Trigonelline insulates against oxidative stress, proinflammatory cytokines and restores BDNF levels in lipopolysaccharide induced cognitive impairment in adult mice

Aldakinah AAA, Al-Shorbagy MY, Abdallah DM, El-Abhar HS (2017) Trigonelline and vildagliptin antidiabetic effect: improvement of insulin signalling pathway. J Pharm Pharmacol 69(7):856–864. https://doi.org/10.1111/jphp.12713 Antonisamy P, Arasu MV, Dhanasekaran M, Choi KC, Aravinthan A, Kim NS, Kang C-W, Kim J-H (2016) Protective effects of trigonelline against indomethacin-induced gastric ulcer in rats and potential underlying mechanisms. Food Funct 7(1):398–408. https://doi.org/10.1039/C5FO00403A Arlt A, Sebens S, Krebs S, Geismann C, Grossmann M, Kruse M, Schreiber S, Schäfer H (2013) Inhibition of the Nrf2 transcription factor by the alkaloid trigonelline renders pancreatic cancer cells more susceptible to apoptosis through decreased proteasomal gene expression and proteasome activity. Oncogene 32(40):4825–4835. https://doi.org/10.1038/onc.2012.493 Association, A. s (2016) 2016 Alzheimer's disease facts and figures. Alzheimers Dement 12(4):459–509. https://doi.org/10.1016/j.jalz.2016.03.001 Badshah H, Ali T, Kim MO (2016) Osmotin attenuates LPS-induced neuroinflammation and memory impairments via the TLR4/NFκB signaling pathway. Sci Rep 6(1):24493. https://doi.org/10.1038/srep24493 Choi D-Y, Lee JW, Lin G, Lee YK, Lee YH, Choi IS, Han SB, Jung JK, Kim YH, Kim KH (2012) Obovatol attenuates LPS-induced memory impairments in mice via inhibition of NF-κB signaling pathway. Neurochem Int 60(1):68–77. https://doi.org/10.1016/j.neuint.2011.11.005 Chowdhury AA, Gawali NB, Bulani VD, Kothavade PS, Mestry SN, Deshpande PS, Juvekar AR (2017) In vitro antiglycating effect and in vivo neuroprotective activity of Trigonelline in D-galactose induced cognitive impairment. Pharmacol Rep. https://doi.org/10.1016/j.pharep.2017.09.006 Dantzer R, O'Connor JC, Freund GG, Johnson RW, Kelley KW (2008) From inflammation to sickness and depression: when the immune system subjugates the brain. Nature. Rev Neurosci 9(1):46–56. https://doi.org/10.1038/nrn2297 Deng X, Meili Li WA, He L, Lu D, Patrylo PR, Cai H, Luo X, Li Z, Yan X (2014) Lipolysaccharide-induced neuroinflammation is associated with Alzheimer-like amyloidogenic axonal pathology and dendritic degeneration in rats. Adv Alzheimer Dis 3(2):78–93. https://doi.org/10.4236/aad.2014.32009 Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7(2):88–95. https://doi.org/10.1016/0006-2952(61)90145-9 García-Ayllón M-S, Small DH, Avila J, Sáez-Valero J (2011) Revisiting the role of acetylcholinesterase in Alzheimer’s disease: cross-talk with P-tau and β-amyloid. Front Mol Neurosci 4. https://doi.org/10.3389/fnmol.2011.00022 Gaur V, Bodhankar SL, Mohan V, Thakurdesai PA (2013) Neurobehavioral assessment of hydroalcoholic extract of Trigonella Foenum-Graecum seeds in rodent models of Parkinson’s disease. Pharm Biol 51(5):550–557. https://doi.org/10.3109/13880209.2012.747547 Ghezzi P, Sacco S, Agnello D, Marullo A, Caselli G, Bertini R (2000) LPS induces IL-6 in the brain and in serum largely through TNF production. Cytokine 12(8):1205–1210. https://doi.org/10.1006/cyto.2000.0697 Gong Q-H, Wang Q, Pan L-L, Liu X-H, Huang H, Zhu Y-Z (2010) Hydrogen sulfide attenuates lipopolysaccharide-induced cognitive impairment: a pro-inflammatory pathway in rats. Pharmacol Biochem Behav 96(1):52–58. https://doi.org/10.1016/j.pbb.2010.04.006 Gonzalez-Scarano F, Baltuch G (1999) Microglia as mediators of inflammatory and degenerative diseases. Annu Rev Neurosci 22(1):219–240. https://doi.org/10.1146/annurev.neuro.22.1.219 Gornall AG, Bardawill CJ, David MM (1949) Determination of serum proteins by means of the biuret reaction. J Biol Chem 177(2):751–766 Götz J, Ittner LM (2008) Animal models of Alzheimer's disease and frontotemporal dementia. Nature. Rev Neurosci 9(7):532–544. https://doi.org/10.1038/nrn2420 Guan Z, Fang J (2006) Peripheral immune activation by lipopolysaccharide decreases neurotrophins in the cortex and hippocampus in rats. Brain Behav Immun 20(1):64–71. https://doi.org/10.1016/j.bbi.2005.04.005 Hauss-Wegrzyniak B, Lukovic L, Bigaud M, Stoeckel M (1998) Brain inflammatory response induced by intracerebroventricular infusion of lipopolysaccharide: an immunohistochemical study. Brain Res 794(2):211–224. https://doi.org/10.1016/S0006-8993(98)00227-3 Helmy AA, Naseer MMA, El Shafie S, Nada MA (2012) Role of interleukin 6 and alpha-globulins in differentiating Alzheimer and vascular dementias. Neurodegener Dis 9(2):81–86. https://doi.org/10.1159/000329568 Heneka MT, Carson MJ, El Khoury J, Landreth GE, Brosseron F, Feinstein DL, Jacobs AH, Wyss-Coray T, Vitorica J, Ransohoff RM (2015) Neuroinflammation in Alzheimer's disease. Lancet Neurol 14(4):388–405. https://doi.org/10.1016/S1474-4422(15)70016-5 Heppner FL, Ransohoff RM, Becher B (2015) Immune attack: the role of inflammation in Alzheimer disease. Nature. Rev Neurosci 16(6):358–372. https://doi.org/10.1038/nrn3880 Hickman SE, Allison EK, El Khoury J (2008) Microglial dysfunction and defective β-amyloid clearance pathways in aging Alzheimer's disease mice. J Neurosci 28(33):8354–8360. https://doi.org/10.1523/JNEUROSCI.0616-08.2008 Hock C, Heese K, Hulette C, Rosenberg C, Otten U (2000) Region-specific neurotrophin imbalances in Alzheimer disease: decreased levels of brain-derived neurotrophic factor and increased levels of nerve growth factor in hippocampus and cortical areas. Arch Neurol 57(6):846–851. https://doi.org/10.1001/archneur.57.6.846 Hong BN, Yi TH, Park R, Kim SY, Kang TH (2008) Coffee improves auditory neuropathy in diabetic mice. Neurosci Lett 441(3):302–306. https://doi.org/10.1016/j.neulet.2008.06.049 Hou Y, Xie G, Miao F, Ding L, Mou Y, Wang L, Su G, Chen G, Yang J, Wu C (2014) Pterostilbene attenuates lipopolysaccharide-induced learning and memory impairment possibly via inhibiting microglia activation and protecting neuronal injury in mice. Prog Neuro-Psychopharmacol Biol Psychiatry 54:92–102. https://doi.org/10.1016/j.pnpbp.2014.03.015 Ilavenil S, Arasu MV, Lee J-C, Kim DH, Roh SG, Park HS, Choi GJ, Mayakrishnan V, Choi KC (2014) Trigonelline attenuates the adipocyte differentiation and lipid accumulation in 3T3-L1 cells. Phytomedicine 21(5):758–765. https://doi.org/10.1016/j.phymed.2013.11.007 Inestrosa NC, Alvarez A, Pérez CA, Moreno RD, Vicente M, Linker C, Casanueva OI, Soto C, Garrido J (1996) Acetylcholinesterase accelerates assembly of amyloid-β-peptides into Alzheimer's fibrils: possible role of the peripheral site of the enzyme. Neuron 16(4):881–891. https://doi.org/10.1016/S0896-6273(00)80108-7 Ittner LM, Götz J (2011) Amyloid-β and tau—a toxic pas de deux in Alzheimer's disease. Nature. Rev Neurosci 12(2):67–72 Jang YJ, Kim J, Shim J, Kim C-Y, Jang J-H, Lee KW, Lee HJ (2013) Decaffeinated coffee prevents scopolamine-induced memory impairment in rats. Behav Brain Res 245:113–119. https://doi.org/10.1016/j.bbr.2013.02.003 Jiang T, Sun Q, Chen S (2016) Oxidative stress: a major pathogenesis and potential therapeutic target of antioxidative agents in Parkinson’s disease and Alzheimer’s disease. Prog Neurobiol 147:1–19. https://doi.org/10.1016/j.pneurobio.2016.07.005 Joshi R, Garabadu D, Teja GR, Krishnamurthy S (2014) Silibinin ameliorates LPS-induced memory deficits in experimental animals. Neurobiol Learn Mem 116:117–131. https://doi.org/10.1016/j.nlm.2014.09.006 Kamble HV, Bodhankar SL (2013) Antihyperglycemic activity of trigonelline and sitagliptin in nicotinamide-streptozotocin induced diabetes in Wistar rats. Biomedicine & Aging Pathology 3(3):125–130. https://doi.org/10.1016/j.biomag.2013.05.006 Kirsten TB, Galvão MC, Reis-Silva TM, Queiroz-Hazarbassanov N, Bernardi MM (2015) Zinc prevents sickness behavior in duced by lipopolysaccharides after a stress challenge in rats. PLoS One 10(3):e0120263. https://doi.org/10.1371/journal.pone.0120263 Kitazawa M, Oddo S, Yamasaki TR, Green KN, LaFerla FM (2005) Lipopolysaccharide-induced inflammation exacerbates tau pathology by a cyclin-dependent kinase 5-mediated pathway in a transgenic model of Alzheimer's disease. J Neurosci 25(39):8843–8853. https://doi.org/10.1523/JNEUROSCI.2868-05.2005 Koenigsknecht-Talboo J, Landreth GE (2005) Microglial phagocytosis induced by fibrillar β-amyloid and IgGs are differentially regulated by proinflammatory cytokines. J Neurosci 25(36):8240–8249. https://doi.org/10.1523/JNEUROSCI.1808-05.2005 Krabbe G, Halle A, Matyash V, Rinnenthal JL, Eom GD, Bernhardt U, Miller KR, Prokop S, Kettenmann H, Heppner FL (2013) Functional impairment of microglia coincides with Beta-amyloid deposition in mice with Alzheimer-like pathology. PLoS One 8(4):e60921. https://doi.org/10.1371/journal.pone.0060921 Ma M, Chen Y, He J, Zeng T, Wang J (2007) Effects of morphine and its withdrawal on Y-maze spatial recognition memory in mice. Neuroscience 147(4):1059–1065. https://doi.org/10.1016/j.neuroscience.2007.05.020 Ma L, Zhang H, Liu N, Wang PQ et al (2016) TSPO ligand PK11195 alleviates neuroinflammation and beta-amyloid generation induced by systemic LPS administration. Brain Res. Bull 121:192–200 Mayakrishnan T, Nakkala JR, Jeepipalli SPK, Raja K, Chandra VK, Mohan VK, Sadras SR (2014) Fenugreek seed extract and its phytocompounds-trigonelline and diosgenin arbitrate their hepatoprotective effects through attenuation of endoplasmic reticulum stress and oxidative stress in type 2 diabetic rats. Eur Food Res Technol 240(1):223–232 McCaulley ME, Grush KA (2015) Alzheimer’s disease: exploring the role of inflammation and implications for treatment. Int J Alzheimers dis. 2015. Article ID 515248 Nandi A, Chatterjee I (1988) Assay of superoxide dismutase activity in animal tissues. J Biosci 13(3):305–315. https://doi.org/10.1007/BF02712155 Noworyta-Sokołowska K, Górska A, Gołembiowska K (2013) LPS-induced oxidative stress and inflammatory reaction in the rat striatum. Pharmacol Rep 65(4):863–869. https://doi.org/10.1016/S1734-1140(13)71067-3 Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95(2):351–335. https://doi.org/10.1016/0003-2697(79)90738-3 Panda S, Biswas S, Kar A (2013) Trigonelline isolated from fenugreek seed protects against isoproterenol-induced myocardial injury through down-regulation of Hsp27 and αB-crystallin. Nutrition 29(11):1395–1403. https://doi.org/10.1016/j.nut.2013.05.006 Patel NS, Paris D, Mathura V, Quadros AN, Crawford FC, Mullan MJ (2005) Inflammatory cytokine levels correlate with amyloid load in transgenic mouse models of Alzheimer's disease. J Neuroinflammation 2(1):9. https://doi.org/10.1186/1742-2094-2-9 Phillips HS, Hains JM, Armanini M, Laramee GR, Johnson SA, Winslow JW (1991) BDNF mRNA is decreased in the hippocampus of individuals with Alzheimer's disease. Neuron 7(5):695–702. https://doi.org/10.1016/0896-6273(91)90273-3 Prince MJ (2015) World Alzheimer Report 2015: the global impact of dementia: an analysis of prevalence, incidence, cost and trends. Alzheimer’s Disease International, London Qin L, Wu X, Block ML, Liu Y, Breese GR, Hong JS, Knapp DJ, Crews FT (2007) Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 55(5):453–462. https://doi.org/10.1002/glia.20467 Satheeshkumar N, Mukherjee PK, Bhadra S, Saha B (2010) Acetylcholinesterase enzyme inhibitory potential of standardized extract of Trigonella foenum graecum L and its constituents. Phytomedicine 17(3):292–295. https://doi.org/10.1016/j.phymed.2009.06.006 Singh M, Kaur M, Kukreja H, Chugh R, Silakari O, Singh D (2013) Acetylcholinesterase inhibitors as Alzheimer therapy: from nerve toxins to neuroprotection. Eur. J. Med Chem 70:165–188 Smith IK, Vierheller TL, Thorne CA (1988) Assay of glutathione reductase in crude tissue homogenates using 5, 5′-dithiobis (2-nitrobenzoic acid). Anal Biochem 175(2):408–413. https://doi.org/10.1016/0003-2697(88)90564-7 Tanila H (2017) The role of BDNF in Alzheimer's disease. Neurobiol Dis 97(Pt B):114–118 Tharaheswari M, Reddy NJ, Kumar R, Varshney K, Kannan M, Rani SS (2014) Trigonelline and diosgenin attenuate ER stress, oxidative stress-mediated damage in pancreas and enhance adipose tissue PPARγ activity in type 2 diabetic rats. Mol Cell Biochem 396(1–2):161–174. https://doi.org/10.1007/s11010-014-2152-x Tohda C, Nakamura N, Komatsu K, Hattori M (1999) Trigonelline-induced neurite outgrowth in human neuroblastoma SK-N-SH cells. Biol Pharm Bull 22(7):679–682. https://doi.org/10.1248/bpb.22.679 Tohda C, Kuboyama T, Komatsu K (2005) Search for natural products related to regeneration of the neuronal network. Neurosignals 14(1–2):34–45. https://doi.org/10.1159/000085384 Wang W-Y, Tan M-S, Yu J-T, Tan L (2015) Role of pro-inflammatory cytokines released from microglia in Alzheimer’s disease. Ann Transl Med 3(10):136. https://doi.org/10.3978/j.issn.2305-5839.2015.03.49 Wei P, Liu Q, Li D, Zheng Q, Zhou J, Li J (2015) Acute nicotine treatment attenuates lipopolysaccharide-induced cognitive dysfunction by increasing BDNF expression and inhibiting neuroinflammation in the rat hippocampus. Neurosci Lett 604:161–166. https://doi.org/10.1016/j.neulet.2015.08.008 Xiao S, Wang T, Ma X, Qin Y, Li X, Zhao Z, Liu X, Wang X, Xie H, Jiang Q (2017) Efficacy and safety of a novel acetylcholinesterase inhibitor octohydroaminoacridine in mild-to-moderate Alzheimer's disease: a phase II multicenter randomised controlled trial. Age Ageing:1–7 Yoshinari O, Takenake A, Igarashi K (2013) Trigonelline ameliorates oxidative stress in type 2 diabetic Goto-Kakizaki rats. J Med Food 16(1):34–41. https://doi.org/10.1089/jmf.2012.2311 Zhang D-F, Zhang F, Zhang J, Zhang R-M, Li R (2015) Protection effect of trigonelline on liver of rats with non-alcoholic fatty liver diseases. Asian Pac J. Trop Biomed 8(8):651–654