Programmed Non-Apoptotic Cell Death in Hereditary Retinal Degeneration: Crosstalk between cGMP-Dependent Pathways and PARthanatos?
Abstract
:1. Introduction
2. Photoreceptor Physiology and Phototransduction
3. Retinal Energy Metabolism and Cell Death
4. Apoptosis
5. PARP Activity and PARthanatos
5.1. The Core of PARthanatos: PARP and PAR Polymers
5.2. PAR-Dependent Translocation of AIF
5.3. Crosstalk between PARthanatos, Ca2+, and Calpain-Type Proteases
6. cGMP-Dependent Cell Death in RD
6.1. RD Mutations Associated with High Photoreceptor cGMP
6.2. cGMP-Gated Ion Channels, Ca2+ -Influx, and Cell Death
6.3. Protein Kinase G: A Link between cGMP-Signaling and Cell Death?
6.4. Histone Deacetylase Activity as an Event Downstream of PKG
6.5. PARP: A Link between PARthanatos and cGMP-Dependent Cell Death
7. Therapy Developments Targeting Programmed Cell Death
7.1. Apoptosis as a Target for Therapeutic Intervention in RD
7.2. Targeting PARthanatos and PARP Activity
7.3. Novel Therapeutic Approaches Targeting cGMP-Dependent Cell Death
8. The Future Therapeutic Research in RD
9. Concluding Remarks
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Maghsoudi, N.; Zakeri, Z.; Lockshin, R.A. Programmed cell death and apoptosis—Where it came from and where it is going: From Elie Metchnikoff to the control of caspases. Exp. Oncol. 2012, 34, 146–152. [Google Scholar]
- Ameisen, J.C. On the origin, evolution, and nature of programmed cell death: A timeline of four billion years. Cell Death Differ. 2002, 9, 367–393. [Google Scholar] [CrossRef] [PubMed]
- Berman-Frank, I.; Bidle, K.D.; Haramaty, L.; Falkowski, P.G. The demise of the marine cyanobacterium, Trichodesmium spp., via an autocatalyzed cell death pathway. Limnol. Oceanogr. 2004, 49, 997–1005. [Google Scholar] [CrossRef] [Green Version]
- Duncan, J.L.; Pierce, E.A.; Laster, A.M.; Daiger, S.P.; Birch, D.G.; Ash, J.D.; Iannaccone, A.; Flannery, J.G.; Sahel, J.A.; Zack, D.J.; et al. Inherited Retinal Degenerations: Current Landscape and Knowledge Gaps. Transl. Vis. Sci. Technol. 2018, 7, 6. [Google Scholar] [CrossRef] [Green Version]
- Bertelsen, M.; Jensen, H.; Bregnhøj, J.F.; Rosenberg, T. Prevalence of Generalized Retinal Dystrophy in Denmark. Ophthalmic Epidemiol. 2014, 21, 217–223. [Google Scholar] [CrossRef] [PubMed]
- O’Neal, T.B.; Luther, E.E. Retinitis Pigmentosa. StatPearls [Internet]. 2021. Available online: https://www.ncbi.nlm.nih.gov/books/NBK519518/ (accessed on 11 August 2021).
- Hamel, C. Retinitis pigmentosa. Orphanet J. Rare Dis. 2006, 1, 1–12. [Google Scholar] [CrossRef]
- Sahel, J.-A.; Marazova, K.; Audo, I. Clinical Characteristics and Current Therapies for Inherited Retinal Degenerations. Cold Spring Harb. Perspect. Med. 2015, 5, a017111. [Google Scholar] [CrossRef]
- Marigo, V. Programmed Cell Death in Retinal Degeneration: Targeting Apoptosis in Photoreceptors as Potential Therapy for Retinal Degeneration. Cell Cycle 2007, 6, 652–655. [Google Scholar] [CrossRef] [Green Version]
- Sanges, D.; Comitato, A.; Tammaro, R.; Marigo, V. Apoptosis in retinal degeneration involves cross-talk between apoptosis-inducing factor (AIF) and caspase-12 and is blocked by calpain inhibitors. PNAS 2006, 103, 17366–17371. [Google Scholar] [CrossRef] [Green Version]
- Doonan, F.; Donovan, M.; Cotter, T.G. Caspase-Independent Photoreceptor Apoptosis in Mouse Models of Retinal Degeneration. J. Neurosci. Res. 2003, 23, 5723–5731. [Google Scholar] [CrossRef] [Green Version]
- Arango-Gonzalez, B.; Trifunovic, D.; Sahaboglu, A.; Kranz, K.; Michalakis, S.; Farinelli, P.; Koch, S.; Koch, F.; Cottet, S.; Janssen-Bienhold, U.; et al. Identification of a Common Non-Apoptotic Cell Death Mechanism in Hereditary Retinal Degeneration. PLoS ONE 2014, 9, e112142. [Google Scholar] [CrossRef]
- Power, M.J.; Rogerson, L.E.; Schubert, T.; Berens, P.; Euler, T.; Paquet-Durand, F. Systematic spatiotemporal mapping reveals divergent cell death pathways in three mouse models of hereditary retinal degeneration. J. Comp. Neurol. 2020, 528, 1113–1139. [Google Scholar] [CrossRef] [Green Version]
- David, K.K.; Andrabi, S.A.; Dawson, T.M.; Dawson, V.L. Parthanatos, a messenger of death. Front. Biosci. 2009, 14, 1116. [Google Scholar] [CrossRef] [Green Version]
- Lamb, T.D.; Hunt, D.M. Evolution of the vertebrate phototransduction cascade activation steps. Dev. Biol. 2017, 431, 77–92. [Google Scholar] [CrossRef]
- Yau, K.W.; Baylor, D.A. Cyclic GMP-Activated Conductance of Retinal Photoreceptor Cells. Annu. Rev. Neurosci. 1989, 12, 289–327. [Google Scholar] [CrossRef] [PubMed]
- Yau, K.-W.; Nakatani, K. Cation selectivity of light-sensitive conductance in retinal rods. Nature 1984, 309, 352–354. [Google Scholar] [CrossRef] [PubMed]
- Biel, M.; Michalakis, S. Function and Dysfunction of CNG Channels: Insights from Channelopathies and Mouse Models. Mol. Neurobiol. 2007, 35, 266–277. [Google Scholar] [CrossRef] [PubMed]
- Biel, M.; Michalakis, S. Cyclic Nucleotide-Gated Channels. In cGMP: Generators, Effectors and Therapeutic Implications; Springer: Berlin/Heidelberg, Germany, 2009; Volume 191, pp. 111–136. [Google Scholar] [CrossRef]
- Donato, L.; Scimone, C.; Alibrandi, S.; Abdalla, E.M.; Nabil, K.M.; D’Angelo, R.; Sidoti, A. New Omics–Derived Perspectives on Retinal Dystrophies: Could Ion Channels-Encoding or Related Genes Act as Modifier of Pathological Phenotype? Int. J. Mol. Sci. 2021, 22, 70. [Google Scholar] [CrossRef] [PubMed]
- Das, S.; Chen, Y.; Yan, J.; Christensen, G.; Belhadj, S.; Tolone, A.; Paquet-Durand, F. The role of cGMP-signalling and calcium-signalling in photoreceptor cell death: Perspectives for therapy development. Pflugers Arch 2021, 473, 1411–1421. [Google Scholar] [CrossRef] [PubMed]
- Arshavsky, V.Y.; Lamb, T.D.; Pugh, E.N., Jr. G Proteins and Phototransduction. Annu. Rev. Physiol. 2002, 64, 153–187. [Google Scholar] [CrossRef] [Green Version]
- Fain, G.L.; Hardie, R.; Laughlin, S.B. Phototransduction and the Evolution of Photoreceptors. Curr. Biol. 2010, 20, R114–R124. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dizhoor, A.M.; Olshevskaya, E.V.; Henzel, W.J.; Wong, S.C.; Stults, J.T.; Ankoudinova, I.; Hurley, J.B. Cloning, Sequencing, and Expression of a 24-kDa Ca2+-binding Protein Activating Photoreceptor Guanylyl Cyclase. J. Biol. Chem. 1995, 270, 25200–25206. [Google Scholar] [CrossRef] [Green Version]
- Gorczyca, W.A.; Gray-Keller, M.P.; Detwiler, P.B.; Palczewski, K. Purification and physiological evaluation of a guanylate cyclase activating protein from retinal rods. PNAS 1994, 91, 4014–4018. [Google Scholar] [CrossRef] [Green Version]
- Palczewski, K.; Subbaraya, I.; Gorczyca, W.A.; Helekar, B.S.; Ruiz, C.C.; Ohguro, H.; Huang, J.; Zhao, X.; Crabb, J.W.; Johnson, R.S. Molecular cloning and characterization of retinal photoreceptor guanylyl cyclase-activating protein. Neuron 1994, 13, 395–404. [Google Scholar] [CrossRef]
- Méndez, A.; Burns, M.E.; Sokal, I.; Dizhoor, A.M.; Baehr, W.; Palczewski, K.; Baylor, D.A.; Chen, J. Role of guanylate cyclase-activating proteins (GCAPs) in setting the flash sensitivity of rod photoreceptors. PNAS 2001, 98, 9948–9953. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Burns, M.E.; Méndez, A.; Chen, J.; Baylor, D.A. Dynamics of Cyclic GMP Synthesis in Retinal Rods. Neuron 2002, 36, 81–91. [Google Scholar] [CrossRef] [Green Version]
- Hurley, J.B.; Lindsay, K.J.; Du, J. Glucose, lactate, and shuttling of metabolites in vertebrate retinas. J. Neurosci. Res. 2015, 93, 1079–1092. [Google Scholar] [CrossRef] [Green Version]
- Ames, A., III. Energy requirements of CNS cells as related to their function and to their vulnerability to ischemia: A commentary based on studies on retina. Can. J. Physiol. Pharmacol. 1992, 70, S158–S164. [Google Scholar] [CrossRef] [PubMed]
- Okawa, H.; Sampath, A.P.; Laughlin, S.B.; Fain, G.L. ATP Consumption by Mammalian Rod Photoreceptors in Darkness and in Light. Curr. Biol. 2008, 18, 1917–1921. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kanow, M.A.; Giarmarco, M.M.; Jankowski, C.S.; Tsantilas, K.; Engel, A.L.; Du, J.; Linton, J.D.; Farnsworth, C.C.; Sloat, S.R.; Rountree, A.; et al. Biochemical adaptations of the retina and retinal pigment epithelium support a metabolic ecosystem in the vertebrate eye. eLife 2017, 6, e28899. [Google Scholar] [CrossRef] [PubMed]
- Warburg, O.; Wind, F.; Negelein, E. The Metabolism of Tumors in The Body. J. Gen. Physiol. 1927, 8, 519–530. [Google Scholar] [CrossRef] [Green Version]
- Venkatesh, A.; Ma, S.; Le, Y.Z.; Hall, M.N.; Rüegg, M.A.; Punzo, C. Activated mTORC1 promotes long-term cone survival in retinitis pigmentosa mice. J. Clin. Investig. 2015, 125, 1446–1458. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, L.; Du, J.; Justus, S.; Hsu, C.-W.; Bonet-Ponce, L.; Wu, W.-H.; Tsai, Y.-T.; Wu, W.-P.; Jia, Y.; Duong, J.K.; et al. Reprogramming metabolism by targeting sirtuin 6 attenuates retinal degeneration. J. Clin. Investig. 2016, 126, 4659–4673. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chinchore, Y.; Begaj, T.; Wu, D.; Drokhlyansky, E.; Cepko, C.L. Glycolytic reliance promotes anabolism in photoreceptors. eLife 2017, 6, e25946. [Google Scholar] [CrossRef]
- Pivovarova, N.B.; Andrews, S.B. Calcium-dependent mitochondrial function and dysfunction in neurons. FEBS J. 2010, 277, 3622–3636. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sancho-Pelluz, J.; Arango-Gonzalez, B.; Kustermann, S.; Romero, F.J.; van Veen, T.; Zrenner, E.; Ekström, P.; Paquet-Durand, F. Photoreceptor Cell Death Mechanisms in Inherited Retinal Degeneration. Mol. Neurobiol. 2008, 38, 253–269. [Google Scholar] [CrossRef]
- Kerr, J.F.; Wyllie, A.H.; Currie, A.R. Apoptosis: A Basic Biological Phenomenon with Wideranging Implications in Tissue Kinetics. Br. J. Cancer 1972, 26, 239–257. [Google Scholar] [CrossRef] [Green Version]
- Kroemer, G.; Galluzzi, L.; Vandenabeele, P.; Abrams, J.; Alnemri, E.S.; Baehrecke, E.; Blagosklonny, M.; El-Deiry, W.S.; Golstein, P.; Green, D.; et al. Classification of cell death: Recommendations of the Nomenclature Committee on Cell Death 2008. Cell Death Differ. 2008, 16, 3–11. [Google Scholar] [CrossRef]
- Di Lisa, F.; Bernardi, P. A CaPful of mechanisms regulating the mitochondrial permeability transition. J. Mol. Cell. Cardiol. 2009, 46, 775–780. [Google Scholar] [CrossRef]
- Rinaldi, C.; Donato, L.; Alibrandi, S.; Scimone, C.; D’Angelo, R.; Sidoti, A. Oxidative Stress and the Neurovascular Unit. Life 2021, 11, 767. [Google Scholar] [CrossRef] [PubMed]
- Scimone, C.; Donato, L.; Alibrandi, S.; Vadalà, M.; Giglia, G.; Sidoti, A.; D’Angelo, R. N-retinylidene-N-retinylethanolamine adduct induces expression of chronic inflammation cytokines in retinal pigment epithelium cells. Exp. Eye Res. 2021, 29, 108641. [Google Scholar] [CrossRef]
- Xie, N.; Zhang, L.; Gao, W.; Huang, C.; Huber, P.E.; Zhou, X.; Li, C.; Shen, G.; Zou, B. NAD+ metabolism: Pathophysiologic mechanisms and therapeutic potential. Signal Transduct. Target. Ther. 2020, 5, 1–37. [Google Scholar] [CrossRef] [PubMed]
- Greenwald, S.H.; Pierce, E.A. Parthanatos as a Cell Death Pathway Underlying Retinal Disease. Retin. Degener. Dis. 2019, 1185, 323–327. [Google Scholar] [CrossRef]
- Orrenius, S.; Zhivotovsky, B.; Nicotera, P. Regulation of cell death: The calcium–apoptosis link. Nat. Rev. Mol. Cell Biol. 2003, 4, 552–565. [Google Scholar] [CrossRef] [PubMed]
- Yuan, S.; Akey, C.W. Apoptosome Structure, Assembly, and Procaspase Activation. Structure 2013, 21, 501–515. [Google Scholar] [CrossRef] [Green Version]
- Power, M.; Das, S.; Schütze, K.; Marigo, V.; Ekström, P.; Paquet-Durand, F. Cellular mechanisms of hereditary photoreceptor degeneration—Focus on cGMP. Prog. Retin. Eye Res. 2020, 74, 100772. [Google Scholar] [CrossRef]
- Fricker, M.; Tolkovsky, A.M.; Borutaite, V.; Coleman, M.; Brown, G.C. Neuronal Cell Death. Physiol. Rev. 2018, 98, 813–880. [Google Scholar] [CrossRef]
- Weinlich, R.; Oberst, A.; Beere, H.M.; Green, D.R. Necroptosis in development, inflammation and disease. Nat. Rev. Mol. Cell Biol. 2017, 18, 127–136. [Google Scholar] [CrossRef]
- Portera-Cailliau, C.; Sung, C.; Nathans, J.; Adler, R. Apoptotic photoreceptor cell death in mouse models of retinitis pigmentosa. PNAS 1994, 91, 974–978. [Google Scholar] [CrossRef] [Green Version]
- Mervin, K.; Stone, J. Developmental Death of Photoreceptors in the C57BL/6JMouse: Association with Retinal Function and Self-protection. Exp. Eye Res. 2002, 75, 703–713. [Google Scholar] [CrossRef]
- Morales, J.; Li, L.; Fattah, F.J.; Dong, Y.; Bey, E.A.; Patel, M.; Gao, J.; Boothman, D.A. Review of Poly (ADP-ribose) Polymerase (PARP) Mechanisms of Action and Rationale for Targeting in Cancer and Other Diseases. Crit. Rev. Eukaryot. Gene Expr. 2014, 24, 15–28. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Teloni, F.; Altmeyer, M. Readers of poly(ADP-ribose): Designed to be fit for purpose. Nucleic Acids Res. 2015, 44, 993–1006. [Google Scholar] [CrossRef] [Green Version]
- Amé, J.C.; Spenlehauer, C.; de Murcia, G. The PARP superfamily. Bioessays 2004, 26, 882–893. [Google Scholar] [CrossRef] [PubMed]
- Ko, H.L.; Ren, E.C. Functional Aspects of PARP1 in DNA Repair and Transcription. Biomolecules 2012, 2, 524–548. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hageman, G.J.; Stierum, R.H. Niacin, poly(ADP-ribose) polymerase-1 and genomic stability. Mutat. Res. Fundam. Mol. Mech. Mutagenesis 2001, 475, 45–56. [Google Scholar] [CrossRef]
- Pan, Y.-R.; Song, J.-Y.; Fan, B.; Wang, Y.; Che, L.; Zhang, S.-M.; Chang, Y.-X.; He, C.; Li, G.-Y. mTOR may interact with PARP-1 to regulate visible light-induced parthanatos in photoreceptors. Cell Commun. Signal. 2020, 18, 1–17. [Google Scholar] [CrossRef] [Green Version]
- Andrabi, S.A.; Dawson, T.M.; Dawson, V.L. Mitochondrial and Nuclear Cross Talk in Cell Death. Ann. N. Y. Acad. Sci. 2008, 1147, 233–241. [Google Scholar] [CrossRef]
- Robinson, N.; Ganesan, R.; Hegedűs, C.; Kovács, K.; Kufer, T.A.; Virág, L. Programmed necrotic cell death of macrophages: Focus on pyroptosis, necroptosis, and parthanatos. Redox Biol. 2019, 26, 101239. [Google Scholar] [CrossRef]
- Krishnakumar, R.; Kraus, W.L. The PARP Side of the Nucleus: Molecular Actions, Physiological Outcomes, and Clinical Targets. Mol. Cell 2010, 39, 8–24. [Google Scholar] [CrossRef] [Green Version]
- Murata, M.M.; Kong, X.; Moncada, E.; Chen, Y.; Imamura, H.; Wang, P.; Berns, M.W.; Yokomori, K.; Digman, M.A. NAD+ consumption by PARP1 in response to DNA damage triggers metabolic shift critical for damaged cell survival. Mol. Biol. Cell 2019, 30, 2584–2597. [Google Scholar] [CrossRef]
- Chambon, P.; Weill, J.D.; Mandel, P. Nicotinamide mononucleotide activation of a new DNA-dependent polyadenylic acid synthesizing nuclear enzyme. Biochem. Biophys. Res. Commun. 1963, 11, 39–43. [Google Scholar] [CrossRef]
- Bai, P. Biology of Poly(ADP-Ribose) Polymerases: The Factotums of Cell Maintenance. Mol. Cell 2015, 58, 947–958. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kraus, W.L. PARPs and ADP-Ribosylation: 50 …Years and Counting. Mol. Cell 2015, 58, 902–910. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kondratova, A.A.; Cheon, H.; Dong, B.; Holvey-Bates, E.G.; Hasipek, M.; Taran, I.; Gaughan, C.; Jha, B.K.; Silverman, R.H.; Stark, G.R. Suppressing PAR ylation by 2′,5′-oligoadenylate synthetase 1 inhibits DNA damage-induced cell death. EMBO J. 2020, 39, e101573. [Google Scholar] [CrossRef] [PubMed]
- Andrabi, S.A.; Kim, N.S.; Yu, S.-W.; Wang, H.; Koh, D.W.; Sasaki, M.; Klaus, J.A.; Otsuka, T.; Zhang, Z.; Koehler, R.C.; et al. Poly(ADP-ribose) (PAR) polymer is a death signal. PNAS 2006, 103, 18308–18313. [Google Scholar] [CrossRef] [Green Version]
- De Murcia, G.; de Murcia, J.M. Poly(ADP-ribose) polymerase: A molecular nick-sensor. Trends Biochem. Sci. 1994, 19, 172–176. [Google Scholar] [CrossRef]
- Barkauskaite, E.; Jankevicius, G.; Ahel, I. Structures and Mechanisms of Enzymes Employed in the Synthesis and Degradation of PARP-Dependent Protein ADP-Ribosylation. Mol. Cell 2015, 58, 935–946. [Google Scholar] [CrossRef] [Green Version]
- D’Amours, D.; Desnoyers, S.; D’Silva, I.; Poirier, G.G. Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem. J. 1999, 342, 249–268. [Google Scholar] [CrossRef]
- Bano, D.; Prehn, J.H. Apoptosis-Inducing Factor (AIF) in Physiology and Disease: The Tale of a Repented Natural Born Killer. EBioMedicine 2018, 30, 29–37. [Google Scholar] [CrossRef] [Green Version]
- Wang, Y.; Kim, N.S.; Haince, J.-F.; Kang, H.C.; David, K.K.; Andrabi, S.A.; Poirier, G.G.; Dawson, V.L.; Dawson, T.M. Poly(ADP-Ribose) (PAR) Binding to Apoptosis-Inducing Factor Is Critical for PAR Polymerase-1-Dependent Cell Death (Parthanatos). Sci. Signal. 2011, 4, ra20. [Google Scholar] [CrossRef] [Green Version]
- Park, H.; Kam, T.-I.; Dawson, T.M.; Dawson, V.L. Poly (ADP-ribose) (PAR)-dependent cell death in neurodegenerative diseases. Int. Rev. Cell Mol. Biol. 2020, 353, 1–29. [Google Scholar] [CrossRef]
- Wang, Y.; Dawson, V.L.; Dawson, T.M. Poly(ADP-ribose) signals to mitochondrial AIF: A key event in parthanatos. Exp. Neurol. 2009, 218, 193–202. [Google Scholar] [CrossRef] [Green Version]
- Cheung, E.C.; Melanson-Drapeau, L.; Cregan, S.P.; Vanderluit, J.L.; Ferguson, K.L.; McIntosh, W.C.; Park, D.S.; Bennett, S.A.; Slack, R.S. Apoptosis-Inducing Factor Is a Key Factor in Neuronal Cell Death Propagated by BAX-Dependent and BAX-Independent Mechanisms. J. Neurosci. 2005, 25, 1324–1334. [Google Scholar] [CrossRef] [Green Version]
- Berger, N.; Sims, J.; Catino, D.; Berger, S. Poly(ADP-ribose) Polymerase Mediates the Suicide Response to Massive DNA Damage: Studies in Normal and DNA-repair Defective Cells. In ADP-Ribosylation, DNA Repair and Cancer; CRC Press: Boka Raton, FL, USA, 2020; pp. 219–226. [Google Scholar]
- Ozaki, T.; Yamashita, T.; Ishiguro, S.-I. Mitochondrial m-calpain plays a role in the release of truncated apoptosis-inducing factor from the mitochondria. Biochim. Biophys. Acta (BBA) Bioenerg. 2009, 1793, 1848–1859. [Google Scholar] [CrossRef] [Green Version]
- Wang, Y.; Kim, N.S.; Li, X.; Greer, P.A.; Koehler, R.C.; Dawson, V.L.; Dawson, T.M. Calpain activation is not required for AIF translocation in PARP-1-dependent cell death (parthanatos). J. Neurochem. 2009, 110, 687–696. [Google Scholar] [CrossRef] [PubMed]
- Zhong, H.; Song, R.; Pang, Q.; Liu, Y.; Zhuang, J.; Chen, Y.; Hu, J.; Hu, J.; Liu, Y.; Liu, Z.; et al. Propofol inhibits parthanatos via ROS–ER–calcium–mitochondria signal pathway in vivo and vitro. Cell Death Dis. 2018, 9, 1–14. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Paul, S.; Jakhar, R.; Bhardwaj, M.; Chauhan, A.K.; Kang, S.C. Fumonisin B1 induces poly (ADP-ribose) (PAR) polymer-mediated cell death (parthanatos) in neuroblastoma. Food Chem. Toxicol. 2021, 154, 112326. [Google Scholar] [CrossRef] [PubMed]
- Paquet-Durand, F.; Hauck, S.M.; Van Veen, T.; Ueffing, M.; Ekström, P. PKG activity causes photoreceptor cell death in two retinitis pigmentosa models. J. Neurochem. 2009, 108, 796–810. [Google Scholar] [CrossRef]
- Yang, P.; Lockard, R.; Titus, H.; Hiblar, J.; Weller, K.; Wafai, D.; Weleber, R.G.; Duvoisin, R.M.; Morgans, C.W.; Pennesi, M.E. Suppression of cGMP-Dependent Photoreceptor Cytotoxicity with Mycophenolate Is Neuroprotective in Murine Models of Retinitis Pigmentosa. Investig. Opthalmol. Vis. Sci. 2020, 61, 25. [Google Scholar] [CrossRef]
- Kulkarni, M.; Trifunovic, D.; Schubert, T.; Euler, T.; Paquet-Durand, F. Calcium dynamics change in degenerating cone photoreceptors. Hum. Mol. Genet. 2016, 25, 3729–3740. [Google Scholar] [CrossRef]
- Paquet-Durand, F.; Beck, S.; Michalakis, S.; Goldmann, T.; Huber, G.; Mühlfriedel, R.; Trifunović, D.; Fischer, M.D.; Fahl, E.; Duetsch, G.; et al. A key role for cyclic nucleotide gated (CNG) channels in cGMP-related retinitis pigmentosa. Hum. Mol. Genet. 2011, 20, 941–947. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hao, Y.; Xu, N.; Box, A.C.; Schaefer, L.; Kannan, K.; Zhang, Y.; Florens, L.; Seidel, C.; Washburn, M.P.; Wiegraebe, W.; et al. Nuclear cGMP-Dependent Kinase Regulates Gene Expression via Activity-Dependent Recruitment of a Conserved Histone Deacetylase Complex. PLoS Genet. 2011, 7, e1002065. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sancho-Pelluz, J.; Alavi, M.V.; Sahaboglu, A.; Kustermann, S.; Farinelli, P.; Azadi, S.; Van Veen, T.; Romero, F.J.; Paquet-Durand, F.; Ekström, P. Excessive HDAC activation is critical for neurodegeneration in the rd1 mouse. Cell Death Dis. 2010, 1, e24. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, T.; Tsang, S.H.; Chen, J. Two pathways of rod photoreceptor cell death induced by elevated cGMP. Hum. Mol. Genet. 2017, 26, 2299–2306. [Google Scholar] [CrossRef] [Green Version]
- Trifunovic, D.; Dengler, K.; Michalakis, S.; Zrenner, E.; Wissinger, B.; Paquet-Durand, F. cGMP-dependent cone photoreceptor degeneration in the cpfl1 mouse retina. J. Comp. Neurol. 2010, 518, 3604–3617. [Google Scholar] [CrossRef]
- Sato, S.; Peshenko, I.V.; Olshevskaya, E.V.; Kefalov, V.J.; Dizhoor, A.M. GUCY2D Cone–Rod Dystrophy-6 Is a “Phototransduction Disease” Triggered by Abnormal Calcium Feedback on Retinal Membrane Guanylyl Cyclase 1. J. Neurosci. Res. 2018, 38, 2990–3000. [Google Scholar] [CrossRef]
- Peshenko, I.V.; Olshevskaya, E.V.; Dizhoor, A.M. Functional Study and Mapping Sites for Interaction with the Target Enzyme in Retinal Degeneration 3 (RD3) Protein. J. Biol. Chem. 2016, 291, 19713–19723. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- McLaughlin, M.E.; Sandberg, M.A.; Berson, E.L.; Dryja, T.P. Recessive mutations in the gene encoding the β–subunit of rod phosphodiesterase in patients with retinitis pigmentosa. Nat. Genet. 1993, 4, 130–134. [Google Scholar] [CrossRef]
- Dryja, T.P.; Finn, J.T.; Peng, Y.W.; McGee, T.L.; Berson, E.L.; Yau, K.W. Mutations in the gene encoding the alpha subunit of the rod cGMP-gated channel in autosomal recessive retinitis pigmentosa. PNAS 1995, 92, 10177–10181. [Google Scholar] [CrossRef] [Green Version]
- Tsang, S.H.; Gouras, P.; Yamashita, C.K.; Kjeldbye, H.; Fisher, J.; Farber, D.B.; Goff, S.P. Retinal Degeneration in Mice Lacking the gamma Subunit of the Rod cGMP Phosphodiesterase. Science 1996, 272, 1026–1029. [Google Scholar] [CrossRef]
- Reuter, P.; Koeppen, K.; Ladewig, T.; Kohl, S.; Baumann, B.; Wissinger, B. Mutations in CNGA3 impair trafficking or function of cone cyclic nucleotide-gated channels, resulting in achromatopsia. Hum. Mutat. 2008, 29, 1228–1236. [Google Scholar] [CrossRef]
- Paquet-Durand, F.; Marigo, V.; Ekström, P. RD Genes Associated with High Photoreceptor cGMP-Levels (Mini-Review). Retin. Degener. Dis. 2019, 1185, 245–249. [Google Scholar] [CrossRef]
- Das, S.; Popp, V.; Power, M.; Groeneveld, K.; Melle, C.; Rogerson, L.; Achury, M.; Schwede, F.; Strasser, T.; Euler, T. Redefining the role of Ca2+-permeable channels in hereditary photoreceptor degeneration using the D-and L-cis enantiomers of diltiazem. bioRxiv 2020. [Google Scholar] [CrossRef]
- Catterall, W.A. Voltage-Gated Calcium Channels. Cold Spring Harb. Perspect. Biol. 2011, 3, a003947. [Google Scholar] [CrossRef]
- Shinkai-Ouchi, F.; Shindo, M.; Doi, N.; Hata, S.; Ono, Y. Calpain-2 participates in the process of calpain-1 inactivation. Biosci. Rep. 2020, 40. [Google Scholar] [CrossRef]
- Goll, D.E.; Thompson, V.F.; Li, H.; Wei, W.; Cong, J. The calpain system. Physiol. Rev. 2003, 83, 731–801. [Google Scholar] [CrossRef] [PubMed]
- Baudry, M.; Bi, X. Calpain-1 and Calpain-2: The Yin and Yang of Synaptic Plasticity and Neurodegeneration. Trends Neurosci. 2016, 39, 235–245. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fox, D.A.; Poblenz, A.T.; He, L. Calcium Overload Triggers Rod Photoreceptor Apoptotic Cell Death in Chemical-Induced and Inherited Retinal Degenerations. Ann. N. Y. Acad. Sci. 1999, 893, 282–285. [Google Scholar] [CrossRef] [PubMed]
- Barabas, P.; Peck, C.C.; Krizaj, D. Do Calcium Channel Blockers Rescue Dying Photoreceptors in the Pde6brd1 Mouse? Retin. Degener. Dis. 2009, 664, 491–499. [Google Scholar] [CrossRef] [Green Version]
- Schön, C.; Paquet-Durand, F.; Michalakis, S. Cav1.4 L-Type Calcium Channels Contribute to Calpain Activation in Degenerating Photoreceptors of rd1 Mice. PLoS ONE 2016, 11, e0156974. [Google Scholar] [CrossRef]
- Read, D.S.; McCallbc, M.A.; Gregg, R.G. Absence of Voltage-dependent Calcium Channels Delays Photoreceptor Degeneration in rd Mice. Exp. Eye Res. 2002, 75, 415–420. [Google Scholar] [CrossRef] [PubMed]
- Hofmann, F.; Bernhard, D.; Lukowski, R.; Weinmeister, P. cGMP regulated protein kinases (cGK). In cGMP: Generators, Effectors and Therapeutic Implications; Springer: Berlin/Heidelberg, Germany, 2009; pp. 137–162. [Google Scholar] [CrossRef]
- Fiscus, R.R. Involvement of Cyclic GMP and Protein Kinase G in the Regulation of Apoptosis and Survival in Neural Cells. Neurosignals 2002, 11, 175–190. [Google Scholar] [CrossRef] [PubMed]
- Frankenreiter, S.; Bednarczyk, P.; Kniess, A.; Bork, N.I.; Straubinger, J.; Koprowski, P.; Wrzosek, A.; Mohr, E.; Logan, A.; Murphy, M.P.; et al. cGMP-Elevating Compounds and Ischemic Conditioning Provide Cardioprotection Against Ischemia and Reperfusion Injury via Cardiomyocyte-Specific BK Channels. Circulation 2017, 136, 2337–2355. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jaumann, M.; Dettling, J.; Gubelt, M.; Zimmermann, U.; Gerling, A.; Paquet-Durand, F.; Feil, S.; Wolpert, S.; Franz, C.; Varakina, K.; et al. cGMP-Prkg1 signaling and Pde5 inhibition shelter cochlear hair cells and hearing function. Nat. Med. 2012, 18, 252–259. [Google Scholar] [CrossRef]
- Canzoniero, L.M.; Adornetto, A.; Secondo, A.; Magi, S.; Dell’Aversano, C.; Scorziello, A.; Amoroso, S.; Di Renzo, G. Involvement of the nitric oxide/protein kinase G pathway in polychlorinated biphenyl-induced cell death in SH-SY 5Y neuroblastoma cells. J. Neurosci. Res. 2006, 84, 692–697. [Google Scholar] [CrossRef]
- Brunetti, M.; Mascetra, N.; Manarini, S.; Martelli, N.; Cerletti, C.; Musiani, P.; Aiello, F.B.; Evangelista, V. Inhibition of cGMP-dependent protein kinases potently decreases neutrophil spontaneous apoptosis. Biochem. Biophys. Res. Commun. 2002, 297, 498–501. [Google Scholar] [CrossRef]
- Vighi, E.; Rentsch, A.; Henning, P.; Comitato, A.; Hoffmann, D.; Bertinetti, D.; Bertolotti, E.; Schwede, F.; Herberg, F.W.; Genieser, H.-G.; et al. New cGMP analogues restrain proliferation and migration of melanoma cells. Oncotarget 2018, 9, 5301–5320. [Google Scholar] [CrossRef] [Green Version]
- Mencl, S.; Trifunović, D.; Zrenner, E.; Paquet-Durand, F. PKG-Dependent Cell Death in 661W Cone Photoreceptor-like Cell Cultures (Experimental Study). In Retinal Degenerative Diseases; Springer: Cham, Switzerland, 2018; Volume 1074, pp. 511–517. [Google Scholar] [CrossRef]
- Farber, D.B.; Lolley, R.N. Cyclic Guanosine Monophosphate: Elevation in Degenerating Photoreceptor Cells of the C3H Mouse Retina. Science 1974, 186, 449–451. [Google Scholar] [CrossRef]
- Vighi, E.; Trifunovic, D.; Veiga-Crespo, P.; Rentsch, A.; Hoffmann, D.; Sahaboglu, A.; Strasser, T.; Kulkarni, M.; Bertolotti, E.; Heuvel, A.V.D.; et al. Combination of cGMP analogue and drug delivery system provides functional protection in hereditary retinal degeneration. PNAS 2018, 115, E2997–E3006. [Google Scholar] [CrossRef] [Green Version]
- Koch, M.; Scheel, C.; Ma, H.; Yang, F.; Stadlmeier, M.; Glück, A.F.; Murenu, E.; Traube, F.R.; Carell, T.; Biel, M.; et al. The cGMP-Dependent Protein Kinase 2 Contributes to Cone Photoreceptor Degeneration in the Cnga3-Deficient Mouse Model of Achromatopsia. Int. J. Mol. Sci. 2021, 22, 52. [Google Scholar] [CrossRef]
- Gamm, D.M.; Barthel, L.K.; Raymond, P.A.; Uhler, M.D. Localization of cGMP-dependent protein kinase isoforms in mouse eye. Investig. Ophthalmol. Vis. Sci. 2000, 41, 2766–2773. [Google Scholar] [CrossRef]
- Feil, S.; Zimmermann, P.; Knorn, A.; Brummer, S.; Schlossmann, J.; Hofmann, F.; Feil, R. Distribution of cGMP-dependent protein kinase type I and its isoforms in the mouse brain and retina. Neuroscience 2005, 135, 863–868. [Google Scholar] [CrossRef]
- Ekstrom, P.; Ueffing, M.; Zrenner, E.; Paquet-Durand, F. Novel in situ activity assays for the quantitative molecular analysis of neurodegenerative processes in the retina. Curr. Med. Chem. 2014, 21, 3478–3493. [Google Scholar] [CrossRef] [PubMed]
- Roy, A.; Groten, J.; Marigo, V.; Tomar, T.; Hilhorst, R. Identification of Novel Substrates for cGMP Dependent Protein Kinase (PKG) through Kinase Activity Profiling to Understand Its Putative Role in Inherited Retinal Degeneration. Int. J. Mol. Sci. 2021, 22, 1180. [Google Scholar] [CrossRef] [PubMed]
- Roth, S.Y.; Allis, C.D. Histone Acetylation and Chromatin Assembly: A Single Escort, Multiple Dances? Cell 1996, 87, 5–8. [Google Scholar] [CrossRef] [Green Version]
- Jaliffa, C.; Ameqrane, I.; Dansault, A.; Leemput, J.; Vieira, V.; Lacassagne, E.; Provost, A.; Bigot, K.; Masson, C.; Menasche, M.; et al. Sirt1 Involvement in rd10 Mouse Retinal Degeneration. PNAS 2009, 50, 3562–3572. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Samardzija, M.; Masarini, K.; Ueffing, M.; Trifunović, D. HDAC Inhibition Prevents Primary Cone Degeneration Even After the Onset of Degeneration. In Retinal Degenerative Diseases; Springer: Cham, Switzerland, 2019; pp. 383–387. [Google Scholar] [CrossRef]
- Trifunović, D.; Petridou, E.; Comitato, A.; Marigo, V.; Ueffing, M.; Paquet-Durand, F. Primary Rod and Cone Degeneration Is Prevented by HDAC Inhibition. In Retinal Degenerative Diseases; Springer: Cham, Switzerland, 2018; pp. 367–373. [Google Scholar] [CrossRef]
- Trifunović, D.; Arango-Gonzalez, B.; Comitato, A.; Barth, M.; del Amo, E.M.; Kulkarni, M.; Sahaboglu, A.; Hauck, S.M.; Urtti, A.; Arsenijevic, Y.; et al. HDAC inhibition in thecpfl1mouse protects degenerating cone photoreceptors in vivo. Hum. Mol. Genet. 2016, 25, 4462–4472. [Google Scholar] [CrossRef] [Green Version]
- Sancho-Pelluz, J.; Paquet-Durand, F. HDAC Inhibition Prevents Rd1 Mouse Photoreceptor Degeneration. In Retinal Degenerative Diseases; Springer: Boston, MA, USA, 2012; Volume 723, pp. 107–113. [Google Scholar] [CrossRef]
- Samardzija, M.; Corna, A.; Gomez-Sintes, R.; Jarboui, M.A.; Armento, A.; Roger, J.E.; Petridou, E.; Haq, W.; Paquet-Durand, F.; Zrenner, E.; et al. HDAC inhibition ameliorates cone survival in retinitis pigmentosa mice. Cell Death Differ. 2020, 28, 1317–1332. [Google Scholar] [CrossRef]
- Sundaramurthi, H.; Roche, S.L.; Grice, G.L.; Moran, A.; Dillion, E.T.; Campiani, G.; Nathan, J.A.; Kennedy, B.N. Selective Histone Deacetylase 6 Inhibitors Restore Cone Photoreceptor Vision or Outer Segment Morphology in Zebrafish and Mouse Models of Retinal Blindness. Front. Cell Dev. Biol. 2020, 8, 689. [Google Scholar] [CrossRef]
- Perron, N.R.; Nasarre, C.; Bandyopadhyay, M.; Beeson, C.C.; Rohrer, B. SAHA is neuroprotective in in vitro and in situ models of retinitis pigmentosa. Mol. Vis. 2021, 27, 151–160. [Google Scholar]
- Tsai, S.-C.; Seto, E. Regulation of Histone Deacetylase 2 by Protein Kinase CK2. J. Biol. Chem. 2002, 277, 31826–31833. [Google Scholar] [CrossRef] [Green Version]
- Kaur, J.; Mencl, S.; Sahaboglu, A.; Farinelli, P.; Van Veen, T.; Zrenner, E.; Ekström, P.; Paquet-Durand, F.; Arango-Gonzalez, B. Calpain and PARP Activation during Photoreceptor Cell Death in P23H and S334ter Rhodopsin Mutant Rats. PLoS ONE 2011, 6, e22181. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Paquet-Durand, F.; Silva, J.; Talukdar, T.; Johnson, L.E.; Azadi, S.; Van Veen, T.; Ueffing, M.; Hauck, S.M.; Ekström, P.A.R. Excessive Activation of Poly(ADP-Ribose) Polymerase Contributes to Inherited Photoreceptor Degeneration in the Retinal Degeneration 1 Mouse. J. Neurosci. Res. 2007, 27, 10311–10319. [Google Scholar] [CrossRef] [PubMed]
- Rasmussen, R.D.; Gajjar, M.K.; Jensen, K.E.; Hamerlik, P. Enhanced efficacy of combined HDAC and PARP targeting in glioblastoma. Mol. Oncol. 2016, 10, 751–763. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sahaboglu, A.; Barth, M.; Secer, E.; del Amo, E.M.; Urtti, A.; Arsenijevic, Y.; Zrenner, E.; Paquet-Durand, F. Olaparib significantly delays photoreceptor loss in a model for hereditary retinal degeneration. Sci. Rep. 2016, 6, 39537. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vidal-Gil, L.; Sancho-Pelluz, J.; Zrenner, E.; Oltra, M.; Sahaboglu, A. Poly ADP ribosylation and extracellular vesicle activity in rod photoreceptor degeneration. Sci. Rep. 2019, 9, 1–10. [Google Scholar] [CrossRef] [PubMed]
- Olivares-González, L.; Velasco, S.; Millán, J.M.; Rodrigo, R. Intravitreal administration of adalimumab delays retinal degeneration in rd10 mice. FASEB J. 2020, 34, 13839–13861. [Google Scholar] [CrossRef]
- Sahaboglu, A.; Miranda, M.; Canjuga, D.; Avci-Adali, M.; Savytska, N.; Secer, E.; Feria-Pliego, J.A.; Kayık, G.; Durdagi, S. Drug repurposing studies of PARP inhibitors as a new therapy for inherited retinal degeneration. Cell. Mol. Life Sci. 2020, 77, 2199–2216. [Google Scholar] [CrossRef]
- Sahaboglu, A.; Tanimoto, N.; Kaur, J.; Sancho-Pelluz, J.; Huber, G.; Fahl, E.; Arango-Gonzalez, B.; Zrenner, E.; Ekström, P.; Löwenheim, H.; et al. PARP1 Gene Knock-Out Increases Resistance to Retinal Degeneration without Affecting Retinal Function. PLoS ONE 2010, 5, e15495. [Google Scholar] [CrossRef] [Green Version]
- Hamann, S.; Schorderet, D.F.; Cottet, S. Bax-Induced Apoptosis in Leber’s Congenital Amaurosis: A Dual Role in Rod and Cone Degeneration. PLoS ONE 2009, 4, e6616. [Google Scholar] [CrossRef] [Green Version]
- Yoshizawa, K.; Kiuchi, K.; Nambu, H.; Yang, J.; Senzaki, H.; Kiyozuka, Y.; Shikata, N.; Tsubura, A. Caspase-3 inhibitor transiently delays inherited retinal degeneration in C3H mice carrying the rd gene. Graefe’s Arch. Clin. Exp. Ophthalmol. 2002, 240, 214–219. [Google Scholar] [CrossRef] [PubMed]
- Zeiss, C.J.; Neal, J.; Johnson, E.A. Caspase-3 in postnatal retinal development and degeneration. IOVS 2004, 45, 964–970. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bennett, J.; Zeng, Y.; Bajwa, R.; Klatt, L.; Li, Y.; Maguire, A.M. Adenovirus-mediated delivery of rhodopsin-promoted bcl-2 results in a delay in photoreceptor cell death in the rd/rd mouse. Gene Ther. 1998, 5, 1156–1164. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Joseph, R.M.; Li, T. Overexpression of Bcl-2 or Bcl-XL transgenes and photoreceptor degeneration. Investig. Ophthalmol. Vis. Sci. 1996, 37, 2434–2446. [Google Scholar]
- Fatokun, A.A.; Dawson, V.L.; Dawson, T.M. Parthanatos: Mitochondrial-linked mechanisms and therapeutic opportunities. Br. J. Pharmacol. 2014, 171, 2000–2016. [Google Scholar] [CrossRef] [Green Version]
- Li, H.; Liu, Z.-Y.; Wu, N.; Chen, Y.-C.; Cheng, Q.; Wang, J. PARP inhibitor resistance: The underlying mechanisms and clinical implications. Mol. Cancer 2020, 19, 1–16. [Google Scholar] [CrossRef]
- Sahaboglu, A.; Sharif, A.; Feng, L.; Secer, E.; Zrenner, E.; Paquet-Durand, F. Temporal progression of PARP activity in the Prph2 mutant rd2 mouse: Neuroprotective effects of the PARP inhibitor PJ34. PLoS ONE 2017, 12, e0181374. [Google Scholar] [CrossRef]
- Hafezi, F.; Abegg, M.; Grimm, C.; Wenzel, A.; Munz, K.; Stürmer, J.; Farber, D.; Remé, C.E. Retinal degeneration in the rd mouse in the absence of c-fos. IOVS 1998, 39, 2239–2244. [Google Scholar]
- Venkatesh, A.; Cheng, S.-Y.; Punzo, C. Loss of the cone-enriched caspase-7 does not affect secondary cone death in retinitis pigmentosa. Mol. Vis. 2017, 23, 944–951. [Google Scholar]
- Comitato, A.; Sanges, D.; Rossi, A.; Humphries, M.M.; Marigo, V. Activation of Bax in Three Models of Retinitis Pigmentosa. IOVS 2014, 55, 3555–3561. [Google Scholar] [CrossRef] [Green Version]
- Bixel, K.; Hays, J.L. Olaparib in the management of ovarian cancer. Pharm. Pers. Med. 2015, 8, 127–135. [Google Scholar] [CrossRef] [Green Version]
- Hüttl, S.; Michalakis, S.; Seeliger, M.; Luo, D.-G.; Acar, N.; Geiger, H.; Hudl, K.; Mader, R.; Haverkamp, S.; Moser, M.; et al. Impaired Channel Targeting and Retinal Degeneration in Mice Lacking the Cyclic Nucleotide-Gated Channel Subunit CNGB1. J. Neurosci. Res. 2005, 25, 130–138. [Google Scholar] [CrossRef] [PubMed]
- Aherne, A.; Kennan, A.; Kenna, P.F.; McNally, N.; Lloyd, D.G.; Alberts, I.L.; Kiang, A.-S.; Humphries, M.M.; Ayuso, C.; Engel, P.C.; et al. On the molecular pathology of neurodegeneration in IMPDH1-based retinitis pigmentosa. Hum. Mol. Genet. 2004, 13, 641–650. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Allison, A.C.; Kowalski, W.J.; Muller, C.D.; Eugui, E.M. Mechanisms of Action of Mycophenolic Acid. Ann. N. Y. Acad. Sci. 1993, 696, 63–87. [Google Scholar] [CrossRef] [PubMed]
- Athanasiou, D.; Aguila, M.; Bellingham, J.; Li, W.; McCulley, C.; Reeves, P.J.; Cheetham, M.E. The molecular and cellular basis of rhodopsin retinitis pigmentosa reveals potential strategies for therapy. Prog. Retin. Eye Res. 2018, 62, 1–23. [Google Scholar] [CrossRef] [Green Version]
- Messchaert, M.; Haer-Wigman, L.; Khan, M.I.; Cremers, F.P.M.; Collin, R.W.J. EYSmutation update: In silico assessment of 271 reported and 26 novel variants in patients with retinitis pigmentosa. Hum. Mutat. 2018, 39, 177–186. [Google Scholar] [CrossRef]
- Berkowitz, B.A. Oxidative stress measured in vivo without an exogenous contrast agent using QUEST MRI. J. Magn. Reson. 2018, 291, 94–100. [Google Scholar] [CrossRef]
- De la Camara, C.; Salom, D.; Sequedo, M.D.; Hervas, D.; Marin-Lambies, C.; Aller, E.; Jaijo, T.; Díaz-Llopis, M.; Millán, J.M.; Rodrigo, R. Altered Antioxidant-Oxidant Status in the Aqueous Humor and Peripheral Blood of Patients with Retinitis Pigmentosa. PLoS ONE 2013, 8, e74223. [Google Scholar] [CrossRef] [Green Version]
- Kjellström, U.; Veiga-Crespo, P.; Andréasson, S.; Ekström, P. Increased Plasma cGMP in a Family with Autosomal Recessive Retinitis Pigmentosa Due to Homozygous Mutations in the PDE6A Gene. IOVS 2016, 57, 6048–6057. [Google Scholar] [CrossRef] [Green Version]
Cell Death Mechanism | Targets | Methods | Results | References |
---|---|---|---|---|
Apoptosis | Caspase-type proteases | Pharmacological inhibition | No effect/minor delay of photoreceptor loss | [136] |
Bcl-2, Bcl-XL, c-fos, caspase-3, caspase-7 | Gene knockout | [137,138,139,140,141] | ||
BAX | Gene knockout | Only saving rods | [135,142] | |
PARthanatos | PARPs | Pharmacological inhibition | Delayed photoreceptor loss | [130,133,143] |
cGMP-dependentcell death | CNGC | Gene knockout, pharmacological inhibition | Photoreceptor protection with gene knockout, no protection after pharmacological inhibition | [95,144] |
VGCC | Gene knockout, pharmacological inhibition | Minor delay after gene knockout, no protection pharmacological inhibition | [102,103] | |
PKG | Pharmacological inhibition | Morphological and functional photoreceptor protection | [111] | |
IMPDH | Pharmacological inhibition | Reduced photoreceptor cGMP, photoreceptor protection | [81,145] |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Yan, J.; Chen, Y.; Zhu, Y.; Paquet-Durand, F. Programmed Non-Apoptotic Cell Death in Hereditary Retinal Degeneration: Crosstalk between cGMP-Dependent Pathways and PARthanatos? Int. J. Mol. Sci. 2021, 22, 10567. https://doi.org/10.3390/ijms221910567
Yan J, Chen Y, Zhu Y, Paquet-Durand F. Programmed Non-Apoptotic Cell Death in Hereditary Retinal Degeneration: Crosstalk between cGMP-Dependent Pathways and PARthanatos? International Journal of Molecular Sciences. 2021; 22(19):10567. https://doi.org/10.3390/ijms221910567
Chicago/Turabian StyleYan, Jie, Yiyi Chen, Yu Zhu, and François Paquet-Durand. 2021. "Programmed Non-Apoptotic Cell Death in Hereditary Retinal Degeneration: Crosstalk between cGMP-Dependent Pathways and PARthanatos?" International Journal of Molecular Sciences 22, no. 19: 10567. https://doi.org/10.3390/ijms221910567