Joubert syndrome: Brain and spinal cord malformations in genotyped cases and implications for neurodevelopmental functions of primary cilia

Acta Neuropathologica

Volumn 123, Issue 5, 2012, Pages 695-709

  Juric Sekhar, Gordana ^a   Adkins, Jonathan ^a   Doherty, Dan ^a   Hevner, Robert F ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Brainstem malformation; Cerebellar malformation; Ciliopathy; Joubert syndrome; Spinal cord malformation; Vermis aplasia

Indexed keywords

ADOLESCENT; ADULT; ARTICLE; AUTOPSY; BRAIN MALFORMATION; BRAIN STEM; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CEREBELLUM; CHILD; CILIARY NERVE; CLINICAL ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; FEMALE; FOREBRAIN; GENE; GENE MUTATION; GENETIC SCREENING; GENOTYPE; GENOTYPE PHENOTYPE CORRELATION; HETEROZYGOSITY; HUMAN; HYPOPLASIA; JOUBERT SYNDROME; MALE; NERVE CELL DIFFERENTIATION; NEUROPATHOLOGY; NEURORADIOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; OFD1 GENE; OLIVARY NUCLEUS; PONTINE NUCLEUS; PRESCHOOL CHILD; PRIORITY JOURNAL; RPGRIP1L GENE; SCHOOL CHILD; SPINAL CORD; SPINAL CORD MALFORMATION; STEM CELL; TCTN2 GENE; TRIGEMINAL NUCLEUS;

ABNORMALITIES, MULTIPLE; BRAIN; CELL MOVEMENT; CELL PROLIFERATION; CEREBELLAR DISEASES; CILIA; EYE ABNORMALITIES; FEMALE; FETUS; GENOTYPE; HUMANS; INTELLECTUAL DISABILITY; KIDNEY DISEASES; MALE; NEUROIMAGING; SPINAL CORD;

EID: 84862654933     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-012-0951-2     Document Type: Article

References (70)

1. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS, Sunyaev SR (2010) A method and server for predicting damaging missense mutations. Nat Methods 7:248-249
2. Altman NR, Naidich TP, Braffman BH (1992) Posterior fossa malformations. AJNR Am J Neuroradiol 13:691-724
3. Baala L, Romano S, Khaddour R, Saunier S, Smith UM, Audollent S, Ozilou C, Faivre L, Laurent N, Foliguet B, Munnich A, Lyonnet S, Salomon R, Encha-Razavi F, Gubler MC, Boddaert N, de Lonlay P, Johnson CA, Vekemans M, Antignac C, Attie- Bitach T (2007) The Meckel-Gruber syndrome gene, MKS3, is mutated in Joubert syndrome. Am J Hum Genet 80:186-194 (Pubitemid 46055178)
4. Boltshauser E, Isler W (1977) Joubert syndrome: episodic hyperpnea, abnormal eye movements, retardation and ataxia, associated with dysplasia of the cerebellar vermis. Neuropadiatrie 8:57-66 (Pubitemid 8086225)
5. Brancati F, Dallapiccola B, Valente EM (2010) Joubert syndrome and related disorders. Orphanet J Rare Dis 5:20
6. Budny B, Chen W, Omran H et al (2006) A novel X-linked recessive mental retardation syndrome comprising macrocephaly and ciliary dysfunction is allelic to oral-facial-digital type I syndrome. Hum Genet 120:171-178 (Pubitemid 44204005)
7. Calogero JA (1977) Vermian agenesis and unsegmented midbrain tectum. Case report. J Neurosurg 47:605-608 (Pubitemid 8193909)
8. Campbell S, Tsannatos C, Pearce JM (1984) The prenatal diagnosis of Joubert's syndrome of familial agenesis of the cerebellar vermis. Prenat Diagn 4:391-395 (Pubitemid 15200928)
9. Caspary T, Larkins CE, Anderson KV (2007) The graded response to sonic hedgehog depends on cilia architecture. Develop Cell 12:767-778 (Pubitemid 46667745)
10. Chizhikov VV, Davenport J, Zhang Q et al (2007) Cilia proteins control cerebellar morphogenesis by promoting expansion of the granule progenitor pool. J Neurosci 27:9780-9789 (Pubitemid 47492193)
11. Coene KL, Roepman R, Doherty D, Afroze B, Kroes HY, Letteboer SJ, Ngu LH, Budny B, van Wijk E, Gorden NT, Azhimi M, Thauvin-Robinet C, Veltman JA, Boink M, Kleefstra T, Cremers FP, van Bokhoven H, de Brouwer AP (2009) OFD1 is mutated in X-linked Joubert syndrome and interacts with LCA5- encoded lebercilin. Am J Hum Genet 85:465-481
12. Dafinger C, Liebau MC, Elsayed SM, Hellenbroich Y, Boltshauser E, Korenke GC, Fabretti F, Janecke AR, Ebermann I, Nürnberg G, Nürnberg P, Zentgraf H, Koerber F, Addicks K, Elsobky E, Benzing T, Schermer B, Bolz HJ (2011) Mutations in KIF7 link Joubert syndrome with Sonic Hedgehog signaling and microtubule dynamics. J Clin Invest 121:2662-2667
13. Dahmane N, Sanchez P, Gitton Y, Palma V, Sun T, Beyna M, Weiner H, Ruiz i Altaba A (2001) The Sonic Hedgehog-Gli pathway regulates dorsal brain growth and tumorigenesis. Development 128:5201-5212 (Pubitemid 34083045)
14. Delous M, Baala L, Salomon R, Laclef C, Vierkotten J, Tory K, Golzio C, Lacoste T, Besse L, Ozilou C, Moutkine I, Hellman NE, Anselme I, Silbermann F, Vesque C, Gerhardt C, Rattenberry E, Wolf MT, Gubler MC, Martinovic J, Encha-Razavi F, Boddaert N, Gonzales M, Macher MA, Nivet H, Champion G, Bertheleme JP, Niaudet P, McDonald F, Hildebrandt F, Johnson CA, Vekemans M, Antignac C, Ruther U, Schneider-Maunoury S, Attie-Bitach T, Saunier S (2007) The ciliary gene RPGRIP1L is mutated in cerebello-oculo-renal syndrome (Joubert syndrome type B) and Meckel syndrome. Nat Genet 39:875-881 (Pubitemid 47014487)
15. Dixon-Salazar T, Silhavy JL, Marsh SE et al (2004) Mutations in the AHI1 gene, encoding Jouberin, cause Joubert syndrome with cortical polymicrogyria. Am J Hum Genet 75:979-987 (Pubitemid 39532068)
16. Doherty D (2009) Joubert syndrome: insights into brain development, cilium biology, and complex disease. Semin Pediatr Neurol 16:143-154
17. Doherty D, Glass IA, Siebert JR, Strouse PJ, Parisi MA, Shaw DW, Chance PF, Barr M Jr, Nyberg D (2005) Prenatal diagnosis in pregnancies at risk for Joubert syndrome by ultrasound and MRI. Prenat Diagn 25:442-447 (Pubitemid 40961117)
18. Doherty D, Parisi MA, Finn LS, Gunay-Aygun M, Al-Mateen M, Bates D, Clericuzio C, Demir H, Dorschner M, van Essen AJ, Gahl WA, Gentile M, Gorden NT, Hikida A, Knutzen D, Ozyurek H, Phelps I, Rosenthal P, Verloes A, Weigand H, Chance PF, Dobyns WB, Glass IA (2010) Mutations in 3 genes (MKS3, CC2D2A and RPGRIP1L) cause COACH syndrome (Joubert syndrome with congenital hepatic fibrosis). J Med Genet 47:8-21
19. Eggenschwiler JT, Anderson KV (2007) Cilia and developmental signaling. Annu Rev Cell Dev Biol 23:345-373
20. Exome Variant Server (2011) NHLBI Exome Sequencing Project (ESP), Seattle, WA. URL: http://snp.gs.washington.edu/EVS/. Accessed Sept. 2011
21. Ferrante MI, Zullo A, Barra A, Bimonte S, Messaddeq N, Studer M, Dolle P, Franco B (2006) Oral-facial-digital type I protein is required for primary cilia formation and left-right axis specification. Nat Genet 38:112-117 (Pubitemid 43011891)
22. Fluss J, Blaser S, Chitayat D, Akoury H, Glanc P, Skidmore M, Raybaud C (2006) Molar tooth sign in fetal brain magnetic resonance imaging leading to the prenatal diagnosis of Joubert syndrome and related disorders. J Child Neurol 21:320-324 (Pubitemid 43891130)
23. Friede RL, Boltshauser E (1978) Uncommon syndromes of cerebellar vermis aplasia. I: Joubert syndrome. Dev Med Child Neurol 20:758-763 (Pubitemid 9073824)
24. Garcia-Gonzalo FR, Corbit KC, Sirerol-Piquer MS, Ramaswami G, Otto EA, Noriega TR, Seol AD, Robinson JF, Bennett CL, Josifova DJ, García-Verdugo JM, Katsanis N, Hildebrandt F, Reiter JF (2011) A transition zone complex regulates mammalian ciliogenesis and ciliary membrane composition. Nat Genet 43:776-784
25. Giordano L, Vignoli A, Pinelli L, Brancati F, Accorsi P, Faravelli F, Gasparotti R, Granata T, Giaccone G, Inverardi F, Frassoni C, Dallapiccola B, Valente EM, Spreafico R (2009) Joubert syndrome with bilateral polymicrogyria: clinical and neuropathological findings in two brothers. Am J Med Genet A 149A:1511-1515
26. Gorden NT, Arts HH, Parisi MA, Coene KL, Letteboer SJ, van Beersum SE, Mans DA, Hikida A, Eckert M, Knutzen D, Alswaid AF, Ozyurek H, Dibooglu S, Otto EA, Liu Y, Davis EE, Hutter CM, Bammler TK, Farin FM, Dorschner M, Topcu M, Zackai EH, Rosenthal P, Owens KN, Katsanis N, Vincent JB, Hildebrandt F, Rubel EW, Raible DW, Knoers NV, Chance PF, Roepman R, Moens CB, Glass IA, Doherty D (2008) CC2D2A is mutated in Joubert syndrome and interacts with the ciliopathyassociated basal body protein CEP290. Am J Hum Genet 83:559-571
27. Goodship J, Platt J, Smith R et al (1991) A male with type I orofaciodigital syndrome. J Med Genet 28:691-694 (Pubitemid 21922532)
28. Harting I, Kotzaeridou U, Poretti A, Seitz A, Pietz J, Bendszus M, Boltshauser E (2011) Interpeduncular heterotopia in Joubert syndrome: a previously undescribed MR finding. AJNR Am J Neuroradiol 32:1286-1289
29. Han YG, Spassky N, Romaguera-Ros M et al (2008) Hedgehog signaling and primary cilia are required for the formation of adult neural stem cells. Nat Neurosci 11:277-284 (Pubitemid 351311806)
30. Heninger E, Otto E, Imm A, Caridi G, Hildebrandt F (2001) Improved strategy for molecular genetic diagnostics in juvenile nephronophthisis. Am J Kidney Dis 37:1131-1139 (Pubitemid 32525147)
31. Ishikawa T, Zhu BL, Li DR, Zhao D, Michiue T, Maeda H (2008) An autopsy case of an infant with Joubert syndrome who died unexpectedly and a review of the literature. Forensic Sci Int 179:e67-e73
32. Ivarsson SA, Bjerre I, Brun A, Ljungberg O, Maly E, Taylor I (1993) Joubert syndrome associated with Leber amaurosis and multicystic kidneys. Am J Med Genet 45:542-547 (Pubitemid 23066411)
33. Joubert M, Eisenring JJ, Robb JP, Andermann F (1969) Familial agenesis of the cerebellar vermis. A syndrome of episodic hyperpnea, abnormal eye movements, ataxia, and retardation. Neurology 19:813-825
34. Koirala S, Jin Z, Piao X, Corfas G (2009) GPR56-regulated granule cell adhesion is essential for rostral cerebellar development. J Neurosci 29:7439-7449
35. Kumandas S, Akcakus M, Coskun A, Gumus H (2004) Joubert syndrome: review and report of seven new cases. Eur J Neurol 11:505-510 (Pubitemid 39062087)
36. Lancaster MA, Gopal DJ, Kim J, Saleem SN, Silhavy JL, Louie CM, Thacker BE, Williams Y, Zaki MS, Gleeson JG (2011) Defective Wnt-dependent cerebellar midline fusion in a mouse model of Joubert syndrome. Nat Med 17:726-731
37. Liu JS (2011) Molecular genetics of neuronal migration disorders. Curr Neurol Neurosci Rep 11(2):171-178
38. Lopes CA, Prosser SL, Romio L, Hirst RA, O'Callaghan C, Woolf AS, Fry AM (2011) Centriolar satellites are assembly points for proteins implicated in human ciliopathies, including oral-facial-digital syndrome 1. J Cell Sci 124:600-612
39. Maria BL, Quisling RG, Rosainz LC, Yachnis AT, Gitten J, Dede D, Fennell E (1999) Molar tooth sign in Joubert syndrome: clinical, radiologic, and pathologic significance. J Child Neurol 14:368-376 (Pubitemid 29321096)
40. McGraw P (2003) The molar tooth sign. Radiology 229:671-672 (Pubitemid 37467567)
41. Millen KJ, Gleeson JG (2008) Cerebellar development and disease. Curr Opin Neurobiol 18:12-19
42. Ocbina PJR, Anderson KV (2008) Intraflagellar transport, cilia and mammalian Hedgehog signaling: analysis in mouse embryonic fibroblasts. Dev Dyn 237:2030-2038
43. Padgett KR, Maria BL, Yachnis AT, Blackband SJ (2002) Ex vivo high-resolution magnetic resonance imaging of the brain in Joubert's syndrome. J Child Neurol 17:911-913 (Pubitemid 36231057)
44. Parisi MA, Dobyns WB (2003) Human malformations of the midbrain and hindbrain: review and proposed classification scheme. Mol Genet Metab 80:36-53 (Pubitemid 37272234)
45. Parisi MA, Doherty D, Chance PF, Glass IA (2007) Joubert syndrome (and related disorders) (OMIM 213300). Eur J Hum Genet 15:511-521 (Pubitemid 46681452)
46. Poretti A, Brehmer U, Scheer I et al (2008) Prenatal and neonatal MR imaging findings in oral-facial-digital syndrome type VI. AJNR 29:1090-1091 (Pubitemid 351954872)
47. Poretti A, Huisman TA, Scheer I, Boltshauser E (2011) Joubert syndrome and related disorders: spectrum of neuroimaging findings in 75 patients. AJNR Am J Neuroradiol 32:1459-1463
48. Prattichizzo C, Macca M, Novelli V, Giorgio G, Barra A, Franco B, Oral-Facial-Digital Type ICG (2008) Mutational spectrum of the oral-facial-digital type I syndrome: a study on a large collection of patients. Hum Mutat 29:1237-1246
49. Putoux A, Thomas S, Coene KL, Davis EE, Alanay Y, Ogur G, Uz E, Buzas D, Gomes C, Patrier S, Bennett CL, Elkhartoufi N, Frison MH, Rigonnot L, Joyé N, Pruvost S, Utine GE, Boduroglu K, Nitschke P, Fertitta L, Thauvin-Robinet C, Munnich A, Cormier-Daire V, Hennekam R, Colin E, Akarsu NA, Bole-Feysot C, Cagnard N, Schmitt A, Goudin N, Lyonnet S, Encha-Razavi F, Siffroi JP, Winey M, Katsanis N, Gonzales M, Vekemans M, Beales PL, Attié-Bitach T (2011) KIF7 mutations cause fetal hydrolethalus and acrocallosal syndromes. Nat Genet 43:601-606
50. Quisling RG, Barkovich AJ, Maria BL (1999) Magnetic resonance imaging features and classification of central nervous system malformations in Joubert syndrome. J Child Neurol 14:628-635 (discussion 669-672) (Pubitemid 29489114)
51. Ribes V, Stutzmann F, Bianchetti L, Guillemot F, Dolle P, Le Roux I (2008) Combinatorial signaling controls Neurogenin2 expression at the onset of spinal neurogenesis. Dev Biol 321:470-481
52. Romano S, Boddaert N, Desguerre I, Hubert L, Salomon R, Seidenwurm D, Bahi-Buisson N, Nabbout R, Sonigo P, Lyonnet S, Brunelle F, Munnich A, de Lonlay P (2006) Molar tooth sign and superior vermian dysplasia: a radiological, clinical, and genetic study. Neuropediatrics 37:42-45
53. Saleem SN, Zaki MS (2010) Role of MR imaging in prenatal diagnosis of pregnancies at risk for Joubert syndrome and related cerebellar disorders. AJNR Am J Neuroradiol 31:424-429
54. Saleem SN, Zaki MS, Soliman NA, Momtaz M (2011) Prenatal magnetic resonance imaging diagnosis of molar tooth sign at 17 to 18 weeks of gestation in two fetuses at risk for Joubert syndrome and related cerebellar disorders. Neuropediatrics 42:35-38
55. Sang L, Miller JJ, Corbit KC, Giles RH, Brauer MJ, Otto EA, Baye LM, Wen X, Scales SJ, Kwong M, Huntzicker EG, Sfakianos MK, Sandoval W, Bazan JF, Kulkarni P, Garcia- Gonzalo FR, Seol AD, O'Toole JF, Held S, Reutter HM, Lane WS, Rafiq MA, Noor A, Ansar M, Devi AR, Sheffield VC, Slusarski DC, Vincent JB, Doherty DA, Hildebrandt F, Reiter JF, Jackson PK (2011) Mapping the NPHP-JBTS-MKS protein network reveals ciliopathy disease genes and pathways. Cell 145:513-528
56. Saraiva JM, Baraitser M (1992) Joubert syndrome: a review. Am J Med Genet 43:726-731
57. Sattar S, Gleeson JG (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
58. Sawamoto K, Wichterie H, Gonzalez-Perez O et al (2006) New neurons follow the flow of cerebrospinal fluid in the adult brain. Science 311:629-632 (Pubitemid 43191300)
59. Schneider L, Cammer M, Lehman J et al (2010) Directional cell migration and chemotaxis in wound healing response to PDGFAA are coordinated by the primary cilium in fibroblasts. Cell Physiol Biochem 25:279-292
60. Senocak EU, Oguz KK, Haliloglu G, Topcu M, Cila A (2010) Structural abnormalities of the brain other than molar tooth sign in Joubert syndrome-related disorders. Diagn Interv Radiol 16:3-6
61. Singla V, Romaguera-Ros M, Garcia-Verdugo JM, Reiter JF (2010) Ofd1, a human disease gene, regulates the length and distal structure of centrioles. Dev Cell 18:410-424
62. Spassky N, Han YG, Aguilar A, Strehl L, Besse L, Laclef C, Ros MR, Garcia-Verdugo JM, Alvarez-Buylla A (2008) Primary cilia are required for cerebellar development and Shh-dependent expansion of progenitor pool. Dev Biol 317:246-259
63. Sztriha L, Al-Gazali LI, Aithala GR, Nork M (1999) Joubert's syndrome: new cases and review of clinicopathologic correlation. Pediatr Neurol 20:274-281 (Pubitemid 29203438)
64. ten Donkelaar HJ, Hoevenaars F, Wesseling P (2000) A case of Joubert's syndrome with extensive cerebral malformations. Clin Neuropathol 19:85-93 (Pubitemid 30141483)
65. ten Donkelaar HJ, Lammens M (2009) Development of the human cerebellum and its disorders. Clin Perinatol 36:513-530
66. Valente EM, Logan CV, Mougou-Zerelli S, Lee JH, Silhavy JL, Brancati F, Iannicelli M, Travaglini L, Romani S, Illi B, Adams M, Szymanska K, Mazzotta A, Lee JE, Tolentino JC, Swistun D, Salpietro CD, Fede C, Gabriel S, Russ C, Cibulskis K, Sougnez C, Hildebrandt F, Otto EA, Held S, Diplas BH, Davis EE, Mikula M, Strom CM, Ben-Zeev B, Lev D, Sagie TL, Michelson M, Yaron Y, Krause A, Boltshauser E, Elkhartoufi N, Roume J, Shalev S, Munnich A, Saunier S, Inglehearn C, Saad A, Alkindy A, Thomas S, Vekemans M, Dallapiccola B, Katsanis N, Johnson CA, Attie-Bitach T, Gleeson JG (2010) Mutations in TMEM216 perturb ciliogenesis and cause Joubert, Meckel and related syndromes. Nat Genet 42:619-625
67. van Dorp DB, Palan A, Kwee ML, Barth PG, van der Harten JJ (1991) Joubert syndrome: a clinical and pathological description of an affected male and a female fetus from the same sibship. Am J Med Genet 40:100-104
68. Watanabe H, Murakami F (2009) Real time analysis of pontine neurons during initial stages of nucleogenesis. Neurosci Res 64:20-29
69. Yachnis AT, Rorke LB (1999) Neuropathology of Joubert syndrome. J Child Neurol 14:655-659 (discussion 669-672) (Pubitemid 29489118)
70. Yu W, McDonnell K, Taketo MM, Bai CB (2008) Wnt signaling determines ventral spinal cord cell fates in a time-dependent manner. Development 135:3687-3696