Neuroprotective Effect of Tauroursodeoxycholic Acid (TUDCA) on In Vitro and In Vivo Models of Retinal Disorders: A Systematic Review


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Abstract

Background:Tauroursodeoxycholic acid (TUDCA) is a naturally produced hydrophilic bile acid that has been used for centuries in Chinese medicine. Numerous recent in vitro and in vivo studies have shown that TUDCA has neuroprotective action in various models of retinal disorders.

Objective:To systematically review the scientific literature and provide a comprehensive summary on the neuroprotective action and the mechanisms involved in the cytoprotective effects of TUDCA.

Methods:A systematic review was conducted in accordance with the PRISMA (The Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines. Systematic literature search of United States National Library of Medicine (PubMed), Web of Science, Embase, Scopus and Cochrane Library was performed, which covered all original articles published up to July 2022. The terms, "TUDCA" in combination with "retina", "retinal protection", "neuroprotection" were searched. Possible biases were identified with the adopted SYRCLE’s tool.

Results:Of the 423 initially gathered studies, 24 articles met inclusion/exclusion criteria for full-text review. Six of them were in vitro experiments, 17 studies reported in vivo data and one study described both in vitro and in vivo data. The results revealed the effect of TUDCA on different retinal diseases, such as retinitis pigmentosa (RP), diabetic retinopathy (DR), retinal degeneration (RD), retinal ganglion cell (RGC) injury, Leber’s hereditary optic neuropathy (LHON), choroidal neovascularization (CNV), and retinal detachment (RDT). The quality scores of the in vivo studies were ranged from 5 to 7 points (total 10 points), according to SYRCLE’s risk of bias tool. Both in vitro and in vivo data suggested that TUDCA could effectively delay degeneration and apoptosis of retinal neurons, preserve retinal structure and function, and its mechanism of actions might be related with inhibiting apoptosis, decreasing inflammation, attenuating oxidative stress, suppressing endoplasmic reticulum (ER) stress, and reducing angiogenesis.

Conclusion:This systematic review demonstrated that TUDCA has neuroprotective effect on in vivo and in vitro models of retinal disorders, reinforcing the currently available evidence that TUDCA could be a promising therapeutic agent in retinal diseases treatment. However, well designed clinical trials are necessary to appraise the efficacy of TUDCA in clinical setting.

About the authors

Jiaxian Li

Department of Eye Function Laboratory, Eye Hospital, China Academy of Chinese Medical Sciences

Email: info@benthamscience.net

Ziyang Huang

Department of Eye Function Laboratory, Eye Hospital, China Academy of Chinese Medical Sciences

Email: info@benthamscience.net

Yu Jin

Department of Eye Function Laboratory, Eye Hospital, China Academy of Chinese Medical Sciences

Email: info@benthamscience.net

Lina Liang

Department of Eye Function Laboratory, Eye Hospital, China Academy of Chinese Medical Sciences

Author for correspondence.
Email: info@benthamscience.net

Yamin Li

Department of Eye Function Laboratory, Eye Hospital, China Academy of Chinese Medical Sciences

Email: info@benthamscience.net

Kai Xu

Department of Eye Function Laboratory, Eye Hospital, China Academy of Chinese Medical Sciences

Email: info@benthamscience.net

Wei Zhou

Department of Eye Function Laboratory, Eye Hospital, China Academy of Chinese Medical Sciences

Email: info@benthamscience.net

Xiaoyu Li

Department of Eye Function Laboratory, Eye Hospital, China Academy of Chinese Medical Sciences

Email: info@benthamscience.net

References

  1. Wang, D.Q.H.; Carey, M.C. Therapeutic uses of animal biles in traditional Chinese medicine: An ethnopharmacological, biophysical chemical and medicinal review. World J. Gastroenterol., 2014, 20(29), 9952-9975. doi: 10.3748/wjg.v20.i29.9952 PMID: 25110425
  2. Monte, M.J.; Marin, J.J.G.; Antelo, A.; Vazquez-Tato, J. Bile acids: Chemistry, physiology, and pathophysiology. World J. Gastroenterol., 2009, 15(7), 804-816. doi: 10.3748/wjg.15.804 PMID: 19230041
  3. Marin, J.J.; Macias, R.I.; Briz, O.; Banales, J.M.; Monte, M.J. Bile acids in physiology, pathology and pharmacology. Curr. Drug Metab., 2015, 17(1), 4-29. doi: 10.2174/1389200216666151103115454 PMID: 26526836
  4. Pardue, M.T.; Allen, R.S. Neuroprotective strategies for retinal disease. Prog. Retin. Eye Res., 2018, 65, 50-76. doi: 10.1016/j.preteyeres.2018.02.002 PMID: 29481975
  5. Li, S.; Tan, H.Y.; Wang, N.; Hong, M.; Li, L.; Cheung, F.; Feng, Y. Substitutes for bear bile for the treatment of liver diseases: Research progress and future perspective. Evid. Based Complement. Alternat. Med., 2016, 2016, 1-10. doi: 10.1155/2016/4305074 PMID: 27087822
  6. Feng, Y.; Siu, K.; Wang, N.; Ng, K.M.; Tsao, S.W.; Nagamatsu, T.; Tong, Y. Bear bile: Dilemma of traditional medicinal use and animal protection. J. Ethnobiol. Ethnomed., 2009, 5(1), 2. doi: 10.1186/1746-4269-5-2 PMID: 19138420
  7. Ðanić, M.; Stanimirov, B.; Pavlović, N.; Goločorbin-Kon, S.; Al-Salami, H.; Stankov, K.; Mikov, M. Pharmacological applications of bile acids and their derivatives in the treatment of metabolic syndrome. Front. Pharmacol., 2018, 9, 1382. doi: 10.3389/fphar.2018.01382 PMID: 30559664
  8. Win, A.; Delgado, A.; Jadeja, R.N.; Martin, P.M.; Bartoli, M.; Thounaojam, M.C. Pharmacological and metabolic significance of bile acids in retinal diseases. Biomolecules, 2021, 11(2), 292. doi: 10.3390/biom11020292 PMID: 33669313
  9. Khalaf, K.; Tornese, P.; Cocco, A.; Albanese, A. Tauroursodeoxycholic acid: A potential therapeutic tool in neurodegenerative diseases. Transl. Neurodegener., 2022, 11(1), 33. doi: 10.1186/s40035-022-00307-z PMID: 35659112
  10. Vang, S.; Longley, K.; Steer, C.J.; Low, W.C. The unexpected uses of urso- and tauroursodeoxycholic acid in the treatment of non-liver diseases. Glob. Adv. Health Med., 2014, 3(3), 58-69. doi: 10.7453/gahmj.2014.017 PMID: 24891994
  11. Li, T.; Chiang, J.Y.L. Bile acid signaling in metabolic disease and drug therapy. Pharmacol. Rev., 2014, 66(4), 948-983. doi: 10.1124/pr.113.008201 PMID: 25073467
  12. Thomas, C.; Pellicciari, R.; Pruzanski, M.; Auwerx, J.; Schoonjans, K. Targeting bile-acid signalling for metabolic diseases. Nat. Rev. Drug Discov., 2008, 7(8), 678-693. doi: 10.1038/nrd2619 PMID: 18670431
  13. Kusaczuk, M. Tauroursodeoxycholate—bile acid with chaperoning activity: Molecular and cellular effects and therapeutic perspectives. Cells, 2019, 8(12), 1471. doi: 10.3390/cells8121471 PMID: 31757001
  14. Bhargava, P.; Smith, M.D.; Mische, L.; Harrington, E.; Fitzgerald, K.C.; Martin, K.; Kim, S.; Reyes, A.A.; Gonzalez-Cardona, J.; Volsko, C.; Tripathi, A.; Singh, S.; Varanasi, K.; Lord, H.N.; Meyers, K.; Taylor, M.; Gharagozloo, M.; Sotirchos, E.S.; Nourbakhsh, B.; Dutta, R.; Mowry, E.M.; Waubant, E.; Calabresi, P.A. Bile acid metabolism is altered in multiple sclerosis and supplementation ameliorates neuroinflammation. J. Clin. Invest., 2020, 130(7), 3467-3482. doi: 10.1172/JCI129401 PMID: 32182223
  15. Huang, F.; Pariante, C.M.; Borsini, A. From dried bear bile to molecular investigation: A systematic review of the effect of bile acids on cell apoptosis, oxidative stress and inflammation in the brain, across pre-clinical models of neurological, neurodegenerative and neuropsychiatric disorders. Brain Behav. Immun., 2022, 99, 132-146. doi: 10.1016/j.bbi.2021.09.021 PMID: 34601012
  16. Keene, C.D.; Rodrigues, C.M.P.; Eich, T.; Linehan-Stieers, C.; Abt, A.; Kren, B.T.; Steer, C.J.; Low, W.C. A bile acid protects against motor and cognitive deficits and reduces striatal degeneration in the 3-nitropropionic acid model of Huntington’s disease. Exp. Neurol., 2001, 171(2), 351-360. doi: 10.1006/exnr.2001.7755 PMID: 11573988
  17. Rodrigues, C.M.P.; Solá, S.; Nan, Z.; Castro, R.E.; Ribeiro, P.S.; Low, W.C.; Steer, C.J. Tauroursodeoxycholic acid reduces apoptosis and protects against neurological injury after acute hemorrhagic stroke in rats. Proc. Natl. Acad. Sci. USA, 2003, 100(10), 6087-6092. doi: 10.1073/pnas.1031632100 PMID: 12721362
  18. Mertens, K.L.; Kalsbeek, A.; Soeters, M.R.; Eggink, H.M. Bile acid signaling pathways from the enterohepatic circulation to the central nervous system. Front. Neurosci., 2017, 11, 617. doi: 10.3389/fnins.2017.00617 PMID: 29163019
  19. Rosa, A.I.; Fonseca, I.; Nunes, M.J.; Moreira, S.; Rodrigues, E.; Carvalho, A.N.; Rodrigues, C.M.P.; Gama, M.J.; Castro-Caldas, M. Novel insights into the antioxidant role of tauroursodeoxycholic acid in experimental models of Parkinson’s disease. Biochim. Biophys. Acta Mol. Basis Dis., 2017, 1863(9), 2171-2181. doi: 10.1016/j.bbadis.2017.06.004 PMID: 28583715
  20. Castro-Caldas, M.; Carvalho, A.N.; Rodrigues, E.; Henderson, C.J.; Wolf, C.R.; Rodrigues, C.M.P.; Gama, M.J. Tauroursodeoxycholic acid prevents MPTP-induced dopaminergic cell death in a mouse model of Parkinson’s disease. Mol. Neurobiol., 2012, 46(2), 475-486. doi: 10.1007/s12035-012-8295-4 PMID: 22773138
  21. Abdelkader, N.F.; Safar, M.M.; Salem, H.A. Ursodeoxycholic acid ameliorates apoptotic cascade in the rotenone model of Parkinson’s Disease: Modulation of mitochondrial perturbations. Mol. Neurobiol., 2016, 53(2), 810-817. doi: 10.1007/s12035-014-9043-8 PMID: 25502462
  22. Lo, A.C.; Callaerts-Vegh, Z.; Nunes, A.F.; Rodrigues, C.M.P.; D’Hooge, R. Tauroursodeoxycholic acid (TUDCA) supplementation prevents cognitive impairment and amyloid deposition in APP/PS1 mice. Neurobiol. Dis., 2013, 50, 21-29. doi: 10.1016/j.nbd.2012.09.003 PMID: 22974733
  23. Nunes, A.F.; Amaral, J.D.; Lo, A.C.; Fonseca, M.B.; Viana, R.J.S.; Callaerts-Vegh, Z.; D’Hooge, R.; Rodrigues, C.M.P. TUDCA, a bile acid, attenuates amyloid precursor protein processing and amyloidβ deposition in APP/PS1 mice. Mol. Neurobiol., 2012, 45(3), 440-454. doi: 10.1007/s12035-012-8256-y PMID: 22438081
  24. Ramalho, R.M.; Nunes, A.F.; Dias, R.B.; Amaral, J.D.; Lo, A.C.; D’Hooge, R.; Sebastião, A.M.; Rodrigues, C.M.P. Tauroursodeoxycholic acid suppresses amyloid β-induced synaptic toxicity in vitro and in APP/PS1 mice. Neurobiol. Aging, 2013, 34(2), 551-561. doi: 10.1016/j.neurobiolaging.2012.04.018 PMID: 22621777
  25. Dionísio, P.A.; Amaral, J.D.; Ribeiro, M.F.; Lo, A.C.; D’Hooge, R.; Rodrigues, C.M.P. Amyloidβ pathology is attenuated by tauroursodeoxycholic acid treatment in APP/PS1 mice after disease onset. Neurobiol. Aging, 2015, 36(1), 228-240. doi: 10.1016/j.neurobiolaging.2014.08.034 PMID: 25443293
  26. Pan, X.; Elliott, C.T.; McGuinness, B.; Passmore, P.; Kehoe, P.G.; Hölscher, C.; McClean, P.L.; Graham, S.F.; Green, B.D. Metabolomic profiling of bile acids in clinical and experimental samples of Alzheimer’s Disease. Metabolites, 2017, 7(2), 28. doi: 10.3390/metabo7020028 PMID: 28629125
  27. Keene, C.D.; Rodrigues, C.M.P.; Eich, T.; Chhabra, M.S.; Steer, C.J.; Low, W.C. Tauroursodeoxycholic acid, a bile acid, is neuroprotective in a transgenic animal model of Huntington’s disease. Proc. Natl. Acad. Sci. USA, 2002, 99(16), 10671-10676. doi: 10.1073/pnas.162362299 PMID: 12149470
  28. Yanguas-Casás, N.; Barreda-Manso, M.A.; Nieto-Sampedro, M.; Romero-Ramírez, L. TUDCA: An agonist of the bile acid receptor GPBAR1/TGR5 with anti-inflammatory effects in microglial cells. J. Cell. Physiol., 2017, 232(8), 2231-2245. doi: 10.1002/jcp.25742 PMID: 27987324
  29. Daruich, A.; Picard, E.; Boatright, J.H.; Behar-Cohen, F. Review: The bile acids urso- and tauroursodeoxycholic acid as neuroprotective therapies in retinal disease. Mol. Vis., 2019, 25, 610-624. PMID: 31700226
  30. Cha, B.H.; Kim, J.S.; Chan Ahn, J.; Kim, H.C.; Kim, B.S.; Han, D.K.; Park, S.G.; Lee, S.H. The role of tauroursodeoxycholic acid on adipogenesis of human adipose-derived stem cells by modulation of ER stress. Biomaterials, 2014, 35(9), 2851-2858. doi: 10.1016/j.biomaterials.2013.12.067 PMID: 24424209
  31. Soares, R.; Ribeiro, F.F.; Xapelli, S.; Genebra, T.; Ribeiro, M.F.; Sebastião, A.M.; Rodrigues, C.M.P.; Solá, S. Tauroursodeoxycholic acid enhances mitochondrial biogenesis, neural stem cell pool, and early neurogenesis in adult rats. Mol. Neurobiol., 2018, 55(5), 3725-3738. doi: 10.1007/s12035-017-0592-5 PMID: 28534273
  32. Yoon, Y.M.; Lee, J.H.; Yun, S.P.; Han, Y.S.; Yun, C.W.; Lee, H.J.; Noh, H.; Lee, S.J.; Han, H.J.; Lee, S.H. Tauroursodeoxycholic acid reduces ER stress by regulating of Akt-dependent cellular prion protein. Sci. Rep., 2016, 6(1), 39838. doi: 10.1038/srep39838 PMID: 28004805
  33. Choi, S.K.; Lim, M.; Byeon, S.H.; Lee, Y.H. Inhibition of endoplasmic reticulum stress improves coronary artery function in the spontaneously hypertensive rats. Sci. Rep., 2016, 6(1), 31925. doi: 10.1038/srep31925 PMID: 27550383
  34. Qin, Y.; Wang, Y.; Liu, O.; Jia, L.; Fang, W.; Du, J.; Wei, Y. Tauroursodeoxycholic acid attenuates angiotensin ii induced abdominal aortic aneurysm formation in apolipoprotein e-deficient mice by inhibiting endoplasmic reticulum stress. Eur. J. Vasc. Endovasc. Surg., 2017, 53(3), 337-345. doi: 10.1016/j.ejvs.2016.10.026 PMID: 27889204
  35. Xie, Y.; He, Y.; Cai, Z.; Cai, J.; Xi, M.; Zhang, Y.; Xi, J. Tauroursodeoxycholic acid inhibits endoplasmic reticulum stress, blocks mitochondrial permeability transition pore opening, and suppresses reperfusion injury through GSK-3ß in cardiac H9c2 cells. Am. J. Transl. Res., 2016, 8(11), 4586-4597. PMID: 27904664
  36. Fan, Y.; Zhang, J.; Xiao, W.; Lee, K.; Li, Z.; Wen, J.; He, L.; Gui, D.; Xue, R.; Jian, G.; Sheng, X.; He, J.C.; Wang, N. Rtn1a-mediated endoplasmic reticulum stress in podocyte injury and diabetic nephropathy. Sci. Rep., 2017, 7(1), 323. doi: 10.1038/s41598-017-00305-6 PMID: 28336924
  37. Walsh, L.K.; Restaino, R.M.; Neuringer, M.; Manrique, C.; Padilla, J. Administration of tauroursodeoxycholic acid prevents endothelial dysfunction caused by an oral glucose load. Clin. Sci., 2016, 130(21), 1881-1888. doi: 10.1042/CS20160501 PMID: 27503949
  38. Zhang, J.; Fan, Y.; Zeng, C.; He, L.; Wang, N. Tauroursodeoxycholic acid attenuates renal tubular injury in a mouse model of type 2 Diabetes. Nutrients, 2016, 8(10), 589. doi: 10.3390/nu8100589 PMID: 27669287
  39. Chen, Y.; Wu, Z.; Zhao, S.; Xiang, R. Chemical chaperones reduce ER stress and adipose tissue inflammation in high fat diet-induced mouse model of obesity. Sci. Rep., 2016, 6(1), 27486. doi: 10.1038/srep27486 PMID: 27271106
  40. Feng, L.; Zhang, W.; Shen, Q.; Miao, C.; Chen, L.; Li, Y.; Gu, X.; Fan, M.; Ma, Y.; Wang, H.; Liu, X.; Zhang, X. Bile acid metabolism dysregulation associates with cancer cachexia: roles of liver and gut microbiome. J. Cachexia Sarcopenia Muscle, 2021, 12(6), 1553-1569. doi: 10.1002/jcsm.12798 PMID: 34585527
  41. Fernández-Sánchez, L.; Lax, P.; Noailles, A.; Angulo, A.; Maneu, V.; Cuenca, N. Natural compounds from saffron and bear bile prevent vision loss and retinal degeneration. Molecules, 2015, 20(8), 13875-13893. doi: 10.3390/molecules200813875 PMID: 26263962
  42. Cuenca, N.; Fernández-Sánchez, L.; Campello, L.; Maneu, V.; De la Villa, P.; Lax, P.; Pinilla, I. Cellular responses following retinal injuries and therapeutic approaches for neurodegenerative diseases. Prog. Retin. Eye Res., 2014, 43, 17-75. doi: 10.1016/j.preteyeres.2014.07.001 PMID: 25038518
  43. Jones, B.W.; Pfeiffer, R.L.; Ferrell, W.D.; Watt, C.B.; Marmor, M.; Marc, R.E. Retinal remodeling in human retinitis pigmentosa. Exp. Eye Res., 2016, 150, 149-165. doi: 10.1016/j.exer.2016.03.018 PMID: 27020758
  44. Jones, B.W.; Watt, C.B.; Frederick, J.M.; Baehr, W.; Chen, C.K.; Levine, E.M.; Milam, A.H.; Lavail, M.M.; Marc, R.E. Retinal remodeling triggered by photoreceptor degenerations. J. Comp. Neurol., 2003, 464(1), 1-16. doi: 10.1002/cne.10703 PMID: 12866125
  45. Marc, R.E.; Jones, B.W.; Watt, C.B.; Strettoi, E. Neural remodeling in retinal degeneration. Prog. Retin. Eye Res., 2003, 22(5), 607-655. doi: 10.1016/S1350-9462(03)00039-9 PMID: 12892644
  46. Antonetti, D.A.; Barber, A.J.; Bronson, S.K.; Freeman, W.M.; Gardner, T.W.; Jefferson, L.S.; Kester, M.; Kimball, S.R.; Krady, J.K.; LaNoue, K.F.; Norbury, C.C.; Quinn, P.G.; Sandirasegarane, L.; Simpson, I.A. JDRF Diabetic Retinopathy Center Group. Diabetic retinopathy: seeing beyond glucose-induced microvascular disease. Diabetes, 2006, 55(9), 2401-2411. doi: 10.2337/db05-1635 PMID: 16936187
  47. Page, M.J.; Moher, D.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; Chou, R.; Glanville, J.; Grimshaw, J.M.; Hróbjartsson, A.; Lalu, M.M.; Li, T.; Loder, E.W.; Mayo-Wilson, E.; McDonald, S.; McGuinness, L.A.; Stewart, L.A.; Thomas, J.; Tricco, A.C.; Welch, V.A.; Whiting, P.; McKenzie, J.E. PRISMA 2020 explanation and elaboration: Updated guidance and exemplars for reporting systematic reviews. BMJ, 2021, 372(160), n160. doi: 10.1136/bmj.n160 PMID: 33781993
  48. Zhang, X.; Tan, R.; Lam, W.C.; Yao, L.; Wang, X.; Cheng, C.W.; Liu, F.; Chan, J.C.P.; Aixinjueluo, Q.; Lau, C.T.; Chen, Y.; Yang, K.; Wu, T.; Lyu, A.; Bian, Z. PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) extension for Chinese Herbal Medicines 2020 (PRISMA-CHM 2020). Am. J. Chin. Med., 2020, 48(6), 1279-1313. doi: 10.1142/S0192415X20500639 PMID: 32907365
  49. Hooijmans, C.R.; Rovers, M.M.; de Vries, R.B.M.; Leenaars, M.; Ritskes-Hoitinga, M.; Langendam, M.W. SYRCLE’s risk of bias tool for animal studies. BMC Med. Res. Methodol., 2014, 14(1), 43. doi: 10.1186/1471-2288-14-43 PMID: 24667063
  50. Bikbova, G.; Oshitari, T.; Baba, T.; Yamamoto, S. Combination of neuroprotective and regenerative agents for AGE-Induced retinal degeneration: In vitro study. BioMed Res. Int., 2017, 2017, 1-9. doi: 10.1155/2017/8604723 PMID: 28573143
  51. Daruich, A.; Picard, E.; Guégan, J.; Jaworski, T.; Parenti, L.; Delaunay, K.; Naud, M.C.; Berdugo, M.; Boatright, J.H.; Behar-Cohen, F. Comparative analysis of Urso- and tauroursodeoxycholic acid neuroprotective effects on retinal degeneration models. Pharmaceuticals, 2022, 15(3), 334. doi: 10.3390/ph15030334 PMID: 35337132
  52. Gaspar, J.M.; Martins, A.; Cruz, R.; Rodrigues, C.M.P.; Ambrósio, A.F.; Santiago, A.R. Tauroursodeoxycholic acid protects retinal neural cells from cell death induced by prolonged exposure to elevated glucose. Neuroscience, 2013, 253, 380-388. doi: 10.1016/j.neuroscience.2013.08.053 PMID: 24012838
  53. Oshitari, T.; Bikbova, G.; Yamamoto, S. Increased expression of phosphorylated c-Jun and phosphorylated c-Jun N-terminal kinase associated with neuronal cell death in diabetic and high glucose exposed rat retinas. Brain Res. Bull., 2014, 101, 18-25. doi: 10.1016/j.brainresbull.2013.12.002 PMID: 24333191
  54. Wang, C.; Yuan, J.; Qin, D.; Gu, J.; Zhao, B.; Zhang, L.; Zhao, D.; Chen, J.; Hou, X.; Yang, N.; Bu, W.; Wang, J.; Li, C.; Tian, G.; Dong, Z.; Feng, L.; Jia, X. Protection of tauroursodeoxycholic acid on high glucose-induced human retinal microvascular endothelial cells dysfunction and streptozotocin-induced diabetic retinopathy rats. J. Ethnopharmacol., 2016, 185, 162-170. doi: 10.1016/j.jep.2016.03.026 PMID: 26988565
  55. Murase, H.; Tsuruma, K.; Shimazawa, M.; Hara, H. TUDCA promotes phagocytosis by retinal pigment epithelium via MerTK activation. Invest. Ophthalmol. Vis. Sci., 2015, 56(4), 2511-2518. doi: 10.1167/iovs.14-15962 PMID: 25804419
  56. Alhasani, R.H.; Almarhoun, M.; Zhou, X.; Reilly, J.; Patterson, S.; Zeng, Z.; Shu, X. Tauroursodeoxycholic acid protects retinal pigment epithelial cells from oxidative injury and endoplasmic reticulum stress in vitro. Biomedicines, 2020, 8(9), 367. doi: 10.3390/biomedicines8090367 PMID: 32967221
  57. Phillips, M.J.; Walker, T.A.; Choi, H.Y.; Faulkner, A.E.; Kim, M.K.; Sidney, S.S.; Boyd, A.P.; Nickerson, J.M.; Boatright, J.H.; Pardue, M.T. Tauroursodeoxycholic acid preservation of photoreceptor structure and function in the rd10 mouse through postnatal day 30. Invest. Ophthalmol. Vis. Sci., 2008, 49(5), 2148-2155. doi: 10.1167/iovs.07-1012 PMID: 18436848
  58. Fernández-Sánchez, L.; Lax, P.; Pinilla, I.; Martín-Nieto, J.; Cuenca, N. Tauroursodeoxycholic acid prevents retinal degeneration in transgenic P23H rats. Invest. Ophthalmol. Vis. Sci., 2011, 52(8), 4998-5008. doi: 10.1167/iovs.11-7496 PMID: 21508111
  59. Oveson, B.C.; Iwase, T.; Hackett, S.F.; Lee, S.Y.; Usui, S.; Sedlak, T.W.; Snyder, S.H.; Campochiaro, P.A.; Sung, J.U. Constituents of bile, bilirubin and TUDCA, protect against oxidative stress-induced retinal degeneration. J. Neurochem., 2011, 116(1), 144-153. doi: 10.1111/j.1471-4159.2010.07092.x PMID: 21054389
  60. Drack, A.V.; Dumitrescu, A.V.; Bhattarai, S.; Gratie, D.; Stone, E.M.; Mullins, R.; Sheffield, V.C. TUDCA slows retinal degeneration in two different mouse models of retinitis pigmentosa and prevents obesity in Bardet-Biedl syndrome type 1 mice. Invest. Ophthalmol. Vis. Sci., 2012, 53(1), 100-106. doi: 10.1167/iovs.11-8544 PMID: 22110077
  61. Noailles, A.; Fernández-Sánchez, L.; Lax, P.; Cuenca, N. Microglia activation in a model of retinal degeneration and TUDCA neuroprotective effects. J. Neuroinflammation, 2014, 11(1), 186. doi: 10.1186/s12974-014-0186-3 PMID: 25359524
  62. Fernández-Sánchez, L.; Bravo-Osuna, I.; Lax, P.; Arranz-Romera, A.; Maneu, V.; Esteban-Pérez, S.; Pinilla, I.; Puebla-González, M.M.; Herrero-Vanrell, R.; Cuenca, N. Controlled delivery of tauroursodeoxycholic acid from biodegradable microspheres slows retinal degeneration and vision loss in P23H rats. PLoS One, 2017, 12(5), e0177998. doi: 10.1371/journal.pone.0177998 PMID: 28542454
  63. Zhang, X.; Shahani, U.; Reilly, J.; Shu, X. Disease mechanisms and neuroprotection by tauroursodeoxycholic acid in Rpgr knockout mice. J. Cell. Physiol., 2019, 234(10), 18801-18812. doi: 10.1002/jcp.28519 PMID: 30924157
  64. Fernández-Sánchez, L.; Albertos-Arranz, H.; Ortuño-Lizarán, I.; Lax, P.; Cuenca, N. Neuroprotective effects of tauroursodeoxicholic acid involves vascular and glial changes in retinitis pigmentosa model. Front. Neuroanat., 2022, 16, 858073. doi: 10.3389/fnana.2022.858073 PMID: 35493706
  65. Lawson, E.C.; Bhatia, S.K.; Han, M.K.; Aung, M.H.; Ciavatta, V.; Boatright, J.H.; Pardue, M.T. Tauroursodeoxycholic acid protects retinal function and structure in rd1 mice. Adv. Exp. Med. Biol., 2016, 854, 431-436. doi: 10.1007/978-3-319-17121-0_57 PMID: 26427442
  66. Tao, Y.; Dong, X.; Lu, X.; Qu, Y.; Wang, C.; Peng, G.; Zhang, J. Subcutaneous delivery of tauroursodeoxycholic acid rescues the cone photoreceptors in degenerative retina: A promising therapeutic molecule for retinopathy. Biomed. Pharmacother., 2019, 117, 109021. doi: 10.1016/j.biopha.2019.109021 PMID: 31387173
  67. Yang, L.; Wu, L.; Wang, D.; Li, Y.; Dou, H.; Tso, M.O.; Ma, Z. Role of endoplasmic reticulum stress in the loss of retinal ganglion cells in diabetic retinopathy. Neural Regen. Res., 2013, 8(33), 3148-3158. PMID: 25206636
  68. Fu, J.; Aung, M.H.; Prunty, M.C.; Hanif, A.M.; Hutson, L.M.; Boatright, J.H.; Pardue, M.T. Tauroursodeoxycholic acid protects retinal and visual function in a mouse model of Type 1 Diabetes. Pharmaceutics, 2021, 13(8), 1154. doi: 10.3390/pharmaceutics13081154 PMID: 34452115
  69. Gómez-Vicente, V.; Lax, P.; Fernández-Sánchez, L.; Rondón, N.; Esquiva, G.; Germain, F.; de la Villa, P.; Cuenca, N. Neuroprotective effect of tauroursodeoxycholic acid on N-Methyl-D-Aspartate-Induced retinal ganglion cell degeneration. PLoS One, 2015, 10(9), e0137826. doi: 10.1371/journal.pone.0137826 PMID: 26379056
  70. Kitamura, Y.; Bikbova, G.; Baba, T.; Yamamoto, S.; Oshitari, T. In vivo effects of single or combined topical neuroprotective and regenerative agents on degeneration of retinal ganglion cells in rat optic nerve crush model. Sci. Rep., 2019, 9(1), 101. doi: 10.1038/s41598-018-36473-2 PMID: 30643179
  71. Woo, S.J.; Kim, J.H.; Yu, H.G. Ursodeoxycholic acid and tauroursodeoxycholic acid suppress choroidal neovascularization in a laser-treated rat model. J. Ocul. Pharmacol. Ther., 2010, 26(3), 223-229. doi: 10.1089/jop.2010.0012 PMID: 20565307
  72. Mantopoulos, D.; Murakami, Y.; Comander, J.; Thanos, A.; Roh, M.; Miller, J.W.; Vavvas, D.G. Tauroursodeoxycholic acid (TUDCA) protects photoreceptors from cell death after experimental retinal detachment. PLoS One, 2011, 6(9), e24245. doi: 10.1371/journal.pone.0024245 PMID: 21961034
  73. Zhang, T.; Baehr, W.; Fu, Y. Chemical chaperone TUDCA preserves cone photoreceptors in a mouse model of Leber congenital amaurosis. Invest. Ophthalmol. Vis. Sci., 2012, 53(7), 3349-3356. doi: 10.1167/iovs.12-9851 PMID: 22531707
  74. Sherrod, C.E.; Vitale, S.; Frick, K.D.; Ramulu, P.Y. Association of vision loss and work status in the United States. JAMA Ophthalmol., 2014, 132(10), 1239-1242. doi: 10.1001/jamaophthalmol.2014.2213 PMID: 25032668
  75. Cumberland, P.M.; Rahi, J.S. UK biobank eye and vision consortium. Visual function, social position, and health and life chances. JAMA Ophthalmol., 2016, 134(9), 959-966. doi: 10.1001/jamaophthalmol.2016.1778 PMID: 27466983
  76. Papadopoulos, K.; Montgomery, A.J.; Chronopoulou, E. The impact of visual impairments in self-esteem and locus of control. Res. Dev. Disabil., 2013, 34(12), 4565-4570. doi: 10.1016/j.ridd.2013.09.036 PMID: 24176255
  77. Sng, K.S.; Li, G.; Zhou, L.; Song, Y.; Chen, X.; Wang, Y.; Yao, M.; Cui, X. Ginseng extract and ginsenosides improve neurological function and promote antioxidant effects in rats with spinal cord injury: A meta-analysis and systematic review. J. Ginseng Res., 2022, 46(1), 11-22. doi: 10.1016/j.jgr.2021.05.009 PMID: 35058723
  78. Elia, A.E.; Lalli, S.; Monsurrò, M.R.; Sagnelli, A.; Taiello, A.C.; Reggiori, B.; La Bella, V.; Tedeschi, G.; Albanese, A. Tauroursodeoxycholic acid in the treatment of patients with amyotrophic lateral sclerosis. Eur. J. Neurol., 2016, 23(1), 45-52. doi: 10.1111/ene.12664 PMID: 25664595
  79. Herrero-Vanrell, R.; Refojo, M.F. Biodegradable microspheres for vitreoretinal drug delivery. Adv. Drug Deliv. Rev., 2001, 52(1), 5-16. doi: 10.1016/S0169-409X(01)00200-9 PMID: 11672871
  80. Wassmer, S.; Rafat, M.; Fong, W.G.; Baker, A.N.; Tsilfidis, C. Chitosan microparticles for delivery of proteins to the retina. Acta Biomater., 2013, 9(8), 7855-7864. doi: 10.1016/j.actbio.2013.04.025 PMID: 23623991
  81. Herrero-Vanrell, R.; Bravo-Osuna, I.; Andrés-Guerrero, V.; Vicario-de-la-Torre, M.; Molina-Martínez, I.T. The potential of using biodegradable microspheres in retinal diseases and other intraocular pathologies. Prog. Retin. Eye Res., 2014, 42, 27-43. doi: 10.1016/j.preteyeres.2014.04.002 PMID: 24819336
  82. Arranz-Romera, A.; Esteban-Pérez, S.; Molina-Martínez, I.T.; Bravo-Osuna, I.; Herrero-Vanrell, R. Co-delivery of glial cell-derived neurotrophic factor (GDNF) and tauroursodeoxycholic acid (TUDCA) from PLGA microspheres: Potential combination therapy for retinal diseases. Drug Deliv. Transl. Res., 2021, 11(2), 566-580. doi: 10.1007/s13346-021-00930-9 PMID: 33641047

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