Piperine improves levodopa availability in the 6-OHDA-lesioned rat model of Parkinson's disease by suppressing gut bacterial tyrosine decarboxylase.

Enterococcus faecalis Parkinson's disease levodopa piperine tyrosine decarboxylase

Journal

CNS neuroscience & therapeutics
ISSN: 1755-5949
Titre abrégé: CNS Neurosci Ther
Pays: England
ID NLM: 101473265

Informations de publication

Date de publication:
01 Aug 2023
Historique:
revised: 11 07 2023
received: 27 01 2023
accepted: 17 07 2023
medline: 2 8 2023
pubmed: 2 8 2023
entrez: 2 8 2023
Statut: aheadofprint

Résumé

Tyrosine decarboxylase (TDC) presented in the gut-associated strain Enterococcus faecalis can convert levodopa (L-dopa) into dopamine (DA), and its increased abundance would potentially minimize the availability and efficacy of L-dopa. However, the known human decarboxylase inhibitors are ineffective in this bacteria-mediated conversion. This study aims to investigate the inhibition of piperine (PIP) on L-dopa bacterial metabolism and evaluates the synergistic effect of PIP combined with L-dopa on Parkinson's disease (PD). Metagenomics sequencing was adopted to determine the regulation of PIP on rat intestinal microbiota structure, especially on the relative abundance of E. faecalis. Then, the inhibitory effects of PIP on L-dopa conversion and TDC expression of E. faecalis were tested in vitro. We examined the synergetic effect of the combination of L-dopa and PIP on 6-hydroxydopamine (6-OHDA)-lesioned rats and tested the regulations of L-dopa bioavailability and brain DA level by pharmacokinetics study and MALDI-MS imaging. Finally, we evaluated the microbiota-dependent improvement effect of PIP on L-dopa availability using pseudo-germ-free and E. faecalis-transplanted rats. We found that PIP combined with L-dopa could better ameliorate the move disorders of 6-OHDA-lesioned rats by remarkably improving L-dopa availability and brain DA level than L-dopa alone, which was associated with the effect of PIP on suppressing the bacterial decarboxylation of L-dopa via effectively downregulating the abnormal high abundances of E. faecalis and TDC in 6-OHDA-lesioned rats. Oral administration of L-dopa combined with PIP can improve L-dopa availability and brain DA level in 6-OHDA-lesioned rats by suppressing intestinal bacterial TDC.

Identifiants

pubmed: 37528534
doi: 10.1111/cns.14383
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : National Natural Science Foundation of China
ID : 82173943
Organisme : National Natural Science Foundation of China
ID : 81473333

Informations de copyright

© 2023 The Authors. CNS Neuroscience & Therapeutics published by John Wiley & Sons Ltd.

Références

Post B, Merkus MP, de Haan RJ, Speelman JD, CARPA Study Group. Prognostic factors for the progression of Parkinson's disease: a systematic review. Mov Disord. 2007;22(13):1839-1851.
Hayes MT. Parkinson's disease and parkinsonism. Am J med. 2019;132(7):802-807.
Dorsey ER, Sherer T, Okun MS, Bloem BR. The emerging evidence of the Parkinson pandemic. J Parkinsons Dis. 2018;8(s1):S3-S8.
Shulman JM, de Jager PL, Feany MB. Parkinson's disease: genetics and pathogenesis. Annu Rev Pathol. 2011;6:193-222.
Obeso JA, Rodriguez-Oroz MC, Goetz CG, et al. Missing pieces in the Parkinson's disease puzzle. Nat med. 2010;16(6):653-661.
Hornykiewicz O. L-DOPA. J Parkinsons Dis. 2017;7(s1):S3-S10.
Hauser RA. Levodopa: past, present, and future. Eur Neurol. 2009;62(1):1-8.
Deleu D, Northway MG, Hanssens Y. Clinical pharmacokinetic and pharmacodynamic properties of drugs used in the treatment of Parkinson's disease. Clin Pharmacokinet. 2002;41(4):261-309.
Food and Drug Administration. [www.fda.gov/default.htm]. SINEMET® CR (carbidopa-levodopa) [EB/OL]. [Updated 2008 Dec 31; Cited 2021 Dec 12]. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2008/019856s025lbl.pdf
PD Med Collaborative Group, Gray R, Ives N, et al. Long-term effectiveness of dopamine agonists and monoamine oxidase B inhibitors compared with levodopa as initial treatment for Parkinson's disease (PD MED): a large, open-label, pragmatic randomised trial. Lancet. 2014;384(9949):1196-1205.
Whitfield AC, Moore BT, Daniels RN. Classics in chemical neuroscience: levodopa. ACS Chem Nerosci. 2014;5(12):1192-1197.
Holmes E, Kinross J, Gibson GR, et al. Therapeutic modulation of microbiota-host metabolic interactions. Sci Transl med. 2018;4(137):137rv6.
Koppel N, Maini Rekdal V, Balskus EP. Chemical transformation of xenobiotics by the human gut microbiota. Science. 2017;356(6344):1246-1257.
Maini Rekdal V, Bess EN, Bisanz JE, Turnbaugh PJ, Balskus EP. Discovery and inhibition of an interspecies gut bacterial pathway for levodopa metabolism. Science. 2019;364(6445):eaau6323.
van Kessel SP, Frye AK, El-Gendy AO, et al. Gut bacterial tyrosine decarboxylases restrict levels of levodopa in the treatment of Parkinson's disease. Nat Commun. 2019;10(1):310-321.
Xu R, Chen X, Wang X, et al. Development and validation of an ultra-high performance supercritical fluid chromatography-photodiode array detection-mass spectrometry method for the simultaneous determination of 12 compounds in Piper longum L. Food Chem. 2019;298:125067.
Zheng L, Wang H, Ba Y, et al. Protective effect of alkaloids from Piper longum in rat dopaminergic neuron injury of 6-OHDA-induced. China J Chin Mater med. 2014;39(9):1660-1665.
He H, Guo W, Xu R, et al. Alkaloids from Piper longum protect dopaminergic neurons against inflammation-mediated damage induced by intranigral injection of lipopolysaccharide. BMC Complement Altern Med. 2016;16(1):412-423.
Bi Y, Qu P, Wang Q, et al. Neuroprotective effects of alkaloids from Piper longum in a MPTP-induced mouse model of Parkinson's disease. Pharm Biol. 2015;53(10):1516-1524.
Huang L, Deng M, He Y, Fang Y. β-Asarone and levodopa co-administration protects against 6-hydroxydopamine-induced damage in parkinsonian rat mesencephalon by regulating autophagy: down-expression Beclin-1 and light chain 3B and up-expression P62. Clin Exp Pharmacol Physiol. 2015;42(3):269-277.
Piyachaturawat P, Glinsukon T, Toskulkao C. Acute and subacute toxicity of piperine in mice, rats and hamsters. Toxicol Lett. 1983;16(3-4):351-359.
Lee CS, Cenci MA, Schulzer M, Björklund A. Embryonic ventral mesencephalic grafts improve levodopa-induced dyskinesia in a rat model of Parkinson's disease. Brain. 2000;123(Pt 7):1365-1379.
Yang G, Zhang F, Deng L, et al. Development and validation of an LC-MS/MS method for simultaneous quantification of levodopa and MD01 in rat plasma and its application to a pharmacokinetic study of Mucuna pruriens extract. Biomed Chromatogr. 2016;30(9):1506-1514.
Wang Y, Tong Q, Ma S, et al. Oral berberine improves brain dopa/dopamine levels to ameliorate Parkinson's disease by regulating gut microbiota. Signal Transduct Target Ther. 2021;6(1):77.
Porter CC, Watson LS, Titus DC, Totaro JA, Byer SS. Inhibition of DOPA decarboxylase by the hydrazino analog of alpha-methylDOPA. Biochem Pharmacol. 1962;11:1067-1077.
Shah SHJ, Malik AH, Zhang B, Bao Y, Qazi J. Metagenomic analysis of relative abundance and diversity of bacterial microbiota in Bemisia tabaci infesting cotton crop in Pakistan. Infect Genet Evol. 2020;84:104381.
Bhowmik SK, An JH, Lee SH, Jung BH. Alteration of bile acid metabolism in pseudo germ-free rats. Arch Pharm Res. 2012;35(12):2219. Corrected and Republished from: Arch Pharm Res 2012;35(11):1969-1977.
Liu H, Luo R, Chen X, et al. Tissue distribution profiles of three antiparkinsonian alkaloids from Piper longum L. in rats determined by liquid chromatography-tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci. 2013;928:78-82.
Connil N, Le Breton Y, Dousset X, Auffray Y, Rincé A, Prévost H. Identification of the Enterococcus faecalis tyrosine decarboxylase operon involved in tyramine production. Appl Environ Microbiol. 2002;68(7):3537-3544.
Ladero V, Fernández M, Calles-Enríquez M, et al. Is the production of the biogenic amines tyramine and putrescine a species-level trait in Enterococci? Food Microbiol. 2012;30(1):132-138.
You H, Mariani LL, Mangone G, et al. Molecular basis of dopamine replacement therapy and its side effects in Parkinson's disease. Cell Tissue Res. 2018;373(1):111-135.
Mosharov EV, Borgkvist A, Sulzer D. Presynaptic effects of levodopa and their possible role in dyskinesia. Mov Disord. 2015;30(1):45-53.
Sun X, Wang D, Wu Z, Li P, Wang W. Synchronous pharmacokinetics study on levodopa in Parkinson's disease rats blood and extracellular fluids of striatum. J Chin Pharm Sci. 2011;46(8):610-614.
Zhang Y, He X, Mo C, et al. Association between microbial tyrosine decarboxylase gene and levodopa responsiveness in patients with Parkinson disease. Neurology. 2022;99(22):e2443-e2453.
Zhang Z, Gao C, Zhang H, et al. Morinda officinalis oligosaccharides increase serotonin in the brain and ameliorate depression via promoting 5-hydroxytryptophan production in the gut microbiota. Acta Pharm Sin B. 2022;12(8):3298-3312.
Schrag A, Dodel R, Spottke A, Bornschein B, Siebert U, Quinn NP. Rate of clinical progression in Parkinson's disease. A prospective study. Mov Disord. 2007;22(7):938-945.
Chi B, Lian X. Ginsenosides combined with levodopa in the treatment of 6-OHDA induced Parkinson's model rats. Chin J Pharmacol Toxicol. 2018;32:702.
Li R, Lu Y, Zhang Q, et al. Piperine promotes autophagy flux by P2RX4 activation in SNCA/α-synuclein-induced Parkinson disease model. Autophagy. 2022;18(3):559-575.
Sivashanmugam A, Velmathi S. Synthesis, in vitro and in silico anti-bacterial analysis of piperine and piperic ester analogues. Chem Biol Drug des. 2021;98(1):19-29.
Chen H, Sheng H, Zhao Y, Zhu G. Piperine inhibits cell proliferation and induces apoptosis of human gastric cancer cells by downregulating phosphatidylinositol 3-kinase (PI3K)/Akt pathway. Med Sci Monit. 2020;26:e928403.
Pellegrini C, Antonioli L, Colucci R, et al. Gastric motor dysfunctions in Parkinson's disease: current pre-clinical evidence. Parkinsonism Relat Disord. 2015;21(12):1407-1414.
Gabrielli M, Bonazzi P, Scarpellini E, et al. Prevalence of small intestinal bacterial overgrowth in Parkinson's disease. Mov Disord. 2011;26(5):889-892.
Freedberg DE, Toussaint NC, Chen SP, et al. Proton pump inhibitors alter specific taxa in the human gastrointestinal microbiome: a crossover trial. Gastroenterology. 2015;149(4):883-885.
Imhann F, Bonder MJ, Vich Vila A, et al. Proton pump inhibitors affect the gut microbiome. Gut. 2016;65(5):740-748.
Kommineni S, Bretl DJ, Lam V, et al. Bacteriocin production augments niche competition by Enterococci in the mammalian gastrointestinal tract. Nature. 2015;526(7575):719-722.
Quan L, Zhang C, Dong M, et al. Myristoleic acid produced by Enterococci reduces obesity through brown adipose tissue activation. Gut. 2020;69(7):1239-1247.
van Kessel SP, Auvinen P, Scheperjans F, El Aidy S. Gut bacterial tyrosine decarboxylase associates with clinical variables in a longitudinal cohort study of Parkinsons disease. NPJ Parkinsons Dis. 2021;7(1):115.
Dhiman P, Malik N, Khatkar A. Natural based piperine derivatives as potent monoamine oxidase inhibitors: an in silico ADMET analysis and molecular docking studies. BMC Chem. 2020;14(1):12.

Auteurs

Xiaolu Hu (X)

Beijing Key Lab of TCM Collateral Disease Theory Research, School of Traditional Chinese Medicine, Capital Medical University, Beijing, China.

Lan Yu (L)

Beijing Key Lab of TCM Collateral Disease Theory Research, School of Traditional Chinese Medicine, Capital Medical University, Beijing, China.

Yatong Li (Y)

Beijing Key Lab of TCM Collateral Disease Theory Research, School of Traditional Chinese Medicine, Capital Medical University, Beijing, China.

Xiaoxi Li (X)

Department of Pharmacy, Xuanwu Hospital of Capital Medical University, Beijing, China.

Yimeng Zhao (Y)

Beijing Key Lab of TCM Collateral Disease Theory Research, School of Traditional Chinese Medicine, Capital Medical University, Beijing, China.

Lijuan Xiong (L)

Beijing Key Lab of TCM Collateral Disease Theory Research, School of Traditional Chinese Medicine, Capital Medical University, Beijing, China.

Jiaxuan Ai (J)

Beijing Key Lab of TCM Collateral Disease Theory Research, School of Traditional Chinese Medicine, Capital Medical University, Beijing, China.

Qijun Chen (Q)

School of Pharmaceutical Sciences, Capital Medical University, Beijing, China.

Xing Wang (X)

Beijing Key Lab of TCM Collateral Disease Theory Research, School of Traditional Chinese Medicine, Capital Medical University, Beijing, China.

Xiaoqing Chen (X)

Beijing Key Lab of TCM Collateral Disease Theory Research, School of Traditional Chinese Medicine, Capital Medical University, Beijing, China.

Yinying Ba (Y)

Beijing Key Lab of TCM Collateral Disease Theory Research, School of Traditional Chinese Medicine, Capital Medical University, Beijing, China.

Yaonan Wang (Y)

Core facilities of modern pharmaceuticals, Capital Medical University, Beijing, China.

Xia Wu (X)

Beijing Key Lab of TCM Collateral Disease Theory Research, School of Traditional Chinese Medicine, Capital Medical University, Beijing, China.

Classifications MeSH