Brain and eye malformations resembling Walker-Warburg syndrome are recapitulated in mice by dystroglycan deletion in the epiblast

Journal of Neuroscience

Volumn 28, Issue 42, 2008, Pages 10567-10575

  Satz, Jakob S ^a   Barresi, Rita ^a   Durbeej, Madeleine ^a   Willer, Tobias ^a   Turner, Amy ^a   Moore, Steven A ^a   Campbell, Kevin P ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b 4283 Carver Biomedical Research Building ^*  (United States)

Author keywords

Congenital muscular dystrophy; Dystroglycan; Hydrocephalus; Lissencephaly; Microphthalmia; Walker Warburg syndrome

Indexed keywords

ALPHA DYSTROGLYCAN; DYSTROGLYCAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTERIOR EYE CHAMBER; ARTICLE; BASEMENT MEMBRANE; BRAIN MALFORMATION; CELL MIGRATION; CONTROLLED STUDY; ECTODERM; EYE MALFORMATION; GENE DELETION; HUMAN; HUMAN TISSUE; HYDROCEPHALUS; LIGAND BINDING; MORPHOGENESIS; MOUSE; NERVE CELL; NONHUMAN; PATHOGENESIS; POSTERIOR EYE CHAMBER; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; WALKER WARBURG SYNDROME; ANIMAL; BRAIN; COMPARATIVE STUDY; CONGENITAL MALFORMATION; GENETICS; GERM LAYER; INFANT; MALE; METABOLISM; MOUSE MUTANT; MULTIPLE MALFORMATION SYNDROME; PATHOLOGY; SYNDROME; TRANSGENIC MOUSE;

ABNORMALITIES, MULTIPLE; ANIMALS; BRAIN; DYSTROGLYCANS; EYE ABNORMALITIES; GERM LAYERS; HUMANS; HYDROCEPHALUS; INFANT; MALE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; SYNDROME;

EID: 54849421206     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2457-08.2008     Document Type: Article

References (49)

1. Barresi R, Michele DE, Kanagawa M, Harper HA, Dovico SA, Satz JS, Moore SA, Zhang W, Schachter H, Dumanski JP, Cohn RD, Nishino I, Campbell KP (2004) LARGE can functionally bypass alpha-dystroglycan glycosylation defects in distinct congenital muscular dystrophies. Nat Med 10:696-703.
2. Beltrán-Valero de Bernabé D, Currier S, Steinbrecher A, Celli J, van Beusekom E, van der Zwaag B, Kayserili H, Merlini L, Chitayat D, Dobyns WB, Cormand B, Lehesjoki AE, Cruces J, Voit T, Walsh CA, van Bokhoven H, Brunner HG (2002) Mutations in the O-mannosyltransferase gene POMT1 give rise to the severe neuronal migration disorder Walker-Warburg syndrome. Am J Hum Genet 71:1033-1043.
3. Beltrán-Valero de Bernabé D, van Bokhoven H, van Beusekom E, Van den Akker W, Kant S, Dobyns WB, Cormand B, Currier S, Hamel B, Talim B, Topaloglu H, Brunner HG (2003) A homozygous nonsense mutation in the fukutin gene causes a Walker-Warburg syndrome phenotype. J Med Genet 40:845-848.
4. Beltran-Valero de Bernabé D, Voit T, Longman C, Steinbrecher A, Straub V, Yuva Y, Herrmann R, Sperner J, Korenke C, Diesen C, Dobyns WB, Brunner HG, van Bokhoven H, Brockington M, Muntoni F (2004) Mutations in the FKRP gene can cause muscle-eye-brain disease and Walker-Warburg syndrome. J Med Genet 41:e61.
5. Bonthius DJ, Wright R, Tseng B, Barton L, Marco E, Karacay B, Larsen PD (2007) Congenital lymphocytic choriomeningitis virus infection: spectrum of disease. Ann Neurol 62:347-355.
6. Chase HB (1942) Studies on an anophthalmic strain of mice. III. Results of crosses with other strains. Genetics 27:339-348.
7. Chiyonobu T, Sasaki J, Nagai Y, Takeda S, Funakoshi H, Nakamura T, Sugimoto T, Toda T (2005) Effects of fukutin deficiency in the developing mouse brain. Neuromuscul Disord 15:416-426.
8. Choi BH, Matthias SC (1987) Cortical dysplasia associated with massive ectopia of neurons and glial cells within the subarachnoid space. Acta Neuropathol 73:105-109.
9. Cohn RD, Henry MD, Michele DE, Barresi R, Saito F, Moore SA, Flanagan JD, Skwarchuk MW, Robbins ME, Mendell JR, Williamson RA, Campbell KP (2002) Disruption of DAG1 in differentiated skeletal muscle reveals a role for dystroglycan in muscle regeneration. Cell 110:639-648.
10. Cotarelo RP, Valero MC, Prados B, Peña A, Rodríguez L, Fano O, Marco JJ, Martínez-Frías ML, Cruces J (2008) Two new patients bearing mutations in the fukutin gene confirm the relevance of this gene in Walker-Warburg syndrome. Clin Genet 73:139-145.
11. Dobyns WB, Pagon RA, Armstrong D, Curry CJ, Greenberg F, Grix A, Holmes LB, Laxova R, Michels VV, Robinow M, Zimmerman RL (1989) Diagnostic criteria for Walker-Warburg syndrome. Am J Med Genet 32:195-210.
12. Duclos F, Straub V, Moore SA, Venzke DP, Hrstka RF, Crosbie RH, Durbeej M, Lebakken CS, Ettinger AJ, van der Meulen J, Holt KH, Lim LE, Sanes JR, Davidson BL, Faulkner JA, Williamson R, Campbell KP (1998) Progressive muscular dystrophy in alpha-sarcoglycan-deficient mice. J Cell Biol 142:1461-1471.
13. Ervasti JM, Campbell KP (1991) Membrane organization of the dystrophin-glycoprotein complex. Cell 66:1121-1131.
14. Ervasti JM, Campbell KP (1993) A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol 122:809-823.
15. Gee SH, Montanaro F, Lindenbaum MH, Carbonetto S (1994) Dystroglycan-alpha, a dystrophin-associated glycoprotein, is a functional agrin receptor. Cell 77:675-686.
16. Godfrey C, Clement E, Mein R, Brockington M, Smith J, Talim B, Straub V, Robb S, Quinlivan R, Feng L, Jimenez-Mallebrera C, Mercuri E, Manzur AY, Kinali M, Torelli S, Brown SC, Sewry CA, Bushby K, Topaloglu H, North K, et al. (2007) Refining genotype phenotype correlations in muscular dystrophies with defective glycosylation of dystroglycan. Brain 130:2725-2735.
17. Górecki DC, Derry JM, Barnard EA (1994) Dystroglycan: brain localisation and chromosome mapping in the mouse. Hum Mol Genet 3:1589-1597.
18. Grewal PK, Holzfeind PJ, Bittner RE, Hewitt JE (2001) Mutant glycosyltransferase and altered glycosylation of alpha-dystroglycan in the myodystrophy mouse. Nat Genet 28:151-154.
19. Holzfeind PJ, Grewal PK, Reitsamer HA, Kechvar J, Lassmann H, Hoeger H, Hewitt JE, Bittner RE (2002) Skeletal, cardiac and tongue muscle pathology, defective retinal transmission, and neuronal migration defects in the Large(myd) mouse defines a natural model for glycosylation-deficient muscle-eye-brain disorders. Hum Mol Genet 11:2673-2687.
20. Ibraghimov-Beskrovnaya O, Ervasti JM, Leveille CJ, Slaughter CA, Sernett SW, Campbell KP (1992) Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 355:696-702.
21. Ibraghimov-Beskrovnaya O, Milatovich A, Ozcelik T, Yang B, Koepnick K, Francke U, Campbell KP (1993) Human dystroglycan: skeletal muscle cDNA, genomic structure, origin of tissue specific isoforms and chromosomal localization. Hum Mol Genet 2:1651-1657.
22. Jayasinha V, Nguyen HH, Xia B, Kammesheidt A, Hoyte K, Martin PT (2003) Inhibition of dystroglycan cleavage causes muscular dystrophy in transgenic mice. Neuromuscul Disord 13:365-375.
23. Kanoff RJ, Curless RG, Petito C, Falcone S, Siatkowski RM, Pegoraro E (1998) Walker-Warburg syndrome: neurologic features and muscle membrane structure. Pediatr Neurol 18:76-80.
24. Kim DS, Hayashi YK, Matsumoto H, Ogawa M, Noguchi S, Murakami N, Sakuta R, Mochizuki M, Michele DE, Campbell KP, Nonaka I, Nishino I (2004) POMT1 mutation results in defective glycosylation and loss of laminin-binding activity in alpha-DG. Neurology 62:1009-1011.
25. Kurahashi H, Taniguchi M, Meno C, Taniguchi Y, Takeda S, Horie M, Otani H, Toda T (2005) Basement membrane fragility underlies embryonic lethality in fukutin-null mice. Neurobiol Dis 19:208-217.
26. Lee Y, Kameya S, Cox GA, Hsu J, Hicks W, Maddatu TP, Smith RS, Naggert JK, Peachey NS, Nishina PM (2005) Ocular abnormalities in Large(myd) and Large(vls) mice, spontaneous models for muscle, eye, and brain diseases. Mol Cell Neurosci 30:160-172.
27. Li S, Harrison D, Carbonetto S, Fassler R, Smyth N, Edgar D, Yurchenco PD (2002) Matrix assembly, regulation, and survival functions of laminin and its receptors in embryonic stem cell differentiation. J Cell Biol 157:1279-1290.
28. Liu J, Ball SL, Yang Y, Mei P, Zhang L, Shi H, Kaminski HJ, Lemmon VP, Hu H (2006) A genetic model for muscle-eye-brain disease in mice lacking protein O-mannose 1,2-N-acetylglucosaminyltransferase (POMGnT1). Mech Dev 123:228-240.
29. Manya H, Chiba A, Yoshida A, Wang X, Chiba Y, Jigami Y, Margolis RU, Endo T (2004) Demonstration of mammalian protein O-mannosyltransferase activity: coexpression of POMT1 and POMT2 required for enzymatic activity. Proc Natl Acad Sci U S A 101:500-505.
30. Michele DE, Barresi R, Kanagawa M, Saito F, Cohn RD, Satz JS, Dollar J, Nishino I, Kelley RI, Somer H, Straub V, Mathews KD, Moore SA, Campbell KP (2002) Post-translational disruption of dystroglycan-ligand interactions in congenital muscular dystrophies. Nature 418:417-422.
31. Moore SA, Saito F, Chen J, Michele DE, Henry MD, Messing A, Cohn RD, Ross-Barta SE, Westra S, Williamson RA, Hoshi T, Campbell KP (2002) Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy. Nature 418:422-425.
32. Muntoni F, Voit T (2004) The congenital muscular dystrophies in 2004: a century of exciting progress. Neuromuscul Disord 14:635-649.
33. Novak A, Guo C, Yang W, Nagy A, Lobe CG (2000) Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon Cre-mediated excision. Genesis 28:147-155.
34. Pagon RA, Chandler JW, Collie WR, Clarren SK, Moon J, Minkin SA, Hall JG (1978) Hydrocephalus, agyria, retinal dysplasia, encephalocele (HARD +/- E) syndrome: an autosomal recessive condition. Birth Defects Orig Artic Ser 14:233-241.
35. Patnaik SK, Stanley P (2005) Mouse large can modify complex N- and mucin O-glycans on alpha-dystroglycan to induce laminin binding. J Biol Chem 280:20851-20859.
36. Peng HB, Ali AA, Daggett DF, Rauvala H, Hassell JR, Smalheiser NR (1998) The relationship between perlecan and dystroglycan and its implication in the formation of the neuromuscular junction. Cell Adhes Commun 5:475-489.
37. Rojek JM, Campbell KP, Oldstone MB, Kunz S (2007) Old World arenavirus infection interferes with the expression of functional alpha-dystroglycan in the host cell. Mol Biol Cell 18:4493-4507.
38. Silan F, Yoshioka M, Kobayashi K, Simsek E, Tunc M, Alper M, Cam M, Guven A, Fukuda Y, Kinoshita M, Kocabay K, Toda T (2003) A new mutation of the fukutin gene in a non-Japanese patient. Ann Neurol 53:392-396.
39. Sugita S, Saito F, Tang J, Satz J, Campbell K, Südhof TC (2001) A stoichiometric complex of neurexins and dystroglycan in brain. J Cell Biol 154:435-445.
40. Takeda S, Kondo M, Sasaki J, Kurahashi H, Kano H, Arai K, Misaki K, Fukui T, Kobayashi K, Tachikawa M, Imamura M, Nakamura Y, Shimizu T, Murakami T, Sunada Y, Fujikado T, Matsumura K, Terashima T, Toda T (2003) Fukutin is required for maintenance of muscle integrity, cortical histiogenesis and normal eye development. Hum Mol Genet 12:1449-1459.
41. Tallquist MD, Soriano P (2000) Epiblast-restricted Cre expression in MORE mice: a tool to distinguish embryonic vs. extra-embryonic gene function. Genesis 26:113-115.
42. Taniguchi K, Kobayashi K, Saito K, Yamanouchi H, Ohnuma A, Hayashi YK, Manya H, Jin DK, Lee M, Parano E, Falsaperla R, Pavone P, Van Coster R, Talim B, Steinbrecher A, Straub V, Nishino I, Topaloglu H, Voit T, Endo T, et al. (2003) Worldwide distribution and broader clinical spectrum of muscle-eye-brain disease. Hum Mol Genet 12:527-534.
43. van Reeuwijk J, Janssen M, van den Elzen C, Beltran-Valero de Bernabé D, Sabatelli P, Merlini L, Boon M, Scheffer H, Brockington M, Muntoni F, Huynen MA, Verrips A, Walsh CA, Barth PG, Brunner HG, van Bokhoven H (2005) POMT2 mutations cause alpha-dystroglycan hypoglycosylation and Walker-Warburg syndrome. J Med Genet 42:907-912.
44. van Reeuwijk J, Grewal PK, Salih MA, Beltrán-Valero de Bernabé D, McLaughlan JM, Michielse CB, Herrmann R, Hewitt JE, Steinbrecher A, Seidahmed MZ, Shaheed MM, Abomelha A, Brunner HG, van Bokhoven H, Voit T (2007) Intragenic deletion in the LARGE gene causes Walker-Warburg syndrome. Hum Genet 121:685-690.
45. Whitley CB, Thompson TR, Mastri AR, Gorlin RJ (1983) Warburg syndrome: lethal neurodysplasia with autosomal recessive inheritance. J Pediatr 102:547-551.
46. Willer T, Prados B, Falcón-Pérez JM, Renner-Müller I, Przemeck GK, Lommel M, Coloma A, Valero MC, de Angelis MH, Tanner W, Wolf E, Strahl S, Cruces J (2004) Targeted disruption of the Walker-Warburg syndrome gene Pomt1 in mouse results in embryonic lethality. Proc Natl Acad Sci U S A 101:14126-14131.
47. Williamson RA, Henry MD, Daniels KJ, Hrstka RF, Lee JC, Sunada Y, Ibraghimov-Beskrovnaya O, Campbell KP (1997) Dystroglycan is essential for early embryonic development: disruption of Reichert's membrane in Dag1-null mice. Hum Mol Genet 6:831-841.
48. Yang Y, Zhang P, Xiong Y, Li X, Qi Y, Hu H (2007) Ectopia of meningeal fibroblasts and reactive gliosis in the cerebral cortex of the mouse model of muscle-eye-brain disease. J Comp Neurol 505:459-477.
49. Zhuo L, Theis M, Alvarez-Maya I, Brenner M, Willecke K, Messing A (2001) hGFAP-cre transgenic mice for manipulation of glial and neuronal function in vivo. Genesis 31:85-94.