Plant-Based Nutritional Supplementation Attenuates LPS-Induced Low-Grade Systemic Activation
Abstract
:1. Introduction
2. Materials and Methods
2.1. Animals Male
2.2. Nutritional Supplementation
2.3. Incremental Loading Test
2.4. Injections and Chronic Infusions of LPS
2.5. Glucose Tolerance Test
2.6. Insulin Tolerance Test
2.7. Neopterin Measurement by HPLC
2.8. Dopamine, DOPAC and 5-HT Measurement by HPLC
2.9. Measurement of Respiratory Chain Complex I Activity
2.10. Protein Determination
2.11. Statistical Analysis
3. Results
3.1. Continuous LPS Injections Reduced Glucose Tolerance
3.2. Acute and Sustained Infusion of LPS over a Two-Week Period on Exercise Activity in Mice
3.3. Continuous Infusion of LPS over a Two-Week Period Provoked Inflammation and Altered Dopamine Metabolism
3.4. Nutritional Diet Mitigated the Exacerbation of Immune System Initiation and Maintained Mitochondrial Activity
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Janssen, H.G.; Davies, I.G.; Richardson, L.D.; Stevenson, L. Determinants of takeaway and fast food consumption: A narrative review. Nutr. Res. Rev. 2018, 31, 16–34. [Google Scholar] [CrossRef] [PubMed]
- Popkin, B.M.; Gordon-Larsen, P. The nutrition transition: Worldwide obesity dynamics and their determinants. Int. J. Obes. Relat. Metab. Disord. 2004, 28, S2–S9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Manzel, A.; Muller, D.N.; Hafler, D.A.; Erdman, S.E.; Linker, R.A.; Kleinewietfeld, M. Role of “Western diet” in inflammatory autoimmune diseases. Curr. Allergy Asthma Rep. 2014, 14, 404. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Van Dam, R.M.; Rimm, E.B.; Willett, W.C.; Stampfer, M.J.; Hu, F.B. Dietary patterns and risk for type 2 diabetes mellitus in US men. Ann. Intern. Med. 2002, 136, 201–209. [Google Scholar] [CrossRef] [Green Version]
- Hills, R.D., Jr.; Pontefract, B.A.; Mishcon, H.R.; Black, C.A.; Sutton, S.C.; Theberge, C.R. Gut Microbiome: Profound Implications for Diet and Disease. Nutrients 2019, 11, 1613. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, H.J.; Seo, H.I.; Cha, H.Y.; Yang, Y.J.; Kwon, S.H.; Yang, S.J. Diabetes and Alzheimer’s Disease: Mechanisms and Nutritional Aspects. Clin. Nutr. Res. 2018, 7, 229–240. [Google Scholar] [CrossRef] [Green Version]
- Pandareesh, M.D.; Kandikattu, H.K.; Razack, S.; Amruta, N.; Choudhari, R.; Vikram, A.; Doddapattar, P. Nutrition and Nutraceuticals in Neuroinflammatory and Brain Metabolic Stress: Implications for Neurodegenerative Disorders. CNS Neurol. Disord. Drug Targets 2018, 17, 680–688. [Google Scholar] [CrossRef]
- Shal, B.; Ding, W.; Ali, H.; Kim, Y.S.; Khan, S. Anti-neuroinflammatory Potential of Natural Products in Attenuation of Alzheimer’s Disease. Front. Pharmacol. 2018, 9, 548. [Google Scholar] [CrossRef]
- Yu, J.; Zhu, H.; Taheri, S.; Mondy, W.; Perry, S.; Kindy, M.S. Impact of nutrition on inflammation, tauopathy, and behavioral outcomes from chronic traumatic encephalopathy. J. Neuroinflamm. 2018, 15, 277. [Google Scholar] [CrossRef]
- Harding, A.; Gonder, U.; Robinson, S.J.; Crean, S.; Singhrao, S.K. Exploring the Association between Alzheimer’s Disease, Oral Health, Microbial Endocrinology and Nutrition. Front. Aging Neurosci. 2017, 9, 398. [Google Scholar] [CrossRef]
- Erro, R.; Brigo, F.; Tamburin, S.; Zamboni, M.; Antonini, A.; Tinazzi, M. Nutritional habits, risk, and progression of Parkinson disease. J. Neurol. 2018, 265, 12–23. [Google Scholar] [CrossRef]
- D’Cunha, N.M.; McKune, A.J.; Panagiotakos, D.B.; Georgousopoulou, E.N.; Thomas, J.; Mellor, D.D.; Naumovski, N. Evaluation of dietary and lifestyle changes as modifiers of S100β levels in Alzheimer’s disease. Nutr. Neurosci 2019, 22, 1–18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lorenzatti, A.J.; Servato, M.L. New evidence on the role of inflammation in CVD risk. Curr. Opin. Cardiol. 2019, 34, 418–423. [Google Scholar] [CrossRef] [PubMed]
- Nasonov, E.L.; Popkova, T.V. Atherosclerosis: Perspectives of anti-inflammatory therapy. Ter. Arkh. 2018, 90, 4–12. [Google Scholar] [PubMed]
- Serino, A.; Salazar, G. Protective Role of Polyphenols against Vascular Inflammation, Aging and Cardiovascular Disease. Nutrients 2018, 11, 53. [Google Scholar] [CrossRef] [Green Version]
- Arrese, M.; Cabrera, D.; Kalergis, A.M.; Feldstein, A.E. Innate Immunity and Inflammation in NAFLD/NASH. Dig. Dis. Sci. 2016, 61, 1294–1303. [Google Scholar] [CrossRef] [Green Version]
- Malynn, B.A.; Ma, A. A20: A multifunctional tool for regulating immunity and preventing disease. Cell. Immunol. 2019, 340, 103914. [Google Scholar] [CrossRef] [PubMed]
- Liew, P.X.; Kubes, P. The Neutrophil’s Role During Health and Disease. Physiol. Rev. 2019, 99, 1223–1248. [Google Scholar] [CrossRef] [PubMed]
- Fazio, F.; Ulivieri, M.; Volpi, C.; Gargaro, M.; Fallarino, F. Targeting metabotropic glutamate receptors for the treatment of neuroinflammation. Curr. Opin. Pharmacol. 2018, 38, 16–23. [Google Scholar] [CrossRef]
- Spagnuolo, C.; Moccia, S.; Russo, G.L. Anti-inflammatory effects of flavonoids in neurodegenerative disorders. Eur. J. Med. Chem. 2018, 153, 105–115. [Google Scholar] [CrossRef]
- Dantas de Lucas, R.; Caputo, F.; Mendes de Souza, K.; Sigwalt, A.R.; Ghisoni, K.; Lock Silveira, P.C.; Remor, A.P.; da Luz Scheffer, D.; Antonacci Guglielmo, L.G.; Latini, A. Increased platelet oxidative metabolism, blood oxidative stress and neopterin levels after ultra-endurance exercise. J. Sports Sci. 2014, 32, 22–30. [Google Scholar] [CrossRef] [PubMed]
- McCauley, M.E.; Baloh, R.H. Inflammation in ALS/FTD pathogenesis. Acta Neuropathol. 2019, 137, 715–730. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, Y.; Lee, S.; Chang, S.C.; Lee, J. Significant roles of neuroinflammation in Parkinson’s disease: Therapeutic targets for PD prevention. Arch. Pharm. Res. 2019, 42, 416–425. [Google Scholar] [CrossRef] [PubMed]
- Van Eldik, L.J.; Carrillo, M.C.; Cole, P.E.; Feuerbach, D.; Greenberg, B.D.; Hendrix, J.A.; Kennedy, M.; Kozauer, N.; Margolin, R.A.; Molinuevo, J.L.; et al. The roles of inflammation and immune mechanisms in Alzheimer’s disease. Alzheimers Dement (N. Y.) 2016, 2, 99–109. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Heneka, M.T.; Golenbock, D.T.; Latz, E. Innate immunity in Alzheimer’s disease. Nat. Immunol. 2015, 16, 229–236. [Google Scholar] [CrossRef] [PubMed]
- Yu, J.; Zhu, H.; Taheri, S.; Mondy, W.; Kirstein, C.; Swindell, W.; Ko, D.; Kindy, M.S. GM6 Attenuates Alzheimer’s Disease Pathology in APP Mice. Mol. Neurobiol. 2019, 56, 6386–6396. [Google Scholar] [CrossRef]
- Yu, J.; Zhu, H.; Taheri, S.; Mondy, W.; Perry, S.; Kirstein, C.; Kindy, M.S. Effects of GrandFusion Diet on Cognitive Impairment in Transgenic Mouse Model of Alzheimer’s Disease. Nutrients 2020, 13, 117. [Google Scholar] [CrossRef] [PubMed]
- Yu, J.; Zhu, H.; Taheri, S.; Monday, W.L.; Perry, S.; Kindy, M.S. Reduced Neuroinflammation and Improved Functional Recovery after Traumatic Brain Injury by Prophylactic Diet Supplementation in Mice. Nutrients 2019, 11, 299. [Google Scholar] [CrossRef] [Green Version]
- Yu, J.; Zhu, H.; Taheri, S.; Perry, S.; Kindy, M.S. The Effect of Diet on Improved Endurance in Male C57BL/6 Mice. Nutrients 2018, 10, 1101. [Google Scholar] [CrossRef] [Green Version]
- Yu, J.; Zhu, H.; Perry, S.; Taheri, S.; Kindy, M.S. Daily supplementation with GrandFusion® improves memory and learning in aged rats. Aging (Albany NY) 2017, 9, 1041–1054. [Google Scholar] [CrossRef] [Green Version]
- Aguiar, A.S.; Duzzioni, M.; Remor, A.P.; Tristão, F.S.M.; Matheus, F.C.; RaismanVozari, R.; Latini, A.; Prediger, R.D. Moderate-intensity physical exercise protects against experimental 6-hydroxydopamine-induced hemiparkinsonism through Nrf2-antioxidant response element pathway. Neurochem. Res. 2016, 41, 64–72. [Google Scholar] [CrossRef] [PubMed]
- Ghisoni, K.; Aguiar, A.S.; de Oliveira, P.A.; Matheus, F.C.; Gabach, L.; Perez, M.; Carlini, V.P.; Barbeito, L.; Mongeau, R.; Lanfumey, L.; et al. Neopterin acts as an endogenous cognitive enhancer. Brain Behav. Immun. 2016, 56, 156–164. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, A.T.; Mandard, S.; Dray, C.; Deckert, V.; Valet, P.; Besnard, P.; Drucker, D.J.; Lagrost, L.; Grober, J. Lipopolysaccharides-mediated increase in glucose-stimulated insulin secretion: Involvement of the GLP-1 pathway. Diabetes 2014, 63, 471–482. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kurien, B.T.; Hal Scofield, R. Mouse urine collection using clear plastic wrap. Lab. Anim. 1999, 33, 83–86. [Google Scholar] [CrossRef] [PubMed]
- Castro, A.A.; Ghisoni, K.; Latini, A.; Quevedo, J.; Tasca, C.I.C.I.; Prediger, R.D.S. Lithium and valproate prevent olfactory discrimination and short-term memory impairments in the intranasal 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) rat model of Parkinson’s disease. Behav. Brain Res. 2012, 229, 208–215. [Google Scholar] [CrossRef]
- Aguiar, A.S.; Stragier, E.; daLuzScheffer, D.; Remor, A.P.; Oliveira, P.A.; Prediger, R.D.; Latini, A.; Raisman-Vozari, R.; Mongeau, R.; Lanfumey, L. Effects of exercise on mitochondrial function, neuroplasticity and anxio-depressive behavior of mice. Neuroscience 2014, 271, 56–63. [Google Scholar] [CrossRef]
- De Paula Martins, R.; Lim, C.K.; Ghisoni, K.; Staats, A.; Dallagnol, K.; Solano, A.; Guillemin, G.J.; Silva Aguiar, A., Jr.; Latini, A. Treating depression with exercise: The inflammasome inhibition perspective. J. Syst. Integr. Neurosci. 2016, 3, 100. [Google Scholar] [CrossRef] [Green Version]
- Handschin, C.; Spiegelman, B.M. The role of exercise and PGC1alpha in inflammation and chronic disease. Nature 2008, 454, 463–469. [Google Scholar] [CrossRef] [Green Version]
- Hotamisligil, G.S. Inflammation and metabolic disorders. Nature 2006, 444, 860–867. [Google Scholar] [CrossRef]
- Creely, S.J.; McTernan, P.G.; Kusminski, C.M.; Fisher, M.; Da Silva, N.F.; Khanolkar, M.; Evans, M.; Harte Kumar, S. Lipopolysaccharide activates an innate immune system response in human adipose tissue in obesity and type 2 diabetes. AJP Endocrinol. Metab. 2006, 292, E740–E747. [Google Scholar] [CrossRef] [Green Version]
- Dasu, M.R.; Devaraj, S.; Park, S.; Jialal, I. Increased Toll-Like Receptor (TLR) activation AL and TLR ligands in recently diagnosed type2 diabetic subjects. Diabetes Care 2010, 33, 861–868. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Piccinin, E.; Villani, G.; Moschetta, A. Metabolic aspects in NAFLD, NASH and hepatocellular carcinoma: The role of PGC1 coactivators. Nat. Rev. Gastroenterol. Hepatol. 2019, 16, 160–174. [Google Scholar] [CrossRef] [PubMed]
- Hallal, P.C.; Andersen, L.B.; Bull, F.C.; Guthold, R.; Haskell, W.; Ekelund, U.; Alkandari, J.R.; Bauman, A.E.; Blair, S.N.; Brownson, R.C.; et al. Global physical activity levels: Surveillance progress, pitfalls, and prospects. Lancet 2012, 380, 247–257. [Google Scholar] [CrossRef]
- Hotamisligil, G.S.; Peraldi, P.; Budavari, A.; Ellis, R.; White, M.F.; Spiegelman, B.M. IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha and obesity-induced insulin resistance. Science 1996, 271, 665–668. [Google Scholar] [CrossRef] [PubMed]
- Gao, Z.; Hwang, D.; Bataille, F.; Lefevre, M.; York, D.; Quon, M.J.; Ye, J. Serine phosphorylation of insulin receptor substrate 1 by inhibitor kappa B kinase complex. J. Biol. Chem. 2002, 277, 48115–48121. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pavlov, V.A.; Tracey, K.J. Neural regulation of immunity: Molecular mechanisms and clinical translation. Nat. Neurosci. 2017, 20, 156–166. [Google Scholar] [CrossRef]
- Obermeier, B.; Daneman, R.; Ransohoff, R.M. Development, maintenance and disruption of the blood-brain barrier. Nat. Med. 2013, 19, 1584–1596. [Google Scholar] [CrossRef]
- Prinz, M.; Priller, J. The role of peripheral immune cells in the CNS in steady state and disease. Nat. Neurosci. 2017, 20, 136–144. [Google Scholar] [CrossRef]
- Estrada, J.A.; Contreras, I. Nutritional Modulation of Immune and Central Nervous System Homeostasis: The Role of Diet in Development of Neuroinflammation and Neurological Disease. Nutrients 2019, 11, 1076. [Google Scholar] [CrossRef] [Green Version]
- Das, M.; Mohapatra, S.; Mohapatra, S.S. New perspectives on central and peripheral immune responses to acute traumatic brain injury. J. Neuroinflamm. 2012, 9, 236. [Google Scholar] [CrossRef] [Green Version]
- McGrattan, A.M.; McGuinness, B.; McKinley, M.C.; Kee, F.; Passmore, P.; Woodside, J.V.; McEvoy, C.T. Diet and Inflammation in Cognitive Ageing and Alzheimer’s Disease. Curr. Nutr. Rep. 2019, 8, 53–65. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Báez-Mendoza, R.; Schultz, W. The role of the striatum in social behavior. Front. Neurosci. 2013, 7, 233. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hollerman, J.R.; Tremblay, L.; Schultz, W. Involvement of basal ganglia and orbitofrontal cortex in goal-directed behavior. Prog. Brain Res. 2000, 126, 193–215. [Google Scholar]
- Seidl, S.E.; Santiago, J.A.; Bilyk, H.; Potashkin, J.A. The emerging role of nutrition in Parkinson’s disease. Front. Aging Neurosci. 2014, 6, 36. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jackson, A.; Forsyth, C.B.; Shaikh, M.; Voigt, R.M.; Engen, P.A.; Ramirez, V.; Keshavarzian, A. Diet in Parkinson’s Disease: Critical Role for the Microbiome. Front. Neurol. 2019, 10, 1245. [Google Scholar] [CrossRef]
- Briguglio, M.; Dell’Osso, B.; Panzica, G.; Malgaroli, A.; Banfi, G.; Zanaboni Dina, C.; Galentino, R.; Porta, M. Dietary Neurotransmitters: A Narrative Review on Current Knowledge. Nutrients 2018, 10, 591. [Google Scholar] [CrossRef] [Green Version]
- Marosi, K.; Kim, S.W.; Moehl, K.; Scheibye-Knudsen, M.; Cheng, A.; Cutler, R.; Camandola, S.; Mattson, M.P. 3-Hydroxybutyrate regulates energy metabolism and induces BDNF expression in cerebral cortical neurons. J. Neurochem. 2016, 139, 769–781. [Google Scholar] [CrossRef]
- Ghisoni, K.; de PRDPMartins, R.; Barbeito, L.; Latini, A. Neopterin as a Potential Cytoprotective Brain Molecule. J. Psych. Res. 2015, 71, 134–139. [Google Scholar] [CrossRef]
- Widner, B.; Leblhuber, F.; Fuchs, D. Increased neopterin production and tryptophan degradation in advanced Parkinson’s disease. J. Neural Transm. 2002, 109, 181–189. [Google Scholar] [CrossRef]
- Biswas, P.; Dellanoce, C.; Vezzoli, A.; Mrakic-Sposta, S.; Malnati, M.; Beretta, A.; Accinni, R. Antioxidant Activity with Increased Endogenous Levels of Vitamin C, E and A Following Dietary Supplementation with a Combination of Glutathione and Resveratrol Precursors. Nutrients 2002, 12, 3224. [Google Scholar] [CrossRef]
- Vasconcelos, A.R.; Dos Santos, N.B.; Scavone, C.; Munhoz, C.D. Nrf2/ARE Pathway Modulation by Dietary Energy Regulation in Neurological Disorders. Front. Pharmacol. 2019, 10, 33. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kuehne, L.K.; Reiber, H.; Bechter, K.; Hagberg, L.; Fuchs, D. Cerebrospinal fluid neopterin is brain-derived and not associated with blood-CSF barrier dysfunction in non-inflammatory affective and schizophrenic spectrum disorders. J. Psychiatr. Res. 2013, 47, 1417–1422. [Google Scholar] [CrossRef] [PubMed]
- De Paula Martins, R.; Ghisoni, K.; Lim, C.K.; Aguiar, A.S., Jr.; Guillemin, G.J.; Latini, A. Neopterin preconditioning prevents inflammasome activation in mammalian astrocytes. Free Radic. Biol. Med. 2018, 115, 371–382. [Google Scholar] [CrossRef] [PubMed]
- Yu, J.; Zhu, H.; Gattoni-Celli, S.; Taheri, S.; Kindy, M.S. Dietary supplementation of GrandFusion® mitigates cerebral ischemia-induced neuronal damage and attenuates inflammation. Nutr. Neurosci. 2016, 19, 290–300. [Google Scholar] [CrossRef] [PubMed]
t6 Essential Vitamins | % dv | Maximum Premix Claim Per 225.00 mg |
---|---|---|
Vitamin A | 50.00 | 2500.00 IU |
Vitamin C | 50.00 | 30.00 mg |
Vitamin D | 50.00 | 200.00 IU |
Vitamin E | 50.00 | 15.00 IU |
Vitamin B1 | 50.00 | 0.7500 mg |
Vitamin B6 | 50.00 | 1.00 mg |
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Yu, J.; Zhu, H.; Taheri, S.; Mondy, W.; Perry, S.; Kindy, M.S. Plant-Based Nutritional Supplementation Attenuates LPS-Induced Low-Grade Systemic Activation. Int. J. Mol. Sci. 2021, 22, 573. https://doi.org/10.3390/ijms22020573
Yu J, Zhu H, Taheri S, Mondy W, Perry S, Kindy MS. Plant-Based Nutritional Supplementation Attenuates LPS-Induced Low-Grade Systemic Activation. International Journal of Molecular Sciences. 2021; 22(2):573. https://doi.org/10.3390/ijms22020573
Chicago/Turabian StyleYu, Jin, Hong Zhu, Saeid Taheri, William Mondy, Stephen Perry, and Mark S. Kindy. 2021. "Plant-Based Nutritional Supplementation Attenuates LPS-Induced Low-Grade Systemic Activation" International Journal of Molecular Sciences 22, no. 2: 573. https://doi.org/10.3390/ijms22020573