Strain-dependent anterior segment dysgenesis and progression to glaucoma in Col4a1 mutant mice

Investigative Ophthalmology and Visual Science

Volumn 56, Issue 11, 2015, Pages 6823-6831

  Mao, Mao ^a   Smith, Richard S ^b   Alavi, Marcel V ^a   Marchant, Jeffrey K ^b,c   Cosma, Mihai ^b   Libby, Richard T ^d   John, Simon W M ^b,c,e   Gould, Douglas B ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b JACKSON LABORATORY   (United States)

^c TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Basement membrane; Genetic context; Glaucoma anterior segment; Phenotypic variation; Type IV collagen

Indexed keywords

AGE; AGED; ANIMAL TISSUE; ANTERIOR SEGMENT DYSGENESIS; ARTICLE; CILIARY BODY; COLLAGEN TYPE IV ALPHA 1 GENE; DISEASE COURSE; FEMALE; GENE; GENE MUTATION; GLAUCOMA; HISTOLOGY; INTRAOCULAR PRESSURE; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; OPHTHALMOSCOPY; OPTIC NERVE; OPTICAL COHERENCE TOMOGRAPHY; PRIORITY JOURNAL; PROGENY; SLIT LAMP; VISUAL DISORDER; ABNORMALITIES; ANIMAL; ANTERIOR EYE SEGMENT; C57BL MOUSE; DISEASE MODEL; EYE MALFORMATION; GENETICS; MUTANT MOUSE STRAIN; OPTIC DISK; PATHOLOGY; PATHOPHYSIOLOGY; PHENOTYPE; PHYSIOLOGY; RETINA GANGLION CELL;

COLLAGEN TYPE 4;

ANIMALS; ANTERIOR EYE SEGMENT; COLLAGEN TYPE IV; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; EYE ABNORMALITIES; GLAUCOMA; INTRAOCULAR PRESSURE; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; OPTIC DISK; PHENOTYPE; RETINAL GANGLION CELLS; TOMOGRAPHY, OPTICAL COHERENCE;

EID: 84945252216     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.15-17527     Document Type: Article

References (54)

1. Quigley HA, Broman AT. The number of people with glaucoma worldwide in 2010 and 2020. Br J Ophthalmol. 2006;90:262-267.
2. Quigley HA. Glaucoma. Lancet. 2011;377:1367-1377.
3. Strungaru MH, Dinu I, Walter MA. Genotype-phenotype correlations in Axenfeld-Rieger malformation and glaucoma patients with FOXC1 and PITX2 mutations. Invest Ophthalmol Vis Sci. 2007;48:228-237.
4. Reis LM, Semina EV. Genetics of anterior segment dysgenesis disorders. Curr Opin Ophthalmol. 2011;22: 314-324.
5. Kuo DS, Labelle-Dumais C, Gould DB. COL4A1 and COL4A2 mutations and disease: insights into pathogenic mechanisms and potential therapeutic targets. Hum Mol Genet. 2012;21:R97-R110.
6. Meuwissen ME, Halley DJ, Smit LS, et al. The expanding phenotype of COL4A1 and COL4A2 mutations: clinical data on 13 newly identified families and a review of the literature [published online ahead of print February 26, 2015]. Genet Med. doi:10.1038/gim.2014.210.
7. Van Agtmael T, Schlotzer-Schrehardt U, McKie L, et al. Dominant mutations of Col4a1 result in basement membrane defects which lead to anterior segment dysgenesis and glomerulopathy. Hum Mol Genet. 2005;14:3161-3168.
8. Favor J, Gloeckner CJ, Janik D, et al. Type IV procollagen missense mutations associated with defects of the eye, vascular stability, the brain, kidney function and embryonic or postnatal viability in the mouse, Mus musculus: an extension of the Col4a1 allelic series and the identification of the first two Col4a2 mutant alleles. Genetics. 2007;175: 725-736.
9. Gould DB, Marchant JK, Savinova OV, Smith RS, John SW. Col4a1 mutation causes endoplasmic reticulum stress and genetically modifiable ocular dysgenesis. Hum Mol Genet. 2007;16:798-807.
10. Gould DB, Phalan FC, Breedveld GJ, et al. Mutations in Col4a1 cause perinatal cerebral hemorrhage and porencephaly. Science. 2005;308:1167-1171.
11. Poschl E, Schlotzer-Schrehardt U, Brachvogel B, Saito K, Ninomiya Y, Mayer U. Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development. 2004; 131:1619-1628.
12. Coupry I, Sibon I, Mortemousque B, Rouanet F, Mine M, Goizet C. Ophthalmological features associated with COL4A1 mutations. Arch Ophthalmol. 2010;128:483-489.
13. Shah S, Kumar Y, McLean B, et al. A dominantly inherited mutation in collagen IV A1 (COL4A1) causing childhood onset stroke without porencephaly. Eur J Paediatr Neurol. 2010;14:182-187.
14. Rouaud T, Labauge P, Tournier Lasserve E, et al. Acute urinary retention due to a novel collagen COL4A1 mutation. Neurology. 2010;75:747-749.
15. Yoneda Y, Haginoya K, Kato M, et al. Phenotypic spectrum of COL4A1 mutations: porencephaly to schizencephaly. Ann Neurol. 2013;73:48-57.
16. Shah S, Ellard S, Kneen R, et al. Childhood presentation of COL4A1 mutations. Dev Med Child Neurol. 2012;54:569-574.
17. Rodahl E, Knappskog PM, Majewski J, et al. Variants of anterior segment dysgenesis and cerebral involvement in a large family with a novel COL4A1 mutation. Am J Ophthalmol. 2013;155:946-953.
18. Decio A, Tonduti D, Pichiecchio A, et al. A novel mutation in COL4A1 gene: a possible cause of early postnatal cerebrovascular events. Am J Med Genet A. 2015;167:810-815.
19. Xia XY, Li N, Cao X, et al. A novel COL4A1 gene mutation results in autosomal dominant non-syndromic congenital cataract in a Chinese family. BMC Med Genet. 2014;15:97.
20. Deml B, Reis LM, Maheshwari M, Griffis C, Bick D, Semina EV. Whole exome analysis identifies dominant COL4A1 mutations in patients with complex ocular phenotypes involving microphthalmia. Clin Genet. 2014;86:475-481.
21. Colin E, Sentilhes L, Sarfati A, et al. Fetal intracerebral hemorrhage and cataract: think COL4A1. J Perinatol. 2014;34:75-77.
22. Slavotinek AM, Garcia ST, Chandratillake G, et al. Exome sequencing in 32 patients with anophthalmia/microphthalmia and developmental eye defects [published online ahead of print December 2, 2014]. Clin Genet. doi:10. 1111/cge.12543.
23. Livingston J, Doherty D, Orcesi S, et al. COL4A1 mutations associated with a characteristic pattern of intracranial calcification. Neuropediatrics. 2011;42:227-233.
24. Kuo DS, Labelle-Dumais C, Mao M, et al. Allelic heterogeneity contributes to variability in ocular dysgenesis, myopathy and brain malformations caused by Col4a1 and Col4a2 mutations. Hum Mol Genet. 2014;23:1709-1722.
25. Jeanne M, Jorgensen J, Gould DB. Molecular and genetic analysis of collagen type IV mutant mouse models of spontaneous intracerebral hemorrhage identify mechanisms for stroke prevention [published online ahead of print March 9, 2015]. Circulation. doi:10.1161/ CIRCULATIONAHA.114.013395.
26. Keane TM, Goodstadt L, Danecek P, et al. Mouse genomic variation and its effect on phenotypes and gene regulation. Nature. 2011;477:289-294.
27. John SW, Hagaman JR, MacTaggart TE, Peng L, Smithes O. Intraocular pressure in inbred mouse strains. Invest Ophthalmol Vis Sci. 1997;38:249-253.
28. Savinova OV, Sugiyama F, Martin JE, et al. Intraocular pressure in genetically distinct mice: an update and strain survey. BMC Genet. 2001;2:12.
29. Libby RT, Smith RS, Savinova OV, et al. Modification of ocular defects in mouse developmental glaucoma models by tyrosinase. Science. 2003;299:1578-1581.
30. Anderson MG, Libby RT, Mao M, et al. Genetic context determines susceptibility to intraocular pressure elevation in a mouse pigmentary glaucoma. BMC Biol. 2006;4:20.
31. Anderson MG, Libby RT, Gould DB, Smith RS, John SW. High-dose radiation with bone marrow transfer prevents neurodegeneration in an inherited glaucoma. Proc Natl Acad Sci U S A. 2005;102:4566-4571.
32. Labelle-Dumais C, Dilworth DJ, Harrington EP, et al. COL4A1 mutations cause ocular dysgenesis, neuronal localization defects, and myopathy in mice and Walker-Warburg syndrome in humans. PLoS Genet. 2011;7: e1002062.
33. Acharya M, Huang L, Fleisch VC, Allison WT, Walter MA. A complex regulatory network of transcription factors critical for ocular development and disease. Hum Mol Genet. 2011;20:1610-1624.
34. Acharya M, Sharp MW, Mirzayans F, et al. Yeast two-hybrid analysis of a human trabecular meshwork cDNA library identified EFEMP2 as a novel PITX2 interacting protein. Mol Vis. 2012;18:2182-2189.
35. Huang L, Chi J, Berry FB, Footz TK, Sharp MW, Walter MA. Human p32 is a novel FOXC1-interacting protein that regulates FOXC1 transcriptional activity in ocular cells. Invest Ophthalmol Vis Sci. 2008;49:5243-5249.
36. Huang Y, Huang K, Boskovic G, et al. Proteomic and genomic analysis of PITX2 interacting and regulating networks. FEBS Lett. 2009;583:638-642.
37. Tamimi Y, Lines M, Coca-Prados M, Walter MA. Identification of target genes regulated by FOXC1 using nickel agarose-based chromatin enrichment. Invest Ophthalmol Vis Sci. 2004;45:3904-3913.
38. Berry FB, Skarie JM, Mirzayans F, et al. FOXC1 is required for cell viability and resistance to oxidative stress in the eye through the transcriptional regulation of FOXO1A. Hum Mol Genet. 2008;17:490-505.
39. Paylakhi SH, Moazzeni H, Yazdani S, et al. FOXC1 in human trabecular meshwork cells is involved in regulatory pathway that includes miR-204, MEIS2, and ITGbeta1. Exp Eye Res. 2013;111:112-121.
40. Hjalt TA, Amendt BA, Murray JC. PITX2 regulates procollagen lysyl hydroxylase (PLOD) gene expression: implications for the pathology of Rieger syndrome. J Cell Biol. 2001;152:545-552.
41. Zacharias AL, Gage PJ. Canonical Wnt/beta-catenin signaling is required for maintenance but not activation of Pitx2 expression in neural crest during eye development. Dev Dyn. 2010;239:3215-3225.
42. Strungaru MH, Footz T, Liu Y, et al. PITX2 is involved in stress response in cultured human trabecular meshwork cells through regulation of SLC13A3. Invest Ophthalmol Vis Sci. 2011;52:7625-7633.
43. Hjalt TA, Semina EV, Amendt BA, Murray JC. The Pitx2 protein in mouse development. Dev Dyn. 2000;218:195-200.
44. Gage PJ, Rhoades W, Prucka SK, Hjalt T. Fate maps of neural crest and mesoderm in the mammalian eye. Invest Ophthalmol Vis Sci. 2005;46:4200-4208.
45. Berry FB, Lines MA, Oas JM, et al. Functional interactions between FOXC1 and PITX2 underlie the sensitivity to FOXC1 gene dose in Axenfeld-Rieger syndrome and anterior segment dysgenesis. Hum Mol Genet. 2006;15: 905-919.
46. Bai X, Dilworth DJ, Weng YC, Gould DB. Developmental distribution of collagen IV isoforms and relevance to ocular diseases. Matrix Biol. 2009;28:194-201.
47. Shi Y, Tu Y, Mecham RP, Bassnett S. Ocular phenotype of Fbn2-null mice. Invest Ophthalmol Vis Sci. 2013;54: 7163-7173.
48. Zenker M, Aigner T,Wendler O, et al. Human laminin beta2 deficiency causes congenital nephrosis with mesangial sclerosis and distinct eye abnormalities. Hum Mol Genet. 2004;13:2625-2632.
49. Ylikarppa R, Eklund L, Sormunen R, et al. Lack of type XVIII collagen results in anterior ocular defects. FASEB J. 2003;17:2257-2259.
50. Fuerst PG, Rauch SM, Burgess RW. Defects in eye development in transgenic mice overexpressing the heparan sulfate proteoglycan agrin. Dev Biol. 2007;303: 165-180.
51. Iwao K, Inatani M, Matsumoto Y, et al. Heparan sulfate deficiency leads to Peters anomaly in mice by disturbing neural crest TGF-beta2 signaling. J Clin Invest. 2009;119: 1997-2008.
52. Khan K, Rudkin A, Parry DA, et al. Homozygous mutations in PXDN cause congenital cataract, corneal opacity, and developmental glaucoma. Am J Hum Genet. 2011;89:464-473.
53. Choi A, Lao R, Ling-Fung Tang P, et al. Novel mutations in PXDN cause microphthalmia and anterior segment dysgenesis. Eur J Hum Genet. 2015;23:337-341.
54. Yan X, Sabrautzki S, Horsch M, et al. Peroxidasin is essential for eye development in the mouse. Hum Mol Genet. 2014;23:5597-5614.