RTTN mutations link primary cilia function to organization of the human cerebral cortex

American Journal of Human Genetics

Volumn 91, Issue 3, 2012, Pages 533-540

  Kia, Sima Kheradmand ^a   Verbeek, Elly ^a   Engelen, Erik ^a   Schot, Rachel ^a   Poot, Raymond A ^a   De coo, Irenaeus F M ^a,b   Lequin, Maarten H ^a,b   Poulton, Cathryn J ^a   Pourfarzad, Farzin ^a   Grosveld, Frank G ^a   Brehm, António ^c   De Wit, Marie Claire Y ^a,b   Oegema, Renske ^a   Dobyns, William B ^d   Verheijen, Frans W ^a   Mancini, Grazia M S ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b SOPHIA CHILDREN S HOSPITAL   (Netherlands)

^c UNIVERSITY OF MADEIRA   (Portugal)

^d SEATTLE CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; PROTEIN; ROTATIN PROTEIN; UNCLASSIFIED DRUG; WNT2 PROTEIN; WNT2B PROTEIN; WNT5A PROTEIN;

ADOLESCENT; ADULT; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CASE REPORT; CELL CULTURE; CHILD; CILIARY MOTILITY; CONTROLLED STUDY; FEMALE; FIBROBLAST; GENE EXPRESSION; GENE MUTATION; HUMAN; HUMAN CELL; MALE; MICROGYRIA; NEURAL STEM CELL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RECEPTOR DOWN REGULATION; SCHOOL CHILD; SENSORY NERVE CELL;

DROSOPHILA MELANOGASTER;

EID: 84866066557     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2012.07.008     Document Type: Article

References (45)

1. Leventer, R.J., Jansen, A., Pilz, D.T., Stoodley, N., Marini, C., Dubeau, F., Malone, J., Mitchell, L.A., Mandelstam, S., Scheffer, I.E., et al. (2010). Clinical and imaging heterogeneity of polymicrogyria: A study of 328 patients. Brain 133, 1415-1427.
2. Tischfield, M.A., Cederquist, G.Y., Gupta, M.L., Jr., and Engle, E.C. (2011). Phenotypic spectrum of the tubulin-related disorders and functional implications of disease-causing mutations. Curr. Opin. Genet. Dev. 21, 286-294.
3. Barkovich, A.J., Guerrini, R., Kuzniecky, R.I., Jackson, G.D., and Dobyns,W.B. (2012). A developmental and genetic classification for malformations of cortical development: update 2012. Brain 135, 1348-1369.
4. Judkins, A.R., Martinez, D., Ferreira, P., Dobyns, W.B., and Golden, J.A. (2011). Polymicrogyria includes fusion of the molecular layer and decreased neuronal populations but normal cortical laminar organization. J. Neuropathol. Exp. Neurol. 70, 438-443.
5. Alkuraya, F.S. (2010). Autozygome decoded. Genet. Med. 12, 765-771.
6. deWit, M.C., Lequin, M.H., de Coo, I.F., Brusse, E., Halley, D.J., van de Graaf, R., Schot, R., Verheijen, F.W., and Mancini, G.M. (2008). Cortical brain malformations: Effect of clinical, neuroradiological, and modern genetic classification. Arch. Neurol. 65, 358-366. (Pubitemid 351398521)
7. Faisst, A.M., Alvarez-Bolado, G., Treichel, D., and Gruss, P. (2002). Rotatin is a novel gene required for axial rotation and left-right specification in mouse embryos. Mech. Dev. 113, 15-28. (Pubitemid 34233721)
8. Chatterjee, B., Richards, K., Bucan, M., and Lo, C. (2007). Nt mutation causing laterality defects associated with deletion of rotatin. Mamm. Genome 18, 310-315. (Pubitemid 47106841)
9. Goetz, S.C., and Anderson, K.V. (2010). The primary cilium: A signalling centre during vertebrate development. Nat. Rev. Genet. 11, 331-344.
10. Badano, J.L., Mitsuma, N., Beales, P.L., and Katsanis, N. (2006). The ciliopathies: An emerging class of human genetic disorders. Annu. Rev. Genomics Hum. Genet. 7, 125-148. (Pubitemid 44627925)
11. Gerdes, J.M., Davis, E.E., and Katsanis, N. (2009). The vertebrate primary cilium in development, homeostasis, and disease. Cell 137, 32-45.
12. Melloy, P.G., Ewart, J.L., Cohen, M.F., Desmond, M.E., Kuehn, M.R., and Lo, C.W. (1998). No turning, a mouse mutation causing left-right and axial patterning defects. Dev. Biol. 193, 77-89. (Pubitemid 28096582)
13. Marszalek, J.R., Ruiz-Lozano, P., Roberts, E., Chien, K.R., and Goldstein, L.S. (1999). Situs inversus and embryonic ciliary morphogenesis defects in mouse mutants lacking the KIF3A subunit of kinesin-II. Proc. Natl. Acad. Sci. USA 96, 5043-5048. (Pubitemid 29214532)
14. Bettencourt-Dias, M., Hildebrandt, F., Pellman, D.,Woods, G., and Godinho, S.A. (2011). Centrosomes and cilia in human disease. Trends Genet. 27, 307-315.
15. Komatsu, Y., Kaartinen, V., and Mishina, Y. (2011). Cell cycle arrest in node cells governs ciliogenesis at the node to break left-right symmetry. Development 138, 3915-3920.
16. Lancaster, M.A., Gopal, D.J., Kim, J., Saleem, S.N., Silhavy, J.L., Louie, C.M., Thacker, B.E., Williams, Y., Zaki, M.S., and Gleeson, J.G. (2011). Defective Wnt-dependent cerebellar midline fusion in a mouse model of Joubert syndrome. Nat. Med. 17, 726-731.
17. Wallingford, J.B., and Mitchell, B. (2011). Strange as it may seem: The many links between Wnt signaling, planar cell polarity, and cilia. Genes Dev. 25, 201-213.
18. Stevens, N.R., Dobbelaere, J., Wainman, A., Gergely, F., and Raff, J.W. (2009). Ana3 is a conserved protein required for the structural integrity of centrioles and basal bodies. J. Cell Biol. 187, 355-363.
19. Jakobsen, L., Vanselow, K., Skogs, M., Toyoda, Y., Lundberg, E., Poser, I., Falkenby, L.G., Bennetzen, M., Westendorf, J., Nigg, E.A., et al. (2011). Novel asymmetrically localizing components of human centrosomes identified by complementary proteomics methods. EMBO J. 30, 1520-1535.
20. Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408. (Pubitemid 34164012)
21. Tallila, J., Jakkula, E., Peltonen, L., Salonen, R., and Kestilä, M. (2008). Identification of CC2D2A as a Meckel syndrome gene adds an important piece to the ciliopathy puzzle. Am. J. Hum. Genet. 82, 1361-1367.
22. Wheatley, D.N. (1995). Primary cilia in normal and pathological tissues. Pathobiology 63, 222-238. (Pubitemid 26044720)
23. Vivancos, V., Chen, P., Spassky, N., Qian, D., Dabdoub, A., Kelley, M., Studer, M., and Guthrie, S. (2009). Wnt activity guides facial branchiomotor neuron migration, and involves the PCP pathway and JNK and ROCK kinases. Neural Dev. 4, 7.
24. Fischer, E., and Pontoglio, M. (2009). Planar cell polarity and cilia. Semin. Cell Dev. Biol. 20, 998-1005.
25. Fliegauf, M., Benzing, T., and Omran, H. (2007). When cilia go bad: Cilia defects and ciliopathies. Nat. Rev. Mol. Cell Biol. 8, 880-893. (Pubitemid 47622564)
26. Fujiwara, T., Dehart, D.B., Sulik, K.K., and Hogan, B.L. (2002). Distinct requirements for extra-embryonic and embryonic bone morphogenetic protein 4 in the formation of the node and primitive streak and coordination of left-right asymmetry in the mouse. Development 129, 4685-4696. (Pubitemid 35277196)
27. Ross, A.J., May-Simera, H., Eichers, E.R., Kai, M., Hill, J., Jagger, D.J., Leitch, C.C., Chapple, J.P., Munro, P.M., Fisher, S., et al. (2005). Disruption of Bardet-Biedl syndrome ciliary proteins perturbs planar cell polarity in vertebrates. Nat. Genet. 37, 1135-1140. (Pubitemid 41486669)
28. Chocron, S., Verhoeven, M.C., Rentzsch, F., Hammerschmidt, M., and Bakkers, J. (2007). Zebrafish Bmp4 regulates left-right asymmetry at two distinct developmental time points. Dev. Biol. 305, 577-588. (Pubitemid 46686622)
29. Piedra, M.E., and Ros, M.A. (2002). BMP signaling positively regulates Nodal expression during left right specification in the chick embryo. Development 129, 3431-3440.
30. Shimogori, T., Banuchi, V., Ng, H.Y., Strauss, J.B., and Grove, E.A. (2004). Embryonic signaling centers expressing BMP, WNTand FGF proteins interact to pattern the cerebral cortex. Development 131, 5639-5647. (Pubitemid 39625207)
31. Subramanian, L., and Tole, S. (2009). Mechanisms underlying the specification, positional regulation, and function of the cortical hem. Cereb. Cortex 19 (Suppl 1), i90-i95.
32. Witze, E.S., Litman, E.S., Argast, G.M., Moon, R.T., and Ahn, N.G. (2008). Wnt5a control of cell polarity and directional movement by polarized redistribution of adhesion receptors. Science 320, 365-369. (Pubitemid 351555657)
33. Antic, D., Stubbs, J.L., Suyama, K., Kintner, C., Scott, M.P., and Axelrod, J.D. (2010). Planar cell polarity enables posterior localization of nodal cilia and left-right axis determination during mouse and Xenopus embryogenesis. PLoS ONE 5, e8999.
34. Conti, L., Pollard, S.M., Gorba, T., Reitano, E., Toselli, M., Biella, G., Sun, Y., Sanzone, S., Ying, Q.L., Cattaneo, E., and Smith, A. (2005). Niche-independent symmetrical selfrenewal of a mammalian tissue stem cell. PLoS Biol. 3, e283.
35. Grove, E.A., Tole, S., Limon, J., Yip, L., and Ragsdale, C.W. (1998). The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3-deficient mice. Development 125, 2315-2325. (Pubitemid 28336391)
36. Abu-Khalil, A., Fu, L., Grove, E.A., Zecevic, N., and Geschwind, D.H. (2004). Wnt genes define distinct boundaries in the developing human brain: Implications for human forebrain patterning. J. Comp. Neurol. 474, 276-288. (Pubitemid 38702687)
37. Goffinet, A.M. (1984). Events governing organization of postmigratory neurons: Studies on brain development in normal and reeler mice. Brain Res. 319, 261-296. (Pubitemid 14039093)
38. D'Arcangelo, G., Miao, G.G., Chen, S.C., Soares, H.D., Morgan, J.I., and Curran, T. (1995). A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374, 719-723.
39. Willaredt, M.A., Hasenpusch-Theil, K., Gardner, H.A., Kitanovic, I., Hirschfeld-Warneken, V.C., Gojak, C.P., Gorgas, K., Bradford, C.L., Spatz, J., Wölfl, S., et al. (2008). A crucial role for primary cilia in cortical morphogenesis. J. Neurosci. 28, 12887-12900.
40. Borrell, V., and Marín, O. (2006). Meninges control tangential migration of hem-derived Cajal-Retzius cells via CXCL12/ CXCR4 signaling. Nat. Neurosci. 9, 1284-1293. (Pubitemid 44454270)
41. Siegenthaler, J.A., and Pleasure, S.J. (2011). We have got you 'covered': How the meninges control brain development. Curr. Opin. Genet. Dev. 21, 249-255.
42. Cheng, X., Hsu, C.M., Currle, D.S., Hu, J.S., Barkovich, A.J., and Monuki, E.S. (2006). Central roles of the roof plate in telencephalic development and holoprosencephaly. J. Neurosci. 26, 7640-7649. (Pubitemid 44315183)
43. Field, M., Scheffer, I.E., Gill, D.,Wilson, M., Christie, L., Shaw, M., Gardner, A., Glubb, G., Hobson, L., Corbett, M., et al. (2012). Expanding the molecular basis and phenotypic spectrum of X-linked Joubert syndrome associated with OFD1 mutations. Eur. J. Hum. Genet. 20, 806-809.
44. Sattar, S., and Gleeson, J.G. (2011). The ciliopathies in neuronal development: A clinical approach to investigation of Joubert syndrome and Joubert syndrome-related disorders. Dev. Med. Child Neurol. 53, 793-798.
45. Hildebrandt, F., Benzing, T., and Katsanis, N. (2011). Ciliopathies. N. Engl. J. Med. 364, 1533-1543.