Gpr75 knockout mice display age-dependent cone photoreceptor cell loss.
G protein-coupled receptor
cone photoreceptor cell
knockout mouse
orphan receptor
retina
retinal degeneration
Journal
Journal of neurochemistry
ISSN: 1471-4159
Titre abrégé: J Neurochem
Pays: England
ID NLM: 2985190R
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
revised:
18
09
2023
received:
07
06
2023
accepted:
20
09
2023
medline:
13
11
2023
pubmed:
16
10
2023
entrez:
16
10
2023
Statut:
ppublish
Résumé
GPR75 is an orphan G protein-coupled receptor for which there is currently limited information and its function in physiology and disease is only recently beginning to emerge. This orphan receptor is expressed in the retina but its function in the eye is unknown. The earliest studies on GPR75 were conducted in the retina, where the receptor was first identified and cloned and mutations in the receptor were identified as a possible contributor to retinal degenerative disease. Despite these sporadic reports, the function of GPR75 in the retina and in retinal disease has yet to be explored. To assess whether GPR75 has a functional role in the retina, the retina of Gpr75 knockout mice was characterized. Knockout mice displayed a mild progressive retinal degeneration, which was accompanied by oxidative stress. The degeneration was because of the loss of both M-cone and S-cone photoreceptor cells. Housing mice under constant dark conditions reduced oxidative stress but did not prevent cone photoreceptor cell loss, indicating that oxidative stress is not a primary cause of the observed retinal degeneration. Studies here demonstrate an important role for GPR75 in maintaining the health of cone photoreceptor cells and that Gpr75 knockout mice can be used as a model to study cone photoreceptor cell loss.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
538-555Subventions
Organisme : NEI NIH HHS
ID : P30EY011373
Pays : United States
Organisme : NEI NIH HHS
ID : R01EY021731
Pays : United States
Organisme : NEI NIH HHS
ID : P30EY011373
Pays : United States
Organisme : NEI NIH HHS
ID : R01EY021731
Pays : United States
Informations de copyright
© 2023 The Authors. Journal of Neurochemistry published by John Wiley & Sons Ltd on behalf of International Society for Neurochemistry.
Références
Akbari, P., Gilani, A., Sosina, O., Kosmicki, J. A., Khrimian, L., Fang, Y. Y., Persaud, T., Garcia, V., Sun, D., Li, A., Mbatchou, J., Locke, A. E., Benner, C., Verweij, N., Lin, N., Hossain, S., Agostinucci, K., Pascale, J. V., Dirice, E., … Lotta, L. A. (2021). Sequencing of 640,000 exomes identifies GPR75 variants associated with protection from obesity. Science, 373(6550), eabf8683. https://doi.org/10.1126/science.abf8683
Applebury, M. L., Antoch, M. P., Baxter, L. C., Chun, L. L., Falk, J. D., Farhangfar, F., Kage, K., Krzystolik, M. G., Lyass, L. A., & Robbins, J. T. (2000). The murine cone photoreceptor: A single cone type expresses both S and M opsins with retinal spatial patterning. Neuron, 27(3), 513-523. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=11055434
Beatty, S., Koh, H., Phil, M., Henson, D., & Boulton, M. (2000). The role of oxidative stress in the pathogenesis of age-related macular degeneration. Survey of Ophthalmology, 45(2), 115-134. https://doi.org/10.1016/S0039-6257(00)00140-5
Benedetto, M. M., & Contin, M. A. (2019). Oxidative stress in retinal degeneration promoted by constant LED light. Frontiers in Cellular Neuroscience, 13, 139. https://doi.org/10.3389/fncel.2019.00139
Blanks, J. C., & Johnson, L. V. (1984). Specific binding of peanut lectin to a class of retinal photoreceptor cells. A species comparison. Investigative Ophthalmology and Visual Science, 25(5), 546-557. https://www.ncbi.nlm.nih.gov/pubmed/6715128
Cardenas, S., Colombero, C., Cruz, M., Mormandi, E., Adebesin, A. M., Falck, J. R., & Nowicki, S. (2023). 20-HETE/GPR75 pairing modulates the expression and transcriptional activity of the androgen receptor in androgen-sensitive prostate cancer cells. Molecular and Cellular Endocrinology, 559, 111784. https://doi.org/10.1016/j.mce.2022.111784
Cardenas, S., Colombero, C., Panelo, L., Dakarapu, R., Falck, J. R., Costas, M. A., & Nowicki, S. (2020). GPR75 receptor mediates 20-HETE-signaling and metastatic features of androgen-insensitive prostate cancer cells. Biochimica et Biophysica Acta-Molecular and Cell Biology of Lipids, 1865(2), 158573. https://doi.org/10.1016/j.bbalip.2019.158573
Carter-Dawson, L. D., & LaVail, M. M. (1979). Rods and cones in the mouse retina. I. Structural analysis using light and electron microscopy. Journal of Comparative Neurology, 188(2), 245-262. https://doi.org/10.1002/cne.901880204
Collin, G. B., Gogna, N., Chang, B., Damkham, N., Pinkney, J., Hyde, L. F., Stone, L., Naggert, J. K., Nishina, P. M., & Krebs, M. P. (2020). Mouse models of inherited retinal degeneration with photoreceptor cell loss. Cells, 9(4), 931. https://doi.org/10.3390/cells9040931
Colozo, A. T., Vasudevan, S., & Park, P. S. (2020). Retinal degeneration in mice expressing the constitutively active G90D rhodopsin mutant. Human Molecular Genetics, 29(6), 881-891. https://doi.org/10.1093/hmg/ddaa008
Contin, M. A., Benedetto, M. M., Quinteros-Quintana, M. L., & Guido, M. E. (2016). Light pollution: The possible consequences of excessive illumination on retina. Eye (London, England), 30(2), 255-263. https://doi.org/10.1038/eye.2015.221
Davenport, A. P., Alexander, S. P., Sharman, J. L., Pawson, A. J., Benson, H. E., Monaghan, A. E., Liew, W. C., Mpamhanga, C. P., Bonner, T. I., Neubig, R. R., Pin, J. P., Spedding, M., & Harmar, A. J. (2013). International Union of Basic and Clinical Pharmacology. LXXXVIII. G protein-coupled receptor list: Recommendations for new pairings with cognate ligands. Pharmacological Reviews, 65(3), 967-986. https://doi.org/10.1124/pr.112.007179
Dedoni, S., Campbell, L. A., Harvey, B. K., Avdoshina, V., & Mocchetti, I. (2018). The orphan G-protein-coupled receptor 75 signaling is activated by the chemokine CCL5. Journal of Neurochemistry, 146(5), 526-539. https://doi.org/10.1111/jnc.14463
Dziak, J. J., Dierker, L. C., & Abar, B. (2020). The interpretation of statistical power after the data have been gathered. Current Psychology, 39(3), 870-877. https://doi.org/10.1007/s12144-018-0018-1
Garcia, V., Gilani, A., Shkolnik, B., Pandey, V., Zhang, F. F., Dakarapu, R., Gandham, S. K., Reddy, N. R., Graves, J. P., Gruzdev, A., Zeldin, D. C., Capdevila, J. H., Falck, J. R., & Schwartzman, M. L. (2017). 20-HETE signals through G-protein-coupled receptor GPR75 (Gq) to affect vascular function and trigger hypertension. Circulation Research, 120(11), 1776-1788. https://doi.org/10.1161/CIRCRESAHA.116.310525
Gehrs, K. M., Anderson, D. H., Johnson, L. V., & Hageman, G. S. (2006). Age-related macular degeneration-Emerging pathogenetic and therapeutic concepts. Annals of Medicine, 38(7), 450-471. https://doi.org/10.1080/07853890600946724
Gonzalez-Fernandez, E., Staursky, D., Lucas, K., Nguyen, B. V., Li, M., Liu, Y., Washington, C., Coolen, L. M., Fan, F., & Roman, R. J. (2020). 20-HETE enzymes and receptors in the neurovascular unit: Implications in cerebrovascular disease. Frontiers in Neurology, 11, 983. https://doi.org/10.3389/fneur.2020.00983
Halliwell, B., & Whiteman, M. (2004). Measuring reactive species and oxidative damage in vivo and in cell culture: How should you do it and what do the results mean? British Journal of Pharmacology, 142(2), 231-255. https://doi.org/10.1038/sj.bjp.0705776
Heidari, R., Rasti, M., Shirazi Yeganeh, B., Niknahad, H., Saeedi, A., & Najibi, A. (2016). Sulfasalazine-induced renal and hepatic injury in rats and the protective role of taurine. BioImpacts: BI, 6(1), 3-8. https://doi.org/10.15171/bi.2016.01
Hollyfield, J. G. (2010). Age-related macular degeneration: The molecular link between oxidative damage, tissue-specific inflammation and outer retinal disease: The Proctor lecture. Investigative Ophthalmology and Visual Science, 51(3), 1275-1281. https://doi.org/10.1167/iovs.09-4478
Hossain, S., Gilani, A., Pascale, J., Villegas, E., Diegisser, D., Agostinucci, K., Kulaprathazhe, M. M., Dirice, E., Garcia, V., & Schwartzman, M. L. (2023). Gpr75-deficient mice are protected from high-fat diet-induced obesity. Obesity, 31(4), 1024-1037. https://doi.org/10.1002/oby.23692
Ignatov, A., Robert, J., Gregory-Evans, C., & Schaller, H. C. (2006). RANTES stimulates Ca2+ mobilization and inositol trisphosphate (IP3) formation in cells transfected with G protein-coupled receptor 75. British Journal of Pharmacology, 149(5), 490-497. https://doi.org/10.1038/sj.bjp.0706910
Karlsson, M., Zhang, C., Mear, L., Zhong, W., Digre, A., Katona, B., Sjostedt, E., Butler, L., Odeberg, J., Dusart, P., Edfors, F., Oksvold, P., von Feilitzen, K., Zwahlen, M., Arif, M., Altay, O., Li, X., Ozcan, M., Mardinoglu, A., … Lindskog, C. (2021). A single-cell type transcriptomics map of human tissues. Science Advances, 7(31), eabh2169. https://doi.org/10.1126/sciadv.abh2169
Komeima, K., Rogers, B. S., Lu, L., & Campochiaro, P. A. (2006). Antioxidants reduce cone cell death in a model of retinitis pigmentosa. Proceedings of the National Academy of Sciences of the United States of America, 103(30), 11300-11305. https://doi.org/10.1073/pnas.0604056103
Lamb, T. D. (2016). Why rods and cones? Eye (London, England), 30(2), 179-185. https://doi.org/10.1038/eye.2015.236
Laschet, C., Dupuis, N., & Hanson, J. (2018). The G protein-coupled receptors deorphanization landscape. Biochemical Pharmacology, 153, 62-74. https://doi.org/10.1016/j.bcp.2018.02.016
Liou, G. Y., & Storz, P. (2015). Detecting reactive oxygen species by immunohistochemistry. Methods in Molecular Biology, 1292, 97-104. https://doi.org/10.1007/978-1-4939-2522-3_7
Liu, B., Hassan, Z., Amisten, S., King, A. J., Bowe, J. E., Huang, G. C., Jones, P. M., & Persaud, S. J. (2013). The novel chemokine receptor, G-protein-coupled receptor 75, is expressed by islets and is coupled to stimulation of insulin secretion and improved glucose homeostasis. Diabetologia, 56(11), 2467-2476. https://doi.org/10.1007/s00125-013-3022-x
Mattapallil, M. J., Wawrousek, E. F., Chan, C. C., Zhao, H., Roychoudhury, J., Ferguson, T. A., & Caspi, R. R. (2012). The Rd8 mutation of the Crb1 gene is present in vendor lines of C57BL/6N mice and embryonic stem cells, and confounds ocular induced mutant phenotypes. Investigative Ophthalmology and Visual Science, 53(6), 2921-2927. https://doi.org/10.1167/iovs.12-9662
Michel, M. C., Wieland, T., & Tsujimoto, G. (2009). How reliable are G-protein-coupled receptor antibodies? Naunyn-Schmiedeberg's Archives of Pharmacology, 379(4), 385-388. https://doi.org/10.1007/s00210-009-0395-y
Molday, R. S., & MacKenzie, D. (1983). Monoclonal antibodies to rhodopsin: Characterization, cross-reactivity, and application as structural probes. Biochemistry, 22(3), 653-660. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=6188482
Ngo, T., Kufareva, I., Coleman, J., Graham, R. M., Abagyan, R., & Smith, N. J. (2016). Identifying ligands at orphan GPCRs: Current status using structure-based approaches. British Journal of Pharmacology, 173(20), 2934-2951. https://doi.org/10.1111/bph.13452
Nikonov, S. S., Brown, B. M., Davis, J. A., Zuniga, F. I., Bragin, A., Pugh, E. N., Jr., & Craft, C. M. (2008). Mouse cones require an arrestin for normal inactivation of phototransduction. Neuron, 59(3), 462-474. https://doi.org/10.1016/j.neuron.2008.06.011
Ortin-Martinez, A., Nadal-Nicolas, F. M., Jimenez-Lopez, M., Alburquerque-Bejar, J. J., Nieto-Lopez, L., Garcia-Ayuso, D., Villegas-Perez, M. P., Vidal-Sanz, M., & Agudo-Barriuso, M. (2014). Number and distribution of mouse retinal cone photoreceptors: Differences between an albino (Swiss) and a pigmented (C57/BL6) strain. PLoS One, 9(7), e102392. https://doi.org/10.1371/journal.pone.0102392
Oyster, C. W. (1999). The human eye: Structure and function. Sinauer Associates, Inc.
Pascale, J. V., Park, E. J., Adebesin, A. M., Falck, J. R., Schwartzman, M. L., & Garcia, V. (2021). Uncovering the signalling, structure and function of the 20-HETE-GPR75 pairing: Identifying the chemokine CCL5 as a negative regulator of GPR75. British Journal of Pharmacology, 178, 3813-3828. https://doi.org/10.1111/bph.15525
Powell, D. R., Doree, D. D., DaCosta, C. M., Platt, K. A., Brommage, R., Buhring, L., Revelli, J. P., & Shadoan, M. K. (2022). Mice lacking Gpr75 are Hypophagic and thin. Diabetes, Metabolic Syndrome and Obesity, 15, 45-58. https://doi.org/10.2147/DMSO.S342799
Power, M. J., Rogerson, L. E., Schubert, T., Berens, P., Euler, T., & Paquet-Durand, F. (2020). Systematic spatiotemporal mapping reveals divergent cell death pathways in three mouse models of hereditary retinal degeneration. Journal of Comparative Neurology, 528(7), 1113-1139. https://doi.org/10.1002/cne.24807
Rakshit, T., Senapati, S., Parmar, V. M., Sahu, B., Maeda, A., & Park, P. S. (2017). Adaptations in rod outer segment disc membranes in response to environmental lighting conditions. Biochimica et Biophysica Acta, 1864(10), 1691-1702. https://doi.org/10.1016/j.bbamcr.2017.06.013
Sahaboglu, A., Paquet-Durand, O., Dietter, J., Dengler, K., Bernhard-Kurz, S., Ekstrom, P. A., Hitzmann, B., Ueffing, M., & Paquet-Durand, F. (2013). Retinitis pigmentosa: Rapid neurodegeneration is governed by slow cell death mechanisms. Cell Death & Disease, 4(2), e488. https://doi.org/10.1038/cddis.2013.12
Samardzija, M., & Grimm, C. (2014). Mouse models for cone degeneration. Advances in Experimental Medicine and Biology, 801, 567-573. https://doi.org/10.1007/978-1-4614-3209-8_72
Sauer, C. G., White, K., Stohr, H., Grimm, T., Hutchinson, A., Bernstein, P. S., Lewis, R. A., Simonelli, F., Pauleikhoff, D., Allikmets, R., & Weber, B. H. (2001). Evaluation of the G protein coupled receptor-75 (GPR75) in age related macular degeneration. British Journal of Ophthalmology, 85(8), 969-975. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=11466257
Sawant, O. B., Horton, A. M., Zucaro, O. F., Chan, R., Bonilha, V. L., Samuels, I. S., & Rao, S. (2017). The circadian clock gene Bmal1 controls thyroid hormone-mediated spectral identity and cone photoreceptor function. Cell Reports, 21(3), 692-706. https://doi.org/10.1016/j.celrep.2017.09.069
Schmittgen, T. D., & Livak, K. J. (2008). Analyzing real-time PCR data by the comparative CT method. Nature Protocols, 3(6), 1101-1108. https://www.ncbi.nlm.nih.gov/pubmed/18546601
Senapati, S., Gragg, M., Samuels, I. S., Parmar, V. M., Maeda, A., & Park, P. S. (2018). Effect of dietary docosahexaenoic acid on rhodopsin content and packing in photoreceptor cell membranes. Biochimica et Biophysica Acta, 1860(6), 1403-1413. https://doi.org/10.1016/j.bbamem.2018.03.030
Shen, J., Yang, X., Dong, A., Petters, R. M., Peng, Y. W., Wong, F., & Campochiaro, P. A. (2005). Oxidative damage is a potential cause of cone cell death in retinitis pigmentosa. Journal of Cellular Physiology, 203(3), 457-464. https://doi.org/10.1002/jcp.20346
Speidell, A., Walton, S., Campbell, L. A., Tomassoni-Ardori, F., Tessarollo, L., Corbo, C., Taraballi, F., & Mocchetti, I. (2023). Mice deficient for G-protein-coupled receptor 75 display altered presynaptic structural protein expression and disrupted fear conditioning recall. Journal of Neurochemistry, 165(6), 827-841. https://doi.org/10.1111/jnc.15818
Sriram, K., & Insel, P. A. (2018). G protein-coupled receptors as targets for approved drugs: How many targets and how many drugs? Molecular Pharmacology, 93(4), 251-258. https://doi.org/10.1124/mol.117.111062
Szel, A., von Schantz, M., Rohlich, P., Farber, D. B., & van Veen, T. (1993). Difference in PNA label intensity between short- and middle-wavelength sensitive cones in the ground squirrel retina. Investigative Ophthalmology and Visual Science, 34(13), 3641-3645. https://www.ncbi.nlm.nih.gov/pubmed/8258523
Tarttelin, E. E., Kirschner, L. S., Bellingham, J., Baffi, J., Taymans, S. E., Gregory-Evans, K., Csaky, K., Stratakis, C. A., & Gregory-Evans, C. Y. (1999). Cloning and characterization of a novel orphan G-protein-coupled receptor localized to human chromosome 2p16. Biochemical and Biophysical Research Communications, 260(1), 174-180. https://doi.org/10.1006/bbrc.1999.0753
Trachsel-Moncho, L., Benlloch-Navarro, S., Fernandez-Carbonell, A., Ramirez-Lamelas, D. T., Olivar, T., Silvestre, D., Poch, E., & Miranda, M. (2018). Oxidative stress and autophagy-related changes during retinal degeneration and development. Cell Death & Disease, 9(8), 812. https://doi.org/10.1038/s41419-018-0855-8
Uhlen, M., Fagerberg, L., Hallstrom, B. M., Lindskog, C., Oksvold, P., Mardinoglu, A., Sivertsson, A., Kampf, C., Sjostedt, E., Asplund, A., Olsson, I., Edlund, K., Lundberg, E., Navani, S., Szigyarto, C. A., Odeberg, J., Djureinovic, D., Takanen, J. O., Hober, S., … Ponten, F. (2015). Proteomics. Tissue-based map of the human proteome. Science, 347(6220), 1260419. https://doi.org/10.1126/science.1260419
Xue, Y., Razafsky, D., Hodzic, D., & Kefalov, V. J. (2020). Mislocalization of cone nuclei impairs cone function in mice. FASEB Journal, 34(8), 10242-10249. https://doi.org/10.1096/fj.202000568R
Youssef, P. N., Sheibani, N., & Albert, D. M. (2011). Retinal light toxicity. Eye (London, England), 25(1), 1-14. https://doi.org/10.1038/eye.2010.149
Zhang, J., Yang, J., Jang, R., & Zhang, Y. (2015). GPCR-I-TASSER: A hybrid approach to G protein-coupled receptor structure modeling and the application to the human genome. Structure, 23(8), 1538-1549. https://doi.org/10.1016/j.str.2015.06.007
Zhu, X., Brown, B., Li, A., Mears, A. J., Swaroop, A., & Craft, C. M. (2003). GRK1-dependent phosphorylation of S and M opsins and their binding to cone arrestin during cone phototransduction in the mouse retina. Journal of Neuroscience, 23(14), 6152-6160. https://doi.org/10.1523/JNEUROSCI.23-14-06152.2003
Zhu, X., Li, A., Brown, B., Weiss, E. R., Osawa, S., & Craft, C. M. (2002). Mouse cone arrestin expression pattern: Light induced translocation in cone photoreceptors. Molecular Vision, 8, 462-471. https://www.ncbi.nlm.nih.gov/pubmed/12486395