Multiple Mechanisms of the Therapeutic Effect of Trehalose in Inhibition of Experimental Neurodegeneration
- Authors: Pupyshev A.B.1, Korolenko T.A.1, Tikhonova M.A.1
- 
							Affiliations: 
							- Scientific Research Institute of Neurosciences and Medicine
 
- Issue: Vol 40, No 4 (2023)
- Pages: 317-330
- Section: Review Articles
- URL: https://rjdentistry.com/1027-8133/article/view/653918
- DOI: https://doi.org/10.31857/S1027813323040192
- EDN: https://elibrary.ru/OVYUKU
- ID: 653918
Cite item
Abstract
The search for effective treatment for neurodegeneration implies attacking the multiple mechanisms of this pathology. Such properties were found in disaccharide trehalose, which shows therapeutic effects in models of many diseases and has been approved by the FDA for use in humans. Trehalose consists of two glucose residues bonded together by a flexible α-1-1'-glycosidic bond, giving it chaperone-like activity. Due to this, it prevents abnormal folding of aberrant proteins and has the properties of a cryo- and bioprotector. However, the main therapeutic effect is determined by the induction of mTOR-independent autophagy mediated by AMPK kinase as the main target. The result is a weakening of the accumulation of cytotoxic proteins and factors and an increase in cell viability. Autophagy activation depends on trehalose-induced lysosome and autophagosome biogenesis through activation of transcription factors TFEB and FOXO1. Trehalose has an anti-inflammatory effect closely related to the inhibition of oxidative stress. Trehalose-induced enhancement of endogenous antioxidant defense involves the regulator Nrf2. The review considers the neuroprotective effects of trehalose in models of major neurodegenerative diseases such as Parkinson’s, Alzheimer’s, Huntington’s and others. Overall, trehalose shows high therapeutic potential in the treatment of experimental neurodegeneration and thus stimulating the study of its clinical application.
Keywords
About the authors
A. B. Pupyshev
Scientific Research Institute of Neurosciences and Medicine
														Email: nchjournal@gmail.com
				                					                																			                												                								Russia, Novosibirsk						
T. A. Korolenko
Scientific Research Institute of Neurosciences and Medicine
														Email: nchjournal@gmail.com
				                					                																			                												                								Russia, Novosibirsk						
M. A. Tikhonova
Scientific Research Institute of Neurosciences and Medicine
														Email: nchjournal@gmail.com
				                					                																			                												                								Russia, Novosibirsk						
References
- Vassar R., Zheng H. // Mol. Neurodegener. 2014. V. 9. P. 34.
- Basha F.H., Waseem M., Srinivasan H. // Cell. Biochem. Funct. 2021. V. 39. № 5. P. 613–622.
- Kurtishi A., Rosen B., Patil K.S., Alves G.W., Møller S.G. // Mol. Neurobiol. 2019. V. 56. № 5. P. 3676–3689.
- Leszek J., Barreto G.E., Gąsiorowski K., Koutsouraki E., Ávila-Rodrigues M., Aliev G. // CNS Neurol. Disord. Drug Targets. 2016. V. 15. № 3. P. 329–336.
- Kwon H.S., Koh S.H. // Transl. Neurodegener. 2020. V. 9. № 1. P. 42.
- Corti O., Blomgren K., Poletti A., Beart P.M. // J. Neurochem. 2020. V. 154. № 4. P. 354–371.
- Tanaka M., Machida Y., Niu S., Ikeda T., Jana N.R., Doi H., Kurosawa M., Nekooki M., Nukina N. // Nat. Med. 2004. V. 10. № 2. P. 148–154.
- Sarkar S., Davies J.E., Huang Z., Tunnacliffe A., Rubinsztein D.C. // J. Biol. Chem. 2007. V. 282. № 8. P. 5641–5652.
- Rodríguez-Navarro J.A., Rodríguez L., Casarejos M.J., Solano R.M., Gómez A., Perucho J., Cuervo A.M., García de Yébenes J., Mena M.A. // Neurobiol. Dis. 2010. V. 39. № 3. P. 423–438.
- Hosseinpour-Moghaddam K., Caraglia M., Sahebkar A. // J. Cell Physiol. 2018. V. 233. № 9. P. 6524–6543.
- Thellung S., Corsaro A., Nizzari M., Barbieri F., Florio T. // Int. J. Mol. Sci. 2019. V. 20. № 4. pii: E901.
- Rubinsztein D.C., Bento C.F., Deretic V. // J. Exp. Med. 2015. V. 212. № 7. P. 979–990.
- Byun S., Lee E., Lee K.W. // Int. J. Mol. Sci. 2017. V. 18. № 9. pii: E1959.
- Lee H., Yoon Y.S., Lee S.J. // Cell Death Dis. 2018. V. 9. № 7. P. 712–720.
- Liu M., Zhang M., Ye H., Lin S., Yang Y., Wang L., Jones G., Trang H. // Food Chem. 2013. V. 136. № 2. P. 485–490.
- Stewart S., He X. // Langmuir. 2018. https://doi.org/10.1021/acs.langmuir.8b02015
- Arguelles J.C. // J. Mol. Evol. 2014. V. 79. P. 111–116.
- Martano G., Gerosa L., Prada I., Garrone G., Krogh V., Verderio C., Passafaro M. // ACS Chem. Neurosci. 2017. V. 8. P. 1865–1872.
- van Elburg R.M., Uil J.J., Kokke F.T., Mulder A.M., van de Broek W.G., Mulder C.J., Heymans H.S. // J. Pediatr. Gastroenterol. Nutr. 1995. V. 20. № 2. P. 184–188.
- Kamiya T., Hirata K., Matsumoto S., Arai C., Yoshizane C., Kyono F., Ariyasu T., Hanaya T., Arai S., Okura T., Yamamoto K., Ikeda M., Kurimoto M. // Nutr. Res. 2004. V. 24. № 2. P. 185–196.
- Howson P.A., Johnston T.H., Ravenscroft P., Hill M.P., Su J., Brotchie J.M., Koprich J.B. // J. Pharmacol. Exp. Ther. 2019. V. 369. № 3. P. 364–374.
- Di Rienzi S.C., Britton R.A. // Adv. Nutr. 2020. V. 11. № 3. P. 616–629.
- Sahebkar A., Hatamipour M., Tabatabaei S.A. // J. Cell Biochem. 2019. V. 120. № 6. P. 9455–9459.
- Mobini M., Radbakhsh S., Kubaski F., Eshraghi P., Vakili S., Vakili R., Khalili M., Varesvazirian M., Jamialahmadi T., Alamdaran S.A., Sayedi S.J., Rajabi O., Emami S.A., Reiner Ž., Sebkar A. // J. Clin. Med. 2022.V. 11. № 1. P. 247.
- Felice V.D., Quigley E.M., Sullivan A.M., O’Keeffe G.W., O’Mahony S.M. // Parkinsonism Relat. Disord. 2016. V. 27. P. 1–8.
- Macias-Ceja D.C., Cosín-Roger J., Ortiz-Masiá D., Salvador P., Hernández C., Esplugues J.V., Calatayud S., Barrachina M.D. // Br. J. Pharmacol. 2017. V. 174. № 15. P. 2501–2511.
- Arai C., Arai N., Arai S., Yoshizane C., Miyata S., Mizote A., Suyama A., Endo S., Ariyasu T., Mitsuzumi H., Ushio S. // Nutr. Metabol. 2019. V. 16. P. 45.
- Kaushik J.K., Bhat R. // J. Biol. Chem. 2003. V. 278. № 28. P. 26458–26465.
- Sarkar S., Chigurupati S., Raymick J., Mann D., Bowyer J.F., Schmitt T., Beger R.D., Hanig J.P., Schmued L.C., Paule M.G. // Neurotoxicology. 2014. V. 44. P. 250–262.
- Liu R., Barkhordarian H., Emadi S., Park C.B., Sierks M.R. // Neurobiol. Dis. 2005. V. 20. P. 74–81.
- Khan S.H., Kumar R. // Pathol. Res. Pract. 2017. V. 213. № 6. P. 643–648.
- Lins R.D., Pereira C.S., Hünenberger P.H. // Proteins. 2004. V. 55. № 1. P. 177–186.
- Casarejos M.J., Perucho J., Lopez-Sendon J.L., Garcia de Yebenes J., Bettencourt C., Gomez A., Ruiz C., Heutink P., Rizzu P., Mena M.A. // PLoS One. 2014. V. 9. № 9. P. e106931.
- Tanji K., Miki Y., Maruyama A., Mimura J., Matsumiya T., Mori F., Imaizumi T., Itoh K., Wakabayashi K. // Biochem. Biophys. Res. Commun. 2015. V. 465. № 4. P. 746–752.
- Chaudhary R.K., Kardani J., Singh K., Banerjee R., Roy I. // Neuromolecular Med. 2014. V. 16. № 2. P. 280–291.
- DeBosch B.J., Heitmeier M.R., Mayer A.L., Higgins C.B., Crowley J.R., Kraft T.E., Chi M., Newberry E.P., Chen Z., Finck B.N., Davidson N.O., Yarasheski K.E., Hruz P.W., Moley K.H. // Sci. Signal. 2016. V. 9. № 416. P. ra21.
- Mayer A.L., Higgins C.B., Heitmeier M.R., Kraft T.E., Qian X., Crowley J.R, Hyrc K.L., Beatty W.L., Yarasheski K.E., Hruz P.W., DeBosch B.J. // Sci. Rep. 2016. V. 6. P. 38586.
- Mardones P., Rubinsztein D.C., Hetz C. // Sci. Signal. 2016. V. 9. № 416. P. fs2.
- Egan D., Kim J., Shaw R.J., Guan K.L. // Autophagy. 2011. V. 7. № 6. P. 643–644.
- Roach P.J. // Mol. Cell. Biol. 2011. V. 31. № 15. P. 3082–3084.
- Narita H., Tanji K., Miki Y., Mori F., Wakabayashi K. // Biochem. Biophys. Res. Commun. 2019. V. 514. № 3. P. 672–677.
- Benito-Cuesta I., Ordonez-Gutierrez L., Wandosell F. // Metabolites. 2021. V. 11. № 7. P. 421.
- Chen M., Huang N., Liu J., Huang J., Shi J., Jin F. // Behav. Brain Res. 2021. V. 400. P. 113043.
- Huang J., Wang X., Zhu Y., Li Z., Zhu Y.T., Wu J.C., Qin Z.H., Xiang M., Lin F. // Neurosci. Ther. 2019. V. 25. № 6. P. 796–807.
- Djajadikerta A., Keshri S., Pavel M., Prestil R., Ryan L., Rubinsztein D.C. // J. Mol. Biol. 2020. V. 432. № 8. P. 2799–2821.
- Chen X., Li M., Li L., Xu S., Huang D., Ju M., Huang J., Chen K., Gu H. // Sci. Rep. 2016. V. 6. P. 28423.
- Jang M., Park R., Kim H., Namkoong S., Jo D., Huh Y.H., Jang I.S., Lee J.I., Park J. // Sci. Rep. 2018. V. 8. № 1. P. 12637.
- Xu C., Chen X., Sheng W.B., Yang P. // Reprod. Toxicol. 2019. V. 85. P. 51–58.
- Kara N.Z., Toker L., Agam G., Anderson G.W., Belmaker R.H., Einat H. // Psychopharmacology. 2013. V. 229. № 2. P. 367–375.
- Sciarretta S., Yee D., Nagarajan N., Bianchi F., Saito T., Valenti V., Tong M., Del Re D.P., Vecchione C., Schirone L., Forte M., Rubattu S., Shirakabe A., Boppana V.S., Volpe M., Frati G., Zhai P., Sadoshima J. // J. Am. Coll. Cardiol. 2018. V. 71. № 18. P. 1999–2010.
- Wang Q., Ren J. // Pharmacol. Res. 2016. V. 111. P. 357–373.
- Casarejos M.J., Solano R.M., Gomez A., Perucho J., de Yebenes J.G., Mena M.A. // Neurochem. Int. 2011. V. 58. № 4. P. 512–520.
- Castillo K., Nassif M., Valenzuela V., Rojas F., Matus S., Mercado G., Court F.A., van Zundert B., Hetz C. // Autophagy. 2013. V. 9. № 9. P. 1308–1320.
- Abokyi S., Shan S.W., To C.H., Chan H.H., Tse D.Y. // Oxid. Med. Cell. Longev. 2020. V. 2020. P. 5296341.
- Lamark T., Svenning S., Johansen T. // Essays Biochem. 2017. V. 61. № 6. P. 609–624.
- Yoon Y.S., Cho E.D., Jung Ahn W., Won Lee K., Lee S.J., Lee H.J. // Cell Death Dis. 2017. V. 8. № 10. P. e3091.
- Tien N.T., Karaca I., Tamboli I.Y., Walter J. // J. Biol. Chem. 2016. V. 291. № 20. P. 10528–10540.
- Lan D.M., Liu F.T., Zhao J., Chen Y., Wu J.J., Ding Z.T., Yue Z.Y., Ren H.M., Jiang Y. P., Wang J. // Neurochem. Res. 2012. V. 37. № 9. P. 2025–2032.
- Redmann M., Wani W.Y., Volpicelli-Daley L., Darley-Usmar V., Zhang J. // Redox Biol. 2017. V. 11. P. 429–437.
- Mizunoe Y., Kobayashi M., Sudo Y., Watanabe S., Yasukawa H., Natori D., Hoshino A., Negishi A., Okita N., Komatsu M., Higami Y. // Redox Biol. 2018. V. 15. P. 115–124.
- Khalifeh M., Barreto G.E., Sahebkar A. // Br. J. Pharmacol. 2019. V. 176. № 9. P. 1173–1189.
- Pierzynowska K., Gaffke L., Cyske Z., Puchalski M., Rintz E., Bartkowski M., Osiadly M., Pierzynowski M., Mantej J., Piotrowska E., Wegrzyn G. // Metab. Brain Dis. 2018. V. 33. № 4. P. 989–1008.
- Tamargo-Gomez I., Marino G. // Int. J. Mol. Sci. 2018. V. 19. № 12. P. 3812
- Di Nardo A., Wertz M.H., Kwiatkowski E., Tsai P.T., Leech J.D., Greene-Colozzi E., Goto J., Dilsiz P., Talos D.M., Clish C.B., Kwiatkowski D.J., Sahin M. // Hum. Mol. Genet. 2014. V. 23. № 14. P. 3865–3874.
- Zimmerman M.A., Biggers C.D., Li P.A. // BMC Neurosci. 2018. V. 19. № 1. P. 82.
- Sarkar S. // Biochem. Soc. Trans. 2013. V. 41. № 5. P. 1103–1130.
- Casarejos M.J., Perucho J., Gomez A., Munoz M.P., Fernandez-Estevez M., Sagredo O., Fernandez Ruiz J., Guzman M., de Yebenes J.G., Mena M.A. // J. Alzheimers Dis. 2013. V. 35. № 3. P. 525–539.
- Rodriguez-Navarro J.A., Rodriguez L., Casarejos M.J., Solano R.M., Gomez A., Perucho J., Cuervo A.M., Garcia de Yebenes J., Mena M.A. // Neurobiol. Dis. 2010. V. 39. № 3. P. 423–438.
- Schaeffer V., Lavenir I., Ozcelik S., Tolnay M., Winkler D.T., Goedert M. // Brain. 2012. V. 135. Pt. 7. P. 2169–2177.
- Wu F., Xu H.D., Guan J.J., Hou Y.S., Gu J.H., Zhen X.C., Qin Z.H. // Neuroscience. 2015. V. 284. P. 900–911.
- Jing M.J., Liu K., Liu C., Yan D.Y., Ma Z., Wang C., Deng Y., Liu W., Xu B. // Environ. Toxicol. 2020. V. 35. № 1. P. 55–65.
- Liu Y., Wang J., Hsiung G.R., Song W. // Mol. Neurobiol. 2020. V. 57. № 7. P. 3150–3157.
- Aguib Y., Heiseke A., Gilch S., Riemer C., Baier M., Schatzl H.M., Ertmer A. // Autophagy. 2009. V. 5. № 3. P. 361–369.
- Beranger F., Crozet C., Goldsborough A., Lehmann S. // Biochem. Biophys. Res. Commun. 2008. V. 374. № 1. P. 44–48.
- Settembre C., Di Malta C., Polito V.A., Garcia Arencibia M., Vetrini F., Erdin S., Erdin S.U., Huynh T., Medina D., Colella P., Sardiello M., Rubinsztein D.C., Ballabio A. // Science. 2011. V. 332. № 6036. P. 1429–1433.
- Rusmini P., Cortese K., Crippa V., Cristofani R., Cicardi M.E., Ferrari V., Vezzoli G., Tedesco B., Meroni M., Messi E., Piccolella M., Galbiati M., Garre M., Morelli E., Vaccari T., Poletti A. // Auto-phagy. 2019. V. 15. № 4. P. 631–651.
- Palmieri M., Pal R., Nelvagal H.R., Lotfi P., Stinnett G.R., Seymour M.L., Chaudhury A., Bajaj L., Bondar V.V., Bremner L., Saleem U., Tse D.Y., Sanagasetti D., Wu S.M., Neilson J.R., Pereira F.A., Pautler R.G., Rodney G.G., Cooper J.D., Sardiello M. // Nat. Commun. 2017. V. 8. P. 14338.
- Cortes C.J., La Spada A.R. // Neurobiol. Dis. 2019. V. 122. P. 83–93.
- Gu Z., Cao H., Zuo C., Huang Y., Miao J., Song Y., Yang Y., Zhu L., Wang F. // Neurobiol. Dis. 2022. V. 173. P. 105855.
- Lu J., Wu M., Yue Z. // Adv. Exp. Med. Biol. 2020. V. 1207. P. 21–51.
- Di Malta C., Cinque L., Settembre C. // Front. Cell. Dev. Biol. 2019. V. 7. P. 114.
- Benaroudj N., Lee D.H., Goldberg A.L. // J. Biol. Chem. 2001. V. 276. № 26. P. 24261–24267.
- Beranger F., Crozet C., Goldsborough A., Lehmann S. // Biochem. Biophys. Res. Commun. 2008. V. 374. № 1. P. 44–48.
- Gao Z., Wang H., Zhang B., Wu X., Zhang Y., Ge P., Chi G., Liang J. // Int. J. Med. Sci. 2018. V. 15. № 10. P. 1014–1024.
- Darabi S., Noori-Zadeh A., Abbaszadeh H.A., Rajaei F., Bakhtiyari S. // Iran. J. Pharm. Res. 2019. V. 18. № 3. P. 1419–1428.
- Tang Q., Zheng G., Feng Z., Chen Y., Lou Y., Wang C., Zhang X., Zhang Y., Xu H., Shang P., Liu H. // Cell. Death Dis. 2017. V. 8. № 10. P. e3081.
- Liu K., Jing M.J., Liu C., Yan D.Y., Ma Z., Wang C., Deng Y., Liu W., Xu B. // Basic Clin. Pharmacol. Toxicol. 2019. V. 25. № 6. P. 536–547.
- Minutoli L., Altavilla D., Bitto A., Polito F., Bellocco E., Lagana G., Fiumara T., Magazu S., Migliardo F., Venuti F.S., Squadrito F. // Eur. J. Pharmacol. 2008. V. 589. № 1–3. P. 272–280.
- Echigo R., Shimohata N., Karatsu K., Yano F., Kayasuga-Kariya Y., Fujisawa A., Ohto T., Kita Y., Nakamura M., Suzuki S., Mochizuki M., Shimizu T., Chung U.I., Sasaki N. // J. Transl. Med. 2012. V. 10. P. 80.
- He Q., Wang Y., Lin W., Zhang Q., Zhao J., Liu F.T., Tang Y.L., Xiao B.G., Wang J. // Neurotox. Res. 2014. V. 26. № 4. P. 430–439.
- Bussi C., Peralta Ramos J.M., Arroyo D.S., Gaviglio E.A., Gallea J.I., Wang J.M., Celej M.S., Iribarren P. // Sci. Rep. 2017. V. 7. P. 43153.
- Nakahira K., Haspel J.A., Rathinam V.A., Lee S.J., Dolinay T., Lam H.C., Englert J.A., Rabinovitch M., Cernadas M., Kim H.P., Fitzgerald K.A., Ryter S.W., Choi A.M. // Nat. Immunol. 2011. V. 12. № 3. P. 222–230.
- Li Y., Luo Y., Luo T., Lu B., Wang C., Zhang Y., Piao M., Feng C., Ge P. // Mol. Neurobiol. 2017. V. 54. № 9. P. 6857–6869.
- Uddin M.S., Mamun A.A., Labu Z.K., Hidalgo-Lanussa O., Barreto G.E., Ashraf G.M. // J. Cell Physiol. 2019. V. 234. № 6. P. 8094–8112.
- Lee J.H., Cheon Y.H., Woo R.S., Song D.Y., Moon C., Baik T.K. // Anat. Cell Biol. 2012. V. 45. № 1. P. 26–37.
- Khan S.H., Kumar R. // Pathol. Res. Pract. 2017. V. 213. № 6. P. 643–648.
- Tien N.T., Karaca I., Tamboli I.Y., Walter J. // J. Biol. Chem. 2016. V. 291. № 20. P. 10528–10540.
- Kruger U., Wang Y., Kumar S., Mandelkow E.M. // Neurobiol. Aging. 2012. V. 33. № 10. P. 2291–2305.
- Schaeffer V., Lavenir I., Ozcelik S., Tolnay M., Winkler D.T., Goedert M. // Brain. 2012. V. 135. Pt. 7. P. 2169–2177.
- Ittner L.M., Ke Y.D., Delerue F., Bi M., Gladbach A., van Eersel J., Wolfing H., Chieng B.C., Christie M.J., Napier I.A., Eckert A., Staufenbiel M., Hardeman E., Gotz J. // Cell. 2010. V. 142. № 3. P. 387–397.
- Perucho J., Casarejos M.J., Gomez A., Solano R.M., de Yebenes J.G., Mena M.A. // Curr. Alzheimer Res. 2012. V. 9. № 3. P. 334–343.
- Lee Y.S., Lai D.M., Huang H.J., Lee-Chen G.J., Chang C.H., Hsieh-Li H.M., Lee G.C. // J. Agric. Food Chem. 2021. V. 69. № 8. P. 2422–2437.
- Pupyshev A.B., Belichenko V.M., Tenditnik M.V., Bashirzade A.A., Dubrovina N.I., Ovsyukova M.V., Akopyan A.A., Fedoseeva L.A., Korolenko T.A., Amstislavskaya T.G., Tikhonova M.A. // Pharmacol. Biochem. Behav. 2022. V. 217. P. 173406.
- Portbury S.D., Hare D.J., Sgambelloni C., Perronnes K., Portbury A.J., Finkelstein D.I., Adlard P.A. // J. Alzheimers Dis. 2017. V. 60. № 2. P. 549–560.
- Du J., Liang Y., Xu F., Sun B., Wang Z. // J. Pharm. Pharmacol. 2013. V. 65. № 12. P. 1753–1756.
- Raza C., Anjum R., Shakeel N.U.A. // Life Sci. 2019. V. 226. P. 77–90.
- Glass C.K., Saijo K., Winner B., Marchetto M.C., Gage F.H. // Cell. 2010. V. 140. № 6. P. 918–934.
- Lan D.M., Liu F.T., Zhao J., Chen Y., Wu J.J., Ding Z.T., Yue Z.Y., Ren H.M., Jiang Y.P., Wang J. // Neurochem. Res. 2012. V. 37. P. 2025–2032.
- Zhao J., Zhi X., Pan L., Zhou P. // Molecules. 2017. V. 22. № 8. P. pii: E1293.
- Pupyshev A.B., Tikhonova M.A., Akopyan A.A., Tenditnik M.V., Dubrovina N.I., Korolenko T.A. // Pharmacol. Biochem. Behav. 2019. V. 177. P. 1–11.
- Darabi S., Noori-Zadeh A., Abbaszadeh H.A., Rajaei F., Bakhtiyari S. // Iran. J. Pharm. Res. 2019. V. 18. № 3. P. 1419–1428.
- Lin C.H., Wei P.C., Chen C.M., Huang Y.T., Lin J.L., Lo Y.S., Lin J.L., Lin C.Y., Wu Y.R., Chang K.H., Lee-Chen G.J. // Front. Aging Neurosci. 2020. V. 12. P. 226.
- Wu F., Xu H.D., Guan J.J., Hou Y.S., Gu J.H., Zhen X.C., Qin Z.H. // Neuroscience. 2015. V. 284. P. 900–911.
- He Q., Koprich J.B., Wang Y., Yu W.B., Xiao B.G., Brotchie J.M., Wang J. // Mol. Neurobiol. 2016. V. 53. № 4. P. 2258–2268.
- Moors T.E., Hoozemans J.J., Ingrassia A., Beccari T., Parnetti L., Chartier-Harlin M.C., van de Berg W.D. // Mol. Neurodegener. 2017. V. 12. № 1. P. 11.
- Perucho J., Gomez A., Munoz M.P., de Yebenes J.G., Mena M.A., Casarejos M.J. // Mol. Cell. Neurosci. 2016. V. 74. P. 128–145.
- Yamashita S. // J. Clin. Med. 2021. V. 10. № 7. P. 1375.
- Davies J.E., Berger Z., Rubinsztein D.C. // J. Biochem. Cell Biol. 2006. V. 38. № 9. P. 1457–1462.
- Davies J.E., Sarkar S., Rubinsztein D.C. // Hum. Mol. Genet. 2006. V. 15. № 1. P. 23–31.
- Argov Z., Vornovitsky H., Blumen S., Caraco Y. // Neurology. 2015. V. 84 (Suppl 14). P. 7.068.
- Argov Z., Gliko-Kabir I., Brais B., Caraco Y., Megiddo D. // Neurology. 2016. V. 86 (Suppl 16). P. S28.004.
- Gomes C., Escrevente C., Costa J. // Neurosci. Lett. 2010. V. 475. № 3. P. 145–149.
- Li Y., Guo Y., Wang X., Yu X., Duan W., Hong K., Wang J., Han H., Li C. // Neuroscience. 2015. V. 298. P. 12–25.
- Zhang X., Chen S., Song L., Tang Y., Shen Y., Jia L., Le W. // Autophagy. 2014. V. 10. № 4. P. 588–602.
- Sahoo A.K., Dandapat J., Dash U.C., Kanhar S. // J. Ethnopharmacol. 2018. V. 215. P. 42–73.
- Halbe L., Rami A. // Curr. Neurovasc. Res. 2019. V. 16. № 1. P. 3–11.
- Schmeisser K., Parker J.A. // Front. Cell. Dev. Biol. 2019. V. 7. P. 192.
- Cejka C., Kubinova S., Cejkova J. // Histol. Histopathol. 2019. V. 34. № 6. P. 611–618.
- Kaplon R.E., Hill S.D., Bispham N.Z., Santos-Parker J.R., Nowlan M.J., Snyder L.L., Chonchol M., LaRocca T.J., McQueen M.B., Seals D.R. // Aging. 2016. V. 8. № 6. P. 1167–1183.
- Noorasyikin M.A., Azizan E.A., Teh P.C., Farah Waheeda T., Siti Hajar M.D., Long K.C., Norlinah M.I. // Park. Relat. Disord. 2020. V. 70. P. 42–44.
- Yap K.H., Azmin S., Makpol S., Damanhuri H.A., Mustapha M., Hamzah J.C., Ibrahim N.M. // Neural Regen. Res. 2023. V. 18. № 6. P. 1179–1185.
- Assoni G., Frapporti G., Colombo E., Gornati D., Perez-Carrion M.D., Polito L., Seneci P., Piccoli G., Arosio D. // Bioorg. Med. Chem. Lett. 2021. V. 40. P. 127929.
- Frapporti G., Colombo E., Ahmed H., Assoni G., Polito L., Randazzo P., Arosio D., Seneci P., Piccoli G. // Pharmaceutics. 2022. V. 14. № 4. P. 862.
- Zhang Y., Shaikh N., Ferey J.L., Wankhade U.D., Chintapalli S.V., Higgins C.B. Crowley J.R., Heitmeier M.R., Stothard A.I., Mihi B., Good M., Higashiyama T., Swarts B.M., Hruz P.W., Shankar K., Tarr P.I., DeBosch B.J. // Gastroenterology. 2020. V. 158. № 5. P. 1402–1416.
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