CNS involvement in OFD1 syndrome: A clinical, molecular, and neuroimaging study

Orphanet Journal of Rare Diseases

Volumn 9, Issue 1, 2014, Pages

  Del Giudice, Ennio ^a   Macca, Marina ^b   Imperati, Floriana ^a   D'Amico, Alessandra ^a   Parent, Philippe ^c   Pasquier, Laurent ^d   Layet, Valerie ^e   Lyonnet, Stanislas ^f   Stamboul Darmency, Veronique ^g   Thauvin Robinet, Christel ^g,h   Franco, Brunella ^a,b  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b TELETHON INSTITUTE OF GENETICS AND MEDICINE TIGEM   (Italy)

^c BREST UNIVERSITY HOSPITAL   (France)

^d RENNES UNIVERSITY HOSPITAL   (France)

^e LE HAVRE HOSPITAL   (France)

^f HÔPITAL NECKER ENFANTS MALADES   (France)

^g Medical University of Dijon   (France)

^h UNIVERSITÉ DE BOURGOGNE   (France)

Author keywords

Ciliopathies; Neurodevelopmental phenotype; Neuroimaging; OFD1

Indexed keywords

ARTICLE; BEHAVIOR DISORDER; BRAIN CYST; BRAIN MALFORMATION; CENTRAL NERVOUS SYSTEM DISEASE; CHILD; CLINICAL ARTICLE; COGNITIVE DEFECT; COHORT ANALYSIS; COMPUTER ASSISTED TOMOGRAPHY; CORPUS CALLOSUM AGENESIS; DEVELOPMENTAL DISORDER; DISEASE COURSE; ECHOGRAPHY; FEMALE; HUMAN; MOLECULAR DIAGNOSIS; MUTATIONAL ANALYSIS; NEUROIMAGING; NEUROLOGIC DISEASE; NEUROLOGIC EXAMINATION; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; ORAL FACIAL DIGITAL TYPE 1 SYNDROME; PORENCEPHALY;

CENTRAL NERVOUS SYSTEM DISEASES; COHORT STUDIES; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MUTATION; NEUROPSYCHOLOGICAL TESTS; OROFACIODIGITAL SYNDROMES;

EID: 84900835157     PISSN: None     EISSN: 17501172     Source Type: Journal    
DOI: 10.1186/1750-1172-9-74     Document Type: Article

References (65)

1. Ciliopathies. Hildebrandt F, Benzing T, Katsanis N, N Eng J Med 2011 364 1533 1543 10.1056/NEJMra1010172
2. Cilia in the CNS: the quiet organelle claims center stage. Louvi A, Grove EA, Neuron 2011 69 1046 1060 10.1016/j.neuron.2011.03.002 21435552
3. Une malformation hereditaire de la muquese buccale: brides et freins anomaux. Papillon-Leage M, Psaume J, Rev Stomatol 1954 55 209 227
4. Oral -facial-digital syndromes: a review and diagnostic guidelines. Gurrieri F, Franco B, Toriello H, Neri G, Am J Med Genet 2007 143A 3314 3323 10.1002/ajmg.a.32032 17963220 (Pubitemid 350274851)
5. The molecular basis of oral-facial-digital syndrome, type 1. Macca M, Franco B, Am J Med Genet C Semin Med Genet 2009 151C 318 325 10.1002/ajmg.c.30224 19876934
6. X-inactivation and human disease: X-linked dominant male-lethal disorders. Franco B, Ballabio A, Curr Opin Genet Dev 2006 16 254 259 10.1016/j.gde.2006.04.012 16650755
7. Clinical, molecular, and genotype-phenotype correlation studies from 25 cases of oral-facial-digital syndrome type 1: a French and Belgian collaborative study. Thauvin-Robinet C, Cossee M, Cormier-Daire V, Van Maldergem L, Toutain A, Alembik Y, Bieth E, Layet V, Parent P, David A, Goldenberg A, Mortier G, Héron D, Sagot P, Bouvier AM, Huet F, Cusin V, Donzel A, Devys D, Teyssier JR, Faivre L, J Med Genet 2006 43 54 61 10.1136/jmg.2006.042440 16397067 (Pubitemid 43099995)
8. Mutational spectrum of the oral-facial-digital type I syndrome: a study on a large collection of patients. Prattichizzo C, Macca M, Novelli V, Giorgio G, Barra A, Franco B, Hum Mutat 2008 29 1237 1246 10.1002/humu.20792 18546297
9. Novel mutations including deletions of the entire OFD1 gene in 30 families with type 1 orofaciodigital syndrome: a study of the extensive clinical variability. Bisschoff IJ, Zeschnigk C, Horn D, Wellek B, Riess A, Wessels M, Willems P, Jensen P, Busche A, Bekkebraten J, Chopra M, Hove HD, Evers C, Heimdal K, Kaiser AS, Kunstmann E, Robinson KL, Linné M, Martin P, McGrath J, Pradel W, Prescott KE, Roesler B, Rudolf G, Siebers-Renelt U, Tyshchenko N, Wieczorek D, Wolff G, Dobyns WB, Morris-Rosendahl DJ, Hum Mutat 2013 34 237 247 10.1002/humu.22224 23033313
10. Characterization of Cxorf5 (71-7A), a novel human cDNA mapping to Xp22 and encoding a protein containing coiled-coil a-helical domains. de Conciliis L, Marchitiello A, Wapenaar MC, Borsani G, Giglio S, Mariani M, Consalez GG, Zuffardi O, Franco B, Ballabio A, Banfi S, Genomics 1998 51 243 250 10.1006/geno.1998.5348 9722947 (Pubitemid 28395030)
11. Identification of the gene for oral-facial-digital type I syndrome. Ferrante MI, Giorgio G, Feather SA, Bulfone A, Wright V, Ghiani M, Selicorni A, Gammaro L, Scolari F, Woolf AS, Sylvie O, Bernard L, Malcolm S, Winter R, Ballabio A, Franco B, Am J Hum Genet 2001 68 569 576 10.1086/318802 11179005 (Pubitemid 32202752)
12. A novel X-linked recessive mental retardation syndrome comprising macrocephaly and ciliary dysfunction is allelic to oral-facial-digital type I syndrome. Budny B, Chen W, Omran H, Fliegauf M, Tzschach A, Wisniewska M, Jensen LR, Raynaud M, Shoichet SA, Badura M, Lenzner S, Latos-Bielenska A, Ropers HH, Hum Genet 2006 120 171 178 10.1007/s00439-006-0210-5 16783569 (Pubitemid 44204005)
13. OFD1 is mutated in X-linked Joubert syndrome and interacts with LCA5-encoded lebercilin. 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, Am J Hum Genet 2009 85 465 481 10.1016/j.ajhg.2009.09.002 19800048
14. Expanding the molecular basis and phenotypic spectrum of X-linked Joubert syndrome associated with OFD1 mutations. Field M, Scheffer IE, Gill D, Wilson M, Christie L, Shaw M, Gardner A, Glubb G, Hobson L, Corbett M, Friend K, Willis-Owen S, Gecz J, Eur J Hum Genet 2012 20 806 809 10.1038/ejhg.2012.9 22353940
15. Joubert syndrome: brain and spinal cord malformations in genotyped cases and implications for neurodevelopmental functions of primary cilia. Juric-Sekhar G, Adkins J, Doherty D, Hevner RF, Acta Neuropathol 2012 123 695 709 10.1007/s00401-012-0951-2 22331178
16. OFD1 mutations in males: phenotypic spectrum and ciliary basal body docking impairment. Thauvin-Robinet C, Thomas S, Sinico M, Aral B, Burglen L, Gigot N, Dollfus H, Rossignol S, Raynaud M, Philippe C, Badens C, Touraine R, Gomes C, Franco B, Lopez E, Elkhartoufi N, Faivre L, Munnich A, Boddaert N, Van Maldergem L, Encha-Razavi F, Lyonnet S, Vekemans M, Escudier E, Attié-Bitach T, Clin Genet 2013 84 86 90 10.1111/cge.12013 23036093
17. Deep intronic mutation in OFD1, identified by targeted genomic next-generation sequencing, causes a severe form of X-linked retinitis pigmentosa (RP23). Webb TR, Parfitt DA, Gardner JC, Martinez A, Bevilacqua D, Davidson AE, Zito I, Thiselton DL, Ressa JH, Apergi M, Schwarz N, Kanuga N, Michaelides M, Cheetham ME, Gorin MB, Hardcastle AJ, Hum Mol Genet 2012 21 3647 3654 10.1093/hmg/dds194 22619378
18. OFD1, the gene mutated in Oral-Facial-Digital Syndrome Type 1, is expressed in the metanephros and in human embryonic renal mesenchymal cells. Romio L, Wright V, Price K, Winyard PJ, Donnai D, Porteous ME, Franco B, Giorgio G, Malcolm S, Woolf AS, Feather SA, J Am Soc Nephrol 2003 14 680 689 10.1097/01.ASN.0000054497.48394.D2 12595504 (Pubitemid 36246012)
19. Functional characterization of the OFD1 protein reveals a nuclear localization and physical interaction with subunits of a chromatin remodeling complex. Giorgio G, Alfieri M, Prattichizzo C, Zullo A, Cairo S, Franco B, Mol Biol Cell 2007 18 4397 4404 10.1091/mbc.E07-03-0198 17761535 (Pubitemid 350060168)
20. Oral-facial-digital type I protein is required for primary cilia formation and left-right axis specification. Ferrante MI, Zullo A, Barra A, Bimonte S, Messaddeq N, Studer M, Dolle P, Franco B, Nat Genet 2006 38 112 117 10.1038/ng1684 16311594 (Pubitemid 43011891)
21. Kif3a constrains beta-catenin-dependent Wnt signalling through dual ciliary and non-ciliary mechanisms. Corbit KC, Shyer AE, Dowdle WE, Gaulden J, Singla V, Chen MH, Chuang PT, Reiter JF, Nat Cell Biol 2008 10 70 76 10.1038/ncb1670 18084282
22. Ofd1, a human disease gene, regulates the length and distal structure of centrioles. Singla V, Romaguera-Ros M, Garcia-Verdugo JM, Reiter JF, Dev Cell 2010 18 410 424 10.1016/j.devcel.2009.12.022 20230748
23. Cerebral abnormalities in the oral-facial-digital syndrome. Wood BP, Young LW, Townes PL, Pediatr Radiol 1975 3 130 136 10.1007/BF01006897 1233426
24. Neuropathology of oral-facial-digital syndromes. Towfighi J, Berlin CM Jr, Ladda RL, Frauenhoffer EE, Lehman RA, Arch Pathol Lab Med 1985 109 642 646 3839363 (Pubitemid 15233243)
25. Central nervous system malformations and early end-stage renal disease in Oro-facio-digital syndrome type 1: A review. Odent S, Le Marec B, Toutain A, David A, Vigneron J, Treguier C, Jouan H, Millon J, Fryns J-P, Verloes A, Am J Med Genet 1998 75 389 394 10.1002/(SICI)1096-8628(19980203)75:4<389::AID- AJMG8>3.0.CO;2-L 9482645 (Pubitemid 28079656)
26. Central nervous system malformations in oral-facial-digital syndrome, type 1. Holub M, Potocki L, Bodamer OA, Am J Med Genet A 2005 136 218 15942947 (Pubitemid 40967119)
27. Ofd1 controls Dorso-Ventral patterning and axoneme elongation during embryonic brain development. D'Angelo A, De Angelis A, Avallone B, Piscopo I, Tammaro R, Studer M, Franco B, PLoS One 2012 7 52937 10.1371/journal.pone. 0052937 23300826
28. Genomic deletions of OFD1 account for 23% of oral-facial-digital type 1 syndrome after negative DNA sequencing. Thauvin-Robinet C, Franco B, Saugier-Veber P, Aral B, Gigot N, Donzel A, Van Maldergem L, Bieth E, Layet V, Mathieu M, Teebi A, Lespinasse J, Callier P, Mugneret F, Masurel-Paulet A, Gautier E, Huet F, Teyssier JR, Tosi M, Frébourg T, Faivre L, Hum Mutat 2009 30 320 E329 10.1002/humu.20888 19023858
29. Improving sequence variant descriptions in mutation databases and literature using the Mutalyzer sequence variation nomenclature checker. Wildeman M, van Ophuizen E, den Dunnen JT, Taschner PE, Hum Mutat 2008 29 6 13 10.1002/humu.20654 18000842
30. Wechsler D, Wechsler Intelligence Scale for Children-Third Edition (WISC III) San Antonio (TX): The Psychological Corporation 1991
31. American Psychiatric Association, DSM-IV-TR Diagnostic and Statistic Manual of Mental Disorders, Text Revision Washington, DC: APA DSM-IV 2000
32. Beery KE, Manual for the Developmental Test of Visual-Motor Integration (VMI) Cleveland, Ohio: Modern Curriculum Press 3 revision 1989
33. Reynolds C, Bigler E, Test of Memory and Learning: Examiner's Manual Austin, TX: PRO-ED 1994
34. L'examen psychologique dans les cas d'encephalopathie traumatique. Rey A, Archives de Psychologie 1941 28 215 285
35. Filetest de copie d'une figure complex: contribution a l'etude de la perception et de la memoire. Osterrieth PA, Archives de Psychologie 1944 30 286
36. Axia G, Test del Primo Linguaggio (TPL) Firenze, Italy: Organizzazioni Speciali 1995
37. Cianchetti C, Fancello S, Test di Valutazione del Linguaggio Trento, Italy: Erickson 1997
38. Standardizzazione di una batteria per la valutazione dei disturbi del linguaggio in età scolare. Ferrari E, De Renzi E, Faglioni P, Barbieri E, Neuropsich Infant 1981 235-236 145 158
39. Heaton RK, Chelune GJ, Talley JL, Kay GG, Curtiss G, The Wisconsin Card Sorting Test (WCST) Odessa, FL: Psychological Assessment Resources 1993
40. Achenbach TM, Rescorla L, Manual for the Child Behavior Checklist (CBCL) Burlington, VT: University of Vermont Department of Psychiatry 2000
41. Renal insufficiency, a frequent complication with age in oral-facial-digital syndrome type I. Saal S, Faivre L, Aral B, Gigot N, Toutain A, Van Maldergem L, Destree A, Maystadt I, Cosyns JP, Jouk PS, Loeys B, Chauveau D, Bieth E, Layet V, Mathieu M, Lespinasse J, Teebi A, Franco B, Gautier E, Binquet C, Masurel-Paulet A, Mousson C, Gouyon JB, Huet F, Thauvin-Robinet C, Clin Genet 2010 77 258 265 10.1111/j.1399-0004.2009.01290.x 19817772
42. Molecular genetics of neuronal migration disorders. Liu JS, Curr Neurol Neurosci Rep 2011 11 171 178 10.1007/s11910-010-0176-5 21222180
43. Cerebellar disorders in childhood: cognitive problems. Steinlin M, Cerebellum 2008 7 607 610 10.1007/s12311-008-0083-3 19057977
44. Joubert syndrome and related disorders: spectrum of neuroimaging findings in 75 patients. Poretti A, Huisman TA, Scheer I, Boltshauser E, Am J Neuroradiol 2011 32 1459 1463 10.3174/ajnr.A2517 21680654
45. Joubert Syndrome and related disorders. Brancati F, Dallapiccola B, Valente EM, Orphanet J Rare Dis 2010 5 20 10.1186/1750-1172-5-20 20615230
46. Delineation and diagnostic criteria of Oral-Facial-Digital Syndrome type VI. Poretti A, Vitiello G, Hennekam RC, Arrigoni F, Bertini E, Borgatti R, Brancati F, D'Arrigo S, Faravelli F, Giordano L, Huisman TA, Iannicelli M, Kluger G, Kyllerman M, Landgren M, Lees MM, Pinelli L, Romaniello R, Scheer I, Schwarz CE, Spiegel R, Tibussek D, Valente EM, Boltshauser E, Orphanet J Rare Dis 2012 7 4 10.1186/1750-1172-7-4 22236771
47. The ciliopathies in neuronal development: a clinical approach to investigation of Joubert syndrome and Joubert syndrome-related disorders. Sattar S, Gleeson JG, Dev Med Child Neurol 2011 53 793 798 10.1111/j.1469-8749.2011. 04021.x 21679365
48. Detailed clinical, genetic and neuroimaging characterization of OFD VI syndrome. Darmency-Stamboul V, Burglen L, Lopez E, Mejean N, Dean J, Franco B, Rodriguez D, Lacombe D, Desguerres I, Cormier-Daire V, Doray B, Pasquier L, Gonzales M, Pastore M, Crenshaw ML, Huet F, Gigot N, Aral B, Callier P, Faivre L, Attié-Bitach T, Thauvin-Robinet C, Eur J Med Genet 2013 56 301 308 10.1016/j.ejmg.2013.03.004 23523602
49. C5orf42 is the major gene responsible for OFD syndrome type VI. Lopez E, Thauvin-Robinet C, Reversade B, Khartoufi NE, Devisme L, Holder M, Ansart-Franquet H, Avila M, Lacombe D, Kleinfinger P, Kaori I, Takanashi J, Le Merrer M, Martinovic J, Noël C, Shboul M, Ho L, Güven Y, Razavi F, Burglen L, Gigot N, Darmency-Stamboul V, Thevenon J, Aral B, Kayserili H, Huet F, Lyonnet S, Le Caignec C, Franco B, Rivière JB, Hum Genet 2014 133 367 377 10.1007/s00439-013-1385-1 24178751
50. Brain pathology in the Meckel syndrome: a study of 59 cases. Paetau A, Salonen R, Haltia M, Clin Neuropathol 1985 4 56 62 3995807 (Pubitemid 15117446)
51. Brain tissue- and region-specific abnormalities on volumetric MRI scans in 21 patients with Bardet-Biedl syndrome (BBS). Keppler-Noreuil KM, Blumhorst C, Sapp JC, Brinckman D, Johnston J, Nopoulos PC, Biesecker LG, BMC Med Genet 2011 12 101 21794117
52. Cognitive, sensory, and psychosocial characteristics in patients with Bardet-Biedl syndrome. Brinckman DD, Keppler-Noreuil KM, Blumhorst C, Biesecker LG, Sapp JC, Johnston JJ, Wiggs EA, Am J Med Genet Part A 2013 161A 2964 2971 24194441
53. Neuronal ciliary signaling in homeostasis and disease. Green JA, Mykytyn K, Cell Mol Life Sci 2010 67 3287 3297 10.1007/s00018-010-0425-4 20544253
54. FGF signalling during embryo development regulates cilia length in diverse epithelia. Neugebauer JM, Amack JD, Peterson AG, Bisgrove BW, Yost HJ, Nature 2009 458 651 654 10.1038/nature07753 19242413
55. Common themes in centriole and centrosome movements. Vaughan S, Dawe HR, Trends Cell Biol 2011 21 57 66 10.1016/j.tcb.2010.09.004 20961761
56. Arl13b in primary cilia regulates the migration and placement of interneurons in the developing cerebral cortex. Higginbotham H, Eom TY, Mariani LE, Bachleda A, Hirt J, Gukassyan V, Cusack CL, Lai C, Caspary T, Anton ES, Dev Cell 2012 23 925 938 10.1016/j.devcel.2012.09.019 23153492
57. Arl13b-regulated cilia activities are essential for polarized radial glial scaffold formation. Higginbotham H, Guo J, Yokota Y, Umberger NL, Su CY, Li J, Verma N, Hirt J, Ghukasyan V, Caspary T, Anton ES, Nat Neurosci 2013 16 1000 1007 10.1038/nn.3451 23817546
58. The ciliogenic protein Oral-Facial-Digital 1 regulates the neuronal differentiation of embryonic stem cells. Hunkapiller J, Singla V, Seol A, Reiter JF, Stem Cells Dev 2011 20 831 841 10.1089/scd.2010.0362 20873986
59. Primary cilia regulate hippocampal neurogenesis by mediating sonic hedgehog signaling. Breunig JJ, Sarkisian MR, Arellano JI, Morozov YM, Ayoub AE, Sojitra S, Wang B, Flavell RA, Rakic P, Town T, Proc Natl Acad Sci U S A 2008 105 13127 13132 10.1073/pnas.0804558105 18728187
60. Hippocampal dysgenesis and variable neuropsychiatric phenotypes in patients with Bardet-Biedl syndrome underline complex CNS impact of primary cilia. Bennouna-Greene V, Kremer S, Stoetzel C, Christmann D, Schuster C, Durand M, Verloes A, Sigaudy S, Holder-Espinasse M, Godet J, Brandt C, Marion V, Danion A, Dietemann JL, Dollfus H, Clin Genet 2011 80 523 531 10.1111/j.1399-0004.2011.01688.x 21517826
61. Normal cognitive functions in joubert syndrome. Poretti A, Dietrich Alber F, Brancati F, Dallapiccola B, Valente EM, Boltshauser E, Neuropediatrics 2009 40 287 290 10.1055/s-0030-1249630 20446224
62. The neuronal primary cilium: driver of neurogenesis and memory formation in the hippocampal dentate gyrus? Whitfield JF, Chakravarthy BR, Cell Signal 2009 21 1351 1355 10.1016/j.cellsig.2009.02.013 19249355
63. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Deng W, Aimone JB, Gage FH, Nat Rev Neurosci 2010 11 339 350 10.1038/nrn2822 20354534
64. Somatostatin signaling in neuronal cilia is critical for object recognition memory. Einstein EB, Patterson CA, Hon BJ, Regan KA, Reddi J, Melnikoff DE, Mateer MJ, Schulz S, Johnson BN, Tallent MK, J Neurosci 2010 30 4306 4314 10.1523/JNEUROSCI.5295-09.2010 20335466
65. Developmental changes in frequency of the ciliary somatostatin receptor 3 protein. Stanic D, Malmgren H, He H, Scott L, Aperia A, Hokfelt T, Brain Res 2009 1249 101 112 18992731