Mutation of ATF6 causes autosomal recessive achromatopsia

Human Genetics

Volumn 134, Issue 9, 2015, Pages 941-950

  Ansar, Muhammad ^a,b   Santos Cortez, Regie Lyn P ^a   Saqib, Muhammad Arif Nadeem ^b   Zulfiqar, Fareeha ^c   Lee, Kwanghyuk ^a   Ashraf, Naeem Mahmood ^b   Ullah, Ehsan ^b   Wang, Xin ^a   Sajid, Sundus ^b   Khan, Falak Sher ^b   Amin ud Din, Muhammad ^d   Smith, Joshua D ^e   Shendure, Jay ^e   Bamshad, Michael J ^e   Nickerson, Deborah A ^e   Hameed, Abdul ^f   Riazuddin, Saima ^c   Ahmed, Zubair M ^c   Ahmad, Wasim ^b   Leal, Suzanne M ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b QUAID I AZAM UNIVERSITY   (Pakistan)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF EDUCATION   (Pakistan)

^e UNIVERSITY OF WASHINGTON   (United States)

^f INSTITUTE OF BIOMEDICAL AND GENETIC ENGINEERING IBGE   (Pakistan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; ACTIVATING TRANSCRIPTION FACTOR 6 ANTIBODY; DNA; DNA BINDING PROTEIN; GLUTAMIC ACID; GLYCINE; MEMBRANE PROTEIN; PROTEIN ANTIBODY; UNCLASSIFIED DRUG; ATF6 PROTEIN, HUMAN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANTIBODY LABELING; ARTICLE; AUTOSOMAL RECESSIVE DISORDER; BLOOD SAMPLING; CELL NUCLEUS; CHROMOSOME 1Q23.1 Q24.3; CHROMOSOME DELETION; CHROMOSOME DUPLICATION; COLOR BLINDNESS; COLOR VISION; CONTROLLED STUDY; CYTOPLASM; DISEASE SEVERITY; ENDOPLASMIC RETICULUM STRESS; ETHNIC GROUP; EXOME; EXOME SEQUENCING; FAMILY; GENE MAPPING; GENE MUTATION; GENETIC LINKAGE; GENETIC VARIABILITY; HOMOZYGOSITY; HUMAN; HUMAN CELL; LINKAGE ANALYSIS; MAJOR CLINICAL STUDY; NONHUMAN; PAKISTANI; PHENOTYPE; PHOTORECEPTOR CELL; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN DOMAIN; RETINA GANGLION CELL; RETINA NERVE CELL; SEQUENCE ANALYSIS; UNFOLDED PROTEIN RESPONSE; WILD TYPE; ADOLESCENT; ANIMAL; ASIAN CONTINENTAL ANCESTRY GROUP; C57BL MOUSE; COLOR VISION DEFECT; CONSANGUINITY; FEMALE; FRAMESHIFT MUTATION; GENETICS; GENOTYPING TECHNIQUE; HOMOZYGOTE; LIMIT OF DETECTION; MALE; METABOLISM; MOUSE; NUCLEOTIDE SEQUENCE; PAKISTAN; PATHOPHYSIOLOGY; PEDIGREE; RETINA; SIGNAL TRANSDUCTION;

ACTIVATING TRANSCRIPTION FACTOR 6; ADOLESCENT; ANIMALS; ASIAN CONTINENTAL ANCESTRY GROUP; COLOR VISION DEFECTS; CONSANGUINITY; DNA MUTATIONAL ANALYSIS; EXOME; FEMALE; FRAMESHIFT MUTATION; GENOTYPING TECHNIQUES; HOMOZYGOTE; HUMANS; LIMIT OF DETECTION; MALE; MICE; MICE, INBRED C57BL; PAKISTAN; PEDIGREE; PHENOTYPE; RETINA; SIGNAL TRANSDUCTION;

EID: 84938987663     PISSN: 03406717     EISSN: 14321203     Source Type: Journal    
DOI: 10.1007/s00439-015-1571-4     Document Type: Article

References (60)

1. Abecasis GR, Cherny SS, Cookson WO, Cardon LR (2002) Merlin-rapid analysis of dense genetic maps using sparse gene flow trees. Nat Genet 30:97–101
2. Aboshiha J, Dubis AM, Cowing J, Fahy RT, Sundaram V, Bainbridge JW, Ali RR, Dubra A, Nardini M, Webster AR, Moore AT, Rubin G, Carroll J, Michaelides M (2014) A prospective longitudinal study of retinal structure and function in achromatopsia. Investig Ophthalmol Vis Sci 55:5733–5743
3. Chang B, Grau T, Dangel S, Hurd R, Jurklies B, Sener EC, Andreasson S, Dollfus H, Baumann B, Bolz S, Artemyev N, Kohl S, Heckenlively J, Wissinger B (2009) A homologous genetic basis of the murine cpfl1 mutant and human achromatopsia linked to mutations in the PDE6C gene. Proc Natl Acad Sci USA 106:19581–19586
4. Chiang WC, Hiramatsu N, Messah C, Kroeger H, Lin JH (2012) Selective activation of ATF6 and PERK endoplasmic reticulum stress signaling pathways prevent mutant rhodopsin accumulation. Investig Ophthalmol Vis Sci 53:7159–7166
5. Cinaroglu A, Gao C, Imrie D, Sadler KC (2011) Activating transcription factor 6 plays protective and pathological roles in steatosis due to endoplasmic reticulum stress in zebrafish. Hepatology 54:495–508
6. Ha Y, Shanmugam AK, Markand S, Zorrilla E, Ganapathy V, Smith SB (2014) Sigma receptor 1 modulates ER stress and Bcl2 in murine retina. Cell Tissue Res 356:15–27
7. Haze K, Yoshida H, Yanagi H, Yura T, Mori K (1999) Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol Biol Cell 10:3787–3799
8. Huang L, Zhang Q, Li S, Guan L, Xiao X, Zhang J, Jia X, Sun W, Zhu Z, Gao Y, Yin Y, Wang P, Guo X, Wang J, Zhang Q (2013) Exome sequencing of 47 Chinese families with cone–rod dystrophy: mutations in 25 known causative genes. PLoS One 8:e65546
9. Ismail M, Abid A, Anwar K, Mehdi SQ, Khaliq S (2006) Refinement of the locus for autosomal recessive cone–rod dystrophy (CORD8) linked to chromosome 1q23-q24 in a Pakistani family and exclusion of candidate genes. J Hum Genet 51:827–831
10. Kelley LA, Sternberg MJ (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4:363–371
11. Khaliq S, Hameed A, Ismail M, Anwar K, Leroy BP, Mehdi SQ, Payne AM, Bhattacharya SS (2000) Novel locus for autosomal recessive cone–rod dystrophy CORD8 mapping to chromosome 1q12–q24. Investig Ophthalmol Vis Sci 41:3709–3712
12. Kohl S, Coppieters F, Meire F, Schaich S, Roosing S, Brennenstuhl C, Bolz S, van Genderen MM, Riemslag FC, European Retinal Disease Consortium, Lukowski R, den Hollander AI, Cremers FP, De Baere E, Hoyng CB, Wissinger B (2012) A nonsense mutation in PDE6H causes autosomal-recessive incomplete achromatopsia. Am J Hum Genet 91:527–532
13. Kohl S, Marx T, Giddings I, Jägle H, Jacobson SG, Apfelstedt-Sylla E, Zrenner E, Sharpe LT, Wissinger B (1998) Total colour blindness is caused by mutations in the gene encoding the alpha-subunit of the cone photoreceptor cGMP-gated cation channel. Nat Genet 19:257–259
14. Kohl S, Baumann B, Broghammer M, Jägle H, Sieving P, Kellner U, Spegal R, Anastasi M, Zrenner E, Sharpe LT, Wissinger B (2000) Mutations in the CNGB3 gene encoding the beta-subunit of the cone photoreceptor cGMP-gated channel are responsible for achromatopsia (ACHM3) linked to chromosome 8q21. Hum Mol Genet 9:2107–2116
15. Kohl S, Baumann B, Rosenberg T, Kellner U, Lorenz B, Vadalà M, Jacobson SG, Wissinger B (2002) Mutations in the cone photoreceptor G-protein alpha-subunit gene GNAT2 in patients with achromatopsia. Am J Hum Genet 71:422–425
16. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760
17. Li GY, Fan B, Jiao YY (2014a) Rapamycin attenuates visible light-induced injury in retinal photoreceptor cells via inhibiting endoplasmic reticulum stress. Brain Res 1563:1–12
18. Li S, Huang L, Xiao X, Jia X, Guo X, Zhang Q (2014b) Identification of CNGA3 mutations in 46 Families: common cause of achromatopsia and cone–rod dystrophies in Chinese patients. JAMA Ophthalmol 132:1076–1083
19. Lin JC, Yang MC (2010) Correlation of visual function with health-related quality of life in glaucoma patients. J Eval Clin Pract 16:134–140
20. Lin JH, Li H, Yasumura D, Cohen HR, Zhang C, Panning B, Shokat KM, Lavail MM, Walter P (2007) IRE1 signaling affects cell fate during the unfolded protein response. Science 318:944–949
21. Matise TC, Chen F, Chen W, De La Vega FM, Hansen M, He C, Hyland FC, Kennedy GC, Kong X, Murray SS, Ziegle JS, Stewart WC, Buyske S (2007) A second-generation combined linkage physical map of the human genome. Genome Res 17:1783–1786
22. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303
23. Michaelides M, Hunt DM, Moore AT (2004) The cone dysfunction syndromes. Br J Ophthalmol 88:291–297
24. Miyagi H, Kanemoto S, Saito A, Asada R, Iwamoto H, Izumi S, Kido M, Gomi F, Nishida K, Kiuchi Y, Imaizumi K (2013) Transcriptional regulation of VEGFA by the endoplasmic reticulum stress transducer OASIS in ARPE-19 cells. PLoS One 8:e55155
25. Nakanishi T, Shimazawa M, Sugitani S, Kudo T, Imai S, Inokuchi Y, Tsuruma K, Hara H (2013) Role of endoplasmic reticulum stress in light-induced photoreceptor degeneration in mice. J Neurochem 125:111–124
26. O’Connell JR, Weeks DE (1998) PedCheck: a program for identification of genotype incompatibilities in linkage analysis. Am J Hum Genet 63:259–266
27. Saito A (2014) Physiological functions of endoplasmic reticulum stress transducer OASIS in central nervous system. Anat Sci Int 89:11–20
28. Saqib MA, Awan BM, Sarfraz M, Khan MN, Rashid S, Ansar M (2011) Genetic analysis of four Pakistani families with achromatopsia and a novel S4 motif mutation of CNGA3. Jpn J Ophthalmol 55:676–680
29. Schwarz JM, Cooper DN, Schuelke M, Seelow D (2014) MutationTaster2: mutation prediction for the deep-sequencing age. Nat Methods 11:361–362
30. Seelow D, Schuelke M, Hildebrandt F, Nurnberg P (2009) HomozygosityMapper—an interactive approach to homozygosity mapping. Nucleic Acids Res 37:593–599
31. Shoji T, Sakurai Y, Sato H, Chihara E, Takeuchi M (2011) Do type 2 diabetes patients without diabetic retinopathy or subjects with impaired fasting glucose have impaired colour vision? The Okubo Color Study Report. Diabet Med 28:865–871
32. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality multiple sequence alignments using clustal Omega. Mol Syst Biol 7:539
33. Silberstein M, Tzemach A, Dovgolevsky N, Fishelson M, Schuster A, Geiger D (2006) Online system for faster multipoint linkage analysis via parallel execution on thousands of personal computers. Am J Hum Genet 78:922–935
34. Thapa A, Morris L, Xu J, Ma H, Michalakis S, Biel M, Ding XQ (2012) Endoplasmic reticulum stress-associated cone photoreceptor degeneration in cyclic nucleotide-gated channel deficiency. J Biol Chem 287:18018–18029
35. Thiadens AA, Somervuo V, van den Born LI, Roosing S, van Schooneveld MJ, Kuijpers RW, van Moll-Ramirez N, Cremers FP, Hoyng CB, Klaver CC (2010) Progressive loss of cones in achromatopsia: an imaging study using spectral-domain optical coherence tomography. Investig Ophthalmol Vis Sci 51:5952–5957
36. Usui M, Yamaguchi S, Tanji Y, Tominaga R, Ishigaki Y, Fukumoto M, Katagiri H, Mori K, Oka Y, Ishihara H (2012) Atf6α-null mice are glucose intolerant due to pancreatic β-cell failure on a high-fat diet but partially resistant to diet-induced insulin resistance. Metabolism 61:1118–1128
37. Wu J, Rutkowski DT, Dubois M, Swathirajan J, Saunders T, Wang J, Song B, Yau GDY, Kaufman RJ (2007) ATF6α optimizes long-term endoplasmic reticulum function to protect cells from chronic stress. Dev Cell 13:351–364
38. Wu J, Sun P, Zhang X, Liu H, Jiang H, Zhu W, Wang H (2012) Inhibition of GPR40 protects MIN6 β cells from palmitate-induced ER stress and apoptosis. J Cell Biochem 113:1152–1158
39. Yamamoto K, Sato T, Matsui T, Sato M, Okada T, Yoshida H, Harada A, Mori K (2007) Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6α and XBP1. Dev Cell 13:165–176
40. Yang LP, Wu LM, Guo XJ, Tso MO (2007) Activation of endoplasmic reticulum stress in degenerating photoreceptors of the rd1 mouse. Investig Ophthalmol Vis Sci 48:5191–5198
41. Yang LP, Wu LM, Guo XJ, Li Y, Tso MO (2008) Endoplasmic reticulum stress is activated in light-induced retinal degeneration. J Neurosci Res 86:910–919
42. Yang C, Diiorio P, Jurczyk A, O’Sullivan-Murphy B, Urano F, Bortell R (2013) Pathological endoplasmic reticulum stress mediated by the IRE1 pathway contributes to pre-insulitic beta cell apoptosis in a virus-induced rat model of type 1 diabetes. Diabetologia 56:2638–2646
43. Yoshikawa T, Ogata N, Izuta H, Shimazawa M, Hara H, Takahashi K (2011) Increased expression of tight junctions in ARPE-19 cells under endoplasmic reticulum stress. Curr Eye Res 36:1153–1163
44. Yoshikawa A, Kamide T, Hashida K, Ta HM, Inahata Y, Takarada-Iemata M, Hattori T, Mori K, Takahashi R, Matsuyama T, Hayashi Y, Kitao Y, Hori O (2015) Deletion of Atf6α impairs astroglial activation and enhances neuronal death following brain ischemia in mice. J Neurochem 132:342–353
45. Zode GS, Sharma AB, Lin X, Searby CC, Bugge K, Kim GH, Clark AF, Sheffield VC (2014) Ocular-specific ER stress reduction rescues glaucoma in murine glucocorticoid-induced glaucoma. J Clin Investig 124:1956–1965
46. Burrows–Wheeler Aligner, http://bio-bwa.sourceforge.net/
47. Clustal Omega, http://www.ebi.ac.uk/Tools/msa/clustalo/
48. dbSNP, http://www.ncbi.nlm.nih.gov/SNP/
49. Exome Aggregation Consortium (ExAC), http://exac.broadinstitute.org/
50. Genome Analysis Toolkit (GATK), https://www.broadinstitute.org/gatk/
51. HomozygosityMapper, http://www.homozygositymapper.org/
52. MERLIN, http://www.sph.umich.edu/csg/abecasis/Merlin/
53. MutationTaster, http://www.mutationtaster.org/
54. Phyre2, http://www.sbg.bio.ic.ac.uk/phyre2/html/page.cgi?id=index
55. Primer3, http://frodo.wi.mit.edu/
56. RCSB Protein Data Bank (PDB), http://www.rcsb.org/pdb/home/home.do
57. SeattleSeq Annotation 137, http://snp.gs.washington.edu/SeattleSeqAnnotation137/
58. Superlink Online SNP 1.1, http://cbl-hapw.cs.technion.ac.il/superlink-snp/
59. UCSC Genome Bioinformatics, http://genome.ucsc.edu/
60. UniProt BLAST, http://www.uniprot.org/blast/