661W is a retinal ganglion precursor-like cell line in which glaucoma-associated optineurin mutants induce cell death selectively

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Sayyad, Zuberwasim ^a   Sirohi, Kapil ^a,b   Radha, Vegesna ^a   Swarup, Ghanshyam ^a  

^a CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

^b DEPARTMENT OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; BX795; EYE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; MTAP2 PROTEIN, MOUSE; NERVE PROTEIN; NEUN PROTEIN, MOUSE; NUCLEAR PROTEIN; OPTN PROTEIN, MOUSE; PYRIMIDINE DERIVATIVE; STAUROSPORINE; THIOPHENE DERIVATIVE; THY 1 MEMBRANE GLYCOPROTEIN; TRANSCRIPTION FACTOR POU4F3; TUBULIN;

ANIMAL; APOPTOSIS; CELL DIFFERENTIATION; CELL LINE; CYTOLOGY; DRUG EFFECT; GENETICS; GLAUCOMA; METABOLISM; MOUSE; NEURAL STEM CELL; PATHOLOGY; RETINA GANGLION CELL; SITE DIRECTED MUTAGENESIS;

ANIMALS; APOPTOSIS; BIOMARKERS; CELL DIFFERENTIATION; CELL LINE; EYE PROTEINS; GLAUCOMA; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MUTAGENESIS, SITE-DIRECTED; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; NUCLEAR PROTEINS; PYRIMIDINES; RETINAL GANGLION CELLS; STAUROSPORINE; THIOPHENES; THY-1 ANTIGENS; TRANSCRIPTION FACTOR BRN-3C; TUBULIN;

EID: 85037030784     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-17241-0     Document Type: Article

References (60)

1. Hamel, C. P. Cone rod dystrophies. Orphanet J Rare Dis 2, 7, https://doi.org/10.1186/1750-1172-2-7 (2007).
2. van Soest, S., Westerveld, A., de Jong, P. T., Bleeker-Wagemakers, E. M. & Bergen, A. A. Retinitis pigmentosa: defined from a molecular point of view. Surv Ophthalmol 43, 321-334 (1999).
3. You, Y., Gupta, V. K., Li, J. C., Klistorner, A. & Graham, S. L. Optic neuropathies: characteristic features and mechanisms of retinal ganglion cell loss. Rev Neurosci 24, 301-321, https://doi.org/10.1515/revneuro-2013-0003 (2013).
4. Quigley, H. A. & Broman, A. T. The number of people with glaucoma worldwide in 2010 and 2020. Br J Ophthalmol 90, 262-267, https://doi.org/10.1136/bjo.2005.081224 (2006).
5. Nork, T. M. et al. Swelling and loss of photoreceptors in chronic human and experimental glaucomas. Arch Ophthalmol 118, 235-245 (2000).
6. Agudo-Barriuso, M., Villegas-Perez, M. P., de Imperial, J. M. & Vidal-Sanz, M. Anatomical and functional damage in experimental glaucoma. Curr Opin Pharmacol 13, 5-11, https://doi.org/10.1016/j.coph.2012.09.006 (2013).
7. Raz, D., Perlman, I., Percicot, C. L., Lambrou, G. N. & Ofri, R. Functional damage to inner and outer retinal cells in experimental glaucoma. Invest Ophthalmol Vis Sci 44, 3675-3684 (2003).
8. Choi, S. S. et al. Evidence of outer retinal changes in glaucoma patients as revealed by ultrahigh-resolution in vivo retinal imaging. Br J Ophthalmol 95, 131-141, https://doi.org/10.1136/bjo.2010.183756 (2011).
9. Wiggs, J. L. & Pasquale, L. R. Genetics of Glaucoma. Hum Mol Genet. https://doi.org/10.1093/hmg/ddx184 (2017).
10. Liu, Y. & Allingham, R. R. Major review: Molecular genetics of primary open-angle glaucoma. Exp Eye Res 160, 62-84, https://doi.org/10.1016/j.exer.2017.05.002 (2017).
11. Stone, E. M. et al. Identification of a gene that causes primary open angle glaucoma. Science 275, 668-670 (1997).
12. Rezaie, T. et al. Adult-onset primary open-angle glaucoma caused by mutations in optineurin. Science 295, 1077-1079, https://doi.org/10.1126/science.1066901 (2002).
13. Sirohi, K. & Swarup, G. Defects in autophagy caused by glaucoma-associated mutations in optineurin. Exp Eye Res 144, 54-63, https://doi.org/10.1016/j.exer.2015.08.020 (2016).
14. Fingert, J. H. et al. Copy number variations on chromosome 12q14 in patients with normal tension glaucoma. Hum Mol Genet 20, 2482-2494, https://doi.org/10.1093/hmg/ddr123 (2011).
15. Monemi, S. et al. Identification of a novel adult-onset primary open-angle glaucoma (POAG) gene on 5q22.1. Hum Mol Genet 14, 725-733, https://doi.org/10.1093/hmg/ddi068 (2005).
16. Pasutto, F. et al. Variants in ASB10 are associated with open-angle glaucoma. Hum Mol Genet 21, 1336-1349, https://doi.org/10.1093/hmg/ddr572 (2012).
17. Pasutto, F. et al. Heterozygous NTF4 mutations impairing neurotrophin-4 signaling in patients with primary open-angle glaucoma. Am J Hum Genet 85, 447-456, https://doi.org/10.1016/j.ajhg.2009.08.016 (2009).
18. Minegishi, Y., Nakayama, M., Iejima, D., Kawase, K. & Iwata, T. Significance of optineurin mutations in glaucoma and other diseases. Prog Retin Eye Res 55, 149-181, https://doi.org/10.1016/j.preteyeres.2016.08.002 (2016).
19. Ying, H. & Yue, B. Y. Cellular and molecular biology of optineurin. Int Rev Cell Mol Biol 294, 223-258, https://doi.org/10.1016/b978-0-12-394305-7.00005-7 (2012).
20. Anderson, D. R. Collaborative normal tension glaucoma study. Curr Opin Ophthalmol 14, 86-90 (2003).
21. Maruyama, H. et al. Mutations of optineurin in amyotrophic lateral sclerosis. Nature 465, 223-226, https://doi.org/10.1038/nature08971 (2010).
22. Tan, E. et al. Expression of cone-photoreceptor-specific antigens in a cell line derived from retinal tumors in transgenic mice. Invest Ophthalmol Vis Sci 45, 764-768 (2004).
23. Kuse, Y., Tsuruma, K., Kanno, Y., Shimazawa, M. & Hara, H. CCR3 Is Associated with the Death of a Photoreceptor Cell-line Induced by Light Exposure. Front Pharmacol 8, 207, https://doi.org/10.3389/fphar.2017.00207 (2017).
24. Thompson, A. F., Crowe, M. E., Lieven, C. J. & Levin, L. A. Induction of Neuronal Morphology in the 661W Cone Photoreceptor Cell Line with Staurosporine. PLoS One 10, e0145270, https://doi.org/10.1371/journal.pone.0145270 (2015).
25. Sippl, C. & Tamm, E. R. What is the nature of the RGC-5 cell line? Adv Exp Med Biol 801, 145-154, https://doi.org/10.1007/978-1-4614-3209-8-19 (2014).
26. Van Bergen, N. J. et al. Recharacterization of the RGC-5 retinal ganglion cell line. Invest Ophthalmol Vis Sci 50, 4267-4272, https://doi.org/10.1167/iovs.09-3484 (2009).
27. Wood, J. P., Chidlow, G., Tran, T., Crowston, J. G. & Casson, R. J. A comparison of differentiation protocols for RGC-5 cells. Invest Ophthalmol Vis Sci 51, 3774-3783, https://doi.org/10.1167/iovs.09-4305 (2010).
28. Chalasani, M. L., Kumari, A., Radha, V. & Swarup, G. E50K-OPTN-induced retinal cell death involves the Rab GTPase-activating protein, TBC1D17 mediated block in autophagy. PLoS One 9, e95758, https://doi.org/10.1371/journal.pone.0095758 (2014).
29. Sirohi, K., Kumari, A., Radha, V. & Swarup, G. A Glaucoma-Associated Variant of Optineurin, M98K, Activates Tbk1 to Enhance Autophagosome Formation and Retinal Cell Death Dependent on Ser177 Phosphorylation of Optineurin. PLoS One 10, e0138289, https://doi.org/10.1371/journal.pone.0138289 (2015).
30. Krishnamoorthy, R. R., Clark, A. F., Daudt, D., Vishwanatha, J. K. & Yorio, T. A forensic path to RGC-5 cell line identification: lessons learned. Invest Ophthalmol Vis Sci 54, 5712-5719, https://doi.org/10.1167/iovs.13-12085 (2013).
31. Chalasani, M. L. et al. A glaucoma-associated mutant of optineurin selectively induces death of retinal ganglion cells which is inhibited by antioxidants. Invest Ophthalmol Vis Sci 48, 1607-1614, https://doi.org/10.1167/iovs.06-0834 (2007).
32. Shen, X. et al. Processing of optineurin in neuronal cells. J Biol Chem 286, 3618-3629, https://doi.org/10.1074/jbc.M110.175810 (2011).
33. Zhu, M., Li, A., Chen, J., Zhang, S. & Wu, J. Effects of optineurin mutants on SH-SY5Y cell survival. Mol Cell Neurosci 74, 18-24, https://doi.org/10.1016/j.mcn.2016.03.003 (2016).
34. Akizuki, M. et al. Optineurin suppression causes neuronal cell death via NF-kappaB pathway. J Neurochem 126, 699-704, https://doi.org/10.1111/jnc.12326 (2013).
35. Aung, T. et al. Clinical features and course of patients with glaucoma with the E50K mutation in the optineurin gene. Invest Ophthalmol Vis Sci 46, 2816-2822, https://doi.org/10.1167/iovs.04-1133 (2005).
36. Chi, Z. L. et al. Overexpression of optineurin E50K disrupts Rab8 interaction and leads to a progressive retinal degeneration in mice. Hum Mol Genet 19, 2606-2615, https://doi.org/10.1093/hmg/ddq146 (2010).
37. Tseng, H. C. et al. Visual impairment in an optineurin mouse model of primary open-angle glaucoma. Neurobiol Aging 36, 2201-2212, https://doi.org/10.1016/j.neurobiolaging.2015.02.012 (2015).
38. Minegishi, Y. et al. Enhanced optineurin E50K-TBK1 interaction evokes protein insolubility and initiates familial primary open-angle glaucoma. Hum Mol Genet 22, 3559-3567, https://doi.org/10.1093/hmg/ddt210 (2013).
39. Sirohi, K. et al. M98K-OPTN induces transferrin receptor degradation and RAB12-mediated autophagic death in retinal ganglion cells. Autophagy 9, 510-527, https://doi.org/10.4161/auto.23458 (2013).
40. Kwong, J. M., Caprioli, J. & Piri, N. RNA binding protein with multiple splicing: a new marker for retinal ganglion cells. Invest Ophthalmol Vis Sci 51, 1052-1058, https://doi.org/10.1167/iovs.09-4098 (2010).
41. Rodriguez, A. R., de Sevilla Muller, L. P. & Brecha, N. C. The RNA binding protein RBPMS is a selective marker of ganglion cells in the mammalian retina. J Comp Neurol 522, 1411-1443, https://doi.org/10.1002/cne.23521 (2014).
42. Surgucheva, I., Weisman, A. D., Goldberg, J. L., Shnyra, A. & Surguchov, A. Gamma-synuclein as a marker of retinal ganglion cells. Mol Vis 14, 1540-1548 (2008).
43. Badea, T. C. & Nathans, J. Morphologies of mouse retinal ganglion cells expressing transcription factors Brn3a, Brn3b, and Brn3c: analysis of wild type and mutant cells using genetically-directed sparse labeling. Vision Res 51, 269-279, https://doi.org/10.1016/j.visres.2010.08.039 (2011).
44. Pan, L., Yang, Z., Feng, L. & Gan, L. Functional equivalence of Brn3 POU-domain transcription factors in mouse retinal neurogenesis. Development 132, 703-712, https://doi.org/10.1242/dev.01646 (2005).
45. Nadal-Nicolas, F. M. et al. Brn3a as a marker of retinal ganglion cells: qualitative and quantitative time course studies in naive and optic nerve-injured retinas. Invest Ophthalmol Vis Sci 50, 3860-3868, https://doi.org/10.1167/iovs.08-3267 (2009).
46. Beale, R. & Osborne, N. N. Localization of the Thy-1 antigen to the surfaces of rat retinal ganglion cells. Neurochem Int 4, 587-595 (1982).
47. Sarthy, P. V., Curtis, B. M. & Catterall, W. A. Retrograde labeling, enrichment, and characterization of retinal ganglion cells from the neonatal rat. J Neurosci 3, 2532-2544 (1983).
48. Barnstable, C. J. & Drager, U. C. Thy-1 antigen: a ganglion cell specific marker in rodent retina. Neuroscience 11, 847-855 (1984).
49. Parekh, R. B., Tse, A. G., Dwek, R. A., Williams, A. F. & Rademacher, T. W. Tissue-specific N-glycosylation, site-specific oligosaccharide patterns and lentil lectin recognition of rat Thy-1. Embo j 6, 1233-1244 (1987).
50. Mullen, R. J., Buck, C. R. & Smith, A. M. NeuN, a neuronal specific nuclear protein in vertebrates. Development 116, 201-211 (1992).
51. Wolf, H. K. et al. NeuN: a useful neuronal marker for diagnostic histopathology. J Histochem Cytochem 44, 1167-1171 (1996).
52. Park, H. Y., Kim, J. H. & Park, C. K. Neuronal cell death in the inner retina and the influence of vascular endothelial growth factor inhibition in a diabetic rat model. Am J Pathol 184, 1752-1762, https://doi.org/10.1016/j.ajpath.2014.02.016 (2014).
53. Eng, L. F., Ghirnikar, R. S. & Lee, Y. L. Glial fibrillary acidic protein: GFAP-thirty-one years (1969-2000). Neurochem Res 25, 1439-1451 (2000).
54. Cashman, N. R. et al. Neuroblastoma x spinal cord (NSC) hybrid cell lines resemble developing motor neurons. Dev Dyn 194, 209-221, https://doi.org/10.1002/aja.1001940306 (1992).
55. Wu, F. et al. Two transcription factors, Pou4f2 and Isl1, are sufficient to specify the retinal ganglion cell fate. Proc Natl Acad Sci USA 112, E1559-1568, https://doi.org/10.1073/pnas.1421535112 (2015).
56. Liu, W., Mo, Z. & Xiang, M. The Ath5 proneural genes function upstream of Brn3 POU domain transcription factor genes to promote retinal ganglion cell development. Proc Natl Acad Sci USA 98, 1649-1654, https://doi.org/10.1073/pnas.98.4.1649 (2001).
57. Yang, Z., Ding, K., Pan, L., Deng, M. & Gan, L. Math5 determines the competence state of retinal ganglion cell progenitors. Dev Biol 264, 240-254 (2003).
58. Cuenca, N. et al. Changes in the inner and outer retinal layers after acute increase of the intraocular pressure in adult albino Swiss mice. Exp Eye Res 91, 273-285, https://doi.org/10.1016/j.exer.2010.05.020 (2010).
59. Shivakrupa, R., Radha, V., Sudhakar, C. & Swarup, G. Physical and functional interaction between Hck tyrosine kinase and guanine nucleotide exchange factor C3G results in apoptosis, which is independent of C3G catalytic domain. J Biol Chem 278, 52188-52194, https://doi.org/10.1074/jbc.M310656200 (2003).
60. Raghawan, A. K. et al. A Disease-associated Mutant of NLRC4 Shows Enhanced Interaction with SUG1 Leading to Constitutive FADD-dependent Caspase-8 Activation and Cell Death. J Biol Chem 292, 1218-1230, https://doi.org/10.1074/jbc.M116.763979 (2017).