FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Journal of molecular neuroscience : MN2016; 61(1); 61-78; doi: 10.1007/s12031-016-0805-9

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

Abstract: 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.
Get Full Text
Publication Date: 2016-08-15 PubMed ID: 27525635DOI: 10.1007/s12031-016-0805-9Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research investigates the development of the central nervous system in horses during embryonic/fetal development, specifically from 19 to 115 days of pregnancy. They tracked the expression of two biomarkers, Nestin and GFAP, in the neuronal system during this development.

Research Methodology:

  • The researchers tracked the development of the central nervous system (CNS) of the equine embryo/fetus from day 19 to day 115 of pregnancy.
  • During this timeframe, they observed the expression of two important biomarkers, Nestin and Glial fibrillary acid protein (GFAP), in the main structure of the nervous system responsible for neurogenesis, and in the choroid plexus.
  • These biomarkers were chosen because of their known relevance in the development of the CNS. Nestin is known as a stem/progenitor cell marker implicated in CNS development, while GFAP is a type III intermediate filament protein that is expressed by numerous cell types of the CNS and is used as a marker to distinguish astrocytes from other glial cells.

Findings:

  • The researchers observed that, on the 29th day of pregnancy, many cells in the undifferentiated lateral ventricle wall express Nestin, while few express GFAP.
  • By day 60 of pregnancy, after differentiation of the lateral ventricle wall zones, the subventricular zone, which initially had more Nestin cells, begins to have more GFAP cells.
  • By day 90 of pregnancy, an increased number of GFAP cells could be observed in the subventricular zone, indicating an upregulation of GFAP expression.
  • These changes reflect the dynamic interactions between these two biomarkers and suggest a down-regulation of Nestin expression and up-regulation of GFAP expression during equine CNS development.
  • The research also found a similar pattern of Nestin and GFAP cells expression during the development of the choroid plexus, a network of cells that produce cerebrospinal fluid in the brain.

Conclusions

  • This research adds new insights into the biological processes involved in the organogenesis of the equine CNS. It demonstrates, for the first time, the detailed chronological aspects of equine CNS organogenesis linked with the down-regulation of Nestin and the up-regulation of GFAP expression.
  • The findings of this research could potentially have significant implications for understanding and addressing developmental and neurological disorders in horses.

Cite This Article

APA
Rigoglio NN, Barreto RS, Favaron PO, Jacob JC, Smith LC, Gastal MO, Gastal EL, Miglino MA. (2016). Central Nervous System and Vertebrae Development in Horses: a Chronological Study with Differential Temporal Expression of Nestin and GFAP. J Mol Neurosci, 61(1), 61-78. https://doi.org/10.1007/s12031-016-0805-9

Publication

Journal of molecular neuroscience : MN
ISSN: 1559-1166
NlmUniqueID: 9002991
Country: United States
Language: English
Volume: 61
Issue: 1
Pages: 61-78

Researcher Affiliations

Rigoglio, Nathia N
  • Department of Surgery, School of Veterinary Medicine and Animal Science, University of Sao Paulo, Sao Paulo, Brazil.
Barreto, Rodrigo S N
  • Department of Surgery, School of Veterinary Medicine and Animal Science, University of Sao Paulo, Sao Paulo, Brazil.
Favaron, Phelipe O
  • Department of Surgery, School of Veterinary Medicine and Animal Science, University of Sao Paulo, Sao Paulo, Brazil.
Jacob, Júlio C F
  • Department of Reproduction and Animal Evaluation, Federal Rural University of Rio de Janeiro, Seropedica, Rio de Janeiro, Brazil.
Smith, Lawrence C
  • Department of Veterinary Biomedicine, Centre de Recherche en Reproduction Animale, Faculty of Veterinary Medicine, University of Montreal, Saint-Hyacinthe, QC, Canada.
Gastal, Melba O
  • Department of Animal Science, Food and Nutrition, Southern Illinois University, Carbondale, IL, USA.
Gastal, Eduardo L
  • Department of Animal Science, Food and Nutrition, Southern Illinois University, Carbondale, IL, USA.
Miglino, Maria Angélica
  • Department of Surgery, School of Veterinary Medicine and Animal Science, University of Sao Paulo, Sao Paulo, Brazil. miglino@usp.br.

MeSH Terms

  • Animals
  • Brain / embryology
  • Brain / metabolism
  • Female
  • Gene Expression Regulation, Developmental
  • Glial Fibrillary Acidic Protein / genetics
  • Glial Fibrillary Acidic Protein / metabolism
  • Horses / embryology
  • Horses / metabolism
  • Nestin / genetics
  • Nestin / metabolism
  • Neurogenesis
  • Pregnancy
  • Spine / embryology
  • Spine / metabolism

References

This article includes 113 references
  1. Sahin Kaya S, Mahmood A, Li Y, Yavuz E, Chopp M. Expression of nestin after traumatic brain injury in rat brain.. Brain Res 1999 Sep 4;840(1-2):153-7.
    pubmed: 10517963doi: 10.1016/s0006-8993(99)01757-6google scholar: lookup
  2. Romanko MJ, Rola R, Fike JR, Szele FG, Dizon ML, Felling RJ, Brazel CY, Levison SW. Roles of the mammalian subventricular zone in cell replacement after brain injury.. Prog Neurobiol 2004 Oct;74(2):77-99.
    pubmed: 15518954doi: 10.1016/j.pneurobio.2004.07.001google scholar: lookup
  3. Chesnut RM. The management of severe traumatic brain injury.. Emerg Med Clin North Am 1997 Aug;15(3):581-604.
    pubmed: 9255134doi: 10.1016/s0733-8627(05)70319-9google scholar: lookup
  4. Nakagawa T, Miyamoto O, Janjua NA, Auer RN, Nagao S, Itano T. Localization of nestin in amygdaloid kindled rat: an immunoelectron microscopic study.. Can J Neurol Sci 2004 Nov;31(4):514-9.
    pubmed: 15595259doi: 10.1017/s0317167100003747google scholar: lookup
  5. Frederiksen K, McKay RD. Proliferation and differentiation of rat neuroepithelial precursor cells in vivo.. J Neurosci 1988 Apr;8(4):1144-51.
    pubmed: 3357014doi: 10.1523/JNEUROSCI.08-04-01144.1988google scholar: lookup
  6. Evans HE, Sack WO. Prenatal development of domestic and laboratory mammals: growth curves, external features and selected references.. Zentralbl Veterinarmed C 1973 Mar;2(1):11-45.
    pubmed: 4745140doi: 10.1111/j.1439-0264.1973.tb00253.xgoogle scholar: lookup
  7. Maherali N, Hochedlinger K. Guidelines and techniques for the generation of induced pluripotent stem cells.. Cell Stem Cell 2008 Dec 4;3(6):595-605.
    pubmed: 19041776doi: 10.1016/j.stem.2008.11.008google scholar: lookup
  8. Aquino DA, Padin C, Perez JM, Peng D, Lyman WD, Chiu FC. 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 1996 Jan 22;91(1):1-10.
    pubmed: 8821474doi: 10.1016/0165-3806(95)00146-8google scholar: lookup
  9. MacKay RJ. Brain injury after head trauma: pathophysiology, diagnosis, and treatment.. Vet Clin North Am Equine Pract 2004 Apr;20(1):199-216.
    pubmed: 15062465doi: 10.1016/j.cveq.2003.11.006google scholar: lookup
  10. Soriano E, Cobas A, Fairén A. Neurogenesis of glutamic acid decarboxylase immunoreactive cells in the hippocampus of the mouse. I: Regio superior and regio inferior.. J Comp Neurol 1989 Mar 22;281(4):586-602.
    pubmed: 2708583doi: 10.1002/cne.902810408google scholar: lookup
  11. Wiese C, Rolletschek A, Kania G, Blyszczuk P, Tarasov KV, Tarasova Y, Wersto RP, Boheler KR, Wobus AM. Nestin expression--a property of multi-lineage progenitor cells?. Cell Mol Life Sci 2004 Oct;61(19-20):2510-22.
    pubmed: 15526158doi: 10.1007/s00018-004-4144-6google scholar: lookup
  12. Johnson VE, Stewart W, Smith DH. Axonal pathology in traumatic brain injury.. Exp Neurol 2013 Aug;246:35-43.
    pubmed: 22285252doi: 10.1016/j.expneurol.2012.01.013google scholar: lookup
  13. Schöler HR, Ruppert S, Suzuki N, Chowdhury K, Gruss P. New type of POU domain in germ line-specific protein Oct-4.. Nature 1990 Mar 29;344(6265):435-9.
    pubmed: 1690859doi: 10.1038/344435a0google scholar: lookup
  14. Rietze RL, Valcanis H, Brooker GF, Thomas T, Voss AK, Bartlett PF. Purification of a pluripotent neural stem cell from the adult mouse brain.. Nature 2001 Aug 16;412(6848):736-9.
    pubmed: 11507641doi: 10.1038/35089085google scholar: lookup
  15. Anderson S, Mione M, Yun K, Rubenstein JL. Differential origins of neocortical projection and local circuit neurons: role of Dlx genes in neocortical interneuronogenesis.. Cereb Cortex 1999 Sep;9(6):646-54.
    pubmed: 10498283doi: 10.1093/cercor/9.6.646google scholar: lookup
  16. Ragle CA. Head trauma.. Vet Clin North Am Equine Pract 1993 Apr;9(1):171-83.
    pubmed: 8472199doi: 10.1016/s0749-0739(17)30422-4google scholar: lookup
  17. Nakamura T, Xi G, Hua Y, Hoff JT, Keep RF. Nestin expression after experimental intracerebral hemorrhage.. Brain Res 2003 Aug 15;981(1-2):108-17.
    pubmed: 12885431doi: 10.1016/s0006-8993(03)02991-3google scholar: lookup
  18. Tramontin AD, García-Verdugo JM, Lim DA, Alvarez-Buylla A. Postnatal development of radial glia and the ventricular zone (VZ): a continuum of the neural stem cell compartment.. Cereb Cortex 2003 Jun;13(6):580-7.
    pubmed: 12764031doi: 10.1093/cercor/13.6.580google scholar: lookup
  19. Lumpkins KM, Bochicchio GV, Keledjian K, Simard JM, McCunn M, Scalea T. Glial fibrillary acidic protein is highly correlated with brain injury.. J Trauma 2008 Oct;65(4):778-82; discussion 782-4.
    pubmed: 18849790doi: 10.1097/TA.0b013e318185db2dgoogle scholar: lookup
  20. Altman J, Das GD. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats.. J Comp Neurol 1965 Jun;124(3):319-35.
    pubmed: 5861717doi: 10.1002/cne.901240303google scholar: lookup
  21. Li Y, Chopp M. Temporal profile of nestin expression after focal cerebral ischemia in adult rat.. Brain Res 1999 Aug 14;838(1-2):1-10.
    pubmed: 10446310doi: 10.1016/s0006-8993(99)01502-4google scholar: lookup
  22. Birse SC, Leonard RB, Coggeshall RE. Neuronal increase in various areas of the nervous system of the guppy, Lebistes.. J Comp Neurol 1980 Nov 15;194(2):291-301.
    pubmed: 7440802doi: 10.1002/cne.901940202google scholar: lookup
  23. Andressen C, Stöcker E, Klinz FJ, Lenka N, Hescheler J, Fleischmann B, Arnhold S, Addicks K. Nestin-specific green fluorescent protein expression in embryonic stem cell-derived neural precursor cells used for transplantation.. Stem Cells 2001;19(5):419-24.
    pubmed: 11553850doi: 10.1634/stemcells.19-5-419google scholar: lookup
  24. deAzevedo LC, Fallet C, Moura-Neto V, Daumas-Duport C, Hedin-Pereira C, Lent R. Cortical radial glial cells in human fetuses: depth-correlated transformation into astrocytes.. J Neurobiol 2003 Jun;55(3):288-98.
    pubmed: 12717699doi: 10.1002/neu.10205google scholar: lookup
  25. Missler U, Wiesmann M, Friedrich C, Kaps M. S-100 protein and neuron-specific enolase concentrations in blood as indicators of infarction volume and prognosis in acute ischemic stroke.. Stroke 1997 Oct;28(10):1956-60.
    pubmed: 9341703doi: 10.1161/01.str.28.10.1956google scholar: lookup
  26. Nottebohm F. Neuronal replacement in adulthood.. Ann N Y Acad Sci 1985;457:143-61.
    pubmed: 3913361doi: 10.1111/j.1749-6632.1985.tb20803.xgoogle scholar: lookup
  27. Eng LF, Ghirnikar RS, Lee YL. Glial fibrillary acidic protein: GFAP-thirty-one years (1969-2000).. Neurochem Res 2000 Oct;25(9-10):1439-51.
    pubmed: 11059815doi: 10.1023/a:1007677003387google scholar: lookup
  28. 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. Nestin- and doublecortin-positive cells reside in adult spinal cord meninges and participate in injury-induced parenchymal reaction.. Stem Cells 2011 Dec;29(12):2062-76.
    pubmed: 22038821doi: 10.1002/stem.766google scholar: lookup
  29. Götz M, Hartfuss E, Malatesta P. 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 2002 Apr;57(6):777-88.
    pubmed: 12031274doi: 10.1016/s0361-9230(01)00777-8google scholar: lookup
  30. Ernst C, Christie BR. Nestin-expressing cells and their relationship to mitotically active cells in the subventricular zones of the adult rat.. Eur J Neurosci 2005 Dec;22(12):3059-66.
    pubmed: 16367772doi: 10.1111/j.1460-9568.2005.04499.xgoogle scholar: lookup
  31. Raymond PA, Easter SS Jr. Postembryonic growth of the optic tectum in goldfish. I. Location of germinal cells and numbers of neurons produced.. J Neurosci 1983 May;3(5):1077-91.
    pubmed: 6842282doi: 10.1523/JNEUROSCI.03-05-01077.1983google scholar: lookup
  32. Finnie JW, Blumbergs PC. Traumatic brain injury.. Vet Pathol 2002 Nov;39(6):679-89.
    pubmed: 12450198doi: 10.1354/vp.39-6-679google scholar: lookup
  33. Gould E, Reeves AJ, Graziano MS, Gross CG. Neurogenesis in the neocortex of adult primates.. Science 1999 Oct 15;286(5439):548-52.
    pubmed: 10521353doi: 10.1126/science.286.5439.548google scholar: lookup
  34. Bakay RA, Ward AA Jr. Enzymatic changes in serum and cerebrospinal fluid in neurological injury.. J Neurosurg 1983 Jan;58(1):27-37.
    pubmed: 6847906doi: 10.3171/jns.1983.58.1.0027google scholar: lookup
  35. Antanitus DS, Choi BH, Lapham LW. The demonstration of glial fibrillary acidic protein in the cerebrum of the human fetus by indirect immunofluorescence.. Brain Res 1976 Feb 27;103(3):613-6.
    pubmed: 766916doi: 10.1016/0006-8993(76)90464-9google scholar: lookup
  36. Doetsch F, Caillé I, Lim DA, García-Verdugo JM, Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain.. Cell 1999 Jun 11;97(6):703-16.
    pubmed: 10380923doi: 10.1016/s0092-8674(00)80783-7google scholar: lookup
  37. Kim J, Efe JA, Zhu S, Talantova M, Yuan X, Wang S, Lipton SA, Zhang K, Ding S. Direct reprogramming of mouse fibroblasts to neural progenitors.. Proc Natl Acad Sci U S A 2011 May 10;108(19):7838-43.
    pubmed: 21521790doi: 10.1073/pnas.1103113108google scholar: lookup
  38. Schöler HR. Octamania: the POU factors in murine development.. Trends Genet 1991 Oct;7(10):323-9.
    pubmed: 1781030doi: 10.1016/0168-9525(91)90422-mgoogle scholar: lookup
  39. You H, Kim YI, Im SY, Suh-Kim H, Paek SH, Park SH, Kim DG, Jung HW. Immunohistochemical study of central neurocytoma, subependymoma, and subependymal giant cell astrocytoma.. J Neurooncol 2005 Aug;74(1):1-8.
    pubmed: 16078101doi: 10.1007/s11060-004-2354-2google scholar: lookup
  40. Parker K, Pilkington GJ. Morphological, immunocytochemical and flow cytometric in vitro characterisation of a surface-adherent medulloblastoma.. Anticancer Res 2005 Nov-Dec;25(6B):3855-63.
    pubmed: 16309171
  41. Lothian C, Lendahl U. 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 1997 Mar;9(3):452-62.
    pubmed: 9104587doi: 10.1111/j.1460-9568.1997.tb01622.xgoogle scholar: lookup
  42. Sasaki S, Maruyama S. Immunocytochemical and ultrastructural studies of the motor cortex in amyotrophic lateral sclerosis.. Acta Neuropathol 1994;87(6):578-85.
    pubmed: 8091950doi: 10.1007/BF00293318google scholar: lookup
  43. Acker DA, Curran S, Bersu ET, Ginther OJ. Morphologic stages of the equine embryo proper on days 17 to 40 after ovulation.. Am J Vet Res 2001 Sep;62(9):1358-64.
    pubmed: 11560260doi: 10.2460/ajvr.2001.62.1358google scholar: lookup
  44. Holmin S, von Gertten C, Sandberg-Nordqvist AC, Lendahl U, Mathiesen T. Induction of astrocytic nestin expression by depolarization in rats.. Neurosci Lett 2001 Nov 16;314(3):151-5.
    pubmed: 11704306doi: 10.1016/s0304-3940(01)02292-3google scholar: lookup
  45. Stagaard M, Møllgård K. The developing neuroepithelium in human embryonic and fetal brain studied with vimentin-immunocytochemistry.. Anat Embryol (Berl) 1989;180(1):17-28.
    pubmed: 2476946doi: 10.1007/BF00321896google scholar: lookup
  46. Honig LS, Herrmann K, Shatz CJ. Developmental changes revealed by immunohistochemical markers in human cerebral cortex.. Cereb Cortex 1996 Nov-Dec;6(6):794-806.
    pubmed: 8922336doi: 10.1093/cercor/6.6.794google scholar: lookup
  47. Gage FH. Neurogenesis in the adult brain.. J Neurosci 2002 Feb 1;22(3):612-3.
    pubmed: 11826087doi: 10.1523/JNEUROSCI.22-03-00612.2002google scholar: lookup
  48. Shaw NA. The neurophysiology of concussion.. Prog Neurobiol 2002 Jul;67(4):281-344.
    pubmed: 12207973doi: 10.1016/s0301-0082(02)00018-7google scholar: lookup
  49. Bifari F, Decimo I, Chiamulera C, Bersan E, Malpeli G, Johansson J, Lisi V, Bonetti B, Fumagalli G, Pizzolo G, Krampera M. Novel stem/progenitor cells with neuronal differentiation potential reside in the leptomeningeal niche.. J Cell Mol Med 2009 Sep;13(9B):3195-208.
    pubmed: 19228261doi: 10.1111/j.1582-4934.2009.00706.xgoogle scholar: lookup
  50. Malatesta P, Hartfuss E, Götz M. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage.. Development 2000 Dec;127(24):5253-63.
    pubmed: 11076748doi: 10.1242/dev.127.24.5253google scholar: lookup
  51. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors.. Cell 2006 Aug 25;126(4):663-76.
    pubmed: 16904174doi: 10.1016/j.cell.2006.07.024google scholar: lookup
  52. Wichterle H, Garcia-Verdugo JM, Herrera DG, Alvarez-Buylla A. Young neurons from medial ganglionic eminence disperse in adult and embryonic brain.. Nat Neurosci 1999 May;2(5):461-6.
    pubmed: 10321251doi: 10.1038/8131google scholar: lookup
  53. Shen Q, Wang Y, Kokovay E, Lin G, Chuang SM, Goderie SK, Roysam B, Temple S. Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions.. Cell Stem Cell 2008 Sep 11;3(3):289-300.
    pubmed: 18786416doi: 10.1016/j.stem.2008.07.026google scholar: lookup
  54. Hartfuss E, Galli R, Heins N, Götz M. Characterization of CNS precursor subtypes and radial glia.. Dev Biol 2001 Jan 1;229(1):15-30.
    pubmed: 11133151doi: 10.1006/dbio.2000.9962google scholar: lookup
  55. 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 Jul 1;17(13):5046-61.
    pubmed: 9185542doi: 10.1523/JNEUROSCI.17-13-05046.1997google scholar: lookup
  56. DeGiorgio LA, Sheu KF, Blass JP. Culture from human leptomeninges of cells containing neurofilament protein and neuron-specific enolase.. J Neurol Sci 1994 Jul;124(2):141-8.
    pubmed: 7964864doi: 10.1016/0022-510x(94)90319-0google scholar: lookup
  57. Bayer SA, Yackel JW, Puri PS. Neurons in the rat dentate gyrus granular layer substantially increase during juvenile and adult life.. Science 1982 May 21;216(4548):890-2.
    pubmed: 7079742doi: 10.1126/science.7079742google scholar: lookup
  58. Ingebrigtsen T, Romner B. Biochemical serum markers for brain damage: a short review with emphasis on clinical utility in mild head injury.. Restor Neurol Neurosci 2003;21(3-4):171-6.
    pubmed: 14530579
  59. Zupanc GK. Neurogenesis, cell death and regeneration in the adult gymnotiform brain.. J Exp Biol 1999 May;202(Pt 10):1435-46.
    pubmed: 10210684doi: 10.1242/jeb.202.10.1435google scholar: lookup
  60. Tyler CM, Davis RE, Begg AP, Hutchins DR, Hodgson DR. A survey of neurological diseases in horses.. Aust Vet J 1993 Dec;70(12):445-9.
    pubmed: 8117210doi: 10.1111/j.1751-0813.1993.tb00846.xgoogle scholar: lookup
  61. Halfter W, Dong S, Yip YP, Willem M, Mayer U. A critical function of the pial basement membrane in cortical histogenesis.. J Neurosci 2002 Jul 15;22(14):6029-40.
    pubmed: 12122064doi: 10.1523/JNEUROSCI.22-14-06029.2002google scholar: lookup
  62. Mokuno K, Kamholz J, Behrman T, Black C, Sessa M, Feinstein D, Lee V, Pleasure D. Neuronal modulation of Schwann cell glial fibrillary acidic protein (GFAP).. J Neurosci Res 1989 Aug;23(4):396-405.
    pubmed: 2769798doi: 10.1002/jnr.490230405google scholar: lookup
  63. Doetsch F. The glial identity of neural stem cells.. Nat Neurosci 2003 Nov;6(11):1127-34.
    pubmed: 14583753doi: 10.1038/nn1144google scholar: lookup
  64. Hockfield S, McKay RD. Identification of major cell classes in the developing mammalian nervous system.. J Neurosci 1985 Dec;5(12):3310-28.
    pubmed: 4078630doi: 10.1523/JNEUROSCI.05-12-03310.1985google scholar: lookup
  65. Middeldorp J, Boer K, Sluijs JA, De Filippis L, Encha-Razavi F, Vescovi AL, Swaab DF, Aronica E, Hol EM. GFAPdelta in radial glia and subventricular zone progenitors in the developing human cortex.. Development 2010 Jan;137(2):313-21.
    pubmed: 20040497doi: 10.1242/dev.041632google scholar: lookup
  66. Neuberger TJ, Cornbrooks CJ. Transient modulation of Schwann cell antigens after peripheral nerve transection and subsequent regeneration.. J Neurocytol 1989 Oct;18(5):695-710.
    pubmed: 2515258doi: 10.1007/BF01187088google scholar: lookup
  67. Cattaneo E, McKay R. Proliferation and differentiation of neuronal stem cells regulated by nerve growth factor.. Nature 1990 Oct 25;347(6295):762-5.
    pubmed: 2172829doi: 10.1038/347762a0google scholar: lookup
  68. Sarnat HB. Regional differentiation of the human fetal ependyma: immunocytochemical markers.. J Neuropathol Exp Neurol 1992 Jan;51(1):58-75.
    pubmed: 1371311doi: 10.1097/00005072-199201000-00008google scholar: lookup
  69. Noctor SC, Flint AC, Weissman TA, Wong WS, Clinton BK, Kriegstein AR. Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia.. J Neurosci 2002 Apr 15;22(8):3161-73.
    pubmed: 11943818doi: 10.1523/JNEUROSCI.22-08-03161.2002google scholar: lookup
  70. Lothian C, Prakash N, Lendahl U, Wahlström GM. Identification of both general and region-specific embryonic CNS enhancer elements in the nestin promoter.. Exp Cell Res 1999 May 1;248(2):509-19.
    pubmed: 10222142doi: 10.1006/excr.1999.4417google scholar: lookup
  71. Nottebohm F. From bird song to neurogenesis.. Sci Am 1989 Feb;260(2):74-9.
    pubmed: 2643827doi: 10.1038/scientificamerican0289-74google scholar: lookup
  72. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke.. Nat Med 2002 Sep;8(9):963-70.
    pubmed: 12161747doi: 10.1038/nm747google scholar: lookup
  73. Almqvist PM, Mah R, Lendahl U, Jacobsson B, Hendson G. Immunohistochemical detection of nestin in pediatric brain tumors.. J Histochem Cytochem 2002 Feb;50(2):147-58.
    pubmed: 11799134doi: 10.1177/002215540205000203google scholar: lookup
  74. Kempermann G, Gage FH. Neurogenesis in the adult hippocampus.. Novartis Found Symp 2000;231:220-35; discussion 235-41, 302-6.
    pubmed: 11131541
  75. Mitchener A, Wyper DJ, Patterson J, Hadley DM, Wilson JT, Scott LC, Jones M, Teasdale GM. SPECT, CT, and MRI in head injury: acute abnormalities followed up at six months.. J Neurol Neurosurg Psychiatry 1997 Jun;62(6):633-6.
    pubmed: 9219753doi: 10.1136/jnnp.62.6.633google scholar: lookup
  76. 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 XC, Dave JR, Schmid K, Tortella F, Robertson CS, Wang KK. Human traumatic brain injury induces autoantibody response against glial fibrillary acidic protein and its breakdown products.. PLoS One 2014;9(3):e92698.
    pubmed: 24667434doi: 10.1371/journal.pone.0092698google scholar: lookup
  77. Liu X, Bolteus AJ, Balkin DM, Henschel O, Bordey A. GFAP-expressing cells in the postnatal subventricular zone display a unique glial phenotype intermediate between radial glia and astrocytes.. Glia 2006 Oct;54(5):394-410.
    pubmed: 16886203doi: 10.1002/glia.20392google scholar: lookup
  78. Fukuda S, Kato F, Tozuka Y, Yamaguchi M, Miyamoto Y, Hisatsune T. Two distinct subpopulations of nestin-positive cells in adult mouse dentate gyrus.. J Neurosci 2003 Oct 15;23(28):9357-66.
    pubmed: 14561863doi: 10.1523/JNEUROSCI.23-28-09357.2003google scholar: lookup
  79. López-García C, Molowny A, Martínez-Guijarro FJ, Blasco-Ibáñez JM, Luis de la Iglesia JA, Bernabeu A, García-Verdugo JM. Lesion and regeneration in the medial cerebral cortex of lizards.. Histol Histopathol 1992 Oct;7(4):725-46.
    pubmed: 1457995
  80. Zhao M, Momma S, Delfani K, Carlen M, Cassidy RM, Johansson CB, Brismar H, Shupliakov O, Frisen J, Janson AM. Evidence for neurogenesis in the adult mammalian substantia nigra.. Proc Natl Acad Sci U S A 2003 Jun 24;100(13):7925-30.
    pubmed: 12792021doi: 10.1073/pnas.1131955100google scholar: lookup
  81. Zhu H, Wang ZY, Hansson HA. Visualization of proliferating cells in the adult mammalian brain with the aid of ribonucleotide reductase.. Brain Res 2003 Jul 11;977(2):180-9.
    pubmed: 12834878doi: 10.1016/s0006-8993(03)02627-1google scholar: lookup
  82. Pesce M, Schöler HR. Oct-4: gatekeeper in the beginnings of mammalian development.. Stem Cells 2001;19(4):271-8.
    pubmed: 11463946doi: 10.1634/stemcells.19-4-271google scholar: lookup
  83. Rosner MH, Vigano MA, Ozato K, Timmons PM, Poirier F, Rigby PW, Staudt LM. A POU-domain transcription factor in early stem cells and germ cells of the mammalian embryo.. Nature 1990 Jun 21;345(6277):686-92.
    pubmed: 1972777doi: 10.1038/345686a0google scholar: lookup
  84. Biagiotti T, D'Amico M, Marzi I, Di Gennaro P, Arcangeli A, Wanke E, Olivotto M. Cell renewing in neuroblastoma: electrophysiological and immunocytochemical characterization of stem cells and derivatives.. Stem Cells 2006 Feb;24(2):443-53.
    pubmed: 16100002doi: 10.1634/stemcells.2004-0264google scholar: lookup
  85. Schöler HR, Dressler GR, Balling R, Rohdewohld H, Gruss P. Oct-4: a germline-specific transcription factor mapping to the mouse t-complex.. EMBO J 1990 Jul;9(7):2185-95.
    pubmed: 2357966doi: 10.1002/j.1460-2075.1990.tb07388.xgoogle scholar: lookup
  86. Parnavelas JG. The origin and migration of cortical neurones: new vistas.. Trends Neurosci 2000 Mar;23(3):126-31.
    pubmed: 10675917doi: 10.1016/s0166-2236(00)01553-8google scholar: lookup
  87. Dahlstrand J, Lardelli M, Lendahl U. 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 1995 Jan 14;84(1):109-29.
    pubmed: 7720210doi: 10.1016/0165-3806(94)00162-sgoogle scholar: lookup
  88. Okamoto K, Okazawa H, Okuda A, Sakai M, Muramatsu M, Hamada H. A novel octamer binding transcription factor is differentially expressed in mouse embryonic cells.. Cell 1990 Feb 9;60(3):461-72.
    pubmed: 1967980doi: 10.1016/0092-8674(90)90597-8google scholar: lookup
  89. Yeom YI, Fuhrmann G, Ovitt CE, Brehm A, Ohbo K, Gross M, Hübner K, Schöler HR. Germline regulatory element of Oct-4 specific for the totipotent cycle of embryonal cells.. Development 1996 Mar;122(3):881-94.
    pubmed: 8631266doi: 10.1242/dev.122.3.881google scholar: lookup
  90. Boiani M, Schöler HR. Regulatory networks in embryo-derived pluripotent stem cells.. Nat Rev Mol Cell Biol 2005 Nov;6(11):872-84.
    pubmed: 16227977doi: 10.1038/nrm1744google scholar: lookup
  91. Pesce M, Wang X, Wolgemuth DJ, Schöler H. Differential expression of the Oct-4 transcription factor during mouse germ cell differentiation.. Mech Dev 1998 Feb;71(1-2):89-98.
    pubmed: 9507072doi: 10.1016/s0925-4773(98)00002-1google scholar: lookup
  92. Marik PE, Varon J, Trask T. Management of head trauma.. Chest 2002 Aug;122(2):699-711.
    pubmed: 12171853doi: 10.1378/chest.122.2.699google scholar: lookup
  93. Kant R, Smith-Seemiller L, Isaac G, Duffy J. Tc-HMPAO SPECT in persistent post-concussion syndrome after mild head injury: comparison with MRI/CT.. Brain Inj 1997 Feb;11(2):115-24.
    pubmed: 9012944doi: 10.1080/026990597123700google scholar: lookup
  94. Messam CA, Hou J, Berman JW, Major EO. Analysis of the temporal expression of nestin in human fetal brain derived neuronal and glial progenitor cells.. Brain Res Dev Brain Res 2002 Mar 31;134(1-2):87-92.
    pubmed: 11947939doi: 10.1016/s0165-3806(01)00325-xgoogle scholar: lookup
  95. Wichterle H, Turnbull DH, Nery S, Fishell G, Alvarez-Buylla A. In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain.. Development 2001 Oct;128(19):3759-71.
    pubmed: 11585802doi: 10.1242/dev.128.19.3759google scholar: lookup
  96. Lendahl U, Zimmerman LB, McKay RD. CNS stem cells express a new class of intermediate filament protein.. Cell 1990 Feb 23;60(4):585-95.
    pubmed: 1689217doi: 10.1016/0092-8674(90)90662-xgoogle scholar: lookup
  97. Tardy M, Fages C, Le Prince G, Rolland B, Nunez J. 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 1990;265:41-52.
    pubmed: 2165732doi: 10.1007/978-1-4757-5876-4_4google scholar: lookup
  98. Krum JM, Rosenstein JM. Transient coexpression of nestin, GFAP, and vascular endothelial growth factor in mature reactive astroglia following neural grafting or brain wounds.. Exp Neurol 1999 Dec;160(2):348-60.
    pubmed: 10619552doi: 10.1006/exnr.1999.7222google scholar: lookup
  99. Cameron HA, McKay RD. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus.. J Comp Neurol 2001 Jul 9;435(4):406-17.
    pubmed: 11406822doi: 10.1002/cne.1040google scholar: lookup
  100. von Bohlen und Halbach O. Immunohistological markers for proliferative events, gliogenesis, and neurogenesis within the adult hippocampus.. Cell Tissue Res 2011 Jul;345(1):1-19.
    pubmed: 21647561doi: 10.1007/s00441-011-1196-4google scholar: lookup
  101. 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. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration.. Nature 2004 Feb 19;427(6976):740-4.
    pubmed: 14973487doi: 10.1038/nature02301google scholar: lookup
  102. Jacobs A, Put E, Ingels M, Put T, Bossuyt A. One-year follow-up of technetium-99m-HMPAO SPECT in mild head injury.. J Nucl Med 1996 Oct;37(10):1605-9.
    pubmed: 8862291
  103. Feary DJ, Magdesian KG, Aleman MA, Rhodes DM. Traumatic brain injury in horses: 34 cases (1994-2004).. J Am Vet Med Assoc 2007 Jul 15;231(2):259-66.
    pubmed: 17630894doi: 10.2460/javma.231.2.259google scholar: lookup
  104. Simonati A, Rosso T, Rizzuto N. DNA fragmentation in normal development of the human central nervous system: a morphological study during corticogenesis.. Neuropathol Appl Neurobiol 1997 Jun;23(3):203-11.
    pubmed: 9223129
  105. Itokazu Y, Kitada M, Dezawa M, Mizoguchi A, Matsumoto N, Shimizu A, Ide C. Choroid plexus ependymal cells host neural progenitor cells in the rat.. Glia 2006 Jan 1;53(1):32-42.
    pubmed: 16158416doi: 10.1002/glia.20255google scholar: lookup
  106. Chambers I, Smith A. Self-renewal of teratocarcinoma and embryonic stem cells.. Oncogene 2004 Sep 20;23(43):7150-60.
    pubmed: 15378075doi: 10.1038/sj.onc.1207930google scholar: lookup
  107. Eriksson PS, Perfilieva E, Björk-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH. Neurogenesis in the adult human hippocampus.. Nat Med 1998 Nov;4(11):1313-7.
    pubmed: 9809557doi: 10.1038/3305google scholar: lookup
  108. Bernier PJ, Bedard A, Vinet J, Levesque M, Parent A. Newly generated neurons in the amygdala and adjoining cortex of adult primates.. Proc Natl Acad Sci U S A 2002 Aug 20;99(17):11464-9.
    pubmed: 12177450doi: 10.1073/pnas.172403999google scholar: lookup
  109. Niwa H. How is pluripotency determined and maintained?. Development 2007 Feb;134(4):635-46.
    pubmed: 17215298doi: 10.1242/dev.02787google scholar: lookup
  110. Fiedorowicz A, Figiel I, Zaremba M, Dzwonek K, Oderfeld-Nowak B. 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 2008 Jan 15;56(2):209-22.
    pubmed: 18023017doi: 10.1002/glia.20605google scholar: lookup
  111. 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. Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the post-stroke adult striatum.. J Neurosci 2006 Jun 14;26(24):6627-36.
    pubmed: 16775151doi: 10.1523/JNEUROSCI.0149-06.2006google scholar: lookup
  112. Zimmerman L, Parr B, Lendahl U, Cunningham M, McKay R, Gavin B, Mann J, Vassileva G, McMahon A. Independent regulatory elements in the nestin gene direct transgene expression to neural stem cells or muscle precursors.. Neuron 1994 Jan;12(1):11-24.
    pubmed: 8292356doi: 10.1016/0896-6273(94)90148-1google scholar: lookup
  113. Kambara H, Okano H, Chiocca EA, Saeki Y. 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 2005 Apr 1;65(7):2832-9.
    pubmed: 15805284doi: 10.1158/0008-5472.CAN-04-3227google scholar: lookup

Citations

This article has been cited 4 times.
  1. Rigoglio NN, Matias GSS, Miglino MA, Mess AM, Jacob JCF, Smith LC. Morphological characteristics of mule conceptuses during early development. Anim Reprod 2018 Dec 5;15(4):1214-1222.
    doi: 10.21451/1984-3143-AR2017-0035pubmed: 34221135google scholar: lookup
  2. Arellano JI, Morozov YM, Micali N, Rakic P. Radial Glial Cells: New Views on Old Questions. Neurochem Res 2021 Oct;46(10):2512-2524.
    doi: 10.1007/s11064-021-03296-zpubmed: 33725233google scholar: lookup
  3. Wang Y, Du X, Wang D, Wang J, Du J. Effects of Bisphenol A Exposure during Pregnancy and lactation on Hippocampal Function in Newborn Rats. Int J Med Sci 2020;17(12):1751-1762.
    doi: 10.7150/ijms.47300pubmed: 32714078google scholar: lookup
  4. Meneses CS, Müller HY, Herzberg DE, Uberti B, Bustamante HA, Werner MP. Immunofluorescence characterization of spinal cord dorsal horn microglia and astrocytes in horses. PeerJ 2017;5:e3965.
    doi: 10.7717/peerj.3965pubmed: 29085760google scholar: lookup
Subscribe to our newsletter
Join 99,970 horse owners like you who receive our email updates on horse health and nutrition.