Papillorenal syndrome-causing missense mutations in PAX2/Pax2 result in hypomorphic alleles in mouse and human

PLoS Genetics

Volumn 6, Issue 3, 2010, Pages

  Alur, Ramakrishna P ^a   Vijayasarathy, Camasamudram ^b   Brown, Jacob D ^a,c   Mehtani, Mohit ^a   Onojafe, Ighovie F ^a   Sergeev, Yuri V ^a   Boobalan, Elangovan ^a   Jones, Marypat ^d   Tang, Ke ^e   Liu, Haiquan ^f   Xia, Chun Hong ^f   Gong, Xiaohua ^f   Brooks, Brian P ^b  

^a NATIONAL EYE INSTITUTE   (United States)

^b NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

^c GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; THREONINE; TRANSCRIPTION FACTOR PAX2; DNA; MUTANT PROTEIN;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLOBOMA; CONTROLLED STUDY; DNA BINDING; EMBRYO; EYE DISEASE; FEMALE; GENE FUNCTION; GENE SEQUENCE; HUMAN; HYDROGEN BOND; IN VITRO STUDY; IN VIVO STUDY; KIDNEY DISEASE; MALE; MISSENSE MUTATION; MOUSE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PAPILLORENAL SYNDROME; PATHOGENESIS; PREDICTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; STEADY STATE; TRANSACTIVATION; AMINO ACID SEQUENCE; ANIMAL; ANIMAL EMBRYO; C57BL MOUSE; CELL LINE; CEREBELLUM; CHEMISTRY; EYE; GENE EXPRESSION REGULATION; GENETICS; KIDNEY; METABOLISM; MOLECULAR GENETICS; MOUSE MUTANT; MULTIPLE MALFORMATION SYNDROME; PATHOLOGY; PHENOTYPE; STRUCTURAL HOMOLOGY; SYNDROME; TIME;

MUS;

ABNORMALITIES, MULTIPLE; ALLELES; AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CEREBELLUM; DNA; EMBRYO, MAMMALIAN; EYE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; KIDNEY; MALE; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION, MISSENSE; PAX2 TRANSCRIPTION FACTOR; PHENOTYPE; RNA, MESSENGER; STRUCTURAL HOMOLOGY, PROTEIN; SYNDROME; TIME FACTORS;

EID: 77950390893     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000870     Document Type: Article

References (53)

1. Eccles MR (2004) PAX2 and the Renal Coloboma Syndrome. In: Epstein CJ, Erickson RP, Wynshaw-Boris A, eds. Inborn errors of development: The molecular basis of clinical disorders of morphogenesis. Oxford: Oxford University Press. pp 633-642.
2. Schimmenti LA, Pierpont ME, Carpenter BL, Kashtan CE, Johnson MR, et al. (1995) Autosomal dominant optic nerve colobomas, vesicoureteral reflux, and renal anomalies. Am J Med Genet 59: 204-208.
3. Eccles MR, Schimmenti LA (1999) Renal-coloboma syndrome: a multi-system developmental disorder caused by PAX2 mutations. Clin Genet 56: 1-9.
4. Sanyanusin P, Schimmenti LA, McNoe LA, Ward TA, Pierpont ME, et al. (1995) Mutation of the PAX2 gene in a family with optic nerve colobomas, renal anomalies and vesicoureteral reflux. Nat Genet 9: 358-364.
5. Dureau P, Attie-Bitach T, Salomon R, Bettembourg O, Amiel J, et al. (2001) Renal coloboma syndrome. Ophthalmology 108: 1912-1916.
6. Schimmenti LA, Manligas GS, Sieving PA (2003) Optic nerve dysplasia and renal insufficiency in a family with a novel PAX2 mutation, Arg115X: further ophthalmologic delineation of the renal-coloboma syndrome. Ophthalmic Genet 24: 191-202.
7. Parsa CF, Silva ED, Sundin OH, Goldberg MF, De Jong MR, et al. (2001) Redefining papillorenal syndrome: an underdiagnosed cause of ocular and renal morbidity. Ophthalmology 108: 738-749.
8. Khan AO, Nowilaty SR (2005) Early diagnosis of the papillorenal syndrome by optic disc morphology. J Neuroophthalmol 25: 209-211.
9. Amiel J, Audollent S, Joly D, Dureau P, Salomon R, et al. (2000) PAX2 mutations in renal-coloboma syndrome: mutational hotspot and germline mosaicism. Eur J Hum Genet 8: 820-826.
10. Chung GW, Edwards AO, Schimmenti LA, Manligas GS, Zhang YH, et al. (2001) Renal-coloboma syndrome: report of a novel PAX2 gene mutation. Am J Ophthalmol 132: 910-914. (Pubitemid 33122172)
11. Ford B, Rupps R, Lirenman D, Van Allen MI, Farquharson D, et al. (2001) Renal-coloboma syndrome: prenatal detection and clinical spectrum in a large family. Am J Med Genet 99: 137-141. (Pubitemid 32204785)
12. Nishimoto K, Iijima K, Shirakawa T, Kitagawa K, Satomura K, et al. (2001) PAX2 gene mutation in a family with isolated renal hypoplasia. J Am Soc Nephrol 12: 1769-1772. (Pubitemid 32674442)
13. Yoshimura K, Yoshida S, Yamaji Y, Komori A, Yoshida A, et al. (2005) De novo insG619 mutation in PAX2 gene in a Japanese patient with papillorenal syndrome. Am J Ophthalmol 139: 733-735.
14. Cheong HI, Cho HY, Kim JH, Yu YS, Ha IS, et al. (2007) A clinico-genetic study of renal coloboma syndrome in children. Pediatr Nephrol 22: 1283-1289. (Pubitemid 47054917)
15. Devriendt K, Matthijs G, Van Damme B, Van Caesbroeck D, Eccles M, et al. (1998) Missense mutation and hexanucleotide duplication in the PAX2 gene in two unrelated families with renal-coloboma syndrome (MIM 120330). Hum Genet 103: 149-153. (Pubitemid 28444651)
16. Higashide T, Wada T, Sakurai M, Yokoyama H, Sugiyama K (2005) Macular abnormalities and optic disk anomaly associated with a new PAX2 missense mutation. Am J Ophthalmol 139: 203-205. (Pubitemid 40094870)
17. Schimmenti LA, Cunliffe HE, McNoe LA, Ward TA, French MC, et al. (1997) Further delineation of renal-coloboma syndrome in patients with extreme variability of phenotype and identical PAX2 mutations. Am J Hum Genet 60: 869-878.
18. Sanyanusin P, McNoe LA, Sullivan MJ, Weaver RG, Eccles MR (1995) Mutation of PAX2 in two siblings with renal-coloboma syndrome. Hum Mol Genet 4: 2183-2184.
19. Schimmenti LA, Shim HH, Wirtschafter JD, Panzarino VA, Kashtan CE, et al. (1999) Homonucleotide expansion and contraction mutations of PAX2 and inclusion of Chiari 1 malformation as part of renal-coloboma syndrome. Hum Mutat 14: 369-376.
20. Nornes HO, Dressler GR, Knapik EW, Deutsch U, Gruss P (1990) Spatially and temporally restricted expression of Pax2 during murine neurogenesis. Development 109: 797-809.
21. Dressler GR, Deutsch U, Chowdhury K, Nornes HO, Gruss P (1990) Pax2, a new murine paired-box-containing gene and its expression in the developing excretory system. Development 109: 787-795.
22. Torres M, Gomez-Pardo E, Dressler GR, Gruss P (1995) Pax-2 controls multiple steps of urogenital development. Development 121: 4057-4065. (Pubitemid 26007357)
23. Torres M, Gomez-Pardo E, Gruss P (1996) Pax2 contributes to inner ear patterning and optic nerve trajectory. Development 122: 3381-3391. (Pubitemid 26395981)
24. Favor J, Sandulache R, Neuhauser-Klaus A, Pretsch W, Chatterjee B, et al. (1996) The mouse Pax2(1Neu) mutation is identical to a human PAX2 mutation in a family with renal-coloboma syndrome and results in developmental defects of the brain, ear, eye, and kidney. Proc Natl Acad Sci U S A 93: 13870-13875. (Pubitemid 26424213)
25. Keller SA, Jones JM, Boyle A, Barrow LL, Killen PD, et al. (1994) Kidney and retinal defects (Krd), a transgene-induced mutation with a deletion of mouse chromosome 19 that includes the Pax2 locus. Genomics 23: 309-320. (Pubitemid 24308251)
26. Porteous S, Torban E, Cho NP, Cunliffe H, Chua L, et al. (2000) Primary renal hypoplasia in humans and mice with PAX2 mutations: evidence of increased apoptosis in fetal kidneys of Pax2(1Neu) +/- mutant mice. Hum Mol Genet 9: 1-11. (Pubitemid 30145283)
27. Xu HE, Rould MA, Xu W, Epstein JA, Maas RL, et al. (1999) Crystal structure of the human Pax6 paired domain-DNA complex reveals specific roles for the linker region and carboxy-terminal subdomain in DNA binding. Genes Dev 13: 1263-1275. (Pubitemid 29250194)
28. Xu W, Rould MA, Jun S, Desplan C, Pabo CO (1995) Crystal structure of a paired domain-DNA complex at 2.5 A resolution reveals structural basis for Pax developmental mutations. Cell 80: 639-650.
29. Cai Y, Brophy PD, Levitan I, Stifani S, Dressler GR (2003) Groucho suppresses Pax2 transactivation by inhibition of JNK-mediated phosphorylation. Embo J 22: 5522-5529. (Pubitemid 37279961)
30. Cai Y, Lechner MS, Nihalani D, Prindle MJ, Holzman LB, et al. (2002) Phosphorylation of Pax2 by the c-Jun N-terminal kinase and enhanced Pax2-dependent transcription activation. J Biol Chem 277: 1217-1222.
31. Otteson DC, Shelden E, Jones JM, Kameoka J, Hitchcock PF (1998) Pax2 expression and retinal morphogenesis in the normal and Krd mouse. Dev Biol 193: 209-224. (Pubitemid 28113563)
32. Lechner MS, Dressler GR (1996) Mapping of Pax-2 transcription activation domains. J Biol Chem 271: 21088-21093. (Pubitemid 26292958)
33. Fickenscher HR, Chalepakis G, Gruss P (1993) Murine Pax-2 protein is a sequence-specific trans-activator with expression in the genital system. DNA Cell Biol 12: 381-391. (Pubitemid 23183516)
34. Gronskov K, Rosenberg T, Sand A, Brondum-Nielsen K (1999) Mutational analysis of PAX6: 16 novel mutations including 5 missense mutations with a mild aniridia phenotype. Eur J Hum Genet 7: 274-286. (Pubitemid 29213733)
35. Saleem RA, Banerjee-Basu S, Berry FB, Baxevanis AD, Walter MA (2001) Analyses of the Effects That Disease-Causing Missense Mutations Have on the Structure and Function of the Winged-Helix Protein FOXC1. The American Journal of Human Genetics 68: 627-641. (Pubitemid 32202758)
36. Footz TK, Idrees F, Acharya M, Kozlowski K, Walter MA (2009) Analysis of mutations of the PITX2 transcription factor found in Axenfeld-Rieger Syndrome patients. Invest Ophthalmol Vis Sci. pp iovs.08-3251.
37. Footz T, Idrees F, Acharya M, Kozlowski K, Walter MA (2009) Analysis of mutations of the PITX2 transcription factor found in patients with Axenfeld-Rieger syndrome. Invest Ophthalmol Vis Sci 50: 2599-2606.
38. D'Elia AV, Puppin C, Pellizzari L, Pianta A, Bregant E, et al. (2006) Molecular analysis of a human PAX6 homeobox mutant. Eur J Hum Genet 14: 744-751. (Pubitemid 43797272)
39. Bowes C, Li T, Danciger M, Baxter LC, Applebury ML, et al. (1990) Retinal degeneration in the rd mouse is caused by a defect in the beta subunit of rod cGMP-phosphodiesterase. Nature 347: 677-680.
40. Ji W, Herron B, Jones JM, Jenkins NA, Gilbert DJ, et al. (1999) Identification of genes within the Krd deletion on mouse chromosome 19. Mamm Genome 10: 399-401. (Pubitemid 29390495)
41. Mi H, Barres BA (1999) Purification and characterization of astrocyte precursor cells in the developing rat optic nerve. J Neurosci 19: 1049-1061. (Pubitemid 29066167)
42. Chan-Ling T, McLeod DS, Hughes S, Baxter L, Chu Y, et al. (2004) Astrocyte-endothelial cell relationships during human retinal vascular development. Invest Ophthalmol Vis Sci 45: 2020-2032. (Pubitemid 38869002)
43. Chu Y, Hughes S, Chan-Ling T (2001) Differentiation and migration of astrocyte precursor cells and astrocytes in human fetal retina: relevance to optic nerve coloboma. Faseb J 15: 2013-2015.
44. Gong KQ, Yallowitz AR, Sun H, Dressler GR, Wellik DM (2007) A Hox-Eya-Pax complex regulates early kidney developmental gene expression. Mol Cell Biol 27: 7661-7668. (Pubitemid 350033671)
45. Du X, Tabeta K, Hoebe K, Liu H, Mann N, et al. (2004) Velvet, a dominant Egfr mutation that causes wavy hair and defective eyelid development in mice. Genetics 166: 331-340. (Pubitemid 38364724)
46. Smith RS, editor (2002) Systematic Evaluation of the Mouse Eye: Anatomy, Pathology and Biomethods. First ed. Boca Raton: CRC Press.
47. Abola E, Bernstein FC, Bryant SH, Koetzle TF, Weng J (1987) Protein data bank. In: Bergerhoff G, Sievers R, eds. Crystallographic databases-information content, software systems, scientific applications. Cambridge: Data Comission on the International Union of Crystallography. pp 107-132.
48. Needleman SB, Wunsch CD (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol 48: 443-453.
49. Lee C, Subbiah S (1991) Prediction of protein side-chain conformation by packing optimization. J Mol Biol 217: 373-388.
50. Lee C (1994) Predicting protein mutant energetics by self-consistent ensemble optimization. J Mol Biol 236: 918-939.
51. Levitt M (1992) Accurate modeling of protein conformation by automatic segment matching. J Mol Biol 226: 507-533.
52. Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Cryst 26: 283-291.
53. Jiang X, Coffino P, Li X (2004) Development of a method for screening shortlived proteins using green fluorescent protein. Genome Biol 5: R81.