The isothiocyanate isolated from moringa oleifera shows potent anti-inflammatory activity in the treatment of murine subacute Parkinson's disease

Rejuvenation Research

Volumn 20, Issue 1, 2017, Pages 50-63

  Giacoppo, Sabrina ^a   Rajan, Thangavelu Soundara ^a   De Nicola, Gina Rosalinda ^b   Iori, Renato ^b   Rollin, Patrick ^c   Bramanti, Placido ^a   Mazzon, Emanuela ^a  

^a IRCCS CENTRO NEUROLESI BONINO PULEJO   (Italy)

^b ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

^c UNIVERSITÉ D'ORLÉANS   (France)

Author keywords

Glucosinolates; MPTP experimental model; Proinflammatory cytokines; RAW 264.7 macrophages

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; ANTIINFLAMMATORY AGENT; CASPASE 9; GLUCOMORINGIN; HERBACEOUS AGENT; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; ISOTHIOCYANIC ACID; LIPOPOLYSACCHARIDE; MORINGIN; PADGEM PROTEIN; PROTEIN P53; THIOGLUCOSIDASE; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; 4-((ALPHA-L-RHAMNOSYLOXY)BENZYL)ISOTHIOCYANATE; BIOLOGICAL MARKER; ISOTHIOCYANIC ACID DERIVATIVE; RHAMNOSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; BRADYKINESIA; BRAIN TISSUE; CONTROLLED STUDY; DENDRITE; DOWN REGULATION; DRUG EFFICACY; DRUG ISOLATION; DRUG POTENCY; DRUG PURIFICATION; DRUG SAFETY; DRUG TOLERANCE; ENZYME ACTIVATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MORINGA OLEIFERA; MOUSE; NEUROMODULATION; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PLANT SEED; POLE TEST; PREMEDICATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAW 264.7 CELL LINE; SIGNAL TRANSDUCTION; SINAPIS ALBA; SUBACUTE PARKINSON DISEASE; UPREGULATION; WEIGHT REDUCTION; ANALOGS AND DERIVATIVES; ANIMAL; BODY WEIGHT; C57BL MOUSE; CHEMISTRY; DRUG EFFECTS; INFLAMMATION; MACROPHAGE; MACROPHAGE ACTIVATION; METABOLISM; MOTOR ACTIVITY; PATHOLOGY; PATHOPHYSIOLOGY;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; ANIMALS; ANTI-INFLAMMATORY AGENTS; BIOMARKERS; BODY WEIGHT; DENDRITES; INFLAMMATION; ISOTHIOCYANATES; LIPOPOLYSACCHARIDES; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED C57BL; MORINGA OLEIFERA; MOTOR ACTIVITY; OXIDATIVE STRESS; PARKINSON DISEASE; RAW 264.7 CELLS; RHAMNOSE; TYROSINE 3-MONOOXYGENASE;

EID: 85013080189     PISSN: 15491684     EISSN: 15578577     Source Type: Journal    
DOI: 10.1089/rej.2016.1828     Document Type: Article

References (57)

1. Beitz JM. Parkinson's disease: A review. Front Biosci 2014;6:65-74.
2. Braak H, Ghebremedhin E, Rub U, Bratzke H, Del Tredici K. Stages in the development of Parkinson's disease-related pathology. Cell Tissue Res 2004;318:121-134.
3. Dawson TM, Dawson VL. Molecular pathways of neurodegeneration in Parkinson's disease. Science 2003;302:819-822.
4. Rai SN, Yadav SK, Singh D, Singh SP. Ursolic acid attenuates oxidative stress in nigrostriatal tissue and improves neurobehavioral activity in MPTP-induced Parkinsonian mouse model. J Chem Neuroanat 2015;71:41-49.
5. Blesa J, Trigo-Damas I, Quiroga-Varela A, Jackson-Lewis VR. Oxidative stress and Parkinson's disease. Front Neuroanat 2015;9:91.
6. Jenner P. Oxidative stress as a cause of Parkinson's disease. Acta Neurol Scand Suppl 1991;136:6-15.
7. Ceravolo R, Rossi C, Del Prete E, Bonuccelli U. A review of adverse events linked to dopamine agonists in the treatment of Parkinson's disease. Expert Opin Drug Saf 2016;15:181-198.
8. Dinkova-Kostova AT, Kostov RV. Glucosinolates and isothiocyanates in health and disease. Trends Mol Med 2012;18:337-347.
9. Tarozzi A, Angeloni C, Malaguti M, et al. Sulforaphane as a potential protective phytochemical against neurodegenerative diseases. Oxid Med Cell Longev 2013;2013:415078.
10. Giacoppo S, Galuppo M, Montaut S, et al. An overview on neuroprotective effects of isothiocyanates for the treatment of neurodegenerative diseases. Fitoterapia 2015;106:12-21.
11. Holst B, Williamson G. A critical review of the bioavailability of glucosinolates and related compounds. Nat Prod Rep 2004;21:425-447.
12. Getahun SM, Chung FL. Conversion of glucosinolates to isothiocyanates in humans after ingestion of cooked watercress. CancerEpidemiol Biomarkers Prev 1999;8:447-451.
13. Agerbirk N, Olsen CE. Glucosinolate structures in evolution. Phytochemistry 2012;77:16-45.
14. Bennett RN, Mellon FA, Foidl N, Pratt JH, Dupont, MS, Perkins, L, Kroon, PA. Profiling glucosinolates and phenolics in vegetative and reproductive tissues of the multi-purpose trees Moringa oleifera L. (horseradish tree) and Moringa stenopetala L. J Agric Food Chem 2003;51:3546-3553.
15. Das N, Ganguli D, Dey S. Moringa oleifera Lam. seed extract prevents fat diet induced oxidative stress in mice and protects liver cell-nuclei from hydroxyl radical mediated damage. Indian J Exp Biol 2015;53:794-802.
16. Vasanth K M, Ilango G C, Mohan Kumar K, Aruna Agrawal R, Dubey GP. Moringa oleifera attenuates the release of proinflammatory cytokines in lipopolysaccharide stimulated human monocytic cell line. Ind Crops Prod 2015;77:44-50.
17. Jung IL, Lee JH, Kang SC. A potential oral anticancer drug candidate, leaf extract, induces the apoptosis of human hepatocellular carcinoma cells. Oncol Lett 2015;10:1597-1604.
18. Vongsak B, Mangmool S, Gritsanapan W. Antioxidant activity and induction of mRNA expressions of antioxidant enzymes in HEK-293 cells of Moringa oleifera leaf extract. Planta Med 2015;81:1084-1089.
19. Muller C, van Loon J, Ruschioni S, De Nicola GR, Olsen CE, Iori R, Agerbirk N. Taste detection of the non-volatile isothiocyanate moringin results in deterrence to glucosinolateadapted insect larvae. Phytochemistry 2015;118:139-148.
20. Galuppo M, Giacoppo S, De Nicola GR, Iori R, Navarra M, Lombardo GE, Bramanti P, Mazzon E. Anti inflammatory activity of glucomoringin isothiocyanate in a mouse model of experimental autoimmune encephalomyelitis. Fitoterapia 2014;95:160-174.
21. Galuppo M, Giacoppo S, Iori R, De Nicola GR, Bramanti P, Mazzon E. Administration of 4-(alpha-L-rhamnosyloxy)- benzyl isothiocyanate delays disease phenotype in SOD1 (G93A) rats: A transgenic model of amyotrophic lateral sclerosis. Biomed Res Int 2015;2015:259417.
22. Giacoppo S, Galuppo M, De Nicola GR, Bramanti P, Mazzon E. 4(Alpha-l-rhamnosyloxy)-benzyl isothiocyanate, a bioactive phytochemical that attenuates secondary damage in an experimental model of spinal cord injury. Bioorg Med Chem 2015;23:80-88.
23. Brunelli D, Tavecchio M, Falcioni C, Frapolli R, Erba E, Iori R, Rollin P, Barillari J, Manzotti C, Morazzoni P, D'Incalci M. The isothiocyanate produced from glucomoringin inhibits NF-kB and reduces myeloma growth in nude mice in vivo. Biochem Pharmacol 2010;79:1141-1148.
24. Maldini M, Maksoud SA, Natella F, Montoro P, Petretto GL, Foddai M, De Nicola GR, Chessa M, Pintore G. Moringa oleifera: Study of phenolics and glucosinolates by mass spectrometry. J Mass Spectrom 2014;49:900-910.
25. EEC Regulation 1864/90, Enclosure VIII. Vol L170:27- 341990.
26. Pessina A, Thomas RM, Palmieri S, Luisi PL. An improved method for the purification of myrosinase and its physicochemical characterization. Arch Biochem Biophys 1990;280:383-389.
27. Rajan TS, De Nicola GR, Iori R, Rollin P, Bramanti P, Mazzon E. Anticancer activity of glucomoringin isothiocyanate in human malignant astrocytoma cells. Fitoterapia 2016;110:1-7.
28. Galuppo M, Nicola GR, Iori R, Dell'utri P, Bramanti P, Mazzon E. Antibacterial activity of glucomoringin bioactivated with myrosinase against two important pathogens affecting the health of long-Term patients in hospitals. Molecules 2013;18:14340-14348.
29. Langston JW, Ballard P, Tetrud JW, Irwin I. Chronic Parkinsonism in humans due to a product of meperidineanalog synthesis. Science 1983;219:979-980.
30. Ogawa N, Hirose Y, Ohara S, Ono T, Watanabe Y. A simple quantitative bradykinesia test in MPTP-Treated mice. Res Commun Chem Pathol Pharmacol 1985;50:435-441.
31. Galuppo M, Iori R, De Nicola GR, Bramanti P, Mazzon E. Anti-inflammatory and anti-Apoptotic effects of (RS)- glucoraphanin bioactivated with myrosinase in murine subacute and acute MPTP-induced Parkinson's disease. Bioorg Med Chem 2013;21:5532-5547.
32. Cao ZH, Zheng QY, Li GQ, Hu XB, Feng SL, Xu GL, Zhang KQ. STAT1-mediated down-regulation of Bcl-2 expression is involved in IFN-gamma/TNF-Alpha-induced apoptosis in NIT-1 cells. Plos One 2015;10:e0120921.
33. Galuppo M, Giacoppo S, Iori R, De Nicola GR, Milardi D, Bramanti P, Mazzon E. 4(alpha-L-Rhamnosyloxy)-benzyl isothiocyanate, a bioactive phytochemical that defends cerebral tissue and prevents severe damage induced by focal ischemia/reperfusion. J Biol Regul Homeost Agents 2015;29:343-356.
34. Mogi M, Harada M, Kondo T, Riederer P, Inagaki H, Minami M, Nagatsu T. Interleukin-1 beta, interleukin-6, epidermal growth factor and transforming growth factoralpha are elevated in the brain from parkinsonian patients. Neurosci Lett 1994;180:147-150.
35. Sabroe I, Parker LC, Dower SK, Whyte MK. The role of TLR activation in inflammation. J Pathol 2008;214:126-135.
36. Takeda K, Akira S. Toll-like receptors in innate immunity. Int Immunol 2005;17:1-14.
37. Nagatsu T, Mogi M, Ichinose H, Togari A. Changes in cytokines and neurotrophins in Parkinson's disease. J Neural Transm Suppl 200060):277-290.
38. Brochard V, Combadiere B, Prigent A, Laouar Y, Perrin A, Beray-Berthat V, Bonduelle O, Alvarez-Fischer D, Callebert J, Launay JM, Duyckaerts C, Flavell RA, Hirsch EC, Hunot S. Infiltration of CD4+ lymphocytes i;:(nto the brain contributes to neurodegeneration in a mouse model of Parkinson disease. J Clin Invest 2009;119:182-192.
39. McGeer PL, Itagaki S, Boyes BE, McGeer EG. Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains. Neurology 1988;38:1285-1291.
40. Ramsey CP, Tansey MG. A survey from 2012 of evidence for the role of neuroinflammation in neurotoxin animal models of Parkinson's disease and potential molecular targets. Exp Neurol 2014;256:126-132.
41. Camicioli R, Grossmann SJ, Spencer PS, Hudnell K, Anger WK. Discriminating mild parkinsonism: Methods for epidemiological research. Mov Disord 2001;16:33-40.
42. Ros-Bernal F, Hunot S, Herrero MT, Parnadeau S, Corvol JC, Lu L, Alvarez-Fischer D, Carrillo-de Sauvage MA, Saurini F, Coussieu C, Kinugawa K, Prigent A, Hoglinger G, Hamon M, Tronche F, Hirsch EC, Vyas S. Microglial glucocorticoid receptors play a pivotal role in regulating dopaminergic neurodegeneration in parkinsonism. Proc Natl Acad Sci U S A 2011;108:6632-6637.
43. Budnowski J, Hanske L, Schumacher F, Glatt H, Platz S, Rohn S, Blaut M. Glucosinolates are mainly absorbed intact in germfree and human microbiota-Associated mice. J Agric Food Chem 2015;63:8418-8428.
44. Abdull Razis AF, Bagatta M, De Nicola GR, Iori R, Ioannides C. Intact glucosinolates modulate hepatic cytochrome P450 and phase II conjugation activities and may contribute directly to the chemopreventive activity of cruciferous vegetables. Toxicology 2010;277:74-85.
45. Sweet MJ, Hume DA. Endotoxin signal transduction in macrophages. J Leukoc Biol 1996;60:8-26.
46. Schletter J, Heine H, Ulmer AJ, Rietschel ET. Molecular mechanisms of endotoxin activity. Arch Microbiol 1995;164: 383-389.
47. Tak PP, Firestein GS. NF-kappaB: A key role in inflammatory diseases. J Clin Invest 2001;107:7-11.
48. Oeckinghaus A, Hayden MS, Ghosh S. Crosstalk in NFkappaB signaling pathways. Nat Immunol 2011;12:695-708.
49. Fimognari C, Turrini E, Ferruzzi L, Lenzi M, Hrelia P. Natural isothiocyanates: Genotoxic potential versus chemoprevention. Mutat Res 2012;750:107-131.
50. Przedborski S, Jackson-Lewis V, Djaldetti R, Liberatore G. Vila M, Vukosavic S, Almer G. The parkinsonian toxin MPTP: Action and mechanism. Restor Neurol Neurosci 2000;16:135-142.
51. Boddupalli S, Mein JR, Lakkanna S, James DR. Induction of phase 2 antioxidant enzymes by broccoli sulforaphane: Perspectives in maintaining the antioxidant activity of vitamins a, C, and e. Front Genet 2012;3:7.
52. Scapagnini G, Vasto S, Abraham NG, Caruso C, Zella D, Fabio G. Modulation of Nrf2/ARE pathway by food polyphenols: A nutritional neuroprotective strategy for cognitive and neurodegenerative disorders. Mol Neurobiol 2011;44:192-201.
53. Tufekci KU, Civi Bayin E, Genc S, Genc K. The Nrf2/ARE pathway: A promising target to counteract mitochondrial dysfunction in Parkinson's disease. Parkinsons Dis 2011; 2011:314082.
54. de Vries HE, Witte M, Hondius D, et al. Nrf2-induced antioxidant protection: A promising target to counteract ROS-mediated damage in neurodegenerative disease? Free Radic Biol Med 2008;45:1375-1383.
55. Montalto MC, Hart ML, Jordan JE, Wada K, Stahl GL. Role for complement in mediating intestinal nitric oxide synthase-2 and superoxide dismutase expression. Am J Physiol Gastrointest Liver Physiol 2003;285:G197-G206.
56. Joshi DC, Bakowska JC. Determination of mitochondrial membrane potential and reactive oxygen species in live rat cortical neurons. J Vis Exp 2011;(51):pii:2704.
57. Abdull Razis AF, Noor NM. Sulforaphane is superior to glucoraphanin in modulating carcinogen-metabolising enzymes in Hep G2 cells. Asian Pac J Cancer Prev 2013;14: 4235-4238.