Aberrant Wnt signalling and cellular over-proliferation in a novel mouse model of Meckel-Gruber syndrome

Developmental Biology

Volumn 377, Issue 1, 2013, Pages 55-66

  Wheway, Gabrielle ^a   Abdelhamed, Zakia ^a,b   Natarajan, Subaashini ^a   Toomes, Carmel ^a   Inglehearn, Chris ^a   Johnson, Colin A ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b AL AZHAR UNIVERSITY   (Egypt)

Author keywords

Cilia; Ciliopathies; Embryonic development; Proliferation; Wnt signalling

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; SMALL INTERFERING RNA; SONIC HEDGEHOG PROTEIN; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BRAIN REGION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; EXON; FEMALE; GENE; GENE FUNCTION; GENOTYPE; GESTATIONAL AGE; HOMOZYGOSITY; INTRON; MECKEL SYNDROME; MKS1 GENE; MOUSE; NONHUMAN; PATHOGENESIS; PHENOTYPE; POLYDACTYLY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; WNT SIGNALING PATHWAY;

ANIMALIA;

EID: 84876338830     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.02.015     Document Type: Article

References (54)

1. Abdelhamed, Z., Wheway, G., Szymanska, K., Natarajan, S., Toomes, C., Inglehearn, C., Johnson, C.A. Variable expressivity of ciliopathy neurological phenotypes that encompass Meckel-Gruber syndrome and Joubert syndrome is caused by complex de-regulated ciliogenesis, Shh and Wnt signalling defects. Hum. Mol. Genet., in press. http://dx.doi.org/10.1093/hmg/dds546.
2. Adams M., Smith U.M., Logan C.V., Johnson C.A. Recent advances in the molecular pathology, cell biology and genetics of ciliopathies. J. Med. Genet. 2008, 45:257-267.
3. Ahdabbarmada M., Claassen D. A distinctive triad of malformations of the central-nervous-system in the Meckel-Gruber syndrome. J. Neuropathol. Exp. Neurol. 1990, 49:610-620.
4. Auber B., Burfeind P., Herold S., Schoner K., Simson G., Rauskolb R., Rehder H. A disease causing deletion of 29 base pairs in intron 15 in the MKS1 gene is highly associated with the campomelic variant of the Meckel-Gruber syndrome. Clin. Genet. 2007, 72:454-459.
5. Baala L., Romano S., Khaddour R., Saunier S., Smith U.M., Audollent S., Ozilou C., Faivre L., Laurent N., Foliguet B., Munnich A., Lyonnet S., Salomon R., Encha-Razavi F., Gubler M.-C., Boddaert N., de Lonlay P., Johnson C.A., Vekemans M., Antignac C., Attié-Bitach T. The Meckel-Gruber syndrome gene, MKS3, is mutated in Joubert syndrome. Am. J. Hum. Genet. 2007, 80:186-194.
6. Bukanov N.O., Smith L.A., Klinger K.W., Ledbetter S.R., Ibraghimov-Beskrovnaya O. Long-lasting arrest of murine polycystic kidney disease with CDK inhibitor roscovitine. Nature 2006, 444:949-952.
7. Consugar M., Kubly V., Lager D., Hommerding C., Wong W., Bakker E., Gattone V., Torres V., Breuning M., Harris P. Molecular diagnostics of Meckel-Gruber syndrome highlights phenotypic differences between MKS1 and MKS3. Hum. Genet. 2007, 121:591-599.
8. Corbit K.C., Shyer A.E., Dowdle W.E., Gaulden J., Singla V., Reiter J.F. Kif3a constrains [beta]-catenin-dependent Wnt signalling through dual ciliary and non-ciliary mechanisms. Nat. Cell Biol. 2008, 10:70-76.
9. Cui C., Chatterjee B., Francis D., Yu Q., SanAgustin J.T., Francis R., Tansey T., Henry C., Wang B., Lemley B., Pazour G.J., Lo C.W. Disruption of Mks1 localization to the mother centriole causes cilia defects and developmental malformations in Meckel-Gruber syndrome. Dis. Models Mechan. 2011, 4:43-56.
10. Dandy W.E., Blackfan K.D. Internal hydrocephalus-an experimental, clinical and pathological study. Am. J. Dis. Child. 1914, 8:406-482.
11. Davis E.E., Brueckner M., Katsanis N. The emerging complexity of the vertebrate cilium: new functional roles for an ancient organelle. Dev. Cell 2006, 11:9-19.
12. Dawe H.R., Adams M., Wheway G., Szymanska K., Logan C.V., Noegel A.A., Gull K., Johnson C.A. Nesprin-2 interacts with meckelin and mediates ciliogenesis via remodelling of the actin cytoskeleton. J. Cell Sci. 2009, 122:2716-2726.
13. Dawe H.R., Smith U.M., Cullinane A.R., Gerrelli D., Cox P., Badano J.L., Blair-Reid S., Sriram N., Katsanis N., Attie-Bitach T., Afford S.C., Copp A.J., Kelly D.A., Gull K., Johnson C.A. The Meckel-Gruber Syndrome proteins MKS1 and meckelin interact and are required for primary cilium formation. Hum. Mol. Genet. 2007, 16:173-186.
14. Dawe H.R., Smith U.M., Cullinane A.R., Gerrelli D., Cox P., Badano J.L., Blair-Reid S., Sriram N., Katsanis N., Attie-Bitach T., Afford S.C., Copp A.J., Kelly D.A., Gull K., Johnson C.A. The Meckel-Gruber syndrome proteins MKS1 and meckelin interact and are required for primary cilium formation. Hum. Mol. Genet. 2007, 16:173-186.
15. Elmehdawi F., Wheway G., Szymanska K., Adams M., High A.S., Johnson C.A., Robinson P.A. Human Homologue of Drosophila Ariadne (HHARI) is a marker of cellular proliferation associated with nuclear bodies. Exp. Cell Res. 2013, 319:161-172.
16. Fraser F.C., Lytwyn A. Spectrum of anomalies in the Meckel syndrome, or maybe there is a malformation syndrome with at least one constant anomaly. Am. J. Med. Genet. 1981, 9:67-73.
17. Garcia-Gonzalo F.R., Corbit K.C., Sirerol-Piquer M.S., Ramaswami G., Otto E.A., Noriega T.R., Seol A.D., Robinson J.F., Bennett C.L., Josifova D.J., Garcia-Verdugo J.M., Katsanis N., Hildebrandt F., Reiter J.F. A transition zone complex regulates mammalian ciliogenesis and ciliary membrane composition. Nat. Genet. 2011, 43:776-784.
18. Genuardi M., Dionisivici C., Sabetta G., Mignozzi M., Rizzoni G., Cotugno G., Neri M.E.M. Cerebro-reno-digital (Meckel-like) syndrome with Dandy-Walker malformation, cystic kidneys, hepatic fibrosis and polydactyly. Am. J. Med. Genet. 1993, 47:50-53.
19. Gerdes J.M., Liu Y., Zaghloul N.A., Leitch C.C., Lawson S.S., Kato M., Beachy P.A., Beales P.L., DeMartino G.N., Fisher S., Badano J.L., Katsanis N. Disruption of the basal body compromises proteasomal function and perturbs intracellular Wnt response. Nat. Genet. 2007, 39:1350-1360.
20. Herriot R., Hallam L.A., Gray E.S. Dandy-Walker malformation in the Meckel syndrome American. J. Med. Genet. 1991, 39:207-210.
21. Isfort R.J., Cody D.B., Doersen C.J., Richards W.G., Yoder B.K., Wilkinson J.E., Kier L.D., Jirtle R.L., Isenberg J.S., Klounig J.E., Woychik R.P. The tetratricopeptide repeat containing Tg737 gene is a liver neoplasia tumor suppressor gene. Oncogene 1997, 15:1797-1803.
22. Jackson P.K. Do cilia put brakes on the cell cycle?. Nat. Cell Biol. 2011, 13:340-342.
23. Khaddour R., Smith U., Baala L., Martinovic J., Clavering D., Shaffiq R., Ozilou C., Cullinane A., Kyttala M., Shalev S., Audollent S., d'Humieres C., Kadhom N., Esculpavit C., Viot G., Boone C., Oien C., Encha-Razavi F., Batman P.A., Bennett C.P., Woods C.G., Roume J., Lyonnet S., Genin E., Le Merrer M., Munnich A., Gubler M.-C., Cox P., Macdonald F., Vekemans M., Johnson C.A., Attie-Bitach T., Soffoet Spectrum of MKS1 and MKS3 mutations in Meckel syndrome: a genotype-phenotype correlation. Mutation in brief #960. Online. Hum. Mutat. 2007, 28:523-524.
24. Kyttala M., Tallila J., Salonen R., Kopra O., Kohlschmidt N., Paavola-Sakki P., Peltonen L., Kestila M. MKS1, encoding a component of the flagellar apparatus basal body proteome, is mutated in Meckel syndrome. Nat. Genet. 2006, 38:155-157.
25. 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., Gleeson J.G. Defective Wnt-dependent cerebellar midline fusion in a mouse model of Joubert syndrome. Nat. Med. 2011, 17:726-731.
26. Lancaster M.A., Schroth J., Gleeson J.G. Subcellular spatial regulation of canonical Wnt signalling at the primary cilium. Nat. Cell Biol. 2011, 13:700-707.
27. Leitch C.C., Zaghloul N.A., Davis E.E., Stoetzel C., Diaz-Font A., Rix S., Alfadhel M., Lewis R.A., Eyaid W., Banin E., Dollfus H., Beales P.L., Badano J.L., Katsanis N. Hypomorphic mutations in syndromic encephalocele genes are associated with Bardet-Biedl syndrome. Nat. Genet. 2008, 40:443-448.
28. Lowry R.B., Hill R.H., Tischler B. Survival and spectrum of anomalies in the meckel syndrome. Am. J. Med. Genet. 1983, 14:417-421.
29. Mans D.A., Voest E.E., Giles R.H. All along the watchtower: is the cilium a tumor suppressor organelle?. Biochim. Biophys. Acta Rev. Cancer 2008, 1786:114-125.
30. Moerman P., Verbeken E., Fryns J.P., Goddeeris P., Lauweryns J.M. Association of Meckel syndrome with m-anisosplenia in one patient. Clin. Genet. 1982, 22:143-147.
31. Moerman P., Verbeken E., Fryns J.P., Goddeeris P., Lauweryns J.M. The Meckel syndrome-pathological and cytogenetic observations in 8 cases. Hum. Genet. 1982, 62:240-245.
32. Murray J.C., Johnson J.A., Bird T.D. Dandy-Walker malformation-etiologic heterogeneity and empiric recurrence risks. Clin. Genet. 1985, 28:272-283.
33. Nagy A., Gertsenstein M., Vintersten K., Behringer R. Manipulating the Mouse Embryo, A Laboratory Manual 2003, Cold Spring Harbor Laboratory Press, New York. 3rd ed.
34. Nauli S.M., Alenghat F.J., Luo Y., Williams E., Vassilev P., Li X., Elia A.E.H., Lu W., Brown E.M., Quinn S.J., Ingber D.E., Zhou J. Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat. Genet. 2003, 33:129-137.
35. Nonaka S., Tanaka Y., Okada Y., Takeda S., Harada A., Kanai Y., Kido M., Hirokawa N. Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein. Cell 1998, 95:829-837.
36. Paetau A., Salonen R., Haltia M. Brain pathology in the Meckel syndrome-a study of 59 cases. Clin. Neuropathol. 1985, 4:56-62.
37. Praetorius H.A., Spring K.R. Bending the MDCK cell primary cilium increases intracellular calcium. J. Membr. Biol. 2001, 184:71-79.
38. Rapola J., Salonen R. Visceral anomalies in the Meckel syndrome. Teratology 1985, 31:193-201.
39. Salonen R. The Meckel syndrome-clinicopathological findings in 67 patients. Am. J. Med. Genet. 1984, 18:671-689.
40. Sang L.Y., Miller J.J., Corbit K.C., Giles R.H., Brauer M.J., Otto E.A., Baye L.M., Wen X.H., Scales S.J., Kwong M., Huntzicker E.G., Sfakianos M.K., Sandoval W., Bazan J.F., Kulkarni P., Garcia-Gonzalo F.R., Seol A.D., O'Toole J.F., Held S., Reutter H.M., Lane W.S., Rafiq M.A., Noor A., Ansar M., Devi A.R.R., Sheffield V.C., Slusarski D.C., Vincent J.B., Doherty D.A., Hildebrandt F., Reiter J.F., Jackson P.K. Mapping the NPHP-JBTS-MKS protein network reveals ciliopathy disease genes and pathways. Cell 2011, 145:513-528.
41. Simpson J., Mills J., Rhoads G.G., Cunningham G.C., Conley M.R., Hoffman H.J. Genetic heterogeneity in neural tube defects. Ann. Genet. 1991, 34:7.
42. Smith U.M., Consugar M., Tee L.J., McKee B.M., Maina E.N., Whelan S., Morgan N.V., Goranson E., Gissen P., Lilliquist S., Aligianis I.A., Ward C.J., Pasha S., Punyashthiti R., Malik Sharif S., Batman P.A., Bennett C.P., Woods C.G., McKeown C., Bucourt M., Miller C.A., Cox P., AlGazali L., Trembath R.C., Torres V.E., Attie-Bitach T., Kelly D.A., Maher E.R., Gattone V.H., Harris P.C., Johnson C.A. The transmembrane protein meckelin (MKS3) is mutated in Meckel-Gruber syndrome and the wpk rat. Nat. Genet. 2006, 38:191-196.
43. Sugiura Y., Suzuki Y., Kobayashi M. The Meckel syndrome: report of two Japanese sibs and a review of literature. Am. J. Med. Genet. 1996, 67:312-314.
44. Summers M.C., Donnenfeld A.E. Dandy-Walker malformation in the Meckel syndrome. Am. J. Med. Genet. 1995, 55:57-61.
45. Taggart J.K., Walker A.E. Congenital atresia of the foramens of Luschka and Magendie. Arch. Neurol. Psychiatry 1942, 48:583-612.
46. Tao Y.X., Kim J., Schrier R.W., Edelstein C.L. Rapamycin markedly slows disease progression in a rat model of polycystic kidney disease. J. Am. Soc. Nephrol. 2005, 16:46-51.
47. Tobin J.L., Beales P.L. Restoration of renal function in zebrafish models of ciliopathies. Pediatr. Nephrol. 2008, 23:2095-2099.
48. Vierkotten J., Dildrop R., Peters T., Wang B.L., Ruther U. Ftm is a novel basal body protein of cilia involved in Shh signalling. Development 2007, 134:2569-2577.
49. Weatherbee S.D., Niswander L.A., Anderson K.V. A mouse model for Meckel syndrome reveals Mks1 is required for ciliogenesis and Hedgehog signalling. Hum. Mol. Genet. 2009, 18:4565-4575.
50. Wen X.H., Lai C.K., Evangelista M., Hongo J.A., de Sauvage F.J., Scales S.J. Kinetics of Hedgehog-dependent full-length Gli3 accumulation in primary cilia and subsequent degradation. Mol. Cell Biol. 2010, 30:1910-1922.
51. Willert K., Brown J.D., Danenberg E., Duncan A.W., Weissman I.L., Reya T., Yates J.R., Nusse R. Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 2003, 423:448-452.
52. Williams C.L., Winkelbauer M.E., Schafer J.C., Michaud E.J., Yoder B.K. Functional redundancy of the B9 proteins and nephrocystins in Caenorhabditis elegans ciliogenesis. Mol. Biol. Cell 2008, 19:2154-2168.
53. Xu J. Preparation, Culture, and Immortalization of Mouse Embryonic Fibroblasts, Current Protocols in Molecular Biology 2001, John Wiley & Sons, Inc., 10.1002/0471142727.mb2801s70.
54. Zaki M.S., Sattar S., Massoudi R.A., Gleeson J.G. Co-occurrence of distinct ciliopathy diseases in single families suggests genetic modifiers. Am. J. Med. Genet. A 2011, 155:3042-3049.