Congenital hydrocephalus associated with abnormal subcommissural organ in mice lacking huntingtin in Wnt1 cell lineages

Human Molecular Genetics

Volumn 18, Issue 1, 2009, Pages 142-150

  Dietrich, Paula ^a   Shanmugasundaram, Revathi ^a   Shuyu, E ^a   Dragatsis, Ioannis ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HUNTINGTIN; WNT1 PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL LINEAGE; CEREBROSPINAL FLUID; CHOROID PLEXUS; CONTROLLED STUDY; DISEASE ASSOCIATION; EMBRYO DEVELOPMENT; GENE INACTIVATION; GENETIC ASSOCIATION; HOMEOSTASIS; HUNTINGTON CHOREA; HYDROCEPHALUS; IMMUNOHISTOCHEMISTRY; MOUSE; NEWBORN; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEQUENCE HOMOLOGY; SUBCOMMISSURAL ORGAN;

ANIMALS; CELL LINEAGE; CHOROID PLEXUS; FEMALE; GENE SILENCING; HUMANS; HYDROCEPHALUS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; SUBCOMMISSURAL ORGAN; WNT1 PROTEIN;

MUS;

EID: 57649228989     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddn324     Document Type: Article

References (71)

1. The Huntington's Disease Collaborative Research Group. (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell, 72, 971-983.
2. Cattaneo, E., Rigamonti, D., Goffredo, D., Zuccato, C., Squitieri, F. and Sipione, S. (2001) Loss of normal huntingtin function: New developments in Huntington's disease research. Trends Neurosci., 24, 182-188.
3. Dragatsis, I., Levine, M.S. and Zeitlin, S. (2000) Inactivation of Hdh in the brain and testis results in progressive neurodegeneration and sterility in mice. Nat. Genet., 26, 300-306.
4. Zhang, Y., Li, M., Drozda, M., Chen, M., Ren, S., Mejia Sanchez, R.O., Leavitt, B.R., Cattaneo, E., Ferrante, R.J., Hayden, M.R. and Friedlander, R.M. (2003) Depletion of wild-type huntingtin in mouse models of neurologic diseases. J. Neurochem., 87, 101-106.
5. Dragatsis, I., Efstratiadis, A. and Zeitlin, S. (1998) Mouse mutant embryos lacking huntingtin are rescued from lethality by wild-type extraembryonic tissues. Development, 125, 1529-1539.
6. Schmitt, I., Bachner, D., Megow, D., Henklein, P., Epplen, J.T. and Riess, O. (1995) Expression of the Huntington disease gene in rodents: cloning the rat homologue and evidence for downregulation in non-neuronal tissues during development. Hum. Mol. Genet., 4 1173-1182.
7. Dragatsis, I. and Zeitlin, S. (2001) A method for the generation of conditional gene repair mutations in mice. Nucleic Acids Res., 29, E10.
8. Duyao, M.P., Auerbach, A.B., Ryan, A., Persichetti, F., Barnes, G.T., McNeil, S.M., Ge, P., Vonsattel, J.P., Gusella, J.F., Joyner, A.L. et al. (1995) Inactivation of the mouse Huntington's disease gene homolog Hdh. Science, 269, 407-410.
9. Nasir, J., Floresco, S.B., O'Kusky, J.R., Diewert, V.M., Richman, J.M., Zeisler, J., Borowski, A., Marth, J.D., Phillips, A.G. and Hayden, M.R. (1995) Targeted disruption Of the Huntington's disease gene results in embryonic lethality and behavioral and morphological changes in heterozygotes. Cell, 81, 811-823.
10. Zeitlin, S., Liu, J.P., Chapman, D.L., Papaioannou, V.E. and Efstratiadis, A. (1995) Increased apoptosis and early embryonic lethality in mice nullizygous for the Huntington's disease gene homologue. Nat. Genet., 11, 155-163.
11. Woda, J.M., Calzonetti, T., Hilditch-Maguire, P., Duyao, M.P., Conlon, R.A. and MacDonald, M.E. (2005) Inactivation ofthe Huntington's disease gene (Hdh) impairs anterior streak formation and early patterning of the mouse embryo. BMC Dev. Biol., 18, 5-17.
12. Hatjes, P. and Wanker, E.E. (2003) The hunt for huntingtin function: interaction partners tell many different stories. Trends Biochem. Sci., 28, 425-433.
13. Awatramani, R., Soriano, P., Rodriguez, C., Mai, J.J. and Dymecki, S.M. (2003) Cryptic boundaries in roof plate and choroid plexus identified by intersectional gene activation. Nat. Genet., 35, 70-75.
14. Danielian, P.S., Echelard, Y., Vassileva, G. and McMahon, A.P. (1997) A 5.5-kb cnhancer is both necessary and sufficient for regulation of Wnt-1 transcription in vivo. Dev. Biol., 192, 300-309.
15. Danielian, P.S., Muccino, D., Rowitch, D.H., Michael, S.K. and McMahon, A.P. (1998) Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr. Biol., 8, 1323-1326.
16. Nichols, D.H. and Bruce, L.L. (2006) Migratory routes and fates of cells transcribing the Wnt-1 gene in the murine hindbrain. Dev. Dyn., 235, 285-300.
17. Brault, V., Moore, R., Kutsch, S., Ishibashi, M., Rowitch, D.H., McMahon, A.P., Sommer, L., Boussadia, O. and Kender, R. (2001) Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development, 128, 1253-1264.
18. Baas, D., Meiniel, A., Benadiba, C., Bonnafe, E., Meiniel, O., Reith, W. and Durand, B. (2006) A deficiency in RFX3 causes hydrocephalus associated with abnormal differentiation of ependymal cells. Eur. J. Neurosci., 24, 1020-1030.
19. Merchant, M., Evangelista, M., Luoh, S.M., Frantz, G.D., Chalasani, S., Carano, R.A., van Hoy, M., Ramirez, J., Ogasawara, A.K., McFarland, L.M. et al. (2005) Loss ofthe serine/threonine kinase fused results in postnatal growth defects and lethality due to progressive hydrocephalus. Mol. Cell. Biol., 25, 7054-7068.
20. Soriano, P. (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet., 21, 70-71.
21. Lindeman, G.J., Dagnino, L., Gaubatz, S., Xu, Y., Bronson, R.T., Warren, H.B. and Livingston, D.M. (1998) A specific, tionproliferative role for E2F-5 in choroid plexus function revealed by gene targeting. Genes Dev., 12, 1092-1098.
22. Meiniel, A. (2007) The secretory ependymal cells of the subcommissural organ: Which role in hydrocephalus? Int. J. Biochem. Cell. Biol., 39, 463-468.
23. Utriainen, A., Sormunen, R., Kettunen, M., Carvalhaes, L.S., Sajanti, E., Eklund, L., Kauppinen, R., Kitten, G.T. and Pihlajaniemi, T. (2004) Structurally altered basement membranes and hydrocephalus in a type XVIII collagen deficient mouse line. Hum. Mol. Genet., 13, 2089-2099.
24. Zhang, J., Williams, M.A. and Rigamonti, D. (2006) Genetics of human hydrocephalus. J. Neurol., 253, 1255-1266.
25. Fernandez-Llebrez, P., Grondona, J.M., Perez, J., Lopez-Aranda, M.F., Estivill-Torrus, G., Llebrez-Zayas, P.F., Soriano, E., Ramos, C., Lallemand, Y., Bach, A. and Robert, B. (2004) Msx1-deficient mice fail to form prosomere 1 derivatives, subcominissural organ, and posterior commissure and develop hydrocephalus. J. Neuropathol. Exp. Neurol. 63, 574-586.
26. Louvi, A. and 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.
27. Brown, P.D., Davies, S.L., Speake, T. and Millar, I.D. (2004) Molecular mechanisms of cerebrospinal fluid production. Neuroscience, 129 957-970.
28. Emerich, D.F., Skinner, S.J., Borlongan, C.V., Vasconcellos, A.V. and Thanos, C.G. (2005) The choroid plexus in the rise, fall and repair of the brain. Bioessays, 27, 262-274.
29. Boassa, D. and Yool, A.J. (2005) Physiological roles of aquaporins in the choroid plexus. Curr. Top. Dev. Biol., 67, 181-206.
30. Mao, X., Enno, T.L. and Del Bigio, M.R. (2006) Aquaporin 4 changes in rat brain with severe hydrocephalus. Eur. J. Neurosci., 23, 2929-2936.
31. Oshio, K., Watanabe, H., Song, Y., Verkman, A.S. and Manley, G.T. (2005) Reduced cerebrospinal fluid production and intracranial pressure in mice lacking choroid plexus water channel Aquaporin-1. FASEB J., 19 76-78.
32. Rodríguez, E.M., Rodríguez, S. and Hein, S. (1998) The subcommissural organ. Microsc. Res. Tech., 41, 98-123.
33. Rodríguez, E.M., Oksche, A., Hein, S., Rodríguez, S. and Yulis, C. (1984) Comparative immunacytochemical study of the SCO. Cell. Tissue Res., 237, 427-441.
34. Gonçalves-Mendes, N., Simon-Chazottes, D., Creveaux, I., Meiniel, A., Guénet, J.L. and Meiniel, R. (2003) Mouse SCO-spondin, a gene of the thrombospondin type 1 repeat (TSR) superfamily expressed in the brain. Gene, 312, 263-270.
35. Bruni, J.E., Del Bigio, M.R., Cardoso, E.R. and Persaud, T.V. (1988) Hereditary hydrocephalus in laboratory animals and humans. Exp. Pathol., 35, 239-246.
36. Garton, H.J. and Piatt, J.H. Jr (2004) Hydrocephadus. Pediatr. Clin. North. Am., 51, 305-325.
37. Rizvi, R. and Anjum, Q. (2005) Hydrocephalus in children. J. Pak. Med. Assoc., 55, 502-507.
38. Koh, L., Zakharov, A. and Johnston, M. (2005) Integration of the subarachnoid space and lymphatics: Is it time to embrace a new concept of cerebrospinal fluid absorption? Cerebrospinal Fluid Res., 20 2-6.
39. Haverkamp, F., Wölfle, J., Aretz, M., Krämer, A., Höhmann, B., Fahnenstich, H. and Zerres, K. (1999) Congenital hydrocephalus internus and aqueduct stenosis; aetiology and implications for genetic counselling. Eur. J. Pediatr., 158, 474-478.
40. Zhang, W., Yi, M.J., Chen, X., Cole, F., Krauss, R.S. and Kang, J.S. (2006) Cortical thinning and hydrocephalus in mice lacking the immunoglobulin superfamily member CDO. Mol. Cell. Biol., 26, 3764-3772.
41. Perez-Figares, J.M., Jimenez, A.J. and Rodríguez, E.M. (2001) Subcommissural organ, cerebrospinal fluid circulation, and hydrocephalus. Microsc. Res. Tech., 52, 591-607.
42. Blackshear, P.J., Graves, J.P., Stumpo, D.J., Cobos, I., Rubenstein, J.L. and Zeldin, D.C. (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.
43. Danielian, P.S. and McMahon, A.P. (1996) Engrailed-1 as a target of the Wnt-1 signalling pathway in vertebrate midbrain development. Nature 383, 332-334.
44. Rowitch, D.H., Danielian, P.S., McMahon, A.P. and Zec, N. (1999) Cystic malformation of the posterior cerebellar vermis in transgenic mice that ectopically express Engrailed-1, a horneodomain trunscription factor. Teratology, 60, 22-28.
45. Estivill-Torrus, G., Vitalis, T., Fernandez-Llebrez, P. and Price, D.J. (2001) The transcription factor Pax6 is required for development of the diencephalic dorsal midline secretory radial glia that form the subcommissural organ. Mech. Dev., 109, 215 -224.
46. Stoykova, A. and Gruss, P. (1994) Roles of Pax-genes in developing and adult brain as suggested by expression patterns. J. Neurosci., 14, 1395-1412.
47. Thomas, K.R. and Capecchi, M.R. (1990) Targeted disruption of the murine int-1 proto-oncogene resulting in severe abnormalities in midbrain and cerebellar development. Nature, 346, 847-850.
48. Andrade, M.A. and Bork, P. (1995) HEAT repeats in the Huntington's disease protein. Nat. Genet., 11, 115-116.
49. Takano, H. and Gusella, J.F. (2002) The predominantly BEAT-like motif structure of huntingtin and its association and coincident nuclear entry with dorsal, an NF-kB/Rel/dorsal family transcription factor. BMC Neurosci., 3, 15.
50. MacDonald, M.E. (2003) Huntingtin: Alive and well and working in middle management. Sci. STKE, 207, e48.
51. Marcora, E., Gowan, K. and Lee, J.E. (2003) Stimulation of NeuroD activity by huntingtin and huntingtin-associated proteins HAP1 and MLK2. Proc. Natl Acad. Sci. USA, 100, 9578-9583.
52. Zuccato, C., Tartari, M., Crotti, A., Goffredo, D., Valenza, M., Conti, L., Cataudella, T., Leavitt, B.R., Hayden, M.R., Timmusk, T., Rigamonti, D. and Cattaneo, E. (2003) Huntingtin interacts with REST/NRSF to modulate the transcription of NRSE-controlled neuronal genes. Nat. Genet., 35, 76-83.
53. Zuccato, C., Belyaev, N., Conforti, P., Ooi, L., Tartari, M., Papadimou, E., MacDonald, M., Fossale, E., Zeitlin, S., Buckley, N. and Cattaneo, E. (2007) Widespread disruption of repressor element-1 silencing transcription factor/neuron-restrictive silencer factor occupancy at its target genes in Huntington's disease. J. Neurosci., 27, 6972-6983.
54. White, J.K., Auerbach, W., Duyao, M.P., Vonsattel, J.P., Gusella, J.F., Joyner, A.L. and MacDonald, M.E. (1997) Huntingtin is required for neurogenesis and is not impaired by the Huntington's disease CAG expansion. Nat. Genet., 17, 404-410.
55. Dunah, A.W., Jeong, H., Griffin, A., Kim, Y.M., Standaert, D.G., Hersch, S.M., Mouradian, M.M., Young, A.B., Tanese, N. and Krainc, D. (2002) Sp1 and TAFII130 transcriptional activity disrupted in early Huntington's disease. Science, 296, 2238-2243.
56. Li, S.H., Cheng, A.L., Zhou, H., Lam, S., Rao, M., Li, H. and Li, X.J. (2002) Interaction of Huntington disease protein with transcriptional activator Sp1. Mol. Cell. Biol., 22, 1277-1287.
57. Takahashi, T., Guron, C., Shetty, S., Matsui, H. and Raghow, R. (1997) A minimal murine Msx-1 gene promoter. Organization of its cis-regulatory motifs and their role in transcriptional activation in cells in culture and in transgenic mice. J. Biol. Chem., 272, 22667-22678.
58. Zheng, J.B., Zhou, Y.H., Maity, T., Liao, W.S. and Saunders, G.F. (2001) Activation of the human PAX6 gene through the exon 1 enhancer by transcription factors SEF and Sp1. Nucleic Acids Res., 29, 4070-4078.
59. Vio, K., Rodríguez, S., Navarrete, E.H., Perez-Figares, J.M., Jimenez, A.J. and Rodríguez, E.M. (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.
60. Davson, H. and Segal, M.B. (1996) Physiology of the CSF and Blood-Brain-Barriers. CRC Press, Boca Raton, FL.
61. Welch, K. (1963) Secretion of cerebrospinal fluid by choroid plexus of the rabbits. Am. J. Physiol., 205, 617-624.
62. Haywood, J.R. and Vogh, B.P. (1979) Some measurements of the autonomic nervous system influence on production of cerebrospinal fluid in cat. J. Pharmacol. Exp. Ther., 208, 341-346.
63. Lindvall, M., Edvinsson, L. and Owman, C. (1978) Sympathetic nervous control of cerebrospinal fluid production from the choroid plexus. Science, 201, 176-178.
64. Caprile, T., Hein, S., Rodriguez, S., Montecinos, H. and Rodriguez, E. (2003) Reissner fiber binds and transports away monoamines present in the cerebrospinal fluid. Brain Res. Mol. Brain. Res., 110, 177-192.
65. Rodríguez, E. and Yulis, C.R. (2001) Subcommissural organ. Cellular, molecular, physiological, and pathological aspects: One 100 years of subcommissural organ research. Microsc. Res. Tech., 52, 459-460.
66. Wagner, C., Batiz, L.F., Rodríguez, S., Jiménez, A.J., Páez, P., Tomé, M., Pérez-Fígares, J.M. and Rodríguez, E.M. (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.
67. Silva-Alvarez, C., Carrasco, M., Balmaceda-Aguilera, C., Pastor, P., García Mde, L., Reinicke, K., Aguayo, L., Molina, B., Cifuentes, M., Medina, R. and Nualart, F. (2005) Ependymal cell differentiation and GLUT1 expression is a synchronous process in the ventricular wall. Neurochem. Res., 30, 1227-1236.
68. Lorenzo, N.Y., Leibrock, L.G. and Lorenzo, A.S. (1991) A single case of Huntington's disease simultaneously occurring with obstructive hydroc ephalus. Surg. Neurol., 35, 136-138.
69. Gusella, J.F. and MacDonald, M.E. (1994) Huntington's disease and repeating trinucleotides. N. Engl. J. Med., 330, 1450-1451.
70. Hogan, B., Beddington, R., Costantini, F. and Lacy, E. (1994) Manipulating the Mouse Embryo: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
71. Kaufman, M.H. (1992) The Atlas of Mouse Development. Academic Press.