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Physiopathology of Foetal Onset Hydrocephalus

  • Esteban M. Rodríguez
  • Maria Montserrat Guerra
  • Eduardo Ortega
Chapter

Abstract

The cerebrospinal fluid (CSF) performs key functions for the developing central nervous system and for the adult brain. It is, indeed, a complex molecular private milieu of the brain clearing a series of compounds and conveying a wealth of signal molecules. The flow of the CSF throughout the ventricular system involves two different mechanisms: the bulk flow, driven by arterio-venous pressure gradients and arterial pulsations, and the laminar flow, driven by cilia beating of ependymal cells. Disruption of normal CSF circulation and turnover contributes to the development of many diseases. This review is aimed to bring into discussion early and new evidence concerning the brain development, ependymogenesis, and the probable mechanisms by which abnormalities in the ependymogenesis program may lead to both foetal onset hydrocephalus and abnormal neurogenesis. Evidence strongly suggests that several genetic mutations and certain foreign signals all convey into a final common pathway leading to a cell junction pathology of cells lining the ventricular walls (ventricular zone, VZ). The early disruption of the VZ of the embryonic telencephalon implies the loss of neural stem cells (NSC) and abnormal neurogenesis, while the disruption of the VZ of the Sylvius aqueduct during the perinatal period results in the loss of multiciliated ependyma, aqueduct stenosis/obliteration, alteration of the laminar, and bulk flow of CSF and hydrocephalus. These findings establish the bases for the transplantation of NSC into the ventricles of foetuses developing hydrocephalus to diminish/repair the outcomes of VZ disruption.

Keywords

Cerebrospinal fluid Congenital hydrocephalus Ependymogenesis Neurogenesis Neural stem cells Junction pathology Ventricular zone disruption Stem cells therapy 

Abbreviations

AQP4

Aquaporin 4

CSF

Cerebrospinal fluid

GW

Gestational week

NPC

Neural progenitor cell

NSC

Neural stem cells

SA

Sylvius aqueduct

SVZ

Subventricular zone

VZ

Ventricular zone

References

  1. 1.
    Adzick NS, Thom EA, Spong CY, Brock JW, Burrows PK, Johnson MP, Howell LJ, Farrell JA, Dabrowiak ME, Sutton LN, Gupta N, Tulipan NB, D’Alton ME, Farmer DL, Investigators MOMS. A randomized trial of prenatal versus postnatal repair of myelomeningocele. N Engl J Med. 2011;364:993–1000.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Afzelius BA. The immotile-cilia syndrome: a microtubule-associated defet. CRC Crit Rev Biochem. 1985;19:63–87.PubMedCrossRefPubMedCentralGoogle Scholar
  3. 3.
    Bai H, Suzuki Y, Noda T, Wu S, Kataoka K, Kitada K, Ohta M, Chou H, Ide C. Dissemination and proliferation of neural stem cells on injection into the fourth ventricle of the rat: a transplantation. J Neurosci Methods. 2003;124:181–7.PubMedCrossRefPubMedCentralGoogle Scholar
  4. 4.
    Bátiz LF, Páez P, Jiménez AJ, Rodríguez S, Wagner C, Pérez-Fígares JM, Rodríguez EM. Heterogeneous expression of hydrocephalic phenotype in the hyh mice carrying a point mutation in alpha-SNAP. Neurobiol Dis. 2006;23:152–68.PubMedCrossRefPubMedCentralGoogle Scholar
  5. 5.
    Bergsneider M, Egnor MR, Johnston M, Kranz D, Madsen JR, JP MA 2nd, Stewart C, Walker ML, Williams MA. What we don’t (but should) know about hydrocephalus. J Neurosurg. 2006;104:157–9.PubMedCrossRefPubMedCentralGoogle Scholar
  6. 6.
    Bonfanti L, Peretto P. Radial glial origin of the adult neural stem cells in the subventricular zone. Prog Neurobiol. 2007;83:24–36.PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    Boop FA. Posthemorrhagic hydrocephalus of prematurity. In: Cinalli C, Maixner WJ, Sainte-Rose C, editors. Pediatric hydrocephalus. Milan: Springer-Verlag; 2004.Google Scholar
  8. 8.
    Brazel CY, Romanko MJ, Rothstein RP, Levison SW. Roles of the mammalian subventricular zone in brain development. Prog Neurobiol. 2003;69:49–69.PubMedCrossRefPubMedCentralGoogle Scholar
  9. 9.
    Buddensiek J, Dressel A, Kowalski M, Runge U, Schroeder H, Hermann A, Kirsch M, Storch A, Sabolek M. Cerebrospinal fluid promotes survival and astroglial differentiation of adult human neural progenitor cells but inhibits proliferation and neuronal differentiation. BMC Neurosci. 2010;11:48.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Cacci E, Villa A, Parmar M, Cavallaro M, Mandahl N, Lindvall O, Martinez-Serrano A, Kokaia Z. Generation of human cortical neurons from a new immortal fetal neural stem cell line. Exp Cell Res. 2007;313:588–601.PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    Chae TH, Kim S, Marz KE, Hanson PI, Walsh CA. The hyh mutation uncovers roles for Snap in apical protein localization and control of neural cell fate. Nat Genet. 2004;36:264–70.PubMedCrossRefPubMedCentralGoogle Scholar
  12. 12.
    Chan-Paly V. Serotonin axons in the supra- and subependymal plexuses and in the leptomeninges; their roles in local alterations of cerebrospinal fluid and vasomotor activity. Brain Res. 1976;102:103–30.CrossRefGoogle Scholar
  13. 13.
    Chiasserini D, van Weering JR, Piersma SR, Pham TV, Malekzadeh A, Teunissen CE, de Wit H, Jiménez CR. Proteomic analysis of cerebrospinal fluid extracellular vesicles: a comprehensive dataset. J Proteome. 2014;106:191–204.CrossRefGoogle Scholar
  14. 14.
    Chodobski A, Szmydynger-Chodobska J. Choroid plexus: target for polypeptides and site of their synthesis. Microsc Res Tech. 2001;52:865–82.CrossRefGoogle Scholar
  15. 15.
    Cifuentes M, Rodríguez S, Pérez J, Grondona JM, Rodríguez EM, Fernández-Llebrez P. Decreased cerebrospinal fluid flow through the central canal of the spinal cord of rats immunologically deprived of Reissner’s fibre. Exp Brain Res. 1994;98:431–40.PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Cushing H. Studies in intracranial physiology and surgery: the third circulation, the hypophysis, the gliomas. Serie: Cameron-prize lecture. London: H. Milford, Oxford University Press; 1926.Google Scholar
  17. 17.
    Davis RE, Swiderski RE, Rahmouni K, Nishimura DY, Mullins RF, Agassandian K, Philp AR, Searby CC, Andrews MP, Thompson S, Berry CJ, Thedens DR, Yang B, Weiss RM, Cassell MD, Stone EM, Sheffield VC. A knockin mouse model of the Bardet-Biedl syndrome 1 M390R mutation has cilia defects, ventriculomegaly, retinopathy, and obesity. Proc Natl Acad Sci U S A. 2007;104:19422–7.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Davson H, Segal MB. Physiology of the CSF and blood–brain barriers. Boca Raton: CRC Press; 1995.Google Scholar
  19. 19.
    Del Bigio MR. Pathophysiologic consequences of hydrocephalus. Neurosurg Clin N Am. 2001;12:639–49.PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Del Bigio MR. Neuropathology and structural changes in hydrocephalus. Dev Disabil Res Rev. 2010;16:16–22.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Domínguez-Pinos MD, Páez P, Jiménez AJ, Weil B, Arráez MA, Pérez-Fígares JM, Rodríguez EM. Ependymal denudation and alterations of the subventricular zone occur in human fetuses with a moderate communicating hydrocephalus. J Neuropathol Exp Neurol. 2005;64:595–604.PubMedCrossRefGoogle Scholar
  22. 22.
    Feliciano DM, Zhang S, Nasrallah CM, Lisgo SN, Bordey A. Embryonic cerebrospinal fluid nanovesicles carry evolutionarily conserved molecules and promote neural stem cell amplification. PLoS One. 2014;9(2):e88810.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Ferland RJ, Bátiz LF, Neal J, Lian G, Bundock E, Lu J, Hsiao YC, Diamond R, Mei D, Banham AH, Brown PJ, Vanderburg CR, Joseph J, Hecht JL, Folkerth R, Guerrini R, Walsh CA, Rodríguez EM, Sheen VL. Disruption of neural progenitors along the ventricular and subventricular zones in periventricular heterotopia. Hum Mol Genet. 2009;18:497–516.PubMedCrossRefGoogle Scholar
  24. 24.
    Ganzler-Odenthal SI, Redies C. Blocking N-cadherin function disrupts the epithelial structure of differentiating neural tissue in the embryonic chicken brain. J Neurosci. 1998;18:5415–25.PubMedCrossRefGoogle Scholar
  25. 25.
    Götz M, Huttner WB. The cell biology of neurogenesis. Nat Rev Mol Cell Biol. 2005;6:777–88.PubMedCrossRefGoogle Scholar
  26. 26.
    Gould SJ, Howard S, Papadaki L. The development of ependyma in the human fetal brain: an immunohistological and electron microscopic study. Dev Brain Res. 1990;55:255–67.CrossRefGoogle Scholar
  27. 27.
    Greenstone MA, Jones RWA, Dewar A, Neville BGR, Cole PJ. Hydrocephalus and primary ciliary dyskinesia. Arch Dis Child. 1984;59:481–2.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Gross PM. Circumventricular organs and body fluids, Vol. I, II, and III. Boca Raton: CRC Press; 1987.Google Scholar
  29. 29.
    Guerra M, Henzi R, Ortloff A, Lichtin N, Vío K, Jimémez A, Dominguez-Pinos MD, González C, Jara MC, Hinostroza F, Rodríguez S, Jara M, Ortega E, Guerra F, Sival DA, den Dunnen WFA, Pérez-Figares JM, McAllister JP, Johanson CE, Rodríguez EM. Cell junction pathology of neural stem cells is associated with ventricular zone disruption, hydrocephalus, and abnormal neurogenesis. J Neuropathol Exp Neurol. 2015;74:653–71.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Guerrini R, Barba C. Malformations of cortical development and aberrant cortical networks: epileptogenesis and functional organization. J Clin Neurophysiol. 2010;27:372–9.PubMedCrossRefPubMedCentralGoogle Scholar
  31. 31.
    Hagenlocher C, Walentek P, M Ller C, Thumberger T, Feistel K. Ciliogenesis and cerebrospinal fluid flow in the developing Xenopus brain are regulated by foxj1. Cilia. 2013;2:12.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Harrington MG, Fonteh AN, Oborina E, Liao P, Cowan RP, McComb G, Chavez JN, Rush J, Biringer RG, Huhmer AF. The morphology and biochemistry of nanostructures provide evidence for synthesis and signaling functions in human cerebrospinal fluid. Cerebrospinal Fluid Res. 2009;6:10.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Henzi R, Guerra M, Vío K, González C, Herrera C, McAllister JP, Johanson C, Rodríguez EM. Neurospheres from neural stem/neural progenitor cells (NSPC) of non-hydrocephalic HTx rats produce neurons, astrocytes and multiciliated ependyma. The cerebrospinal fluid of normal and hydrocephalic rats supports such a differentiation. Cell Tissue Res. 2018;373:421–38.PubMedCrossRefGoogle Scholar
  34. 34.
    Ibañez-Tallon I, Pagenstecher A, Fliegauf M, Olbrich H, Kispert A, Ketelsen UP, North A, Heintz N, Omran H. Dysfunction of axonemal dynein heavy chain Mdnah5 inhibits ependymal flow and reveals a novel mechanism for hydrocephalus formation. Hum Mol Genet. 2004;13:2133–41.PubMedCrossRefGoogle Scholar
  35. 35.
    Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, Benveniste H, Vates GE, Deane R, Goldman SA, Nagelhus EA, Nedergaard M. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci Transl Med. 2012;4(147):147ra111.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Iliff JJ, Wang M, Zeppenfeld DM, Venkataraman A, Plog BA, Liao Y, Deane R, Nedergaard M. Cerebral arterial pulsation drives paravascular CSF-interstitial fluid exchange in the murine brain. J Neurosci. 2013;33:18190–9.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Iliff JJ, Chen MJ, Plog BA, Zeppenfeld DM, Soltero M, Yang L, Singh I, Deane R, Nedergaard M. Impairment of glymphatic pathway function promotes tau pathology after traumatic brain injury. J Neurosci. 2014;34:16180–93.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Imai F, Akimoto K, Koyama H, Miyata T, Ogawa M, Noguchi S, Sasaoka T, Noda T, Ohno S. Inactivation of aPKClambda results in the loss of adherens junctions in neuroepithelial cells without affecting neurogenesis in mouse neocortex. Development. 2006;133:1735–44.PubMedCrossRefGoogle Scholar
  39. 39.
    Jacobsen M. Developmental neurobiology. New York: Plenum; 1991.CrossRefGoogle Scholar
  40. 40.
    Jellinger G. Anatomopathology of nontumoral aqueductal stenosis. J Neurosurg Sci. 1986;30:1Y16.Google Scholar
  41. 41.
    Jiménez AJ, Tomé M, Páez P, Wagner C, Rodríguez S, Fernández-Llebrez P, Rodríguez EM, Pérez-Fígares JM. A programmed ependymal denudation precedes congenital hydrocephalus in the hyh mutant mouse. J Neuropathol Exp Neurol. 2001;60:1105–19.PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    Johanson CE, Duncan JA 3rd, Klinge PM, Brinker T, Stopa EG, Silverberg GD. Multiplicity of cerebrospinal fluid functions: new challenges in health and disease. Cerebrospinal Fluid Res. 2008;5:10.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Johansson PA. The choroid plexuses and their impact on developmental neurogenesis. Front Neurosci. 2014;8:340.PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Johnson RT, Johnson KP, Edmonds CJ. Virus-induced hydrocephalus: development of aqueductal stenosis in hamsters after mumps infection. Science. 1967;157:1066Y67.Google Scholar
  45. 45.
    Johnson AK, Gross PM. Sensory circumventricular organs and brain homeostatic pathways. FASEB J. 1993;7:678–86.PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Jones HC, Klinge PM. Hydrocephalus, 17–20th September, Hannover Germany: a conference report. Cerebrospinal Fluid Res. 2008;5:19.PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Kazanis I, Lathia J, Moss L, ffrench-Constant C. The neural stem cell microenvironment. StemBook [Internet]. Cambridge, MA: Harvard Stem Cell Institute; 2008.Google Scholar
  48. 48.
    Klezovitch O, Fernandez TE, Tapscott SJ, Vasioukhin V. Loss of cell polarity causes severe brain dysplasia in Lgl1 knockout mice. Genes Dev. 2004;18:559–71.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Krueger RC, Wu H, Zandian M, Daniel-PouRM KP, Yu JS, Sun YE. Neural progenitors populate the cerebrospinal fluid of pre-term patients with hydrocephalus. J Pediatr. 2006;148:337–40.PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Lechtreck KF, Delmotte P, Robinson ML, Sanderson MJ, Witman GB. Mutations in Hydin impair ciliary motility in mice. J Cell Biol. 2008;180:633–43.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Lee L. Riding the wave of ependymal cilia: genetic susceptibility to hydrocephalus in primary ciliary dyskinesia. J Neurosci Res. 2013;91:1117–32.CrossRefGoogle Scholar
  52. 52.
    Ma X, Bao J, Adelstein RS. Loss of cell adhesion causes hydrocephalus in nonmuscle myosin II-B-ablated and mutated mice. Mol Biol Cell. 2007;18:2305–12.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Malatesta P, Appolloni I, Calzolari F. Radial glia and neural stem cells. Cell Tissue Res. 2008;331:165–78.PubMedCrossRefGoogle Scholar
  54. 54.
    Markham NO, Doll CA, Dohn MR, Miller RK, Yu H, Coffey RJ, McCrea PD, Gamse JT, Reynolds AB. DIPA-family coiled-coils bind conserved isoform-specific head domain of p120-catenin family: potential roles in hydrocephalus and heterotopia. Mol Biol Cell. 2014;25:2592–603.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Marzesco AM, Janich P, Wilsch-Bräuninger M, Dubreuil V, Langenfeld K, Corbeil D, Huttner WB. Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells. J Cell Sci. 2005;118:2849–58.PubMedCrossRefGoogle Scholar
  56. 56.
    Mashayekhi F, Draper CE, Bannister CM, Pourghasem M, Owen-Lynch PJ, Miyan JA. Deficient cortical development in the hydrocephalic Texas (H-Tx) rat: a role for CSF. Brain. 2002;125:1859–74.PubMedCrossRefGoogle Scholar
  57. 57.
    McAllister P, Guerra M, Lc R, Jimenez AJ, Dominguez-Pinos D, Sival D, den Dunnen W, Morales DM, Schmidt RE, Rodríguez EM, Limbrick DD. Ventricular zone disruption in human neonates with intraventricular hemorrhage. J Neuropathol Exp Neurol. 2017;76(5):358–75.PubMedCrossRefPubMedCentralGoogle Scholar
  58. 58.
    Merkle FT, Alvarez-Buylla A. Neural stem cells in mammalian development. Curr Opin Cell Biol. 2006;18:704–9.PubMedCrossRefGoogle Scholar
  59. 59.
    Milhorat TH. The third circulation revisited. J Neurosurg. 1975;42:628–45.CrossRefGoogle Scholar
  60. 60.
    Miyan J, Sobkowiak C, Draper C. Humanity lost: the cost of cortical maldevelopment. Is there light ahead? Eur J Pediatr Surg. 2001;11(Suppl 1):S4–9.PubMedCrossRefPubMedCentralGoogle Scholar
  61. 61.
    Miyan JA, Nabiyouni M, Zendah M. Development of the brain: a vital role for cerebrospinal fluid. Can J Physiol Pharmacol. 2003;81:317–28.PubMedCrossRefGoogle Scholar
  62. 62.
    Miyan JA, Zendah M, Mashayekhi F, Owen-Lynch PJ. Cerebrospinal fluid supports viability and proliferation of cortical cells in vitro, mirroring in vivo development. Cerebrospinal Fluid Res. 2006;3:2.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Monni E, Cusulin C, Cavallaro M, Lindvall O, Kokaia Z. Human fetal striatum-derived neural stem (NS) cells differentiate to mature neurons in vitro and in vivo. Curr Stem Cell Res Ther. 2014;9:338–46.PubMedCrossRefGoogle Scholar
  64. 64.
    Mori T, Buffo A, Gotz M. The novel roles of glial cells revisited: the contribution of radial glia and astrocytes to neurogenesis. Curr Top Dev Biol. 2005;69:67–99.PubMedCrossRefGoogle Scholar
  65. 65.
    Nechiporuk T, Fernández TE, Vasioukhin V. Failure of epithelial tube maintenance causes hydrocephalus and renal cysts in Dlg5-/- mice. Dev Cell. 2007;13:338–50.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Nelson DJ, Wright EM. The distribution, activity, and function of the cilia in the frog brain. J Physiol Lond. 1974;243:63–78.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Neuhuber B, Barshinger AL, Paul C, Shumsky JS, Mitsui T, Fischer I. Stem cell delivery by lumbar puncture as a therapeutic alternative to direct injection into injured spinal cord. J Neurosurg Spine. 2008;9:390–9.PubMedCrossRefGoogle Scholar
  68. 68.
    Nguyen T, Chin WC, O'Brien JA, Verdugo P, Berger AJ. Intracellular pathways regulating ciliary beating of rat brain ependymal cells. J Physiol. 2001;531.(Pt 1:131–40.PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Nicholson C. Signals that go with the flow. Trends Neurosci. 1999;22:143–5.PubMedCrossRefGoogle Scholar
  70. 70.
    Ohta M, Suzuki Y, Noda T, Kataoka K, Chou H, Ishikawa N, Kitada M, Matsumoto N, Dezawa M, Suzuki S, Ide C. Implantation of neural stem cells via cerebrospinal fluid into the injured root. Neuroreport. 2004;15:1249–53.PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Oliver C, González C, Alvial G, Flores CA, Rodríguez EM, Batiz LF. Disruption of CDH2/N-cadherin-based adherens junctions leads to apoptosis of ependymal cells and denudation of brain ventricular walls. J Neuropathol Exp Neurol. 2013;72:846–60.PubMedCrossRefPubMedCentralGoogle Scholar
  72. 72.
    Ortega E, Muñoz RI, Luza N, Guerra F, Guerra M, Vio K, Henzi R, Jaque J, Rodriguez S, McAllister JP, Rodriguez EM. The value of early and comprehensive diagnoses in a human fetus with hydrocephalus and progressive obliteration of the aqueduct of Sylvius: case report. BMC Neurol. 2016;16:45.PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Ortloff A, Lichtin N, Guerra M, Vío K, Rodríguez EM. The disruption of the ventricular zone that occurs in foetal life of the hydrocephalic HTx rat is followed by a second disruption in the postnatal life. 57th annual meeting of Society of Research into Hydrocephalus and Spina Bifida, Cologne, Germany, 2013.Google Scholar
  74. 74.
    Páez P, Bátiz LF, Roales-Buján R, Rodríguez-Pérez LM, Rodríguez S, Jiménez AJ, Rodríguez EM, Pérez-Fígares JM. Patterned neuropathologic events occurring in hyh congenital hydrocephalic mutant mice. J Neuropathol Exp Neurol. 2007;66:1082–92.PubMedCrossRefPubMedCentralGoogle Scholar
  75. 75.
    Pluchino S, Quattrini A, Brambilla E, Gritti A, Salani G, Dina G, Galli R, Del Carro U, Amadio S, Bergami A, Furlan R, Comi G, Vescovi AL, Martino G. Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature. 2003;422:688–94.PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    Rakic P. Elusive radial glial cells: historical and evolutionary perspective. Glia. 2003;43:19–32.PubMedCrossRefPubMedCentralGoogle Scholar
  77. 77.
    Rasin M, Gazula V, Breunig J, Kwan KY, Johnson MB, Liu-Chen S, Li HS, Jan LY, Jan YN, Rakic P, Sestan N. Numb and Numbl are required for maintenance of cadherin-based adhesion and polarity of neural progenitors. Nat Neurosci. 2007;10:819–27.PubMedCrossRefPubMedCentralGoogle Scholar
  78. 78.
    Redzic ZB, Segal MB. The structure of the choroid plexus and the physiology of the choroid plexus epithelium. Adv Drug Deliv Rev. 2004;56:1695–716.PubMedCrossRefPubMedCentralGoogle Scholar
  79. 79.
    Roales-Buján R, Páez P, Guerra M, Rodríguez S, Vío K, Ho-Plagaro A, García-Bonilla M, Rodríguez-Pérez LM, Domínguez-Pinos MD, Rodríguez EM, Pérez-Fígares JM, Jiménez AJ. Astrocytes acquire morphological and functional characteristics of ependymal cells following disruption of ependyma in hydrocephalus. Acta Neuropathol. 2012;124:531–46.PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Rodríguez EM. The cerebrospinal fluid as a pathway in neuroendocrine integration. J Endocrinol. 1976;71:407–43.PubMedCrossRefPubMedCentralGoogle Scholar
  81. 81.
    Rodríguez EM, Blázquez JL, Guerra M. The design of barriers in the hypothalamus allows the median eminence and the arcuate nucleus to enjoy private milieus: the former opens to the portal blood and the latter to the cerebrospinal fluid. Peptides. 2010;31:757–76.PubMedCrossRefPubMedCentralGoogle Scholar
  82. 82.
    Rodríguez EM, Guerra MM, Vío K, González C, Ortloff A, Bátiz LF, Rodríguez S, Jara MC, Muñoz RI, Ortega E, Jaque J, Guerra F, Sival DA, den Dunnen WF, Jiménez AJ, Domínguez-Pinos MD, Pérez-Fígares JM, McAllister JP, Johanson C. A cell junction pathology of neural stem cells leads to abnormal neurogenesis and hydrocephalus. Biol Res. 2012;45:231–42.PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    Rodríguez EM, Guerra M. Neural stem cells and fetal onset hydrocephalus. Pediatr Neurosurg. 2017;  https://doi.org/10.1159/000453074.PubMedCrossRefPubMedCentralGoogle Scholar
  84. 84.
    Satake K, Lou J, Lenke LG. Migration of mesenchymal stem cells through cerebrospinal fl uid into injured spinal cord tissue. Spine. 2004;29:1971–9.PubMedCrossRefPubMedCentralGoogle Scholar
  85. 85.
    Sarnat HB. Role of human fetal ependyma. Pediatr Neurol. 1992a;8:163–78.PubMedCrossRefPubMedCentralGoogle Scholar
  86. 86.
    Sarnat HB. Regional differentiation of the human fetal ependyma: immunocytochemical markers. J Neuropathol Exp Neurol. 1992b;51:58–75.PubMedCrossRefPubMedCentralGoogle Scholar
  87. 87.
    Sarnat HB. Ependymal reactions to injury. A review. J Neuropathol Exp Neurol. 1995;54:1–15.PubMedCrossRefPubMedCentralGoogle Scholar
  88. 88.
    Sarnat HB. Histochemistry and immunocytochemistry of the developing ependyma and choroid plexus. Microsc Res Tech. 1998;41:14–28.PubMedCrossRefPubMedCentralGoogle Scholar
  89. 89.
    Sato O, Yamguchi T, Kittaka M, Toyama H. Hydrocephalus and epilepsy. Childs Nerv Syst. 2001;17(1–2):76–86.PubMedCrossRefPubMedCentralGoogle Scholar
  90. 90.
    Shaw RF, Fay AJ, Puthenveedu M, et al. Microtubule plus-end-tracking proteins target gap junctions directly from the cell interior to adherens junctions. Cell. 2007;128:547–60.PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Shibasaki T, Tokunaga A, Sakamoto R, Sagara H, Noguchi S, Sasaoka T, Yoshida N. PTB deficiency causes the loss of adherens junctions in the dorsal telencephalon and leads to lethal hydrocephalus. Cereb Cortex. 2013;23:1824–35.PubMedCrossRefGoogle Scholar
  92. 92.
    Shim JW, Sandlund J, Han CH, Hameed MQ, Connors S, Klagsbrun M, Madsen JR, Irwin N. VEGF, which is elevated in the CSF of patients with hydrocephalus, causes ventriculomegaly and ependymal changes in rats. Exp Neurol. 2013;247:703–9.PubMedCrossRefGoogle Scholar
  93. 93.
    Shimizu A, Koto M. Ultrastructure and movement of the ependymal and tracheal cilia in congenitally hydrocephalic WIC-Hyd rats. Childs Nerv Syst. 1992;8:25–32.PubMedCrossRefGoogle Scholar
  94. 94.
    Sival DA, Guerra M, den Dunnen WFA, Bátiz LF, Alvial G, Rodríguez EM. Neuroependymal denudation is in progress in full-term human foetal spina bifida aperta. Brain Pathol. 2011;21:163–79.PubMedCrossRefGoogle Scholar
  95. 95.
    Siyahhan B, Knobloch V, de Zélicourt D, Asgari M, Schmid Daners M, Poulikakos D, Kurtcuoglu V. Flow induced by ependymal cilia dominates near-wall cerebrospinal fluid dynamics in the lateral ventricles. J R Soc Interface. 2014;11:20131189.PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Street JM, Barran PE, Mackay CL, Weidt S, Balmforth C, Walsh TS, Chalmers RT, Webb DJ, Dear JW. Identification and proteomic profiling of exosomes in human cerebrospinal fluid. J Transl Med. 2012;5:10–5.Google Scholar
  97. 97.
    Tissir F, Qu Y, Montcouquiol M, et al. Lack of cadherins Celsr2 and Celsr3 impairs ependymal ciliogenesis, leading to fatal hydrocephalus. Nat Neurosci. 2010;13:700–7.PubMedCrossRefGoogle Scholar
  98. 98.
    Veening JG, Barendregt HP. The regulation of brain states by neuroactive substances distributed via the cerebrospinal fluid; a review. Cerebrospinal Fluid Res. 2010;7:1.PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Vigh-Teichmann I, Vigh B. The cerebrospinal fluid-contacting neuron: a peculiar cell type of the central nervous system. Immunocytochemical aspects. Arch Histol Cytol. 1989;52:195–207.PubMedCrossRefPubMedCentralGoogle Scholar
  100. 100.
    Vigh B, Manzano e Silva MJ, Frank CL, Vincze C, Czirok SJ, Szabó A, Lukáts A, Szél A. The system of cerebrospinal fluid-contacting neurons. Its supposed role in the nonsynaptic signal transmission of the brain. Histol Histopathol. 2004;19:607–28.PubMedGoogle Scholar
  101. 101.
    Vío K, Rodríguez S, Yulis CR, Oliver C, Rodríguez EM. The subcommissural organ of the rat secretes Reissner’s fiber glycoproteins and CSF-soluble proteins reaching the internal and external CSF compartments. Cerebrospinal Fluid Res. 2008;5:3.PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Voutsinos B, Chouaf L, Mertens P, Ruiz-Flandes P, Joubert Y, Belin MF, Didier-Bazes M. Tropism of serotonergic neurons towards glial targets in the rat ependyma. Neuroscience. 1994;59:663–72.PubMedCrossRefGoogle Scholar
  103. 103.
    Wagner C, Bátiz LF, Rodríguez S, Jiménez AJ, Páez P, Tomé M, Pérez-Fígares JM, Rodríguez EM. Cellular mechanisms involved in the stenosis and obliteration of the cerebral aqueduct of hyh mutant mice developing congenital hydrocephalus. J Neuropathol Exp Neurol. 2003;62:1019–40.PubMedCrossRefGoogle Scholar
  104. 104.
    Wei CJ, Francis R, Xu X, Lo CW. Connexin43 associated with an N-cadherin-containing multiprotein complex is required for gap junction formation in NIH3T3 cells. J Biol Chem. 2005;280:19925–36.PubMedCrossRefGoogle Scholar
  105. 105.
    Williams MA, McAllister JP, Walker ML, Kranz DA, Bergsneider M, Del Bigio MR, Fleming L, Frim DM, Gwinn K, Kestle JR, Luciano MG, Madsen JR, Oster-Granite ML, Spinella G. Priorities for hydrocephalus research: report from a National Institutes of Health-sponsored workshop. J Neurosurg. 2007;107:345–57.PubMedPubMedCentralGoogle Scholar
  106. 106.
    Wrigh EM. Transport processes in the formation of the cerebrospinal fluid. Rev Physiol Biochem Pharmacol. 1978;83:1–34.Google Scholar
  107. 107.
    Wright EM. Secretion and circulation of the cerebrospinal fluid. In: Rodriguez EM, van Wimersma Greidanus TB, editors. Front Horm Res. Basel: Karger; 1981.Google Scholar
  108. 108.
    Wood JH. Neurobiology of cerebrospinal fluid. New York: Plenum; 1983.CrossRefGoogle Scholar
  109. 109.
    Worthington WC Jr, Cathcart RS 3rd. Ciliary currents on ependymal surfaces. Ann N Y Acad Sci. 1966;130:944–50.PubMedCrossRefGoogle Scholar
  110. 110.
    Wu S, Suzuki Y, Noda Y, Bai H, Kitada M, Kataoka K, Nishimura Y, Ide C. Immunohistochemical and electron microscopic study of invasion and differentiation in spinal cord lesion of neural stem cells grafted through cerebrospinal fluid in rat. J Neurosci Res. 2002;69:940–5.PubMedCrossRefPubMedCentralGoogle Scholar
  111. 111.
    Yamadori T, Nara K. The directions of ciliary beat on the wall of the lateral ventricle and the currents of the cerebrospinal fluid in the brain ventricles. Scan Electron Microsc. 1979;3:335–40.Google Scholar
  112. 112.
    Yung YC, Mutoh T, Lin ME, Noguchi K, Rivera RR, Choi JW, Kingsbury MA, Chun J. Lysophosphatidic acid signaling may initiate fetal hydrocephalus. Sci Transl Med. 2011;3:99ra87.PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Zappaterra MD, Lisgo SN, Lindsay S, Gygi SP, Walsh CA, Ballif BA. A comparative proteomic analysis of human and rat embryonic cerebrospinal fluid. J Proteome Res. 2007;6:3537–48.PubMedCrossRefPubMedCentralGoogle Scholar
  114. 114.
    Zecevic N. Specific characteristic of radial glia in the human fetal telencephalon. Glia. 2004;48:27–35.PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Esteban M. Rodríguez
    • 1
  • Maria Montserrat Guerra
    • 1
  • Eduardo Ortega
    • 2
  1. 1.Instituto de Anatomía, Histología y Patología, Facultad de MedicinaUniversidad Austral de ChileValdiviaChile
  2. 2.Hospital Regional de Valdivia, Unidad de Neurocirugía, Instituto de Neurociencias Clínicas, Medical SchoolValdiviaChile

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