Molecular modeling indicates distinct classes of missense variants with mild and severe XLRS phenotypes

Human Molecular Genetics

Volumn 22, Issue 23, 2013, Pages 4756-4767

  Sergeev, Yuri V ^a   Vitale, Susan ^b   Sieving, Paul A ^c   Vincent, Ajoy ^d   Robson, Anthony G ^d,e   Moore, Anthony T ^e   Webster, Andrew R ^e   Holder, Graham E ^d,e  

^a Ophthalmic Genetics and Visual Function Branch   (United States)

^b Division of Epidemiology and Clinical Applications   (United States)

^c NATIONAL EYE INSTITUTE   (United States)

^d MOORFIELDS EYE HOSPITAL   (United Kingdom)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; CYSTEINE; PROLINE; RETINOSCHISIN;

ADOLESCENT; ADULT; ARTICLE; DARK ADAPTATION; DISEASE ASSOCIATION; DISEASE SEVERITY; ELECTRORETINOGRAM; GENETIC VARIABILITY; GENOTYPE; HUMAN; HYDROPHOBICITY; MAJOR CLINICAL STUDY; MISSENSE MUTATION; MOLECULAR MODEL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN STRUCTURE; RETINOSCHISIS; UNITED KINGDOM; VALIDITY; X CHROMOSOME RECESSIVE DISORDER; X LINKED RETINOSCHISIS;

ADOLESCENT; ADULT; COHORT STUDIES; ELECTRORETINOGRAPHY; EYE PROTEINS; FEMALE; GENETIC VARIATION; GENOTYPE; HUMANS; MODELS, MOLECULAR; MUTATION, MISSENSE; PHENOTYPE; PROTEIN CONFORMATION; PROTEIN STABILITY; RETINA; RETINOSCHISIS; YOUNG ADULT;

EID: 84887513092     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt329     Document Type: Article

References (60)

1. Sikkink, S.K., Biswas, S., Parry, N.R., Stanga, P.E. and Trump, D. (2007) X-linked retinoschisis: an update. J. Med. Genet., 44, 225-232.
2. [1998] Functional implications of the spectrum of mutations found in 234 cases with X-linked juvenile retinoschisis. The Retinoschisis Consortium. Hum. Mol. Genet., 7, 1185-1192.
3. Sauer, C.G., Gehrig, A., Warneke-Wittstock, R., Marquardt, A., Ewing, C.C., Gibson, A., Lorenz, B., Jurklies, B. and Weber, B.H. (1997) Positional cloning of the gene associated with X-linked juvenile retinoschisis. Nat. Genet., 17, 164-170.
4. Wu, W.W. and Molday, R.S. (2003) Defective discoidin domain structure, subunit assembly, and endoplasmic reticulum processing of retinoschisin are primary mechanisms responsible for X-linked retinoschisis. J. Biol. Chem., 278, 28139-28146.
5. Macedo-Ribeiro, S., Bode, W., Huber, R., Quinn-Allen, M.A., Kim, S.W., Ortel, T.L., Bourenkov, G.P., Bartunik, H.D., Stubbs, M.T., Kane, W.H. and Fuentes-Prior, P. (1999) Crystal structures of the membrane-binding C2 domain of human coagulation factor V. Nature, 402, 434-439.
6. Carafoli, F., Bihan, D., Stathopoulos, S., Konitsiotis, A.D., Kvansakul, M., Farndale, R.W., Leitinger, B. and Hohenester, E. (2009) Crystallographic insight into collagen recognition by discoidin domain receptor 2. Structure., 17, 1573-1581.
7. Adams, T.E., Hockin, M.F., Mann, K.G. and Everse, S.J. (2004) The crystal structure of activated protein C-inactivated bovine factor Va: implications for cofactor function. Proc. Natl Acad. Sci. U S A, 101, 8918-8923.
8. Baumgartner, S., Hofmann, K., Chiquet-Ehrismann, R. and Bucher, P. (1998) The discoidin domain family revisited: new members from prokaryotes and a homology-based fold prediction. Protein Sci., 7, 1626- 1631.
9. Kiedzierska, A., Smietana, K., Czepczynska, H. and Otlewski, J. (2007) Structural similarities and functional diversity of eukaryotic discoidin-like domains. Biochim. Biophys. Acta, 1774, 1069-1078.
10. Sunyaev, S., Ramensky, V., Koch, I., Lathe, W. III, Kondrashov, A.S. and Bork, P. (2001) Prediction of deleterious human alleles. Hum. Mol. Genet., 10, 591-597.
11. Tavtigian, S.V., Greenblatt, M.S., Lesueur, F. and Byrnes, G.B. (2008) In silico analysis of missense substitutions using sequence-alignment based methods. Hum. Mutat., 29, 1327-1336.
12. Monteiro, A.N. and Couch, F.J. (2006) Cancer risk assessment at the atomic level. Cancer Res., 66, 1897-1899.
13. Sergeev, Y.V., Caruso, R.C., Meltzer, M.R., Smaoui, N., MacDonald, I.M. and Sieving, P.A. (2010) Molecular modeling of retinoschisin with functional analysis of pathogenic mutations from human X-linked retinoschisis. Hum. Mol. Genet., 19, 1302-1313.
14. Kjellstrom, S., Bush, R.A., Zeng, Y., Takada, Y. and Sieving, P.A. (2007) Retinoschisin gene therapy and natural history in the Rs1h-KO mouse: long-term rescue from retinal degeneration. Invest Ophthalmol. Vis. Sci., 48, 3837-3845.
15. Vincent, A., Robson, A.G., Neveu, M.M., Wright, G.A., Moore, A.T., Webster, A.R. and Holder, G.E. (2013) A phenotype-genotype correlation study of X-linked retinoschisis. Ophthalmology, 120, 1454-1464.
16. Wu, W.W., Wong, J.P., Kast, J. and Molday, R.S. (2005) RS1, A discoidin domain-containing retinal cell adhesion protein associated with X-linked retinoschisis, exists as a novel disulfide-linked octamer. J. Biol. Chem., 280, 10721-10730.
17. Wang, T., Zhou, A., Waters, C.T., O'Connor, E., Read, R.J. and Trump, D. (2006) Molecular pathology of X linked retinoschisis: mutations interfere with retinoschisin secretion and oligomerisation. Br. J. Ophthalmol., 90, 81-86.
18. Wang, T., Waters, C.T., Rothman, A.M., Jakins, T.J., Romisch, K. and Trump, D. (2002) Intracellular retention of mutant retinoschisin is the pathological mechanism underlying X-linked retinoschisis. Hum. Mol. Genet., 11, 3097-3105.
19. Fraternali, F., Cavallo, L. and Musco, G. (2003) Effects of pathological mutations on the stability of a conserved amino acid triad in retinoschisin. FEBS Lett., 544, 21-26.
20. Breton, M.E., Schueller, A.W., Lamb, T.D. and Pugh, E.N. Jr. (1994) Analysis ofERGa-wave amplification and kinetics in terms of the G-protein cascade of phototransduction. Invest. Ophthalmol. Vis. Sci., 35, 295-309.
21. Penn, R.D. and Hagins, W.A. (1969) Signal transmission along retinal rods and the origin of the electroretinographic a-wave. Nature, 223, 201-204.
22. Newman, E.A. and Odette, L.L. (1984) Model of electroretinogram b-wave generation: a test of the K+ hypothesis. J. Neurophysiol., 51, 164-182.
23. Robson, J.G. and Frishman, L.J. (1995) Response linearity and kinetics of the cat retina: the bipolar cell component of the dark-adapted electroretinogram. Vis. Neurosci., 12, 837-850.
24. Stockton, R.A. and Slaughter, M.M. (1989) B-wave of the electroretinogram. A reflection of ON bipolar cell activity. J. Gen. Physiol, 93, 101-122.
25. Xu, X. and Karwoski, C.J. (1994) Current source density analysis of retinal field potentials. II. Pharmacological analysis of the b-wave and M-wave. J. Neurophysiol., 72, 96-105.
26. McBain, V.A., Egan, C.A., Pieris, S.J., Supramaniam, G., Webster, A.R., Bird, A.C. and Holder, G.E. (2007) Functional observations in vitamin A deficiency: diagnosis and time course of recovery. Eye (Lond), 21, 367-376.
27. Bradshaw, K., George, N., Moore, A. and Trump, D. (1999) Mutations of the XLRS1 gene cause abnormalities of photoreceptor as well as inner retinal responses of the ERG. Doc. Ophthalmol., 98, 153-173.
28. Peachey, N.S., Fishman, G.A., Derlacki, D.J. and Brigell, M.G. (1987) Psychophysical and electroretinographic findings in X-linked juvenile retinoschisis. Arch. Ophthalmol., 105, 513-516.
29. Sieving, P.A., Bingham, E.L., Kemp, J., Richards, J. and Hiriyanna, K. (1999) Juvenile X-linked retinoschisis from XLRS1 Arg213Trp mutation with preservation of the electroretinogram scotopic b-wave. Am. J. Ophthalmol., 128, 179-184.
30. Min, S.H., Molday, L.L., Seeliger, M.W., Dinculescu, A., Timmers, A.M., Janssen, A., Tonagel, F., Tanimoto, N., Weber, B.H., Molday, R.S. and Hauswirth, W.W. (2005) Prolonged recovery of retinal structure/function after gene therapy in an Rs1h-deficient mouse model of x-linked juvenile retinoschisis. Mol. Ther., 12, 644-651.
31. Park, T.K., Wu, Z., Kjellstrom, S., Zeng, Y., Bush, R.A., Sieving, P.A. and Colosi, P. (2009) Intravitreal delivery of AAV8 retinoschisin results in cell type-specific gene expression and retinal rescue in the Rs1-KO mouse. Gene Ther., 16, 916-926.
32. Sieving, P.A., Yashar, B.M. and Ayyagari, R. (1999) Juvenile retinoschisis: a model for molecular diagnostic testing of X-linked ophthalmic disease. Trans. Am. Ophthalmol. Soc., 97, 451-464.
33. Eksandh, L.C., Ponjavic, V., Ayyagari, R., Bingham, E.L., Hiriyanna, K.T., Andreasson, S., Ehinger, B. and Sieving, P.A. (2000) Phenotypic expression of juvenile X-linked retinoschisis in Swedish families with different mutations in the XLRS1 gene. Arch. Ophthalmol., 118, 1098-1104.
34. Inoue, Y.,Yamamoto, S., Okada, M., Tsujikawa, M., Inoue, T., Okada, A.A., Kusaka, S., Saito, Y., Wakabayashi, K., Miyake, Y. et al. (2000) X-linked retinoschisis with point mutations in the XLRS1 gene. Arch. Ophthalmol., 118, 93-96.
35. Shinoda, K., Ishida, S., Oguchi, Y. and Mashima, Y. (2000) Clinical characteristics of 14 japanese patients with X-linked juvenile retinoschisis associated with XLRS1 mutation. Ophthalmic Genet., 21, 171-180.
36. Hiraoka, M., Trese, M.T. and Shastry, B.S. (2000) X-Linked juvenile retinoschisis associated with a 4-base pair insertion at codon 55 of the XLRS1 gene. Biochem. Biophys. Res. Commun., 268, 370-372.
37. Nakamura, M., Ito, S., Terasaki, H. and Miyake, Y. (2001) Japanese X-linked juvenile retinoschisis: conflict of phenotype and genotype with novel mutations in the XLRS1 gene. Arch. Ophthalmol., 119, 1553-1554.
38. Shinoda, K., Mashima, Y., Ishida, S. and Oguchi, Y. (1999) Severe juvenile retinoschisis associated with a 33-bps deletion in XLRS1 gene. Ophthalmic Genet., 20, 57-61.
39. Simonelli, F., Cennamo, G., Ziviello, C., Testa, F., de, C.G., Nesti, A., Manitto, M.P., Ciccodicola, A., Banfi, S., Brancato, R. and Rinaldi, E. (2003) Clinical features of X linked juvenile retinoschisis associated with new mutations in the XLRS1 gene in Italian families. Br. J. Ophthalmol., 87, 1130-1134.
40. Pimenides, D., George, N.D., Yates, J.R., Bradshaw, K., Roberts, S.A., Moore, A.T. and Trump, D. (2005) X-linked retinoschisis: clinical phenotype and RS1 genotype in 86 UK patients. J. Med. Genet., 42, e35.
41. Noiva, R. (1999) Protein disulfide isomerase: the multifunctional redox chaperone of the endoplasmic reticulum. Semin. Cell Dev. Biol., 10, 481-493.
42. Tsai, B., Rodighiero, C., Lencer, W.I. and Rapoport, T.A. (2001) Protein disulfide isomerase acts as a redox-dependent chaperone to unfold cholera toxin. Cell, 104, 937-948.
43. Gruber, C.W., Cemazar, M., Heras, B., Martin, J.L. and Craik, D.J. (2006) Protein disulfide isomerase: the structure of oxidative folding. Trends Biochem. Sci., 31, 455-464.
44. Anfinsen, C.B., Haber, E., Sela, M. and White, F.H. Jr. (1961) The kinetics of formation of native ribonuclease during oxidation of the reduced polypeptide chain. Proc. Natl Acad. Sci. USA, 47, 1309-1314.
45. Dobson, C.M. (2004) Principles of protein folding, misfolding and aggregation. Semin. Cell Dev. Biol., 15, 3-16.
46. Kaushik, S. and Cuervo, A.M. (2008) Chaperone-mediated autophagy. Methods Mol. Biol., 445, 227-244.
47. Goldberg, A.L. (2003) Protein degradation and protection against misfolded or damaged proteins. Nature, 426, 895-899.
48. Vijayasarathy, C., Sui, R., Zeng, Y., Yang, G., Xu, F., Caruso, R.C., Lewis, R.A., Ziccardi, L. and Sieving, P.A. (2010) Molecular mechanisms leading to null-protein product from retinoschisin (RS1) signal-sequence mutants in X-linked retinoschisis (XLRS) disease. Hum. Mutat., 31, 1251-1260.
49. Marmor, M.F., Fulton, A.B., Holder, G.E., Miyake, Y., Brigell,M.and Bach, M. (2008) ISCEV Standard for full-field clinical electroretinography (2008 update). Doc. Ophthalmol., 119, 69-77.
50. Abola, E., Bernstein, F.C., Bryant, S.H., Koetzle, T.F. and Weng, J. (1987) Crystallographic databases-Information contene, software systems, scientific applications, In Allen, F.H., Bergerhoff, G. and Sievers, R. (eds), Data Comission of the International Union of Crystallography, Cambridge, pp. 107-132.
51. Lee, C. and Subbiah, S. (1991) Prediction of protein side-chain conformation by packing optimization. J. Mol. Biol., 217, 373-388.
52. Levitt, M. (1992) Accurate modeling of protein conformation by automatic segment matching. J. Mol. Biol., 226, 507-533.
53. Lee, C. (1994) Predicting protein mutant energetics by self-consistent ensemble optimization. J. Mol. Biol., 236, 918-939.
54. Tsodikov, O.V., Record, M.T. Jr and Sergeev, Y.V. (2002) Novel computer program for fast exact calculation of accessible and molecular surface areas and average surface curvature. J. Comput. Chem., 23, 600-609.
55. Kabsch,W.and Sander, C. (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22, 2577-2637.
56. Schymkowitz, J., Borg, J., Stricher, F., Nys, R., Rousseau, F. and Serrano, L. (2005) The FoldX web server: an online force field. Nucleic Acids Res., 33, W382-W388.
57. Grantham, R. (1974) Amino acid difference formula to help explain protein evolution. Science, 185, 862-864.
58. Bowles, K., Cukras, C., Turriff, A., Sergeev, Y., Vitale, S., Bush, R.A. and Sieving, P.A. (2011) X-linked retinoschisis: RS1 mutation severity and age affect the ERG phenotype in a cohort of 68 affected male subjects. Invest Ophthalmol. Vis. Sci., 52, 9250-9256.
59. Birch,D.G.and Anderson,J.L.(1992)Standardized full-fieldelectroretinography. Normal values and their variationwith age. Arch.Ophthalmol., 110, 1571-1576.
60. Weleber, R.G. (1981) The effect of age on human cone and rod ganzfeld electroretinograms. Invest Ophthalmol. Vis. Sci., 20, 392-399.