Role of the subcommissural organ in the pathogenesis of congenital hydrocephalus in the HTx rat

Cell and Tissue Research

Volumn 352, Issue 3, 2013, Pages 707-725

  Ortloff, Alexander R ^a,b   Vío, Karin ^a   Guerra, Montserrat ^a   Jaramillo, Katherine ^a   Kaehne, Thilo ^c   Jones, Hazel ^d   McAllister II, James P ^e   Rodríguez, Esteban ^a  

^a UNIVERSIDAD AUSTRAL DE CHILE   (Chile)

^b UNIVERSIDAD CATÓLICA DE TEMUCO   (Chile)

^c OTTO VON GUERICKE UNIVERSITY   (Germany)

^d Gagle Brook House ^*  (United Kingdom)

^e UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Cerebrospinal fluid; HTx rat; Hydrocephalus; Reissner's fibre; Subcommissural organ

Indexed keywords

GLYCOPROTEIN; LECTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN AQUEDUCT STENOSIS; BRAIN TISSUE; CEREBROSPINAL FLUID; CONGENITAL HYDROCEPHALUS; CONTROLLED STUDY; DISEASE SEVERITY; ELECTRON MICROSCOPY; ELECTROSPRAY MASS SPECTROMETRY; EMBRYO; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; LATERAL BRAIN VENTRICLE; NONHUMAN; PATHOGENESIS; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN BINDING; RAT; SUBCOMMISSURAL ORGAN; TWO DIMENSIONAL ELECTROPHORESIS;

AMINO ACID SEQUENCE; ANIMALS; CELL DIFFERENTIATION; CEREBRAL AQUEDUCT; CONSTRICTION, PATHOLOGIC; EMBRYO, MAMMALIAN; FETUS; HYDROCEPHALUS; MOLECULAR SEQUENCE DATA; PREALBUMIN; RATS; SUBCOMMISSURAL ORGAN;

RATTUS;

EID: 84878609151     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-013-1615-9     Document Type: Article

References (70)

1. Baas D, Meiniel A, Benadiba C, Bonnafe E, Meiniel O, Reith W, Durand B (2006) A deficiency in RFX3 causes hydrocephalus associated with abnormal differentiation of ependymal cells. Eur J Neurosci 24:1020-1030
2. Blackshear PJ, Graves JP, Stumpo DJ, Cobos I, Rubenstein JL, Zeldin DC (2003) Graded phenotypic response to partial and complete deficiency of a brain-specific transcript variant of the winged helix transcription factor RFX4. Development 130:4539-4552
3. Bruni JE, Del Bigio MR, Cardoso ER, Persaud TV (1988a) Hereditary hydrocephalus in laboratory animals and humans. Exp Pathol 35:239-246
4. Bruni JE, Del Bigio MR, Cardoso ER, Persaud TV (1988b) Neuropathology of congenital hydrocephalus in the SUMS/NP mouse. Acta Neurochir (Wien) 92:118-122
5. Buxbaum JN, Ye Z, Reixach N, Friske L, Levy C, Das P, Golde T, Masliah E, Roberts AR, Bartfai T (2008) Transthyretin protects Alzheimer's mice from the behavioral and biochemical effects of Aβ toxicity. Proc Natl Acad Sci USA 105:2681-2686
6. Caprile T, Hein S, Rodríguez S, Montecinos H, Rodríguez EM (2003) Reissner fiber binds and transports away monoamines present in the cerebrospinal fluid. Brain Res Mol Brain Res 110:177-192
7. Chae TH, Kim S, Marz KE, Hanson PI, Walsh CA (2004) The hyh mutation uncovers roles for alpha Snap in apical protein localization and control of neural cell fate. Nat Genet 36:264-270
8. Cheung KK, Mok SC, Rezaei P, Chan WY (2008) Dynamic expression of Dab2 in the mouse embryonic central nervous system. BMC Dev Biol 8:76
9. Cifuentes M, Rodríguez S, Pérez J, Grondona JM, Rodríguez EM, Fernández-Llebrez P (1994) Decreased cerebrospinal fluid flow though the central canal of the spinal cord of rats immunologically deprived of Reissner's fibre. Exp Brain Res 98:431-440
10. Estivill-Torrus G, Vitalis T, Fernández-Llebrez P, Price DJ (2001) The transcription factor Pax6 is required for development of the diencephalic dorsal mid-line secretory radial glia that form the subcommissural organ. Mech Dev 109:215-224
11. Etus V, Belce A (2003) Total sialic acid levels decrease in the periventricular area of infantile rats with hydrocephalus. Childs Nerv Syst 19:825-828
12. Fernández-Llebrez P, Grondona JM, Pérez J, López-Aranda MF, Estivill-Torrus G, Llebrez-Zayas PF, Soriano E, Ramos C, Lallemand Y, Bach A, Robert B (2004) Msx1-deficient mice fail to form prosomere 1 derivatives, subcommissural organ, and posterior commissure and develop hydrocephalus. J Neuropathol Exp Neurol 63:574-586
13. Ferran JL, Sánchez-Arrones L, Bardet SM, Sandoval JE, Martínez-de-la-Torre M, Puelles L (2008) Early pretectal gene expression pattern shows a conserved anteroposterior tripartition in mouse and chicken. Brain Res Bull 75:295-298
14. Fleming CE, Mar FM, Franquinho F, Saraiva MJ, Sousa MM (2009) Transthyretin internalization by sensory neurons is megalin mediated and necessary for its neuritogenic activity. J Neurosci 29:3220-3232
15. Gobron S, Monnerie H, Meiniel R, Creveaux I, Lehmann W, Lamalle D, Dastugue B, Meiniel A (1996) SCO-spondin: a new member of the thrombospondin family secreted by the subcommissural organ is a candidate in the modulation of neuronal aggregation. J Cell Sci 109:1053-1061
16. Gobron S, Creveaux I, Meiniel R, Didier R, Herbet A, Bamdad M, El Bitar F, Dastugue B, Meiniel A (2000) Subcommissural organ/Reissner's fiber complex: characterization of SCO-spondin, a glycoprotein with potent activity on neurite outgrowth. Glia 32:177-191
17. Hofer H (1976) Beobachtungen an dem Sogenannten "Supracommissuralen Organ" (Fuse) und am Recessus Mesocoelicus der Primaten. Folia Primatol 5:190-200
18. Hoyo-Becerra C, Lopez-Avalos MD, Perez J, Miranda E, Rojas-Rios P, Fernández-Llebrez P, Grondona JM (2006) Continuous delivery of a monoclonal antibody against Reissner's fiber into CSF reveals CSF-soluble material immunorelated to the sub-commissural organ in early chick embryos. Cell Tissue Res 326:771-786
19. Huh MS, Todd MA, Picketts DJ (2009) SCO-ping out the mechanisms underlying the etiology of hydrocephalus. Physiology (Bethesda) 24:117-126
20. Johanson CE, Duncan JA III, Klinge PM, Brinker T, Stopa EG, Silverberg GD (2008) Multiplicity of cerebrospinal fluid functions: new challenges in health and disease. Cerebrospinal Fluid Res 5:10
21. Jones HC, Bucknall RM (1988) Inherited prenatal hydrocephalus in the H-Tx rat: a morphological study. Neuropathol Appl Neurobiol 14:263-274
22. Jones HC, Dack S, Ellis C (1987) Morphological aspects of the development of hydrocephalus in a mouse mutant (SUMS/NP). Acta Neuropathol 72:268-276
23. Jones HC, Depelteau JS, Carter BJ, Somera KC (2002) The frequency of inherited hydrocephalus is influenced by intrauterine factors in H-Tx rats. Exp Neurol 176:213-220
24. Jones HC, Yehia B, Chen GF (2004) Genetic analysis of inherited hydrocephalus in a rat model. Exp Neurol 190:79-90
25. Kanai M, Raz A, Goodman DS (1968) Retinol-binding protein: the transport protein for vitamin A in human plasma. J Clin Invest 47:2025-2044
26. Krebs DL, Metcalf D, Merson TD, Voss AK, Thomas T, Zhang JG, Rakar S, O'Bryan MK, Willson TA, Viney EM, Mielke LA, Nicola NA, Hilton DJ, Alexander WS (2004) Development of hydrocephalus in mice lacking SOCS7. Proc Natl Acad Sci USA 101:15446-15451
27. Lang B, Song B, Davidson W, MacKenzie A, Smith N, McCaig CD, Harmar AJ, Shen S (2006) Expression of the human PAC1 receptor leads to dose-dependent hydrocephalus-related abnormalities in mice. J Clin Invest 116:1924-1934
28. Larsen KB, Lutterodt MC, Møllgård K, Møller M (2010) Expression of the homeobox genes OTX2 and OTX1 in the early developing human brain. J Histochem Cytochem 58:669-678
29. Li X, Buxbaum JN (2011) Transthyretin and the brain re-visited: is neuronal synthesis of transthyretin protective in Alzheimer's disease? Mol Neurodegener 6:79
30. Li X, Masliah E, Reixach N, Buxbaum JN (2011) Neuronal production of transthyretin in human and murine Alzheimer's disease: is it protective? J Neurosci 31:12483-12490
31. Louvi A, Wassef M (2000) Ectopic engrailed 1 expression in the dorsal midline causes cell death, abnormal differentiation of circumventricular organs and errors in axonal pathfinding. Development 127:4061-4071
32. Mashayekhi F, Draper CE, Bannister CM, Pourghasem M, Owen-Lynch PJ, Miyan JA (2002) Deficient cortical development in the hydrocephalic Texas (H-Tx) rat: a role for CSF. Brain 125:1859-1874
33. Meiniel A (2001) SCO-spondin, a glycoprotein of the subcommissural organ/Reissner's fiber complex: evidence of a potent activity on neuronal development in primary cell cultures. Microsc Res Tech 52:484-495
34. Miller JM, Kumar R, McAllister JP II, Krause GS (2006) Gene expression analysis of the development of congenital hydrocephalus in the H-Tx rat. Brain Res 1075:36-47
35. Miranda E, Almonacid JA, Rodriguez S, Perez J, Hein S, Cifuentes M, Fernández-Llebrez P, Rodríguez EM (2001) Searching for specific binding sites of the secretory glycoproteins of the subcommissural organ. Microsc Res Tech 52:541-551
36. Monnerie H, Dastugue B, Meiniel A (1998) Effect of synthetic peptides derived from SCO-spondin conserved domains on chick cortical and spinal-cord neurons in cell cultures. Cell Tissue Res 293:407-418
37. Montecinos HA, Richter H, Caprile T, Rodríguez EM (2005) Synthesis of transthyretin by the ependymal cells of the subcommissural organ. Cell Tissue Res 320:487-499
38. Overholser MD, Whitley JR, O'Dell BL, Hogan AG (1954) The ventricular system in hydrocephalic rat brains produced by a deficiency of vitamin B12 or of folic acid in the maternal diet. Anat Rec 120:917-934
39. Palkovitts M (1965) Morphology and function of the subcommissural organ. Stud Biol Acad Sci Hung 4:1-103
40. Pérez-Fígares JM, Jiménez AJ, Pérez- Martín M, Fernández-Llebrez P, Cifuentes M, Riera P, Rodríguez S, Rodríguez EM (1998) Spontaneous congenital hydrocephalus in the mutant mouse hyh. Changes in the ventricular system and the subcommissural organ. J Neuropathol Exp Neurol 57:188-202
41. Pérez-Fígares JM, Jiménez AJ, Rodríguez EM (2001) Subcommissural organ, cerebrospinal fluid circulation, and hydrocephalus. Microsc Res Tech 52:591-607
42. Peruzzo B, Rodríguez S, Delannoy L, Hein S, Rodríguez EM (1987) Ultrastructural immunocytochemical study of the massa caudalis of lamprey larvae (Geotria australis). Evidence for the vascular fate of Reissner's fiber material. Cell Tissue Res 247:367-376
43. Picketts DJ (2006) Neuropeptide signaling and hydrocephalus: SCO with the flow. J Clin Invest 116:1828-1832
44. Ramos C, Fernández-Llebrez P, Bach A, Robert B, Soriano E (2004) Msx1 disruption leads to diencephalon defects and hydrocephalus. Dev Dyn 230:446-460
45. Redies C, Ast M, Nakagawa S, Takeichi M, Martinez-de-la-Torre M, Puelles L (2000) Morphologic fate of diencephalic prosomeres and their subdivisions revealed by mapping cadherin expression. J Comp Neurol 421:481-514
46. Richardson SJ, Lemkine GF, Alfama G, Hassani Z, Demeneix BA (2007) Cell division and apoptosis in the adult neural stem cell niche are differentially affected in transthyretin null mice. Neurosci Lett 421:234-238
47. Rodríguez S, Caprile T (2001) Functional aspects of the subcommissural organ-Reissner's fiber complex with emphasis in the clearance of brain monoamines. Microsc Res Tech 52:564-572
48. Rodríguez EM, Oksche A, Hein S, Rodríguez S, Yulis CR (1984a) Comparative immunocytochemical study of the subcommissural organ. Cell Tissue Res 237:427-441
49. Rodríguez EM, Oksche A, Hein S, Rodríguez S, Yulis CR (1984b) Spatial and structural interrelationships between secretory cells of the subcommissural organ and blood vessels. An immunocytochemical study. Cell Tissue Res 237:443-449
50. Rodríguez EM, Oksche A, Rodríguez S, Hein S, Peruzzo B, Schöbitz K, Herrera H (1987) The subcommissural organ-Reissner's fiber unit. In: Gross PM (ed) Circumventricular organs and body fluids, vol II. CRC Press, Florida, pp 1-41
51. Rodríguez S, Rodríguez EM, Jará P, Peruzzo B, Oksche A (1990) Single injection into the cerebrospinal fluid of antibodies against the secretory material of the subcommissural organ reversibly blocks formation of Reissner's fiber: immunocytochemical investigations in the rat. Exp Brain Res 81:113-124
52. Rodríguez EM, Oksche A, Hein S, Yulis CR (1992) Cell biology of the subcommissural organ. Int Rev Cytol 135:39-121
53. Rodríguez EM, Rodríguez S, Hein S (1998) The subcommissural organ. Microsc Res Tech 41:98-123
54. Rodríguez S, Vío K, Wagner C, Barría M, Navarrete EH, Ramírez VD, Pérez-Fígares JM, Rodríguez EM (1999) Changes in the cerebrospinal-fluid monoamines in rats with an immunoneutralization of the subcommissural organ-Reissner's fiber complex by maternal delivery of antibodies. Exp Brain Res 128:278-290
55. Rodríguez EM, Oksche A, Montecinos H (2001) Human subcommissural organ, with particular emphasis on its secretory activity during the fetal life. Microsc Res Tech 52:573-590
56. Rodríguez S, Bátiz F, Ortloff A, Vío K, Muñoz RI, DeGraff LM, Graves JP, Stumpo DJ, Blackshear PJ, Zeldin DC, Goto J, Tezuka T, Yamamoto Y, Rodríguez EM (2007) Lack of formation of Reissner fiber leads to hydrocephalus. Cerebrospinal Fluid Research 4 (Suppl 1):S25
57. Schoebitz K, Garrido O, Heinrichs M, Speer L, Rodríguez EM (1986) Ontogenetical development of the chick and duck subcommissural organ. An immunocytochemical study. Histochemistry 84:31-40
58. Schoebitz K, Rodríguez EM, Garrido O, Del Brio Leon MA (1993) Ontogenetic development of the subcommissural organ with reference to the flexural organ. In: Oksche A, Rodriguez EM, Fernandez-Llebrez P (eds) The subcommissural organ, an ependymal brain gland. Springer, Berlin, pp 41-49
59. Schreiber G (2002) The evolutionary and integrative roles of transthyretin in thyroid hormone homeostasis. J Endocrinol 175:61-73
60. Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins from silver stained polyacrylamide gels. Anal Chem 68:850-858
61. Somera KC, Jones HC (2004) Reduced subcommissural organ glycoprotein immunoreactivity precedes aqueduct closure and ventricular dilatation in H-Tx rat hydrocephalus. Cell Tissue Res 315:361-373
62. Sternberger LA, Hardy PH, Cuculis JJ, Meyer HG (1970) The unlabeled antobody enzyme method of immunohistochemistry. Preparation and properties of soluble antigen-antibody complex (horseradish peroxidase-antihorseradish peroxidase) and its use in identification of spirochetes. J Histochem Cytochem 18:315-333
63. Takeuchi IK, Takeuchi YK (1986) Congenital hydrocephalus following X-irradiation of pregnant rats on an early gestational day. Neurobehav Toxicol Teratol 8:143-150
64. Takeuchi IK, Kimura R, Matsuda M, Shoji R (1987) Absence of subcommissural organ in the cerebral aqueduct of congenital hydrocephalus spontaneously occurring in MT/HokIdr mice. Acta Neuropathol 73:320-322
65. Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350-4354
66. Vío K, Rodríguez S, Navarrete EH, Pérez- Fígares JM, Jiménez AJ, Rodríguez EM (2000) Hydrocephalus induced by immunological blockage of the subcommissural organ-Reissner's fiber (RF) complex by maternal transfer of anti-RF antibodies. Exp Brain Res 135:41-52
67. Vío K, Rodríguez S, Yulis CR, Oliver C, Rodríguez EM (2008) 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 5:1-14
68. Wagner C, Bátiz LF, Rodríguez S, Jiménez AJ, Páez P, Tomé M, Pérez-Fígares JM, Rodríguez EM (2003) Cellular mechanisms involved in the stenosis and obliteration of the cerebral aqueduct of hyh mutant mice developing congenital hydrocephalus. J Neuropathol Exp Neurol 62:1019-1040
69. Woeber KA, Ingbar SH (1986) The contribution of thyroxine-binding prealbumin to the binding of thyroxine in human serum, as assessed by immunoadsorption. J Clin Invest 47:1710-1721
70. Zhang D, Zeldin DC, Blackshear PJ (2007) Regulatory factor X4 variant 3: a transcription factor involved in brain development and disease. J Neurosci Res 85:3515-3522