Journal of Molecular Neuroscience

, Volume 61, Issue 1, pp 61–78 | Cite as

Central Nervous System and Vertebrae Development in Horses: a Chronological Study with Differential Temporal Expression of Nestin and GFAP

  • Nathia N. Rigoglio
  • Rodrigo S. N. Barreto
  • Phelipe O. Favaron
  • Júlio C. F. Jacob
  • Lawrence C. Smith
  • Melba O. Gastal
  • Eduardo L. Gastal
  • Maria Angélica Miglino


The neural system is one of the earliest systems to develop and the last to be fully developed after birth. This study presents a detailed description of organogenesis of the central nervous system (CNS) at equine embryonic/fetal development between 19 and 115 days of pregnancy. The expression of two important biomarkers in the main structure of the nervous system responsible for neurogenesis in the adult individual, and in the choroid plexus, was demonstrated by Nestin and glial fibrillary acid protein (GFAP) co-labeling. In the 29th day of pregnancy in the undifferentiated lateral ventricle wall, the presence of many cells expressing Nestin and few expressing GFAP was observed. After the differentiation of the lateral ventricle wall zones at 60 days of pregnancy, the subventricular zone, which initially had greater number of Nestin+ cells, began to show higher numbers of GFAP+ cells at 90 days of pregnancy. A similar pattern was observed for Nestin+ and GFAP+ cells during development of the choroid plexus. This study demonstrates, for the first time, detailed chronological aspects of the equine central nervous system organogenesis associated with downregulation of Nestin and upregulation of GFAP expression.


Neurodevelopment Equine Fetal brain development Spinal cord Nerves Ganglia Head trauma 



The authors are grateful to Andre L. R. Franciolli for producing some pictures and to Rosangela F. Rodrigues, Márcio N. Rodrigues, and Rafael C. Carvalho for helping during processing of the collected materials.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflicts of interests.


  1. Acker DA, Curran S, Bersu ET, Ginther OJ (2001) Morphologic stages of the equine embryo proper on days 17 to 40 after ovulation. Am J Vet Res 62:1358–1364PubMedCrossRefGoogle Scholar
  2. Almqvist PM, Mah R, Lendahl U, Jacobsson B, Hendson G (2002) Immunohistochemical detection of nestin in pediatric brain tumors. J Histochem Cytochem 50:147–158PubMedCrossRefGoogle Scholar
  3. Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319–335PubMedCrossRefGoogle Scholar
  4. Anderson R, McLean J (2005) Biomechanics of closed head injury. In: Reilly PL, Bullock R (eds) Head injury, pathophysiology and management. Hodder Arnold, London, pp. 26–31CrossRefGoogle Scholar
  5. Anderson S, Mione M, Yun K, Rubenstein JL (1999) Differential origins of neocortical projection and local circuit neurons: a role of Dix genes in neocortical interneurogenesis. Cereb Cortex 9:646–654PubMedCrossRefGoogle Scholar
  6. Andressen C, Stöcker E, Klinz FJ, Lenka N, Hescheler J, Fleischmann B, Arnhold S, Addicks K (2001) Nestin-specific green fluorescent protein expression in embryonic stem cell-derived neural precursor cells used for transplantation. Stem Cells 19:419–424PubMedCrossRefGoogle Scholar
  7. Antanitus DS, Choi BH, Lapham LW (1976) The demonstration of glial fibrillary acidic protein in the cerebrum of the human fetus by indirect immunofluorescence. Brain Res 103:613–616PubMedCrossRefGoogle Scholar
  8. Aquino DA, Padin C, Perez JM, Peng D, Lyman WD, Chiu FC (1996) Analysis of glial fibrillary acidic protein, neurofilament protein, actin and heat shock proteins in human fetal brain during the second trimester. Brain Res Dev Brain Res 91:1–10PubMedCrossRefGoogle Scholar
  9. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O (2002) Neural replacement from endogenous precursors in the adult brain after stroke. Nat Med 8:963–970PubMedCrossRefGoogle Scholar
  10. Bakay RA, Ward AA Jr (1983) Enzymatic changes in serum and cerebrospinal fluid in neurological injury. J Neurosurg 58:27–37PubMedCrossRefGoogle Scholar
  11. Bayer SA, Yackel JW, Puri PS (1982) Neuronsin the rat dentate gyrus granular layer substantially increase during juvenile and adult life. Science 216:890–892PubMedCrossRefGoogle Scholar
  12. Bernier PJ, Bedard A, Vinet J, Levesque M, Parent A (2002) Newly generated neurons in the amygdala and adjoining cortex of adult primates. Proc Natl Acad Sci U S A 99:11464–11469PubMedPubMedCentralCrossRefGoogle Scholar
  13. Biagiotti T, D’Amico M, Marzi I, Di Gennaro P, Arcangeli A, Wanke E, Olivotto M (2006) Cell renewing in neuroblastoma: electrophysiological and immunocytochemical characterization of stem cells and derivatives. Stem Cells 24:443–453PubMedCrossRefGoogle Scholar
  14. Bifari F, Decimo I, Chiamulera C, Bersan E, Malpeli G, Johansson J, Lisi V, Bonetti B, Fumagalli G, Pizzolo G, Krampera M (2009) Novel stem/progenitor cells with neuronal differentiation potential reside in the leptomeningeal niche. J Cell Mol Med 13:3195–3208PubMedPubMedCentralCrossRefGoogle Scholar
  15. Birse SC, Leonard RB, Coggeshall RE (1980) Neuronal increase in various areas of the nervous system of the guppy, Lebistes. J Comp Neurol 194:291–301PubMedCrossRefGoogle Scholar
  16. Blumbergs PC (2005) Pathology. In: Reilly PL, Bullock R (eds) Head injury, pathophysiology and management. Hodder Arnold, London, pp. 41–72CrossRefGoogle Scholar
  17. Blumbergs PC, Reilly PL, Vink R (2008) Trauma. In: Louis DN, Love S, Ellison DW (eds) Greenfield’s neuropathology, vol vol. 1. Greenfield’s Neuropathology, Arnold, London, pp. 733–832Google Scholar
  18. Boiani M, Scholer HR (2005) Regulatory networks in embryo-derived pluripotent stem cells. Nat Rev Mol Cell Biol 6:872–884PubMedCrossRefGoogle Scholar
  19. Cameron HA, McKay RD (2001) Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435:406–417PubMedCrossRefGoogle Scholar
  20. Cattaneo E, McKay R (1990) Proliferation and differentiation of neuronal stem cells regulated by nerve growth factor. Nature 347:762–765PubMedCrossRefGoogle Scholar
  21. Chambers I, Smith A (2004) Self-renewal of teratocarcinoma and embryonic stem cells. Oncogene 23:7150–7160PubMedCrossRefGoogle Scholar
  22. Chesnut RM (1997) The management of severe traumatic brain injury. Emerg Med Clin North Am 15:581–604PubMedCrossRefGoogle Scholar
  23. Coumbe C (1996) Head trauma. In: Dyson S (ed) A guide to the management of emergencies at equine competitions. Equine Veterinary Journal Ltd., Newmarket, pp. 71–84Google Scholar
  24. Dahlstrand J, Lardelli M, Lendahl U (1995) Nestin mRNA expression correlates with the central nervous system progenitor cell state in many, but not all, regions of developing central nervous system. Brain Res Dev Brain Res 84:109–129PubMedCrossRefGoogle Scholar
  25. De Azevedo LC, Fallet C, Moura-Neto V, Daumas-Duport C, HedinPereira C, Lent R (2003) Cortical radial glial cells in human fetuses: depth-correlated transformation into astrocytes. J Neurobiol 3:288–298CrossRefGoogle Scholar
  26. Decimo I, Bifari F, Rodriguez FJ, Malpeli G, Dolci S, Lavarini V, Pretto S, Vasquez S, Sciancalepore M, Montalbano A, Berton V, Krampera M, Fumagalli G (2011) Nestin and double cortin-positive cells reside in adult spinal cord meninges and participate in injury-induced parenchymal reaction. Stem Cells 29:2062–2076PubMedPubMedCentralCrossRefGoogle Scholar
  27. DeGiorgio LA, Sheu KF, Blass JP (1994) Culture from human leptomeninges of cells containing neurofilament protein and neuron-specific enolase. J Neurol Sci 124:141–148PubMedCrossRefGoogle Scholar
  28. Doetsch F, García-Verdugo JM, Alvarez-Buylla A (1997) Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17:5046–5061PubMedGoogle Scholar
  29. Doetsch F, Caillé I, Lim DA, García-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703–716PubMedCrossRefGoogle Scholar
  30. Doetsch F (2003) The glial identity of neural stem cells. Nat Neurosci 6:1127–1134PubMedCrossRefGoogle Scholar
  31. Dyson S (1996) Neck trauma. In: Dyson S (ed) A guide to the management of emergencies at equine competitions. Equine Veterinary Journal Ltd., Newmarket, pp. 89–91Google Scholar
  32. Eng LF, Ghirnikar RS, Lee YL (2000) Glial fibrillary acidic protein: GFAP-thirty-one years (1969-2000). Neurochem Res 25:1439–1451PubMedCrossRefGoogle Scholar
  33. Eriksson PS, Perfilieva E, Björk-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313–1317PubMedCrossRefGoogle Scholar
  34. Ernst C, Christie BR (2005) Nestin-expressing cells and their relationship to mitotically active cells in the subventricular zones of the adult rat. Eur J Neurosci 22:3059–3066PubMedCrossRefGoogle Scholar
  35. Eurell JA, Frappier BL (2007) Dellmann’s textbook of veterinary histology, 6th edn. Blackwell, IowaGoogle Scholar
  36. Evans HE, Sack WO (1973) Prenatal development of domestic and laboratory mammals: growth curves, external features and selected references. Anat Histol Embryol 2:11–45CrossRefGoogle Scholar
  37. Feary DJ, Magdesian KG, Aleman MA, Rhodes DM (2007) Traumatic brain injury in horses: 34 cases (1994-2004). J Am Vet Med Assoc 231:259–266PubMedCrossRefGoogle Scholar
  38. Feige K, Fürst A, Kaser-Hotz B, Ossent P (2000) Traumatic injury to the central nervous system in horses: occurrence, diagnosis and outcome. Equine Vet Educ 12:220–224CrossRefGoogle Scholar
  39. Fiedorowicz A, Figiel I, Zaremba M, Dzwonek K, Oderfeld Nowak B (2008) The ameboid phenotype of NG2(+) cells in the region of apoptotic dentate granule neurons in trimethyltin intoxicated mice shares antigen properties with microglia/ macrophages. Glia 56:209–222PubMedCrossRefGoogle Scholar
  40. Finnie JW, Blumbergs PC (2002) Traumatic brain injury. Vet Pathol 39:679–689PubMedCrossRefGoogle Scholar
  41. Frederiksen K, McKay RD (1988) Proliferation and differentiation of rat neuroepithelial precursor cells in vivo. J Neurosci 8:1144–1151PubMedGoogle Scholar
  42. Fukuda S, Kato F, Tozuka Y, Yamaguchi M, Miyamoto Y, Hisatsune T (2003) Two distinct subpopulations of nestin-positive cells in adult mouse dentate gyrus. J Neurosci 23:9357–9366PubMedGoogle Scholar
  43. Gage FH (2002) Neurogenesis in the adult brain. J Neurosci 22:612–613PubMedGoogle Scholar
  44. Götz M, Hartfuss E, Malatesta P (2002) Radial glial cells as neuronal precursors: a new perspective on the correlation of morphology and lineage restriction in the developing cerebral cortex of mice. Brain Res Bull 57:777–788PubMedCrossRefGoogle Scholar
  45. Gould E, Reeves AJ, Graziano MS, Gross CG (1999) Neurogenesis in the neocortex of adult primates. Science 286:548–552PubMedCrossRefGoogle Scholar
  46. Halfter W, Dong S, Yip YP, Willem M, Mayer U (2002) A critical function of the pial basement membrane in cortical histogenesis. J Neurosci 22:6029–6040PubMedGoogle Scholar
  47. Hartfuss E, Galli R, Heins N, Götz M (2001) Characterization of CNS precursor subtypes and radial glia. Dev Biol 229:15–30PubMedCrossRefGoogle Scholar
  48. Hockfield S, McKay RD (1985) Identification of major cell classes in the developing mammalian nervous system. J Neurosci 5:3310–3328PubMedGoogle Scholar
  49. Holmin S, von Gertten C, Sandberg-Nordqvist AC, Lendahl U, Mathiesen T (2001) Induction of astrocytic nestin expression by depolarization in rats. Neurosci Lett 314:151–155PubMedCrossRefGoogle Scholar
  50. Honig LS, Herrmann K, Shatz CJ (1996) Developmental changes revealed by immunohistochemical markers in human cerebral cortex. Cereb Cortex 6:794–806PubMedCrossRefGoogle Scholar
  51. Ingebrigtsen T, Romner B (2003) Biochemical serum markers for brain damage: a short review with emphasis on clinical utility in mild head injury. Restor Neurol Neurosci 21:171–176PubMedGoogle Scholar
  52. Itokazu Y, Kitada M, Dezawa M, Mizoguchi A, Matsumoto N, Shimizu A, Ide C (2006) Choroid plexus ependymal cells host neural progenitor cells in the rat. Glia 53:32–42PubMedCrossRefGoogle Scholar
  53. Jacobs A, Put E, Ingels M, Put T, Bossuyt A (1996) One-year follow-up of technetium-99m-HMPAO SPECT in mild head injury. J Nucl Med 37:1605–1609PubMedGoogle Scholar
  54. Johnson VE, Stewart W, Smith DH (2013) Axonal pathology in traumatic brain injury. Exp Neurol 246:35–43PubMedCrossRefGoogle Scholar
  55. Kambara H, Okano H, Chiocca EA, Saeki Y (2005) An oncolytic HSV-1 mutant expressing ICP34.5 under control of a nestin promoter increases survival of animals even when symptomatic from a brain tumor. Cancer Res 65:2832–2839PubMedCrossRefGoogle Scholar
  56. Kant R, Smith-Seemiller L, Isaac G, Duffy J (1997) Tc-HMPAO SPECT in persistent post-concussion syndrome after mild head injury: comparison with MRI/CT. Brain Inj 11:115–124PubMedCrossRefGoogle Scholar
  57. Kaya SS, Mahmood A (1999) Expression of nestin after traumatic brain injury in rat brain. Brain Res 840:153–157CrossRefGoogle Scholar
  58. Kempermann G, Gage FH (2000) Neurogenesis in the adult hippocampus. Novartis Found Symp 231:220–235PubMedCrossRefGoogle Scholar
  59. Kim J, Efe JA, Zhu S, Talantova M, Yuan X, Wang S, Lipton SA, Zhang K, Ding S (2011) Direct reprogramming of mouse fibroblasts to neural progenitors. Proc Natl Acad Sci U S A 108:7838–7843PubMedPubMedCentralCrossRefGoogle Scholar
  60. Krum JM, Rosenstein JM (1999) Transient coexpression of nestin, GFAP, and vascular endothelial growth factor in mature reactive astroglia following neural grafting or brain wounds. Exp Neurol 160:348–360PubMedCrossRefGoogle Scholar
  61. Lendahl U, Zimmerman LB, McKay RD (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60:585–595PubMedCrossRefGoogle Scholar
  62. Li Y, Chopp M (1999) Temporal profile of nestin expression after focal cerebral ischemia in adult rat. Brain Res 838:1–10PubMedCrossRefGoogle Scholar
  63. Liu X, Bolteus AJ, Balkin DM, Henschel O, Bordey A (2006) GFAP-expressing cells in the postnatal subventricular zone display a unique glial phenotype intermediate between radial glia and astrocytes. Glia 54:394–410PubMedCrossRefGoogle Scholar
  64. López-García C, Molowny A, Martínez-Guijarro FJ, Blasco-Ibáñez JM, Luis de la Iglesia JA, Bernabeu A, García-Verdugo JM (1992) Lesion and regeneration in the medial cerebral córtex of lizards. Histol Histopathol 7:725–746PubMedGoogle Scholar
  65. Lothian C, Lendahl U (1997) An evolutionarily conserved region in the second intron of the human nestin gene directs gene expression to CNS progenitor cells and to early neural crest cells. Eur J Neurosci 9:452–462PubMedCrossRefGoogle Scholar
  66. Lothian C, Prakash N, Lendahl U, Wahlström GM (1999) Identification of both general and region-specific embryonic CNS enhancer elements in the nestin promoter. Exp Cell Res 248:509–519PubMedCrossRefGoogle Scholar
  67. Lumpkins KM, Bochicchio GV, Keledjian K, Simard JM, McCunn M, Scalea T (2008) Glial fibrillary acidic protein is highly correlated with brain injury. J Trauma 65:778–782PubMedCrossRefGoogle Scholar
  68. MacKay RJ (2004) Brain injury after head trauma: pathophysiology, diagnosis, and treatment. Vet Clin N Am Equine Pract 20:199–216CrossRefGoogle Scholar
  69. Maherali N, Hochedlinger K (2008) Guidelines and techniques for the generation of induced pluripotent stem cells. Cell Stem Cell 3:595–605PubMedCrossRefGoogle Scholar
  70. Malatesta P, Hartfuss E, Gotz M (2000) Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127:5253–5263PubMedGoogle Scholar
  71. Marik PE, Varon J, Trask T (2002) Management of head trauma. Chest 122:699–711PubMedCrossRefGoogle Scholar
  72. Messam CA, Hou J, Berman JW, Major EO (2002) Analysis of the temporal expression of nestin in human fetal brain derived neuronal and glial progenitor cells. Brain Res Dev Brain Res 134:87–92PubMedCrossRefGoogle Scholar
  73. Middeldorp J, Boer K, Sluijs JA, De Filippis L, Encha-Razavi F, Vescovi AL, Swaab DF, Aronica E, Hol EM (2010) GFAP delta in radial glia and subventricular zone progenitors in the developing human cortex. Development 137:313–321PubMedCrossRefGoogle Scholar
  74. Mitchener A, Wyper DJ, Patterson J, Hadley DM, Wilson JT, Scott LC, Jones M, Teasdale GM (1997) SPECT, CT, and MRI in head injury: acute abnormalities followed up at six months. J Neurol Neurosurg Psychiatry 62:633–636PubMedPubMedCentralCrossRefGoogle Scholar
  75. Missler U, Wiesmann M, Friedrich C, Kaps M (1997) S-100 protein and neuron-specific enolase concentrations in blood as indicators of infarction volume and prognosis in acute ischemic stroke. Stroke 28:1956–1960PubMedCrossRefGoogle Scholar
  76. Mokuno K, Kamholz J, Behrman T, Black C, Sessa M, Feinstein D, Lee V, Pleasure D (1989) Neuronal modulation of Schwann cell glial fibrillary acidic protein (GFAP). J Neurosci Res 23:396–405PubMedCrossRefGoogle Scholar
  77. Moore Rush B (1997) Central nervous system trauma. In: Robinson NE (ed) Current therapy in equine medicine, 4th edn. Saunders, Philadelphia, pp. 301–305Google Scholar
  78. Nakagawa T, Miyamoto O, Janjua NA, Auer RN, Nagao S, Itano T (2004) Localization of nestin in amygdaloid kindled rat: an immunoelectron microscopic study. Can J Neurol Sci 31:514–519PubMedCrossRefGoogle Scholar
  79. Nakamura T, Xi G, Hua Y, Hoff JT, Keep RF (2003) Nestin expression after experimental intracerebral hemorrhage. Brain Res 981:108–117PubMedCrossRefGoogle Scholar
  80. Neuberger TJ, Cornbrooks CJ (1989) Transient modulation of Schwann cell antigens after peripheral nerve transection and subsequent regeneration. J Neurocytol 18:695–710PubMedCrossRefGoogle Scholar
  81. Niwa H (2007) How is pluripotency determined and maintained? Development 134:635–646PubMedCrossRefGoogle Scholar
  82. Noctor SC, Flint AC, Weissman TA, Wong WS, Clinton BK, Kriegstein AR (2002) Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J Neurosci 22:3161–3173PubMedGoogle Scholar
  83. Nottebohm F (1985) Neuronal replacement in adulthood. Ann N Y Acad Sci 457:143–161PubMedCrossRefGoogle Scholar
  84. Nottebohm F (1989) From bird song to neurogenesis. Sci Am 260:74–79PubMedCrossRefGoogle Scholar
  85. Nottebohm F, Alvarez-Buylla A (1993) Neurogenesis and neuronal replacement in adult birds. In: Cuello AC (ed) Restorative neurology, vol 6. Elsevier, Amsterdam, pp. 227–236Google Scholar
  86. Okamoto K, Okazawa H, Okuda A, Sakai M, Muramatsu M, Hamada H (1990) A novel octamer binding transcription factor is differentially expressed in mouse embryonic cells. Cell 60:461–472PubMedCrossRefGoogle Scholar
  87. Parker K, Pilkington GJ (2005) Morphological, immunocytochemical and flow cytometric in vitro characterisation of a surface-adherent medulloblastoma. Anticancer Res 25:3855–3863PubMedGoogle Scholar
  88. Parnavelas JG (2000) The origin and migration of cortical neurones: new vistas. Trends Neurosci 23:126–131PubMedCrossRefGoogle Scholar
  89. Pesce M, Wang X, Wolgemuth DJ, Schöler H (1998) Differential expression of the Oct-4 transcription factor during mouse germ cell differentiation. Mech Dev 71:89–98PubMedCrossRefGoogle Scholar
  90. Pesce M, Scholer HR (2001) Oct-4: gatekeeper in the beginnings of mammalian development. Stem Cells 19:271–278PubMedCrossRefGoogle Scholar
  91. Pimentel L, Oliveira D, Galiza G, Rego R, Dantas A, Riet-Correa F (2009) Doenças do Sistema Nervoso Central de Equideos no Semi-Árido. Pesqui Vet Bras 29:589–597CrossRefGoogle Scholar
  92. Ragle CA, Koblik PD, Pascoe JR, Honnas CM (1988) Computed tomographic evaluation of head trauma in a foal. Vet Radiol 29:206–208CrossRefGoogle Scholar
  93. Ragle CA (1993) Head trauma. Vet Clin N Am Equine Pract 9:171–183Google Scholar
  94. Raymond PA, Easter SS Jr (1983) Postembryonic growth of the optic tectumin goldfish. I. Location of germinal cells and numbers of neurons produced. J Neurosci 3:1077–1091Google Scholar
  95. Rietze RL, Valcanis H, Brooker GF, Thomas T, Voss AK, Bartlett PF (2001) Purification of a pluripotent neural stem cell from the adult mouse brain. Nature 412:736–739PubMedCrossRefGoogle Scholar
  96. Romanko MJ, Rola R, Fike JR, Szele FG, Dizon ML, Felling RJ, Brazel CY, Levison SW (2004) Roles of the mammalian subventricular zone in cell replacement after brain injury. Prog Neurobiol 74:77–99PubMedCrossRefGoogle Scholar
  97. Rosner MH, Vigano MA, Ozato K, Timmons PM, Poirier F, Rigby P, Staudt LM (1990) A POU-domain transcription factor in early stem cells and germ cells of the mammalian embryo. Nature 345:686–692PubMedCrossRefGoogle Scholar
  98. Sanai N, Tramontin AD, Quiñones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, McDermott MW, Parsa AT, Manuel-García Verdugo J, Berger MS, Alvarez-Buylla A (2004) Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427:740–744PubMedCrossRefGoogle Scholar
  99. Sarnat HB (1992) Regional differentiation of the human fetal ependyma: immunocytochemical markers. J Neuropathol Exp Neurol 51:58–75PubMedCrossRefGoogle Scholar
  100. Sasaki S, Maruyama S (1994) Immunocytochemical and ultrastructural studies of the motor cortex in amyotrophic lateral sclerosis. Acta Neuropathol 87:578–585PubMedCrossRefGoogle Scholar
  101. Schöler HR, Dressler GR, Balling R, Rohdewohld H, Gruss P (1990a) Oct-4: a germline-specific transcription factor mapping to the mouse t-complex. EMBO J 9:2185–2195PubMedPubMedCentralGoogle Scholar
  102. Schöler HR, Ruppert S, Suzuki N, Chowdhury K, Gruss P (1990b) New type of POU domain in germ line-specific protein Oct-4. Nature 344:435–439PubMedCrossRefGoogle Scholar
  103. Schöler HR (1991) Octamania: the POU factors in murine development. Trends Genet 7:323–329PubMedCrossRefGoogle Scholar
  104. Shaw NA (2002) The neurophysiology of concussion. Prog Neurobiol 67:281–344PubMedCrossRefGoogle Scholar
  105. Shen Q, Wang Y, Kokovay E, Lin G, Chuang SM, Goderie SK, Roysam B, Temple S (2008) Adult SVZ stem cells lie in avascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 3:289–300PubMedPubMedCentralCrossRefGoogle Scholar
  106. Simonati A, Rosso T, Rizzuto N (1997) DNA fragmentation in normal development of the human central nervous system: a morphological study during corticogenesis. Neuropathol Appl Neurobiol 23:203–211PubMedCrossRefGoogle Scholar
  107. Soriano E, Cobas A, Fairén A (1989) Neurogenesis of glutamic acid decarboxylase immunoreactive cells in the hippocampus of the mouse. I: regio superior and regio inferior. J Comp Neurol 281:586–602PubMedCrossRefGoogle Scholar
  108. Stagaard M, Møllgård K (1989) The developing neuroepithelium in human embryonic and fetal brain studied with vimentin-immunocytochemistry. Anat Embryol (Berl) 180:17–28CrossRefGoogle Scholar
  109. Summers BA, Cummings JF, de Lahunta A (1995) Veterinary neuropathology. Mosby, St Louis, pp. 189–192Google Scholar
  110. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676PubMedCrossRefGoogle Scholar
  111. Tardy M, Fages C, Le Prince G, Rolland B, Nunez J (1990) Regulation of the glial fibrillary acidic protein (GFAP) and of its encoding mRNA in the developing brain and in cultured astrocytes. Adv Exp Med Biol 265:41–52PubMedCrossRefGoogle Scholar
  112. Tramontin AD, García-Verdugo JM, Lim DA, Alvarez-Buylla A (2003) Postnatal development of radial glia and the ventricular zone (VZ): a continuum of the neural stem cell compartment. Cereb Cortex 13:580–587PubMedCrossRefGoogle Scholar
  113. Tyler CM, Davis RE, Begg AP, Hutchins DR, Hodgson DR (1993) A survey of neurological diseases in horses. Aust Vet J 70:445–449PubMedCrossRefGoogle Scholar
  114. von Bohlen und Halbach O (2011) Immunohistological markers for proliferative events, gliogenesis, and neurogenesis within the adult hippocampus. Cell Tissue Res 345:1–19CrossRefGoogle Scholar
  115. Wichterle H, Garcia-Verdugo JM, Herrera DG, Alvarez-Buylla A (1999) Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat Neurosci 2:461–466PubMedCrossRefGoogle Scholar
  116. Wichterle H, Turnbull DH, Nery S, Fishell G, Alvarez-Buylla A (2001) In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128:3759–3771PubMedGoogle Scholar
  117. Wiese C, Rolletschek A, Kania G, Blyszczuk P, Tarasov KV, Tarasova Y, Wersto RP, Boheler KR, Wobus AM (2004) Nestin expression–a property of multi-lineage progenitor cells? Cell Mol Life Sci 61:2510–2522PubMedCrossRefGoogle Scholar
  118. Yamashita T, Ninomiya M, Hernández Acosta P, García-Verdugo JM, Sunabori T, Sakaguchi M, Adachi K, Kojima T, Hirota Y, Kawase T, Araki N, Abe K, Okano H, Sawamoto K (2006) Subventricular zone derived neuroblasts migrate and differentiate into mature neurons in th epost-stroke adult striatum. J Neurosci 26:6627–6636PubMedCrossRefGoogle Scholar
  119. Yeom YI, Fuhrmann G, Ovitt CE, Brehm A, Ohbo K, Gross M, Hubner K, Schöler HR (1996) Germline regulatory element of Oct-4 specific for the totipotent cycle of embryonal cells. Development 122:881–894PubMedGoogle Scholar
  120. You H, Kim YI, Im SY, Suh-Kim H, Paek SH, Park SH, Kim DG, Jung HW (2005) Immunohistochemical study of central neurocytoma, subependymoma, and subependymal giant cell astrocytoma. J Neuro-Oncol 74:1–8CrossRefGoogle Scholar
  121. Zhang Z, Zoltewicz JS, Mondello S, Newsom KJ, Yang Z, Yang B, Kobeissy F, Guingab J, Glushakova O, Robicsek S, Heaton S, Buki A, Hannay J, Gold MS, Rubenstein R, Lu Xi-chun M, Dave JR, Schmid K, Tortella F, Robertson CS, Wang KKW (2014) Human traumatic brain injury induces autoantibody response against glial fibrillary acidic protein and its brake down products. PLoS One 9:e92698PubMedPubMedCentralCrossRefGoogle Scholar
  122. Zhao M, Momma S, Delfani K, Carlen M, Cassidy RM, Johansson CB, Brismar H, Shupliakov O, Frisen J, Janson AM (2003) Evidence for neurogenesis in the adult mammalian substantia nigra. Proc Natl Acad Sci U S A 100:7925–7930PubMedPubMedCentralCrossRefGoogle Scholar
  123. Zhu H, Wang ZY, Hansson HA (2003) Visualization of proliferating cells in the adult mammalian brain with the aid of ribonucleotide reductase. Brain Res 977:180–189PubMedCrossRefGoogle Scholar
  124. Zimmerman L, Parr B, Lendahl U, Cunningham M, McKay R, Gavin B, Mann J, Vassileva G, McMahon A (1994) Independent regulatory elements in the nestin gene direct transgene expression to neural stem cells or muscle precursors. Neuron 12:11–24PubMedCrossRefGoogle Scholar
  125. Zupanc GK (1999) Neurogenesis, cell death and regeneration in the adult gymnotiform brain. J Exp Biol 202:1435–1446PubMedGoogle Scholar

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© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Nathia N. Rigoglio
    • 1
  • Rodrigo S. N. Barreto
    • 1
  • Phelipe O. Favaron
    • 1
  • Júlio C. F. Jacob
    • 2
  • Lawrence C. Smith
    • 3
  • Melba O. Gastal
    • 4
  • Eduardo L. Gastal
    • 4
  • Maria Angélica Miglino
    • 1
  1. 1.Department of Surgery, School of Veterinary Medicine and Animal ScienceUniversity of Sao PauloSao PauloBrazil
  2. 2.Department of Reproduction and Animal EvaluationFederal Rural University of Rio de JaneiroSeropedicaBrazil
  3. 3.Department of Veterinary Biomedicine, Centre de Recherche en Reproduction Animale, Faculty of Veterinary MedicineUniversity of MontrealSaint-HyacintheCanada
  4. 4.Department of Animal Science, Food and NutritionSouthern Illinois UniversityCarbondaleUSA

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