Redolat JM, Delgado AC, Farinas I. Vascular niche factor PEDF modulates Notch-dependent stemness in the adult subependymal zone. Nat Neurosci. 2009;12(12):1514–23.PubMedCrossRefGoogle Scholar
  47. 47.
    Chou CH, Sinden JD, Couraud PO, Modo M. In vitro modeling of the neurovascular environment by coculturing adult human brain endothelial cells with human neural stem cells. PLoS One. 2014;9(9):e106346.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T. Identification of novel genes coding for small expressed RNAs. Science. 2001;294(5543):853–8.PubMedCrossRefGoogle Scholar
  49. 49.
    Zhang C. Novel functions for small RNA molecules. Curr Opin Mol Ther. 2009;11(6):641–51.PubMedPubMedCentralGoogle Scholar
  50. 50.
    Li X, Jin P. Roles of small regulatory RNAs in determining neuronal identity. Nat Rev Neurosci. 2010;11(5):329–38.PubMedCrossRefGoogle Scholar
  51. 51.
    Cochella L, Hobert O. Diverse functions of microRNAs in nervous system development. Curr Top Dev Biol. 2012;99:115–43.PubMedCrossRefGoogle Scholar
  52. 52.
    Lau P, Hudson LD. MicroRNAs in neural cell differentiation. Brain Res. 2010;1338:14–9.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Goldie BJ, Cairns MJ. Post-transcriptional trafficking and regulation of neuronal gene expression. Mol Neurobiol. 2012;45(1):99–108.PubMedCrossRefGoogle Scholar
  54. 54.
    Qin J, Functions XQ. application of exosomes. Acta Pol Pharm. 2014;71(4):537–43.PubMedGoogle Scholar
  55. 55.
    Faure J, Lachenal G, Court M, Hirrlinger J, Chatellard-Causse C, Blot B, et al. Exosomes are released by cultured cortical neurones. Mol Cell Neurosci. 2006;31(4):642–8.PubMedCrossRefGoogle Scholar
  56. 56.
    Taylor DD, Gercel-Taylor C. Exosomes/microvesicles: mediators of cancer-associated immunosuppressive microenvironments. Semin Immunopathol. 2011;33(5):441–54.PubMedCrossRefGoogle Scholar
  57. 57.
    Vella LJ, Greenwood DL, Cappai R, Scheerlinck JP, Hill AF. Enrichment of prion protein in exosomes derived from ovine cerebral spinal fluid. Vet Immunol Immunopathol. 2008;124(3-4):385–93.PubMedCrossRefGoogle Scholar
  58. 58.
    Bachy I, Kozyraki R, Wassef M. The particles of the embryonic cerebrospinal fluid: how could they influence brain development? Brain Res Bull. 2008;75(2-4):289–94.PubMedCrossRefGoogle Scholar
  59. 59.
    Ailawadi S, Wang X, Gu H, Fan GC. Pathologic function and therapeutic potential of exosomes in cardiovascular disease. Biochim Biophys Acta. 2015;1852(1):1–11.PubMedCrossRefGoogle Scholar
  60. 60.
    Xin H, Li Y, Buller B, Katakowski M, Zhang Y, Wang X, et al. Exosome-mediated transfer of miR-133b from multipotent mesenchymal stromal cells to neural cells contributes to neurite outgrowth. Stem Cells. 2012;30(7):1556–64.PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Morel L, Regan M, Higashimori H, Ng SK, Esau C, Vidensky S, et al. Neuronal exosomal miRNA-dependent translational regulation of astroglial glutamate transporter GLT1. J Biol Chem. 2013;288(10):7105–16.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Kucharzewska P, Christianson HC, Welch JE, Svensson KJ, Fredlund E, Ringner M, et al. Exosomes reflect the hypoxic status of glioma cells and mediate hypoxia-dependent activation of vascular cells during tumor development. Proc Natl Acad Sci U S A. 2013;110(18):7312–7.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Colombo E, Borgiani B, Verderio C, Furlan R. Microvesicles: novel biomarkers for neurological disorders. Front Physiol. 2012;3:63.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Rao P, Benito E, Fischer A. MicroRNAs as biomarkers for CNS disease. Front Mol Neurosci. 2013;6:39.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Felder RA, White MJ, Williams SM, Jose PA. Diagnostic tools for hypertension and salt sensitivity testing. Curr Opin Nephrol Hypertens. 2013;22(1):65–76.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Braccioli L, van Velthoven C, Heijnen CJ. Exosomes: a new weapon to treat the central nervous system. Mol Neurobiol. 2014;49(1):113–9.PubMedCrossRefGoogle Scholar
  67. 67.
    Li Y, Liu Z, Xin H, Chopp M. The role of astrocytes in mediating exogenous cell-based restorative therapy for stroke. Glia. 2014;62(1):1–16.PubMedCrossRefGoogle Scholar
  68. 68.
    Xin H, Li Y, Chopp M. Exosomes/miRNAs as mediating cell-based therapy of stroke. Front Cell Neurosci. 2014;8:377.PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    O’Loughlin AJ, Woffindale CA, Wood MJ. Exosomes and the emerging field of exosome-based gene therapy. Curr Gene Ther. 2012;12(4):262–74.PubMedCrossRefGoogle Scholar
  70. 70.
    Ponting CP, Oliver PL, Reik W. Evolution and functions of long noncoding RNAs. Cell. 2009;136(4):629–41.PubMedCrossRefGoogle Scholar
  71. 71.
    Clark MB, Mattick JS. Long noncoding RNAs in cell biology. Semin Cell Dev Biol. 2011;22(4):366–76.PubMedCrossRefGoogle Scholar
  72. 72.
    Qureshi IA, Mattick JS, Mehler MF. Long non-coding RNAs in nervous system function and disease. Brain Res. 2010;1338:20–35.PubMedCrossRefGoogle Scholar
  73. 73.
    Guennewig B, Cooper AA. The central role of noncoding RNA in the brain. Int Rev Neurobiol. 2014;116:153–94.PubMedCrossRefGoogle Scholar
  74. 74.
    Hallmann AL, Arauzo-Bravo MJ, Zerfass C, Senner V, Ehrlich M, Psathaki OE, et al. Comparative transcriptome analysis in induced neural stem cells reveals defined neural cell identities in vitro and after transplantation into the adult rodent brain. Stem Cell Res. 2016;16(3):776–81.PubMedCrossRefGoogle Scholar
  75. 75.
    Gao S, Tao L, Hou X, Xu Z, Liu W, Zhao K, et al. Genome-wide gene expression analyses reveal unique cellular characteristics related to the amenability of HPC/HSCs into high-quality induced pluripotent stem cells. Stem Cell Res Ther. 2016;7:40.PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Zhang Y, Wong CH, Birnbaum RY, Li G, Favaro R, Ngan CY, et al. Chromatin connectivity maps reveal dynamic promoter-enhancer long-range associations. Nature. 2013;504(7479):306–10.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Wang Y, Liu H, Lin Y, Liu G, Chu H, Zhao P, et al. Network-Based Approach to Identify Potential Targets and Drugs that Promote Neuroprotection and Neurorepair in Acute Ischemic Stroke. Sci Rep. 2017;7:40137.PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Francis F, Koulakoff A, Boucher D, Chafey P, Schaar B, Vinet MC, et al. Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron. 1999;23(2):247–56.PubMedCrossRefGoogle Scholar
  79. 79.
    Gleeson JG, Lin PT, Flanagan LA, Walsh CA. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron. 1999;23(2):257–71.PubMedCrossRefGoogle Scholar
  80. 80.
    Nacher J, Crespo C, McEwen BS. Doublecortin expression in the adult rat telencephalon. Eur J Neurosci. 2001;14(4):629–44.PubMedCrossRefGoogle Scholar
  81. 81.
    Sherafat MA, Heibatollahi M, Mongabadi S, Moradi F, Javan M, Ahmadiani A. Electromagnetic field stimulation potentiates endogenous myelin repair by recruiting subventricular neural stem cells in an experimental model of white matter demyelination. J Mol Neurosci. 2012;48(1):144–53.PubMedCrossRefGoogle Scholar
  82. 82.
    Cuccurazzu B, Leone L, Podda MV, Piacentini R, Riccardi E, Ripoli C, et al. Exposure to extremely low-frequency (50 Hz) electromagnetic fields enhances adult hippocampal neurogenesis in C57BL/6 mice. Exp Neurol. 2010;226(1):173–82.PubMedCrossRefGoogle Scholar
  83. 83.
    Arias-Carrion O, Verdugo-Diaz L, Feria-Velasco A, Millan-Aldaco D, Gutierrez AA, Hernandez-Cruz A, et al. Neurogenesis in the subventricular zone following transcranial magnetic field stimulation and nigrostriatal lesions. J Neurosci Res. 2004;78(1):16–28.PubMedCrossRefGoogle Scholar
  84. 84.
    Zhao C, Sun G, Li S, Shi Y. A feedback regulatory loop involving microRNA-9 and nuclear receptor TLX in neural stem cell fate determination. Nat Struct Mol Biol. 2009;16(4):365–71.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Cremisi F. MicroRNAs and cell fate in cortical and retinal development. Front Cell Neurosci. 2013;7:141.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Perruisseau-Carrier C, Jurga M, Forraz N, McGuckin CP. miRNAs stem cell reprogramming for neuronal induction and differentiation. Mol Neurobiol. 2011;43(3):215–27.PubMedCrossRefGoogle Scholar
  87. 87.
    Brett JO, Renault VM, Rafalski VA, Webb AE, Brunet A. The microRNA cluster miR-106b~25 regulates adult neural stem/progenitor cell proliferation and neuronal differentiation. Aging. 2011;3(2):108–24.PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Peck B, Schulze A. A role for the cancer-associated miR-106b~25 cluster in neuronal stem cells. Aging. 2011;3(4):329–31.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Liu H, Han XH, Chen H, Zheng CX, Yang Y, Huang XL. Repetitive magnetic stimulation promotes neural stem cells proliferation by upregulating MiR-106b in vitro. J Huazhong Univ Sci Technolog Med Sci. 2015;35(5):766–72.PubMedCrossRefGoogle Scholar
  90. 90.
    Luo J, Hu X, Zhang L, Li L, Zheng H, Li M, et al. Physical exercise regulates neural stem cells proliferation and migration via SDF-1alpha/CXCR4 pathway in rats after ischemic stroke. Neurosci Lett. 2014;578:203–8.PubMedCrossRefGoogle Scholar
  91. 91.
    Morris DC, Chopp M, Zhang L, Lu M, Zhang ZG. Thymosin beta4 improves functional neurological outcome in a rat model of embolic stroke. Neuroscience. 2010;169(2):674–82.PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Leone L, Fusco S, Mastrodonato A, Piacentini R, Barbati SA, Zaffina S, et al. Epigenetic modulation of adult hippocampal neurogenesis by extremely low-frequency electromagnetic fields. Mol Neurobiol. 2014;49(3):1472–86.PubMedCrossRefGoogle Scholar
  93. 93.
    Bai G, Sheng N, Xie Z, Bian W, Yokota Y, Benezra R, et al. Id sustains Hes1 expression to inhibit precocious neurogenesis by releasing negative autoregulation of Hes1. Dev Cell. 2007;13(2):283–97.PubMedCrossRefGoogle Scholar
  94. 94.
    Hatakeyama J, Kageyama R. Retinal cell fate determination and bHLH factors. Semin Cell Dev Biol. 2004;15(1):83–9.PubMedCrossRefGoogle Scholar
  95. 95.
    Ishibashi M, Ang SL, Shiota K, Nakanishi S, Kageyama R, Guillemot F. Targeted disruption of mammalian hairy and Enhancer of split homolog-1 (HES-1) leads to up-regulation of neural helix-loop-helix factors, premature neurogenesis, and severe neural tube defects. Genes Dev. 1995;9(24):3136–48.PubMedCrossRefGoogle Scholar
  96. 96.
    Tomita K, Nakanishi S, Guillemot F, Kageyama R. Mash1 promotes neuronal differentiation in the retina. Genes Cells. 1996;1(8):765–74.PubMedCrossRefGoogle Scholar
  97. 97.
    Jessberger S. Neural repair in the adult brain. F1000Res. 2016;5:F1000 Faculty Rev-169.PubMedPubMedCentralGoogle Scholar
  98. 98.
    Hemphill JC, Andrews P, De Georgia M. Multimodal monitoring and neurocritical care bioinformatics. Nat Rev Neurol. 2011;7(8):451–60.PubMedCrossRefGoogle Scholar
  99. 99.
    White TE, Ford BD. Gene interaction hierarchy analysis can be an effective tool for managing big data related to unilateral traumatic brain injury. In: Kobeissy FH, editor. Brain neurotrauma: molecular, neuropsychological, and rehabilitation aspects. Boca Raton, FL: Frontiers in Neuroengineering; 2015.Google Scholar

Copyright information

© Springer International Publishing AG 2018

Authors and Affiliations

  1. 1.Department of Neurosurgery, Southwest HospitalThird Military Medical UniversityChongqingChina
  2. 2.Department of NeurosurgeryThe 184th Hospital of People’s Liberation ArmyYingtan, CityChina

Personalised recommendations