Functional validation of a human CAPN5 exome variant by lentiviral transduction into mouse retina

Human Molecular Genetics

Volumn 23, Issue 10, 2014, Pages 2665-2677

  Wert, Katherine J ^a,b   Skeie, Jessica M ^c,d   Bassuk, Alexander G ^c,d   Olivier, Alicia K ^d   Tsang, Stephen H ^a,b,c   Mahajan, Vinit B ^c,d  

^a Bernard and Shirlee Brown Glaucoma Laboratory Department of Pathology and Cell Biology College of Physicians and Surgeons Columbia University ^*  (United States)

^b Edward S Harkness Eye Institute   (United States)

^c UNIVERSITY OF IOWA   (United States)

^d UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN; CALPAIN 5 PROTEASE; GREEN FLUORESCENT PROTEIN; LENTIVIRUS VECTOR; PROTEINASE; RHODOPSIN; UNCLASSIFIED DRUG; AUTACOID; CAPN5 PROTEIN, HUMAN;

ADULT; ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B WAVE; BLURRED VISION; CASE REPORT; ELECTRORETINOGRAM; ELECTRORETINOGRAPHY; EPIRETINAL MEMBRANE; EXOME; FEMALE; FUNCTIONAL ASSESSMENT; GAIN OF FUNCTION MUTATION; GENE EXPRESSION PROFILING; GENETIC MODEL; GENETIC VARIABILITY; HAPLOINSUFFICIENCY; HISTOPATHOLOGY; HUMAN; IMMUNOCOMPETENT CELL; INFLAMMATION; INTRAOCULAR DRUG ADMINISTRATION; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PHENOTYPE; PHOTORECEPTOR; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RETINA; RETINA DEGENERATION; RETINA INNER PLEXIFORM LAYER; SEQUENCE ANALYSIS; VALIDATION STUDY; VIRAL GENE DELIVERY SYSTEM; WILD TYPE; AMINO ACID SEQUENCE; ANIMAL; C57BL MOUSE; DISEASE MODEL; GENETIC TRANSDUCTION; GENETICS; IMMUNOLOGY; LENTIVIRINAE; METABOLISM; MISSENSE MUTATION; MOLECULAR GENETICS; PATHOLOGY; PHOTORECEPTOR CELL; TRANSGENIC MOUSE; VITREORETINOPATHY;

ADULT; AMINO ACID SEQUENCE; ANIMALS; CALPAIN; DISEASE MODELS, ANIMAL; EXOME; HUMANS; INFLAMMATION MEDIATORS; LENTIVIRUS; MICE, INBRED C57BL; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PHOTORECEPTOR CELLS, VERTEBRATE; RETINA; TRANSDUCTION, GENETIC; VITREORETINOPATHY, PROLIFERATIVE;

EID: 84898793831     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt661     Document Type: Article

References (37)

1. Pastor, J.C., de la Rua, E.R. and Martin, F. (2002) Proliferative vitreoretinopathy: risk factors and pathobiology. Prog. Retin. Eye Res., 21, 127-144.
2. Frank, R.N. (2004) Diabetic retinopathy. N. Engl. J. Med., 350, 48-58.
3. Caspi, R.R. (2010) A look at autoimmunity and inflammation in the eye. J. Clin. Invest., 120, 3073-3083.
4. Mahajan, V.B., Skeie, J.M., Bassuk, A.G., Fingert, J.H., Braun, T.A., Daggett, H.T., Folk, J.C., Sheffield, V.C. and Stone, E.M. (2012) Calpain-5 mutations cause autoimmune uveitis, retinal neovascularization, and photoreceptor degeneration. PLoS Genet., 8, e1003001.
5. Syntichaki, P., Xu, K., Driscoll, M. and Tavernarakis, N. (2002) Specific aspartyl and calpain proteases are required for neurodegeneration in C. elegans. Nature, 419, 939-944.
6. Zatz, M. and Starling, A. (2005) Calpains and disease. N. Engl. J. Med., 352, 2413-2423.
7. Campbell, R.L. and Davies, P.L. (2012) Structure-function relationships in calpains. Biochem. J., 447, 335-351.
8. Polster, B.M., Basanez, G., Etxebarria, A., Hardwick, J.M. and Nicholls, D.G. (2005) Calpain I induces cleavage and release of apoptosis-inducing factor from isolated mitochondria. J. Biol. Chem., 280, 6447-6454.
9. Tlucek, P.S., Folk, J.C., Orien, J.A., Stone, E.M. and Mahajan, V.B. (2012) Inhibition of neovascularization but not fibrosis with the fluocinolone acetonide implant in autosomal dominant neovascular inflammatory vitreoretinopathy. Arch. Ophthalmol., 130, 1395-1401.
10. Tlucek, P.S., Folk, J.C., Sobol, W.M. and Mahajan, V.B. (2013) Surgical management of fibrotic encapsulation of the fluocinolone acetonide implant in CAPN5-associated proliferative vitreoretinopathy. Clin. Ophthalmol., 7, 1093-1098.
11. Bennett, S.R., Folk, J.C., Kimura, A.E., Russell, S.R., Stone, E.M. and Raphtis, E.M. (1990) Autosomal dominant neovascular inflammatory vitreoretinopathy. Ophthalmology, 97, 1125-1135; discussion 1135-1126.
12. Davis, R.J., Tosi, J., Janisch, K.M., Kasanuki, J.M., Wang, N.K., Kong, J., Tsui, I., Cilluffo, M., Woodruff, M.L., Fain, G.L. et al. (2008) Functional rescue of degenerating photoreceptors in mice homozygous for a hypomorphic cGMP phosphodiesterase 6 b allele (Pde6bH620Q). Invest. Ophthalmol. Vis. Sci., 49, 5067-5076.
13. Tosi, J., Sancho-Pelluz, J., Davis, R.J., Hsu, C.W., Wolpert, K.V., Sengillo, J.D., Lin, C.S. and Tsang, S.H. (2011) Lentivirus-mediated expression of cDNA and shRNA slows degeneration in retinitis pigmentosa. Exp. Biol. Med., 236, 1211-1217.
14. Neumar, R.W., Xu, Y.A., Gada, H., Guttmann, R.P. and Siman, R. (2003) Cross-talk between calpain and caspase proteolytic systems during neuronal apoptosis. J. Biol. Chem., 278, 14162-14167.
15. Feng, Z.H., Hao, J., Ye, L., Dayao, C., Yan, N., Yan, Y., Chu, L. and Shi, F.D. (2011) Overexpression of μ-calpain in the anterior temporal neocortex of patients with intractable epilepsy correlates with clinicopathological characteristics. Seizure, 20, 395-401.
16. Lakshmikuttyamma, A., Selvakumar, P., Kanthan, R., Kanthan, S.C. and Sharma, R.K. (2004) Overexpression of m-calpain in human colorectal adenocarcinomas. Cancer Epidemiol. Biomarkers Prev., 13, 1604-1609.
17. Storr, S.J., Carragher, N.O., Frame, M.C., Parr, T. and Martin, S.G. (2011) The calpain system and cancer. Nat. Rev. Cancer, 11, 364-374.
18. Wert, K.J., Davis, R.J., Sancho-Pelluz, J., Nishina, P.M. and Tsang, S.H. (2013) Gene therapy provides long-term visual function in a pre-clinical model of retinitis pigmentosa. Hum. Mol. Genet., 22, 558-567.
19. Mahajan, V.B., Vallone, J.G., Lin, J.H., Mullins, R.F., Ko, A.C., Folk, J.C. and Stone, E.M. (2010) T-cell infiltration in autosomal dominant neovascular inflammatory vitreoretinopathy. Mol. Vis., 16, 1034-1040.
20. Mahajan, V.B. and Lin, J.H. (2013) Lymphocyte Infiltration in CAPN5 autosomal dominant neovascular inflammatory vitreoretinopathy. Clin. Ophthalmol., 7, 1339-1345.
21. Burkard, N., Becher, J., Heindl, C., Neyses, L., Schuh, K. and Ritter, O. (2005) Targeted proteolysis sustains calcineurin activation. Circulation, 111, 1045-1053.
22. Curcio, C.A., Owsley, C. and Jackson, G.R. (2000) Spare the rods, save the cones in aging and age-related maculopathy. Invest. Ophthalmol. Vis. Sci., 41, 2015-2018.
23. Jackson, G.R., Owsley, C. and Curcio, C.A. (2002) Photoreceptor degeneration and dysfunction in aging and age-related maculopathy. Ageing Res. Rev., 1, 381-396.
24. Koh, A.H., Hogg, C.R. and Holder, G.E. (2001) The incidence of negative ERG in clinical practice. Doc. Ophthalmol., 102, 19-30.
25. Forrester, J.V., Klaska, I.P., Yu, T. and Kuffova, L. (2013) Uveitis in mouse and man. Int. Rev. Immunol., 32, 76-96.
26. Yadav, U.C. and Ramana, K.V. (2013) Endotoxin-induced uveitis in rodents. Methods Mol. Biol., 1031, 155-162.
27. Wert, K.J., Skeie, J.M., Davis, R.J., Tsang, S.H. and Mahajan, V.B. (2012) Subretinal injection of gene therapy vectors and stem cells in the perinatal mouse eye. J. Visual. Exp., (69), e4286.
28. Imai, S., Shimazawa, M., Nakanishi, T., Tsuruma, K. and Hara, H. (2010) Calpain inhibitor protects cells against light-induced retinal degeneration. J. Pharmacol. Exp. Ther., 335, 645-652.
29. David, J., Melamud, A., Kesner, L., Roth, S., Rosenbaum, P.S., Barone, F.C., Popp, S., Hassen, G.W., Stracher, A. and Rosenbaum, D.M. (2011) A novel calpain inhibitor for treatment of transient retinal ischemia in the rat. Neuroreport, 22, 633-636.
30. Nguyen, A.T., Campbell, M., Kenna, P.F., Kiang, A.S., Tam, L., Humphries, M.M. and Humphries, P. (2012) Calpain and photoreceptor apoptosis. Adv. Exp. Med. Biol., 723, 547-552.
31. Ozaki, T., Nakazawa, M., Yamashita, T., Sorimachi, H., Hata, S., Tomita, H., Isago, H., Baba, A. and Ishiguro, S. (2012) Intravitreal injection or topical eye-drop application of a mu-calpain C2L domain peptide protects against photoreceptor cell death in Royal College of Surgeons' rats, a model of retinitis pigmentosa. Biochim. Biophys. Acta, 1822, 1783-1795.
32. Rowell, H.A., Bassuk, A.G. and Mahajan, V.B. (2012) Monozygotic twins with CAPN5 autosomal dominant neovascular inflammatory vitreoretinopathy. Clin. Ophthalmol., 6, 2037-2044.
33. Wert, K.J., Sancho-Pelluz, J. and Tsang, S.H. (2014) Mid-stage intervention achieves similar efficacy as conventional early-stage treatment using gene therapy in a pre-clinical model of retinitis pigmentosa. Hum. Mol. Genet., 23, 514-523.
34. Hood, D.C. and Birch, D.G. (1992) Acomputational model of the amplitude and implicit time of the b-wave of the human ERG. Vis. Neurosci., 8, 107-126.
35. Hood, D.C. and Birch, D.G. (1994) Rod phototransduction in retinitis pigmentosa: estimation and interpretation of parameters derived from the rod a-wave. Invest. Ophthalmol. Vis. Sci., 35, 2948-2961.
36. Tsang, S.H., Burns, M.E., Calvert, P.D., Gouras, P., Baylor, D.A., Goff, S.P. and Arshavsky, V.Y. (1998) Role for the target enzyme in deactivation of photoreceptor G protein in vivo. Science, 282, 117-121.
37. Skeie, J.M., Tsang, S.H. and Mahajan, V.B. (2011) Evisceration of mouse vitreous and retina for proteomic analyses. J. Visual. Exp., (50), e2795.