Protection effect of piperine and piperlonguminine from Piper longum L. alkaloids against rotenone-induced neuronal injury

Brain Research

Volumn 1639, Issue , 2016, Pages 214-227

  Wang, Hao ^a   Liu, Jia ^a   Gao, Ge ^a   Wu, Xia ^a   Wang, Xiaomin ^a   Yang, Hui ^a  

^a BEIJING INSTITUTE FOR BRAIN DISORDERS   (China)

Author keywords

Mitochondrial permeability transition pore; Parkinson s disease; Treatment

Indexed keywords

ALKALOID DERIVATIVE; CASPASE 3; CYCLOSPORIN A; CYTOCHROME C; LACTATE DEHYDROGENASE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; NEUROPROTECTIVE AGENT; PIPER LONGUM EXTRACT; PIPERINE; PIPERLONGUMININE; PLANT EXTRACT; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROTENONE; RUTHENIUM RED; UNCLASSIFIED DRUG; 1,3 BENZODIOXOLE DERIVATIVE; 1,3 DIOXOLANE DERIVATIVE; ALKALOID; AMIDE; ANTIPARKINSON AGENT; CARRIER PROTEIN; PIPERIDINE DERIVATIVE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL VIABILITY; CONTROLLED STUDY; CYTOSOL; DOPAMINERGIC NERVE CELL; DRUG MECHANISM; IMMUNOHISTOCHEMISTRY; MALE; MESENCEPHALON; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; MITOPHAGY; MOTOR COORDINATION; MOTOR DYSFUNCTION; NERVE CELL CULTURE; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PIPER LONGUM; PRIORITY JOURNAL; RAT; WESTERN BLOTTING; ANIMAL; BRAIN; CELL LINE; DRUG EFFECTS; HUMAN; METABOLISM; MOUSE; NERVE CELL; PARKINSONIAN DISORDERS; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PHYTOTHERAPY; PIPER (PLANT); PRECLINICAL STUDY; RANDOMIZATION; WISTAR RAT;

ALKALOIDS; ANIMALS; ANTIPARKINSON AGENTS; APOPTOSIS; AUTOPHAGY; BENZODIOXOLES; BRAIN; CELL LINE; DIOXOLANES; DRUG EVALUATION, PRECLINICAL; HUMANS; MALE; MICE; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; NEURONS; NEUROPROTECTIVE AGENTS; PARKINSONIAN DISORDERS; PHYTOTHERAPY; PIPER; PIPERIDINES; PLANT EXTRACTS; POLYUNSATURATED ALKAMIDES; RANDOM ALLOCATION; RATS, WISTAR; ROTENONE;

EID: 84939138181     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2015.07.029     Document Type: Article

References (66)

1. Al-Baghdadi, O.B., Prater, N.I., et al. Inhibition of monoamine oxidase by derivatives of piperine, an alkaloid from the pepper plant Piper nigrum, for possible use in Parkinson׳s disease. Bioorg. Med. Chem. Lett. 22:23 (2012), 7183–7188.
2. Brooks, M.M., Neelam, S., et al. Lenticular mitoprotection. Part A: monitoring mitochondrial depolarization with JC-1 and artifactual fluorescence by the glycogen synthase kinase-3beta inhibitor, SB216763.”. Mol. Vis. 19 (2013), 1406–1412.
3. Cai, K., Yang, J., et al. Single UV excitation of Hoechst 33342 and propidium iodide for viability assessment of rhesus monkey spermatozoa using flow cytometry. Arch. Androl. 51:5 (2005), 371–383.
4. Chonpathompikunlert, P., Yoshitomi, T., et al. The use of nitroxide radical-containing nanoparticles coupled with piperine to protect neuroblastoma SH-SY5Y cells from Abeta-induced oxidative stress. Biomaterials 32:33 (2011), 8605–8612.
5. Chuang, C.S., Su, H.L., et al. Quantitative evaluation of motor function before and after engraftment of dopaminergic neurons in a rat model of Parkinson׳s disease. J. Biomed. Sci., 17, 2010, 9.
6. Costa, G., Frau, L., et al. MPTP-induced dopamine neuron degeneration and glia activation is potentiated in MDMA-pretreated mice. Mov. Disord. 28:14 (2013), 1957–1965.
7. Das, J., Jha, D.K., et al. Isolation and characterization of antidermatophytic bioactive molecules from Piper longum L. s. Indian J. Microbiol. 52:4 (2012), 624–629.
8. Duzenli, S., Bakuridze, K., et al. The effects of ruthenium red, dantrolene and nimodipine, alone or in combination, in NMDA induced neurotoxicity of cerebellar granular cell culture of rats. Toxicol. In Vitro 19:5 (2005), 589–594.
9. Emanuelsson, I., Norlin, M., Protective effects of 27- and 24-hydroxycholesterol against staurosporine-induced cell death in undifferentiated neuroblastoma SH-SY5Y cells. Neurosci. Lett. 525:1 (2012), 44–48.
10. Fernandes, M.P., Leite, A.C., et al. The Cratylia mollis seed lectin induces membrane permeability transition in isolated rat liver mitochondria and a cyclosporine A-insensitive permeability transition in Trypanosoma cruzi mitochondria. J. Eukaryot. Microbiol. 61:4 (2014), 381–388.
11. Fernandez-Vizarra, E., Ferrin, G., et al. Isolation of mitochondria for biogenetical studies: an update. Mitochondrion 10:3 (2010), 253–262.
12. Gasparri, F., An overview of cell phenotypes in HCS: limitations and advantages. Expert Opin. Drug Discov. 4:6 (2009), 643–657.
13. Gautier, C.A., Giaime, E., et al. Regulation of mitochondrial permeability transition pore by PINK1. Mol. Neurodegener., 7, 2012, 22.
14. Hauser, D.N., Hastings, T.G., Mitochondrial dysfunction and oxidative stress in Parkinson׳s disease and monogenic parkinsonism. Neurobiol. Dis. 51 (2013), 35–42.
15. Hsieh, T.H., Chen, J.J., et al. Time-course gait analysis of hemiparkinsonian rats following 6-hydroxydopamine lesion. Behav. Brain Res. 222:1 (2011), 1–9.
16. Huehnchen, P., Boehmerle, W., et al. Assessment of paclitaxel induced sensory polyneuropathy with “Catwalk” automated gait analysis in mice. PLoS One, 8(10), 2013, e76772.
17. Huttemann, M., Pecina, P., et al. The multiple functions of cytochrome c and their regulation in life and death decisions of the mammalian cell: from respiration to apoptosis. Mitochondrion 11:3 (2011), 369–381.
18. Jarvius, M., Fryknas, M., et al. Piperlongumine induces inhibition of the ubiquitin–proteasome system in cancer cells. Biochem. Biophys. Res. Commun. 431:2 (2013), 117–123.
19. Joza, N., Pospisilik, J.A., et al. AIF: not just an apoptosis-inducing factor. Ann. N. Y. Acad. Sci. 1171 (2009), 2–11.
20. Koopmans, G.C., Deumens, R., et al. Strain and locomotor speed affect over-ground locomotion in intact rats. Physiol. Behav. 92:5 (2007), 993–1001.
21. Kuan, W.L., Poole, E., et al. A novel neuroprotective therapy for Parkinson׳s disease using a viral noncoding RNA that protects mitochondrial complex I activity. J. Exp. Med. 209:1 (2012), 1–10.
22. Kumar, A., Panghal, S., et al. Antiinflammatory activity of Piper longum fruit oil. Indian J. Pharm. Sci. 71:4 (2009), 454–456.
23. Kumar, S., Kamboj, J., et al. Overview for various aspects of the health benefits of Piper longum linn. fruit. J. Acupunct. Meridian Stud. 4:2 (2011), 134–140.
24. Lee, E., Park, H.R., et al. Baicalein attenuates astroglial activation in the 1-methyl-4-phenyl-1,2,3,4-tetrahydropyridine-induced Parkinson׳s disease model by downregulating the activations of nuclear factor-kappaB, ERK, and JNK. J. Neurosci. Res. 92:1 (2014), 130–139.
25. Lee, W., Yoo, H., et al. Barrier protective effects of piperlonguminine in LPS-induced inflammation in vitro and in vivo. Food Chem. Toxicol. 58 (2013), 149–157.
26. Lees, A.J., Hardy, J., et al. Parkinson׳s disease. Lancet 373:9680 (2009), 2055–2066.
27. Liang, Q., Liou, A.K., et al. 6-Hydroxydopamine induces dopaminergic cell degeneration via a caspase-9-mediated apoptotic pathway that is attenuated by caspase-9dn expression. J. Neurosci. Res. 77:5 (2004), 747–761.
28. Liao, T.T., Jia, R.W., et al. Propidium iodide staining method for testing the cytotoxicity of 2,4,6-trichlorophenol and perfluorooctane sulfonate at low concentrations with Vero cells.”. J. Environ. Sci. Health A Tox Hazard. Subst. Environ. Eng. 46:14 (2011), 1769–1775.
29. Liu, J., Bi, Y., et al. Simultaneous UFLC-ESI-MS/MS determination of piperine and piperlonguminine in rat plasma after oral administration of alkaloids from Piper longum L.: application to pharmacokinetic studies in rats. J. Chromatogr. B. Analyt. Technol. Biomed. Life Sci. 879:27 (2011), 2885–2890.
30. Lu, L., Zhao, C., et al. Therapeutic benefit of TH-engineered mesenchymal stem cells for Parkinson׳s disease. Brain Res. Brain Res. Protoc. 15:1 (2005), 46–51.
31. Mandemakers, W., Morais, V.A., et al. A cell biological perspective on mitochondrial dysfunction in Parkinson disease and other neurodegenerative diseases. J. Cell Sci. 120:Pt 10 (2007), 1707–1716.
32. Martin, L.J., Mitochondrial pathobiology in Parkinson׳s disease and amyotrophic lateral sclerosis. J. Alzheimers Dis. 20:Suppl 2 (2010), S335–S356.
33. Mashayekhi, V., Eskandari, M.R., et al. Induction of mitochondrial permeability transition (MPT) pore opening and ROS formation as a mechanism for methamphetamine-induced mitochondrial toxicity. Naunyn Schmiedebergs Arch. Pharmacol. 387:1 (2014), 47–58.
34. Monian, P., Jiang, X., Clearing the final hurdles to mitochondrial apoptosis: regulation post cytochrome C release. Exp. Oncol. 34:3 (2012), 185–191.
35. Murunikkara, V., Pragasam, S.J., et al. Anti-inflammatory effect of piperine in adjuvant-induced arthritic rats – a biochemical approach. Inflammation 35:4 (2012), 1348–1356.
36. Nabi, S.A., Kasetti, R.B., et al. Antidiabetic and antihyperlipidemic activity of Piper longum root aqueous extract in STZ induced diabetic rats. BMC Complement. Altern. Med., 13, 2013, 37.
37. Naoi, M., Maruyama, W., et al. Rasagiline prevents apoptosis induced by PK11195, a ligand of the outer membrane translocator protein (18 kDa), in SH-SY5Y cells through suppression of cytochrome c release from mitochondria. J. Neural. Transm. 120:11 (2013), 1539–1551.
38. Olanow, C.W., The scientific basis for the current treatment of Parkinson׳s disease. Annu. Rev. Med. 55 (2004), 41–60.
39. Olanow, C.W., The pathogenesis of cell death in Parkinson׳s disease – 2007. Mov. Disord. 22:Suppl. 17 (2007), S335–S342.
40. Olanow, C.W., Stern, M.B., Parkinson׳s disease: unresolved issues. Ann. Neurol. 64:Suppl 2 (2008), S1–S2.
41. Ouyang, D.Y., Zeng, L.H., et al. Piperine inhibits the proliferation of human prostate cancer cells via induction of cell cycle arrest and autophagy. Food Chem. Toxicol. 60 (2013), 424–430.
42. Palmi, M., Youmbi, G., et al. Antagonism by taurine on the ruthenium red-induced and 6-hydroxydopamine plus 1-methyl-4-phenylpyridinium-induced Ca2+ release from rat liver mitochondria. Adv. Exp. Med. Biol. 442 (1998), 91–98.
43. Parker, W.J., Swerdlow, R.H., Mitochondrial dysfunction in idiopathic Parkinson disease. Am. J. Hum. Genet. 62:4 (1998), 758–762.
44. Penna, C., Perrelli, M.G., et al. Mitochondrial pathways, permeability transition pore, and redox signaling in cardioprotection: therapeutic implications. Antioxid. Redox Signal. 18:5 (2013), 556–599.
45. Petronilli, V., Miotto, G., et al. Transient and long-lasting openings of the mitochondrial permeability transition pore can be monitored directly in intact cells by changes in mitochondrial calcein fluorescence. Biophys. J. 76:2 (1999), 725–734.
46. Qi, H.S., Liu, P., et al. Inhibitory effect of piperlonguminine/dihydropiperlonguminine on the production of amyloid beta and APP in SK-N-SH cells. Chin. J. Physiol. 52:3 (2009), 160–168.
47. Raj, L., Ide, T., et al. Selective killing of cancer cells by a small molecule targeting the stress response to ROS. Nature 475:7355 (2011), 231–234.
48. Rao, V.K., Carlson, E.A., Yan, S.S., Mitochondrial permeability transition pore is a potential drug target for neurodegeneration. Biochim. Biophys. Acta. 1842:8 (2014), 1267–1272.
49. Reale, M., Pesce, M., et al. Mitochondria as an easy target to oxidative stress events in Parkinson׳s disease. CNS Neurol. Disord. Drug Targets 11:4 (2012), 430–438.
50. Sanders, L.H., Greenamyre, J.T., Oxidative damage to macromolecules in human Parkinson disease and the rotenone model. Free Radic. Biol. Med. 62 (2013), 111–120.
51. Schapira, A.H., Targeting mitochondria for neuroprotection in Parkinson׳s disease. Antioxid. Redox Signal. 16:9 (2012), 965–973.
52. Schapira, A.H., Olanow, C.W., Neuroprotection in Parkinson disease: mysteries, myths, and misconceptions. JAMA 291:3 (2004), 358–364.
53. Sevrioukova, I.F., Apoptosis-inducing factor: structure, function, and redox regulation. Antioxid. Redox. Signal. 14:12 (2011), 2545–2579.
54. Shoba, G., Joy, D., et al. Influence of piperine on the pharmacokinetics of curcumin in animals and human volunteers. Planta Med. 64:4 (1998), 353–356.
55. Shrivastava, P., Vaibhav, K., et al. Anti-apoptotic and anti-inflammatory effect of Piperine on 6-OHDA induced Parkinson׳s rat model. J. Nutr. Biochem. 24:4 (2013), 680–687.
56. Siletsky, S.A., Steps of the coupled charge translocation in the catalytic cycle of cytochrome c oxidase. Front. Biosci. (Landmark Ed) 18 (2013), 36–57.
57. Surendran, S., Rajasankar, S., Parkinson׳s disease: oxidative stress and therapeutic approaches. Neurol. Sci. 31:5 (2010), 531–540.
58. Szelechowski, M., Betourne, A., et al. A viral peptide that targets mitochondria protects against neuronal degeneration in models of Parkinson׳s disease. Nat. Commun., 5, 2014, 5181.
59. Toy, W.A., Petzinger, G.M., et al. Treadmill exercise reverses dendritic spine loss in direct and indirect striatal medium spiny neurons in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) mouse model of Parkinson׳s disease. Neurobiol. Dis. 63C (2013), 201–209.
60. Umar, S., Golam, S.A., et al. Piperine ameliorates oxidative stress, inflammation and histological outcome in collagen induced arthritis. Cell Immunol. 284:1–2 (2013), 51–59.
61. Uren, R.T., Dewson, G., et al. Mitochondrial release of pro-apoptotic proteins: electrostatic interactions can hold cytochrome c but not Smac/DIABLO to mitochondrial membranes. J. Biol. Chem. 280:3 (2005), 2266–2274.
62. Yarana, C., Sripetchwandee, J., et al. Calcium-induced cardiac mitochondrial dysfunction is predominantly mediated by cyclosporine A-dependent mitochondrial permeability transition pore. Arch. Med. Res. 43:5 (2012), 333–338.
63. Youdim, M.B., Bar, A.O., et al. Rasagiline: neurodegeneration, neuroprotection, and mitochondrial permeability transition. J. Neurosci. Res. 79:1–2 (2005), 172–179.
64. Youle, R.J., van der Bliek, A.M., Mitochondrial fission, fusion, and stress. Science 337:6098 (2012), 1062–1065.
65. Yuste, V.J., Moubarak, R.S., et al. Cysteine protease inhibition prevents mitochondrial apoptosis-inducing factor (AIF) release. Cell Death Differ. 12:11 (2005), 1445–1448.
66. Zhou, J.S., Wang, J.F., et al. Ginsenoside Rd attenuates mitochondrial permeability transition and cytochrome C release in isolated spinal cord mitochondria: involvement of kinase-mediated pathways. Int. J. Mol. Sci. 15:6 (2014), 9859–9877.