Escherichia coli triggers α-synuclein pathology in the LRRK2 transgenic mouse model of PD

References

• Kalia LV, Lang AE. Parkinson’s disease. The Lancet. 2015;386(9996):896–23. doi:10.1016/S0140-6736(14)61393-3.
   PubMed Web of Science ®Google Scholar
• Braak H, Del Tredici K, Rüb U, de Vos RAI, Jansen Steur ENH, Braak E. Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging. 2003;24(2):197–211. doi:10.1016/S0197-4580(02)00065-9.
   PubMed Web of Science ®Google Scholar
• Ahn EH, Kang SS, Liu X, Chen G, Zhang Z, Chandrasekharan B, Alam AM, Neish AS, Cao X, Ye K, et al. Initiation of Parkinson’s disease from gut to brain by δ-secretase. Cell Res. 2020;30(1):70–87. doi:10.1038/s41422-019-0241-9.
   PubMed Web of Science ®Google Scholar
• Dickson DW, Braak H, Duda JE, Duyckaerts C, Gasser T, Halliday GM, Hardy J, Leverenz JB, Del Tredici K, Wszolek ZK, et al. Neuropathological assessment of Parkinson’s disease: refining the diagnostic criteria. Lancet Neurol. 2009;8(12):1150–1157. doi:10.1016/S1474-4422(09)70238-8.
   PubMed Web of Science ®Google Scholar
• Breen DP, Halliday GM, Lang AE. Gut–brain axis and the spread of α-synuclein pathology: vagal highway or dead end? Mov Disord. 2019;34(3):307–316. doi:10.1002/mds.27556.
   PubMed Web of Science ®Google Scholar
• Horsager J, Andersen KB, Knudsen K, Skjærbæk C, Fedorova TD, Okkels N, Schaeffer E, Bonkat SK, Geday J, Otto M, et al. Brain-first versus body-first Parkinson’s disease: a multimodal imaging case-control study. Brain. 2020;143(10):3077–3088. doi:10.1093/brain/awaa238.
   PubMed Web of Science ®Google Scholar
• Kim S, Kwon S-H, Kam T-I, Panicker N, Karuppagounder SS, Lee S, Lee JH, Kim WR, Kook M, Foss CA, et al. Transneuronal propagation of pathologic α-synuclein from the gut to the brain models Parkinson’s disease. Neuron. 2019;103:627–641.e7. doi:10.1016/j.neuron.2019.05.035.
   PubMed Web of Science ®Google Scholar
• Hilton D, Stephens M, Kirk L, Edwards P, Potter R, Zajicek J, Broughton E, Hagan H, Carroll C. Accumulation of α-synuclein in the bowel of patients in the pre-clinical phase of Parkinson’s disease. Acta Neuropathol. 2014;127(2):235–241. doi:10.1007/s00401-013-1214-6.
   PubMed Web of Science ®Google Scholar
• Ross OA, Soto-Ortolaza AI, Heckman MG, Aasly JO, Abahuni N, Annesi G, Bacon JA, Bardien S, Bozi M, Brice A, et al. Association of LRRK2 exonic variants with susceptibility to Parkinson’s disease: a case–control study. Lancet Neurol. 2011;10(10):898–908. doi:10.1016/S1474-4422(11)70175-2.
   PubMed Web of Science ®Google Scholar
• de Guilhem de Lataillade A, Verchere J, Oullier T, Prigent A, Durand T, Pellegrini C, Neunlist M, Baron T, Rolli-Derkinderen M, Derkinderen P. LRRK2 is reduced in Parkinson’s disease gut. Acta Neuropathol. 2021;142(3):601–603. doi:10.1007/s00401-021-02334-y.
   PubMed Web of Science ®Google Scholar
• Liang D, Shu L, Pan H, Xu Q, Guo J, Yan X, Tang B, Sun Q. Clinical characteristics of PD patients with LRRK2 G2385R and R1628P variants. Neurosci Lett. 2018;685:185–189. doi:10.1016/j.neulet.2018.08.015.
   PubMed Web of Science ®Google Scholar
• Hou Y, Luo C, Yang J, Ou R, Song W, Chen Y, Gong Q, Shang H. Altered intrinsic brain functional connectivity in drug-naïve Parkinson’s disease patients with LRRK2 mutations. Neurosci Lett. 2018;675:145–151. doi:10.1016/j.neulet.2018.03.038.
   PubMed Web of Science ®Google Scholar
• Fu X, Zheng Y, Hong H, He Y, Zhou S, Guo C, Liu Y, Xian W, Zeng J, Li J, et al. LRRK2 G2385R and LRRK2 R1628P increase risk of Parkinson’s disease in a Han Chinese population from Southern Mainland China. Parkinsonism Relat Disord. 2013;19(3):397–398. doi:10.1016/j.parkreldis.2012.08.007.
   PubMed Web of Science ®Google Scholar
• Wang C, Cai Y, Zheng Z, Tang B-S, Xu Y, Wang T, Ma J, Chen S-D, Langston JW, Tanner CM, et al. Penetrance of LRRK2 G2385R and R1628P is modified by common PD-associated genetic variants. Parkinsonism Relat Disord. 2012;18(8):958–963. doi:10.1016/j.parkreldis.2012.05.003.
   PubMed Web of Science ®Google Scholar
• Witoelar A, Jansen IE, Wang Y, Desikan RS, Gibbs JR, Blauwendraat C, Thompson WK, Hernandez DG, Djurovic S, Schork AJ, et al. Genome-wide Pleiotropy Between Parkinson Disease and Autoimmune Diseases. JAMA Neurol. 2017;74(7):780–792. doi:10.1001/jamaneurol.2017.0469.
   PubMed Web of Science ®Google Scholar
• Liu Z, Lenardo MJ. The role of LRRK2 in inflammatory bowel disease. Cell Res. 2012;22(7):1092–1094. doi:10.1038/cr.2012.42.
   PubMed Web of Science ®Google Scholar
• Hui KY, Fernandez-Hernandez H, Hu J, Schaffner A, Pankratz N, Hsu N-Y, Chuang L-S, Carmi S, Villaverde N, Li X, et al. Functional variants in the LRRK2 gene confer shared effects on risk for Crohn’s disease and Parkinson’s disease. Sci Transl Med. 2018;10(423):10. doi:10.1126/scitranslmed.aai7795.
   Web of Science ®Google Scholar
• Lee H-S, Lobbestael E, Vermeire S, Sabino J, Cleynen I. Inflammatory bowel disease and Parkinson’s disease: common pathophysiological links. Gut. 2021;70:408–417. doi:10.1136/gutjnl-2020-322429.
   PubMed Web of Science ®Google Scholar
• Zhang JR, Jin H, Li K, Mao CJ, Yang YP, Wang F, Gu, CC, Zhang, HJ, Chen, J, Liu, CF. Genetic analysis of LRRK2 in Parkinson’s disease in han Chinese population. Neurobiol Aging. 2018;72:187 e5–e10 . doi:10.1016/j.neurobiolaging.2018.06.036.
   PubMed Web of Science ®Google Scholar
• Teichman EM, O’Riordan KJ, Gahan CGM, Dinan TG, Cryan JF. When rhythms meet the blues: circadian interactions with the microbiota-gut-brain axis. Cell Metab. 2020;31(3):448–471. doi:10.1016/j.cmet.2020.02.008.
   PubMed Web of Science ®Google Scholar
• Bedarf JR, Hildebrand F, Coelho LP, Sunagawa S, Bahram M, Goeser F, Bork P, Wüllner U. Functional implications of microbial and viral gut metagenome changes in early stage L-DOPA-naïve Parkinson’s disease patients. Genome Med. 2017;9(1):39. doi:10.1186/s13073-017-0428-y.
   PubMedGoogle Scholar
• Sampson TR, Debelius JW, Thron T, Janssen S, Shastri GG, Ilhan ZE, Challis C, Schretter CE, Rocha S, Gradinaru V, et al. Gut Microbiota Regulate Motor Deficits and Neuroinflammation in a Model of Parkinson’s Disease. Cell. 2016;167(6):1469–1480.e12. doi:10.1016/j.cell.2016.11.018.
   PubMed Web of Science ®Google Scholar
• Cirstea MS, Yu AC, Golz E, Sundvick K, Kliger D, Radisavljevic N, Foulger LH, Mackenzie M, Huan T, Finlay BB, et al. Microbiota composition and metabolism are associated with gut function in Parkinson’s disease. Mov Disord. 2020;35(7):1208–1217. doi:10.1002/mds.28052.
   PubMed Web of Science ®Google Scholar
• Munoz-Pinto MF, Empadinhas N, Cardoso SM. The neuromicrobiology of Parkinson’s disease: a unifying theory. Ageing Res Rev. 2021;70:101396. doi:10.1016/j.arr.2021.101396.
   PubMed Web of Science ®Google Scholar
• Boer CG, Radjabzadeh D, Medina-Gomez C, Garmaeva S, Schiphof D, Arp P, Koet T, Kurilshikov A, Fu J, Ikram MA, et al. Intestinal microbiome composition and its relation to joint pain and inflammation. Nat Commun. 2019;10(1):4881. doi:10.1038/s41467-019-12873-4.
   PubMedGoogle Scholar
• Quince C, Walker AW, Simpson JT, Loman NJ, Segata N. Shotgun metagenomics, from sampling to analysis. Nat Biotechnol. 2017;35(9):833–844. doi:10.1038/nbt.3935.
   PubMed Web of Science ®Google Scholar
• Parodi S, Verda D, Bagnasco F, Muselli M. The clinical meaning of the area under a receiver operating characteristic curve for the evaluation of the performance of disease markers. Epidemiol Health. 2022;44:e2022088. doi:10.4178/epih.e2022088.
   PubMed Web of Science ®Google Scholar
• Sampson TR, Challis C, Jain N, Moiseyenko A, Ladinsky MS, Shastri GG, Thron T, Needham BD, Horvath I, Debelius JW, et al. A gut bacterial amyloid promotes α-synuclein aggregation and motor impairment in mice. Elife. 2020;9:e53111. doi:10.7554/eLife.53111.
   PubMed Web of Science ®Google Scholar
• Chapman MR, Robinson LS, Pinkner JS, Roth R, Heuser J, Hammar M, Normark S, Hultgren SJ. Role of Escherichia coli curli operons in directing amyloid fiber formation. Sci. 2002;295(5556):851–855. doi:10.1126/science.1067484.
   PubMed Web of Science ®Google Scholar
• Prasad K, Richfield EK. Number and nuclear morphology of TH+ and TH− neurons in the mouse ventral midbrain using epifluorescence stereology. Exp Neurol. 2010;225(2):328–340. doi:10.1016/j.expneurol.2010.07.004.
   PubMed Web of Science ®Google Scholar
• Wirtz S, Neufert C, Weigmann B, Neurath MF. Chemically induced mouse models of intestinal inflammation. Nat Protoc. 2007;2(3):541–546. doi:10.1038/nprot.2007.41.
   PubMed Web of Science ®Google Scholar
• Hernández-Chirlaque C, Aranda CJ, Ocón B, Capitán-Cañadas F, Ortega-González M, Carrero JJ, Suárez MD, Zarzuelo A, Sánchez de Medina F, Martínez-Augustin O, et al. Germ-free and antibiotic-treated mice are highly susceptible to epithelial injury in DSS colitis. J Crohns Colitis. 2016;10(11):1324–1335. doi:10.1093/ecco-jcc/jjw096.
   PubMed Web of Science ®Google Scholar
• Chen SG, Stribinskis V, Rane MJ, Demuth DR, Gozal E, Roberts AM, Jagadapillai R, Liu R, Choe K, Shivakumar B, et al. Exposure to the functional bacterial amyloid protein curli enhances alpha-synuclein aggregation in aged Fischer 344 rats and Caenorhabditis elegans. Sci Rep. 2016;6(1):34477. doi:10.1038/srep34477.
   PubMedGoogle Scholar
• Park K-S, Choi K-H, Kim Y-S, Hong BS, Kim OY, Kim JH, Yoon CM, Koh G-Y, Kim Y-K, Gho YS, et al. Outer membrane vesicles derived from Escherichia coli induce systemic inflammatory response syndrome. PloS One. 2010;5(6):e11334. doi:10.1371/journal.pone.0011334.
   PubMed Web of Science ®Google Scholar
• Hong J, Dauros-Singorenko P, Whitcombe A, Payne L, Blenkiron C, Phillips A, Swift S. Analysis of the Escherichia coli extracellular vesicle proteome identifies markers of purity and culture conditions. J Extracell Vesicles. 2019;8(1):1632099. doi:10.1080/20013078.2019.1632099.
   PubMed Web of Science ®Google Scholar
• Shin WH, Chung KC. Death-associated protein kinase 1 phosphorylates α-synuclein at Ser129 and exacerbates rotenone-induced toxic aggregation of α-synuclein in dopaminergic SH-SY5Y cells. Exp Neurobiol. 2020;29(3):207–218. doi:10.5607/en20014.
   PubMed Web of Science ®Google Scholar
• Wang S-L, Shao B-Z, Zhao S-B, Chang X, Wang P, Miao C-Y, Li Z-S, Bai Y. Intestinal autophagy links psychosocial stress with gut microbiota to promote inflammatory bowel disease. Cell Death Disease. 2019;10(6):391. doi:10.1038/s41419-019-1634-x.
   PubMedGoogle Scholar
• Winham SJ, Biernacka JM. Gene–environment interactions in genome-wide association studies: current approaches and new directions. J Child Psychol Psychiatry. 2013;54(10):1120–1134. doi:10.1111/jcpp.12114.
   PubMed Web of Science ®Google Scholar
• Vázquez-Vélez GE, Zoghbi HY. Parkinson’s disease genetics and pathophysiology. Annu Rev Neurosci. 2021;44(1):87–108. doi:10.1146/annurev-neuro-100720-034518.
   PubMedGoogle Scholar
• Ascherio A, Schwarzschild MA. The epidemiology of Parkinson’s disease: risk factors and prevention. Lancet Neurol. 2016;15(12):1257–1272. doi:10.1016/S1474-4422(16)30230-7.
   PubMed Web of Science ®Google Scholar
• Wiley J, Lynch T, Lincoln S, Skipper L, Hulihan M, Gosal D, Bisceglio G, Kachergus J, Hardy J, Farrer MJ, et al. Parkinson’s disease in Ireland: clinical presentation and genetic heterogeneity in patients with parkin mutations. Mov Disord. 2004;19(6):677–681. doi:10.1002/mds.10703.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Sun Q, Yi M, Zhou X, Guo J, Xu Q, Tang B, Yan X. Genetic analysis of LRRK2 R1628P in Parkinson’s disease in Asian populations. Parkinsons Dis. 2017;2017:1–6. doi:10.1155/2017/8093124.
   Web of Science ®Google Scholar
• Joossens M, Huys G, Cnockaert M, De Preter V, Verbeke K, Rutgeerts P, et al. Dysbiosis of the faecal microbiota in patients with Crohn’s disease and their unaffected relatives. Gut. 2011;60:631–637. doi:10.1136/gut.2010.223263.
   PubMed Web of Science ®Google Scholar
• Imhann F, Vich Vila A, Bonder MJ, Fu J, Gevers D, Visschedijk MC, Spekhorst LM, Alberts R, Franke L, van Dullemen HM, et al. Interplay of host genetics and gut microbiota underlying the onset and clinical presentation of inflammatory bowel disease. Gut. 2018;67(1):108–119. doi:10.1136/gutjnl-2016-312135.
   PubMed Web of Science ®Google Scholar
• Weindel CG, Bell SL, Vail KJ, West KO, Patrick KL, Watson RO. LRRK2 maintains mitochondrial homeostasis and regulates innate immune responses to Mycobacterium tuberculosis. Elife. 2020;9:e51071. doi:10.7554/eLife.51071.
   PubMed Web of Science ®Google Scholar
• Russo I, Bubacco L, Greggio E. LRRK2 and neuroinflammation: partners in crime in Parkinson’s disease? J Neuroinflammation. 2014;11(1):52. doi:10.1186/1742-2094-11-52.
   PubMedGoogle Scholar
• Barbara G, Barbaro MR, Fuschi D, Palombo M, Falangone F, Cremon C, Marasco G, Stanghellini V. Inflammatory and microbiota-related regulation of the intestinal epithelial barrier. Front Nutr. 2021;8:718356. doi:10.3389/fnut.2021.718356.
   PubMed Web of Science ®Google Scholar
• Kim S, Kwon SH, Kam TI, Panicker N, Karuppagounder SS, Lee S, Lee JH, Kim WR, Kook M, Foss CA, et al. Transneuronal propagation of pathologic α-synuclein from the gut to the brain models Parkinson’s disease. Neuron. 2019;103(4):627–641.e7. doi:10.1016/j.neuron.2019.05.035.
   PubMed Web of Science ®Google Scholar
• Wang XJ, Ma MM, Zhou LB, Jiang XY, Hao MM, Teng RKF, Wu E, Tang B-S, Li J-Y, Teng J-F, et al. Autonomic ganglionic injection of α-synuclein fibrils as a model of pure autonomic failure α-synucleinopathy. Nat Commun. 2020;11(1):934. doi:10.1038/s41467-019-14189-9.
   PubMed Web of Science ®Google Scholar
• Silberger DJ, Zindl CL, Weaver CT. Citrobacter rodentium: a model enteropathogen for understanding the interplay of innate and adaptive components of type 3 immunity. Mucosal Immunol. 2017;10(5):1108–1117. doi:10.1038/mi.2017.47.
   PubMed Web of Science ®Google Scholar
• Gill S, Catchpole R, Forterre P. Extracellular membrane vesicles in the three domains of life and beyond. FEMS Microbiol Rev. 2019;43(3):273–303. doi:10.1093/femsre/fuy042.
   PubMed Web of Science ®Google Scholar
• Kalluri R, LeBleu VS. The biology, function, and biomedical applications of exosomes. Science. 2020;367(6478):eaau6977. doi:10.1126/science.aau6977.
   PubMed Web of Science ®Google Scholar
• Hammar M, Bian Z, Normark S. Nucleator-dependent intercellular assembly of adhesive curli organelles in Escherichia coli. Proc Natl Acad Sci U S A. 1996;93(13):6562–6566. doi:10.1073/pnas.93.13.6562.
   PubMed Web of Science ®Google Scholar
• Saldaña Z, Xicohtencatl-Cortes J, Avelino F, Phillips AD, Kaper JB, Puente JL, Girón JA. Synergistic role of curli and cellulose in cell adherence and biofilm formation of attaching and effacing Escherichia coli and identification of fis as a negative regulator of curli. Environ Microbiol. 2009;11(4):992–1006. doi:10.1111/j.1462-2920.2008.01824.x.
   PubMed Web of Science ®Google Scholar
• Wang J, Chen WD, Wang YD. The relationship between gut microbiota and inflammatory diseases: the role of macrophages. Front Microbiol. 2020;11:1065. doi:10.3389/fmicb.2020.01065.
   PubMed Web of Science ®Google Scholar
• Zuo T, Wong SH, Cheung CP, Lam K, Lui R, Cheung K, Zhang F, Tang W, Ching JYL, Wu JCY, et al. Gut fungal dysbiosis correlates with reduced efficacy of fecal microbiota transplantation in Clostridium difficile infection. Nat Commun. 2018;9(1):3663. doi:10.1038/s41467-018-06103-6.
   PubMedGoogle Scholar
• D’Haens GR, Jobin C. Fecal microbial transplantation for diseases beyond recurrent Clostridium difficile infection. Gastroenterology. 2019;157(3):624–636. doi:10.1053/j.gastro.2019.04.053.
   PubMed Web of Science ®Google Scholar
• Zhao Z, Ning J, Bao X-Q, Shang M, Ma J, Li G, Zhang D. Fecal microbiota transplantation protects rotenone-induced Parkinson’s disease mice via suppressing inflammation mediated by the lipopolysaccharide-TLR4 signaling pathway through the microbiota-gut-brain axis. Microbiome. 2021;9(1):226. doi:10.1186/s40168-021-01107-9.
   PubMed Web of Science ®Google Scholar
• Sun M-F, Zhu Y-L, Zhou Z-L, Jia X-B, Xu Y-D, Yang Q, Cui C, Shen Y-Q. Neuroprotective effects of fecal microbiota transplantation on MPTP-induced Parkinson’s disease mice: gut microbiota, glial reaction and TLR4/TNF-α signaling pathway. Brain Behav Immun. 2018;70:48–60. doi:10.1016/j.bbi.2018.02.005.
   PubMed Web of Science ®Google Scholar
• Kuai X-Y, Yao X-H, Xu L-J, Zhou Y-Q, Zhang L-P, Liu Y, Pei, SF, Zhou, CL. Evaluation of fecal microbiota transplantation in Parkinson’s disease patients with constipation. Microb Cell Fact. 2021;20(1):98. doi:10.1186/s12934-021-01589-0.
   PubMed Web of Science ®Google Scholar
• Li J, Jin M, Wang L, Qin B, Wang K. MDS clinical diagnostic criteria for Parkinson’s disease in China. J Neurol. 2017;264(3):476–481. doi:10.1007/s00415-016-8370-2.
   PubMed Web of Science ®Google Scholar
• Desai M, Seekatz A, Koropatkin N, Kamada N, Hickey C, Wolter M, Pudlo NA, Kitamoto S, Terrapon N, Muller A, et al. A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell. 2016;167(5):1339–53.e21. doi:10.1016/j.cell.2016.10.043.
   PubMed Web of Science ®Google Scholar
• Liu Y, Wang Y, Ni Y, Cheung C, Lam K, Wang Y, Xia Z, Ye D, Guo J, Tse MA, et al. Gut microbiome fermentation determines the efficacy of exercise for diabetes prevention. Cell Metab. 2020;31(1):77–91.e5. doi:10.1016/j.cmet.2019.11.001.
   PubMed Web of Science ®Google Scholar
• Matheoud D, Cannon T, Voisin A, Penttinen A-M, Ramet L, Fahmy AM, Ducrot C, Laplante A, Bourque M-J, Zhu L, et al. Intestinal infection triggers Parkinson’s disease-like symptoms in Pink1−/− mice. Nature. 2019;571(7766):565–569. doi:10.1038/s41586-019-1405-y.
   PubMed Web of Science ®Google Scholar
• Bárcena C, Valdés-Mas R, Mayoral P, Garabaya C, Durand S, Rodríguez F, Fernández-García MT, Salazar N, Nogacka AM, Garatachea N, et al. Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice. Nat Med. 2019;25(8):1234–1242. doi:10.1038/s41591-019-0504-5.
   PubMed Web of Science ®Google Scholar
• Liu H, Chen X, Hu X, Niu H, Tian R, Wang H, Pang H, Jiang L, Qiu B, Chen X, et al. Alterations in the gut microbiome and metabolism with coronary artery disease severity. Microbiome. 2019;7(1):68. doi:10.1186/s40168-019-0683-9.
   PubMed Web of Science ®Google Scholar
• Caporaso J, Kuczynski J, Stombaugh J, Bittinger K, Bushman F, Costello E, Fierer N, Peña AG, Goodrich JK, Gordon JI, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335–336. doi:10.1038/nmeth.f.303.
   PubMed Web of Science ®Google Scholar
• Chiu C, McArdle A, Brown R, Scott H, Gurd F. Intestinal mucosal lesion in low-flow states. I. A morphological, hemodynamic, and metabolic reappraisal. Arch Surg (Chicago, Ill: 1960). 1970;101(4):478–483. doi:10.1001/archsurg.1970.01340280030009.
   PubMedGoogle Scholar
• Gerber DJ, Sotnikova TD, Gainetdinov RR, Huang SY, Caron MG, Tonegawa S. Hyperactivity, elevated dopaminergic transmission, and response to amphetamine in M1 muscarinic acetylcholine receptor-deficient mice. Proc Natl Acad Sci USA. 2001;98(26):15312–15317. doi:10.1073/pnas.261583798.
   PubMed Web of Science ®Google Scholar
• Gao JX, Li Y, Wang SN, Chen XC, Lin LL, Zhang H. Overexpression of microRNA-183 promotes apoptosis of substantia nigra neurons via the inhibition of OSMR in a mouse model of Parkinson’s disease. Int J Mol Med. 2019;43:209–220. doi:10.3892/ijmm.2018.3982.
   PubMed Web of Science ®Google Scholar
• Xu D, Liu L, Zhao Y, Yang L, Cheng J, Hua R, Zhang Z, Li Q. Melatonin protects mouse testes from palmitic acid-induced lipotoxicity by attenuating oxidative stress and DNA damage in a SIRT1-dependent manner. J Pineal Res. 2020;69(4):e12690. doi:10.1111/jpi.12690.
   PubMed Web of Science ®Google Scholar