Login Register Cart 0
Generic placeholder image

Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Systematic Review Article

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

Author(s): Jiaxian Li, Ziyang Huang, Yu Jin, Lina Liang*, Yamin Li, Kai Xu, Wei Zhou and Xiaoyu Li

Volume 22, Issue 8, 2024

Published on: 08 September, 2023

Page: [1374 - 1390] Pages: 17

DOI: 10.2174/1570159X21666230907152207

Price: $65

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.

« Previous Next »
Graphical Abstract

[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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/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.
[http://dx.doi.org/10.1007/s13346-021-00930-9] [PMID: 33641047]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy