Skip to main content
Top
Published in: Journal of Neuroinflammation 1/2018

Open Access 01-12-2018 | Research

Curcumin attenuates collagen-induced inflammatory response through the “gut-brain axis”

Authors: Yannong Dou, Jinque Luo, Xin Wu, Zhifeng Wei, Bei Tong, Juntao Yu, Ting Wang, Xinyu Zhang, Yan Yang, Xusheng Yuan, Peng Zhao, Yufeng Xia, Huijuan Hu, Yue Dai

Published in: Journal of Neuroinflammation | Issue 1/2018

Login to get access

Abstract

Background

Previous studies have demonstrated that oral administration of curcumin exhibited an anti-arthritic effect despite its poor bioavailability. The present study aimed to explore whether the gut-brain axis is involved in the therapeutic effect of curcumin.

Methods

The collagen-induced arthritis (CIA) rat model was induced by immunization with an emulsion of collagen II and complete Freund’s adjuvant. Sympathetic and parasympathetic tones were measured by electrocardiographic recordings. Unilateral cervical vagotomy (VGX) was performed before the induction of CIA. The ChAT, AChE activities, and serum cytokine levels were determined by ELISA. The expression of the high-affinity choline transporter 1 (CHT1), ChAT, and vesicular acetylcholine transporter (VAChT) were determined by real-time PCR and immunohistochemical staining. The neuronal excitability of the vagus nerve was determined by whole-cell patch clamp recording.

Results

Oral administration of curcumin restored the imbalance between the sympathetic and parasympathetic tones in CIA rats and increased ChAT activity and expression of ChAT and VAChT in the gut, brain, and synovium. Additionally, VGX eliminated the effects of curcumin on arthritis and ACh biosynthesis and transport. Electrophysiological data showed that curcumin markedly increased neuronal excitability of the vagus nerve. Furthermore, selective α7 nAChR antagonists abolished the effects of curcumin on CIA.

Conclusions

Our results demonstrate that curcumin attenuates CIA through the “gut-brain axis” by modulating the function of the cholinergic system. These findings provide a novel approach for mechanistic studies of anti-arthritic compounds with low oral absorption and bioavailability.
Literature
1.
go back to reference Scott DL, Wolfe F, Huizinga TW. Rheumatoid arthritis. Lancet. 2013;376:1094–108.CrossRef Scott DL, Wolfe F, Huizinga TW. Rheumatoid arthritis. Lancet. 2013;376:1094–108.CrossRef
3.
go back to reference van Maanen MA, Vervoordeldonk MJ, Tak PP. The cholinergic anti-inflammatory pathway: towards innovative treatment of rheumatoid arthritis. Nat Rev Rheumatol. 2009;5:229–32.CrossRefPubMed van Maanen MA, Vervoordeldonk MJ, Tak PP. The cholinergic anti-inflammatory pathway: towards innovative treatment of rheumatoid arthritis. Nat Rev Rheumatol. 2009;5:229–32.CrossRefPubMed
4.
go back to reference Olofsson PS, Rosas-Ballina M, Levine YA, Tracey KJ. Rethinking inflammation: neural circuits in the regulation of immunity. Immunol Rev. 2012;248:188–204.CrossRefPubMedPubMedCentral Olofsson PS, Rosas-Ballina M, Levine YA, Tracey KJ. Rethinking inflammation: neural circuits in the regulation of immunity. Immunol Rev. 2012;248:188–204.CrossRefPubMedPubMedCentral
5.
go back to reference Waldburger JM, Boyle DL, Pavlov VA, Tracey KJ, Firestein GS. Acetylcholine regulation of synoviocyte cytokine expression by the alpha7 nicotinic receptor. Arthritis Rheum. 2008;58:3439–49.CrossRefPubMedPubMedCentral Waldburger JM, Boyle DL, Pavlov VA, Tracey KJ, Firestein GS. Acetylcholine regulation of synoviocyte cytokine expression by the alpha7 nicotinic receptor. Arthritis Rheum. 2008;58:3439–49.CrossRefPubMedPubMedCentral
6.
go back to reference Wang H, Liao H, Ochani M, Justiniani M, Lin X, Yang L, et al. Cholinergic agonists inhibit HMGB1 release and improve survival in experimental sepsis. Nat Med. 2004;10:1216–21.CrossRefPubMed Wang H, Liao H, Ochani M, Justiniani M, Lin X, Yang L, et al. Cholinergic agonists inhibit HMGB1 release and improve survival in experimental sepsis. Nat Med. 2004;10:1216–21.CrossRefPubMed
7.
go back to reference Wang H, Yu M, Ochani M, Amella CA, Tanovic M, Susarla S, et al. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature. 2003;421:384–8.CrossRefPubMed Wang H, Yu M, Ochani M, Amella CA, Tanovic M, Susarla S, et al. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature. 2003;421:384–8.CrossRefPubMed
8.
go back to reference Jurenka JS. Anti-inflammatory properties of curcumin, a major constituent of Curcuma longa: a review of preclinical and clinical research. Altern Med Rev. 2009;14:141–53.PubMed Jurenka JS. Anti-inflammatory properties of curcumin, a major constituent of Curcuma longa: a review of preclinical and clinical research. Altern Med Rev. 2009;14:141–53.PubMed
9.
go back to reference Dhouib IB, Annabi A, Doghri R, Rejeb I, Dallagi Y, Bdiri Y, et al. Neuroprotective effects of curcumin against acetamiprid-induced neurotoxicity and oxidative stress in the developing male rat cerebellum: biochemical, histological, and behavioral changes. Environ Sci Pollut Res In. 2017; [Epub ahead of print] Dhouib IB, Annabi A, Doghri R, Rejeb I, Dallagi Y, Bdiri Y, et al. Neuroprotective effects of curcumin against acetamiprid-induced neurotoxicity and oxidative stress in the developing male rat cerebellum: biochemical, histological, and behavioral changes. Environ Sci Pollut Res In. 2017; [Epub ahead of print]
10.
go back to reference Lahiff C, Moss AC. Curcumin for clinical and endoscopic remission in ulcerative colitis. Inflamm Bowel Dis. 2011;17:E66.CrossRefPubMed Lahiff C, Moss AC. Curcumin for clinical and endoscopic remission in ulcerative colitis. Inflamm Bowel Dis. 2011;17:E66.CrossRefPubMed
11.
go back to reference Choi GY, Kim HB, Hwang ES, Lee S, Kim MJ, Choi JY, et al. Curcumin alters neural plasticity and viability of intact hippocampal circuits and attenuates behavioral despair and COX-2 expression in chronically stressed rats. Mediat Inflamm. 2017;2017:6280925. Choi GY, Kim HB, Hwang ES, Lee S, Kim MJ, Choi JY, et al. Curcumin alters neural plasticity and viability of intact hippocampal circuits and attenuates behavioral despair and COX-2 expression in chronically stressed rats. Mediat Inflamm. 2017;2017:6280925.
12.
go back to reference Xu Y, Lin D, Li S, Li G, Shyamala SG, Barish PA, et al. Curcumin reverses impaired cognition and neuronal plasticity induced by chronic stress. Neuropharmacology. 2009;57:463–71.CrossRefPubMed Xu Y, Lin D, Li S, Li G, Shyamala SG, Barish PA, et al. Curcumin reverses impaired cognition and neuronal plasticity induced by chronic stress. Neuropharmacology. 2009;57:463–71.CrossRefPubMed
13.
go back to reference Mun SH, Kim HS, Kim JW, Ko NY, Kim do K, Lee BY, et al. Oral administration of curcumin suppresses production of matrix metalloproteinase (MMP)-1 and MMP-3 to ameliorate collagen-induced arthritis: inhibition of the PKCdelta/JNK/c-Jun pathway. J Pharmacol Sci. 2009;111:13–21.CrossRefPubMed Mun SH, Kim HS, Kim JW, Ko NY, Kim do K, Lee BY, et al. Oral administration of curcumin suppresses production of matrix metalloproteinase (MMP)-1 and MMP-3 to ameliorate collagen-induced arthritis: inhibition of the PKCdelta/JNK/c-Jun pathway. J Pharmacol Sci. 2009;111:13–21.CrossRefPubMed
14.
go back to reference Moon DO, Kim MO, Choi YH, Park YM, Kim GY. Curcumin attenuates inflammatory response in IL-1beta-induced human synovial fibroblasts and collagen-induced arthritis in mouse model. Int Immunopharmacol. 2010;10:605–10.CrossRefPubMed Moon DO, Kim MO, Choi YH, Park YM, Kim GY. Curcumin attenuates inflammatory response in IL-1beta-induced human synovial fibroblasts and collagen-induced arthritis in mouse model. Int Immunopharmacol. 2010;10:605–10.CrossRefPubMed
15.
go back to reference Chandran B, Goel A. A randomized, pilot study to assess the efficacy and safety of curcumin in patients with active rheumatoid arthritis. Phytother Res. 2012;26:1719–25.CrossRefPubMed Chandran B, Goel A. A randomized, pilot study to assess the efficacy and safety of curcumin in patients with active rheumatoid arthritis. Phytother Res. 2012;26:1719–25.CrossRefPubMed
16.
go back to reference Heger M, van Golen RF, Broekgaarden M, Michel MC. The molecular basis for the pharmacokinetics and pharmacodynamics of curcumin and its metabolites in relation to cancer. Pharmacol Rev. 2012;66:222–307.CrossRef Heger M, van Golen RF, Broekgaarden M, Michel MC. The molecular basis for the pharmacokinetics and pharmacodynamics of curcumin and its metabolites in relation to cancer. Pharmacol Rev. 2012;66:222–307.CrossRef
17.
go back to reference Anand P, Kunnumakkara AB, Newman RA, Aggarwal BB. Bioavailability of curcumin: problems and promises. Mol Pharm. 2007;4:807–18.CrossRefPubMed Anand P, Kunnumakkara AB, Newman RA, Aggarwal BB. Bioavailability of curcumin: problems and promises. Mol Pharm. 2007;4:807–18.CrossRefPubMed
18.
go back to reference Goel A, Kunnumakkara AB, Aggarwal BB. Curcumin as “Curecumin”: from kitchen to clinic. Biochem Pharmacol. 2008;75:787–809.CrossRefPubMed Goel A, Kunnumakkara AB, Aggarwal BB. Curcumin as “Curecumin”: from kitchen to clinic. Biochem Pharmacol. 2008;75:787–809.CrossRefPubMed
19.
go back to reference Yang Y, Wu X, Wei Z, Dou Y, Zhao D, Wang T, et al. Oral curcumin has anti-arthritic efficacy through somatostatin generation via cAMP/PKA and Ca(2+)/CaMKII signaling pathways in the small intestine. Pharmacol Res. 2015;95-96:71–81.CrossRefPubMed Yang Y, Wu X, Wei Z, Dou Y, Zhao D, Wang T, et al. Oral curcumin has anti-arthritic efficacy through somatostatin generation via cAMP/PKA and Ca(2+)/CaMKII signaling pathways in the small intestine. Pharmacol Res. 2015;95-96:71–81.CrossRefPubMed
20.
go back to reference Furness JB, Rivera LR, Cho HJ, Bravo DM, Callaghan B. The gut as a sensory organ. Nat Rev Gastroenterol Hepatol. 2013;10:729–40.CrossRefPubMed Furness JB, Rivera LR, Cho HJ, Bravo DM, Callaghan B. The gut as a sensory organ. Nat Rev Gastroenterol Hepatol. 2013;10:729–40.CrossRefPubMed
21.
go back to reference Bonaz BL, Bernstein CN. Brain-gut interactions in inflammatory bowel disease. Gastroenterology. 2013;144:36–49.CrossRefPubMed Bonaz BL, Bernstein CN. Brain-gut interactions in inflammatory bowel disease. Gastroenterology. 2013;144:36–49.CrossRefPubMed
22.
go back to reference Perez-Burgos A, Mao YK, Bienenstock J, Kunze WA. The gut-brain axis rewired: adding a functional vagal nicotinic “sensory synapse”. FASEB J. 2014;28:3064–74.CrossRefPubMed Perez-Burgos A, Mao YK, Bienenstock J, Kunze WA. The gut-brain axis rewired: adding a functional vagal nicotinic “sensory synapse”. FASEB J. 2014;28:3064–74.CrossRefPubMed
23.
go back to reference Petra AI, Panagiotidou S, Hatziagelaki E, Stewart JM, Conti P, Theoharides TC. Gut-microbiota-brain axis and its effect on neuropsychiatric disorders with suspected immune dysregulation. Clin Ther. 2015;37:984–95.CrossRefPubMedPubMedCentral Petra AI, Panagiotidou S, Hatziagelaki E, Stewart JM, Conti P, Theoharides TC. Gut-microbiota-brain axis and its effect on neuropsychiatric disorders with suspected immune dysregulation. Clin Ther. 2015;37:984–95.CrossRefPubMedPubMedCentral
24.
go back to reference Wolkmer P, Silva CB, Paim FC, Duarte MM, Castro V, Palma HE, et al. Pre-treatment with curcumin modulates acetylcholinesterase activity and proinflammatory cytokines in rats infected with Trypanosoma evansi. Parasitol Int. 2013;62:144–9.CrossRefPubMed Wolkmer P, Silva CB, Paim FC, Duarte MM, Castro V, Palma HE, et al. Pre-treatment with curcumin modulates acetylcholinesterase activity and proinflammatory cytokines in rats infected with Trypanosoma evansi. Parasitol Int. 2013;62:144–9.CrossRefPubMed
25.
go back to reference Bonaz B, Sinniger V, Pellissier S. Anti-inflammatory properties of the vagus nerve: potential therapeutic implications of vagus nerve stimulation. J Physiol. 2016;594:5781–90.CrossRefPubMedPubMedCentral Bonaz B, Sinniger V, Pellissier S. Anti-inflammatory properties of the vagus nerve: potential therapeutic implications of vagus nerve stimulation. J Physiol. 2016;594:5781–90.CrossRefPubMedPubMedCentral
26.
go back to reference Ishrat T, Hoda MN, Khan MB, Yousuf S, Ahmad M, Khan MM, et al. Amelioration of cognitive deficits and neurodegeneration by curcumin in rat model of sporadic dementia of Alzheimer’s type (SDAT). Eur Neuropsychopharmacol. 2009;19:636–47.CrossRefPubMed Ishrat T, Hoda MN, Khan MB, Yousuf S, Ahmad M, Khan MM, et al. Amelioration of cognitive deficits and neurodegeneration by curcumin in rat model of sporadic dementia of Alzheimer’s type (SDAT). Eur Neuropsychopharmacol. 2009;19:636–47.CrossRefPubMed
27.
go back to reference Yadav RS, Chandravanshi LP, Shukla RK, Sankhwar ML, Ansari RW, Shukla PK, et al. Neuroprotective efficacy of curcumin in arsenic induced cholinergic dysfunctions in rats. Neurotoxicology. 2011;32:760–8.CrossRefPubMed Yadav RS, Chandravanshi LP, Shukla RK, Sankhwar ML, Ansari RW, Shukla PK, et al. Neuroprotective efficacy of curcumin in arsenic induced cholinergic dysfunctions in rats. Neurotoxicology. 2011;32:760–8.CrossRefPubMed
28.
go back to reference Tong B, Yuan X, Dou Y, Wu X, Wang Y, Xia Y, et al. Sinomenine induces the generation of intestinal Treg cells and attenuates arthritis via activation of aryl hydrocarbon receptor. Lab Investig. 2016;96:1076–86.CrossRefPubMed Tong B, Yuan X, Dou Y, Wu X, Wang Y, Xia Y, et al. Sinomenine induces the generation of intestinal Treg cells and attenuates arthritis via activation of aryl hydrocarbon receptor. Lab Investig. 2016;96:1076–86.CrossRefPubMed
29.
go back to reference van Maanen MA, Lebre MC, van der Poll T, LaRosa GJ, Elbaum D, Vervoordeldonk MJ, et al. Stimulation of nicotinic acetylcholine receptors attenuates collagen-induced arthritis in mice. Arthritis Rheum. 2009;60:114–22.CrossRefPubMed van Maanen MA, Lebre MC, van der Poll T, LaRosa GJ, Elbaum D, Vervoordeldonk MJ, et al. Stimulation of nicotinic acetylcholine receptors attenuates collagen-induced arthritis in mice. Arthritis Rheum. 2009;60:114–22.CrossRefPubMed
30.
go back to reference Matsumoto S, Yoshida S, Ikeda M, Kadoi J, Takahashi M, Tanimoto T, et al. Effects of acetazolamide on transient K+ currents and action potentials in nodose ganglion neurons of adult rats. CNS Neurosci Ther. 2011;17:66–79.CrossRefPubMedPubMedCentral Matsumoto S, Yoshida S, Ikeda M, Kadoi J, Takahashi M, Tanimoto T, et al. Effects of acetazolamide on transient K+ currents and action potentials in nodose ganglion neurons of adult rats. CNS Neurosci Ther. 2011;17:66–79.CrossRefPubMedPubMedCentral
31.
go back to reference HJ H, Carrasquillo Y, Karim F, Jung WE, Nerbonne JM, Schwarz TL, et al. The kv4.2 potassium channel subunit is required for pain plasticity. Neuron. 2006;50:89–100.CrossRef HJ H, Carrasquillo Y, Karim F, Jung WE, Nerbonne JM, Schwarz TL, et al. The kv4.2 potassium channel subunit is required for pain plasticity. Neuron. 2006;50:89–100.CrossRef
32.
go back to reference Koopman FA, Chavan SS, Miljko S, Grazio S, Sokolovic S, Schuurman PR, et al. Vagus nerve stimulation inhibits cytokine production and attenuates disease severity in rheumatoid arthritis. Proc Natl Acad Sci U S A. 2016;113:8284–9.CrossRefPubMedPubMedCentral Koopman FA, Chavan SS, Miljko S, Grazio S, Sokolovic S, Schuurman PR, et al. Vagus nerve stimulation inhibits cytokine production and attenuates disease severity in rheumatoid arthritis. Proc Natl Acad Sci U S A. 2016;113:8284–9.CrossRefPubMedPubMedCentral
33.
go back to reference Koopman FA, van Maanen MA, Vervoordeldonk MJ, Tak PP. Balancing the autonomic nervous system to reduce inflammation in rheumatoid arthritis. J Intern Med. 2017;282:64–75.CrossRefPubMed Koopman FA, van Maanen MA, Vervoordeldonk MJ, Tak PP. Balancing the autonomic nervous system to reduce inflammation in rheumatoid arthritis. J Intern Med. 2017;282:64–75.CrossRefPubMed
34.
go back to reference Huston JM, Tracey KJ. The pulse of inflammation: heart rate variability, the cholinergic anti-inflammatory pathway and implications for therapy. J Intern Med. 2011;269:45–53.CrossRefPubMedPubMedCentral Huston JM, Tracey KJ. The pulse of inflammation: heart rate variability, the cholinergic anti-inflammatory pathway and implications for therapy. J Intern Med. 2011;269:45–53.CrossRefPubMedPubMedCentral
35.
go back to reference Prado VF, Roy A, Kolisnyk B, Gros R, Prado MA. Regulation of cholinergic activity by the vesicular acetylcholine transporter. Biochem J. 2013;450:265–74.CrossRefPubMed Prado VF, Roy A, Kolisnyk B, Gros R, Prado MA. Regulation of cholinergic activity by the vesicular acetylcholine transporter. Biochem J. 2013;450:265–74.CrossRefPubMed
36.
go back to reference Ulloa L. The vagus nerve and the nicotinic anti-inflammatory pathway. Nat Rev Drug Discov. 2005;4:673–84.CrossRefPubMed Ulloa L. The vagus nerve and the nicotinic anti-inflammatory pathway. Nat Rev Drug Discov. 2005;4:673–84.CrossRefPubMed
37.
go back to reference Bernik TR, Friedman SG, Ochani M, DiRaimo R, Ulloa L, Yang H, et al. Pharmacological stimulation of the cholinergic antiinflammatory pathway. J Exp Med. 2002;195:781–8.CrossRefPubMedPubMedCentral Bernik TR, Friedman SG, Ochani M, DiRaimo R, Ulloa L, Yang H, et al. Pharmacological stimulation of the cholinergic antiinflammatory pathway. J Exp Med. 2002;195:781–8.CrossRefPubMedPubMedCentral
38.
go back to reference Zhao X, Ye J, Sun Q, Xiong Y, Li R, Jiang Y. Antinociceptive effect of spirocyclopiperazinium salt compound LXM-15 via activating peripheral α7 nAChR and M4 mAChR in mice. Neuropharmacology. 2011;60:446–52.CrossRefPubMed Zhao X, Ye J, Sun Q, Xiong Y, Li R, Jiang Y. Antinociceptive effect of spirocyclopiperazinium salt compound LXM-15 via activating peripheral α7 nAChR and M4 mAChR in mice. Neuropharmacology. 2011;60:446–52.CrossRefPubMed
39.
go back to reference Liao KP, Costenbader KH. Getting them even earlier: identifying individuals before clinical presentation with rheumatoid arthritis. Arthritis Rheum. 2009;61:1620–2.CrossRefPubMedPubMedCentral Liao KP, Costenbader KH. Getting them even earlier: identifying individuals before clinical presentation with rheumatoid arthritis. Arthritis Rheum. 2009;61:1620–2.CrossRefPubMedPubMedCentral
40.
41.
go back to reference Steinman L. Elaborate interactions between the immune and nervous systems. Nat Immunol. 2004;5:575–81.CrossRefPubMed Steinman L. Elaborate interactions between the immune and nervous systems. Nat Immunol. 2004;5:575–81.CrossRefPubMed
43.
go back to reference Koopman FA, Stoof SP, Straub RH, Van Maanen MA, Vervoordeldonk MJ, Tak PP. Restoring the balance of the autonomic nervous system as an innovative approach to the treatment of rheumatoid arthritis. Mol Med. 2011;17:937–48.CrossRefPubMedPubMedCentral Koopman FA, Stoof SP, Straub RH, Van Maanen MA, Vervoordeldonk MJ, Tak PP. Restoring the balance of the autonomic nervous system as an innovative approach to the treatment of rheumatoid arthritis. Mol Med. 2011;17:937–48.CrossRefPubMedPubMedCentral
44.
go back to reference Bonaz B, Sinniger V, Pellissier S. Vagus nerve stimulation: a new promising therapeutic tool in inflammatory bowel disease. J Intern Med. 2017;282:46–63.CrossRefPubMed Bonaz B, Sinniger V, Pellissier S. Vagus nerve stimulation: a new promising therapeutic tool in inflammatory bowel disease. J Intern Med. 2017;282:46–63.CrossRefPubMed
45.
go back to reference Bonaz B, Sinniger V, Hoffmann D, Clarençon D, Mathieu N, Dantzer C, et al. Chronic vagus nerve stimulation in Crohn’s disease: a 6-month follow-up pilot study. Neurogastroenterol Motil. 2016;28:948–53.CrossRefPubMed Bonaz B, Sinniger V, Hoffmann D, Clarençon D, Mathieu N, Dantzer C, et al. Chronic vagus nerve stimulation in Crohn’s disease: a 6-month follow-up pilot study. Neurogastroenterol Motil. 2016;28:948–53.CrossRefPubMed
46.
go back to reference Jin H, Guo J, Liu J, Lyu B, Foreman RD, Yin J, et al. Anti-inflammatory effects and mechanisms of vagal nerve stimulation combined with electroacupuncture in a rodent model of TNBS-induced colitis. Am J Physiol Gastrointest Liver Physiol. 2017;313:G192–202.CrossRefPubMed Jin H, Guo J, Liu J, Lyu B, Foreman RD, Yin J, et al. Anti-inflammatory effects and mechanisms of vagal nerve stimulation combined with electroacupuncture in a rodent model of TNBS-induced colitis. Am J Physiol Gastrointest Liver Physiol. 2017;313:G192–202.CrossRefPubMed
48.
go back to reference Borovikova LV, Ivanova S, Zhang M, Yang H, Botchkina GI, Watkins LR, et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature. 2000;405:458–62.CrossRefPubMed Borovikova LV, Ivanova S, Zhang M, Yang H, Botchkina GI, Watkins LR, et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature. 2000;405:458–62.CrossRefPubMed
49.
go back to reference van Maanen MA, Stoof SP, Larosa GJ, Vervoordeldonk MJ, Tak PP. Role of the cholinergic nervous system in rheumatoid arthritis: aggravation of arthritis in nicotinic acetylcholine receptor α7 subunit gene knockout mice. Ann Rheum Dis. 2010;69:1717–23.CrossRefPubMed van Maanen MA, Stoof SP, Larosa GJ, Vervoordeldonk MJ, Tak PP. Role of the cholinergic nervous system in rheumatoid arthritis: aggravation of arthritis in nicotinic acetylcholine receptor α7 subunit gene knockout mice. Ann Rheum Dis. 2010;69:1717–23.CrossRefPubMed
50.
go back to reference Yamakawa K, Matsumoto N, Imamura Y, Muroya T, Yamada T, Nakagawa J, et al. Electrical vagus nerve stimulation attenuates systemic inflammation and improves survival in a rat heatstroke model. PLoS One. 2013;8:e56728.CrossRefPubMedPubMedCentral Yamakawa K, Matsumoto N, Imamura Y, Muroya T, Yamada T, Nakagawa J, et al. Electrical vagus nerve stimulation attenuates systemic inflammation and improves survival in a rat heatstroke model. PLoS One. 2013;8:e56728.CrossRefPubMedPubMedCentral
51.
go back to reference Wang PY, Caspi L, Lam CK, Chari M, Li X, Light PE, et al. Upper intestinal lipids trigger a gut-brain-liver axis to regulate glucose production. Nature. 2008;452:1012–6.CrossRefPubMed Wang PY, Caspi L, Lam CK, Chari M, Li X, Light PE, et al. Upper intestinal lipids trigger a gut-brain-liver axis to regulate glucose production. Nature. 2008;452:1012–6.CrossRefPubMed
52.
go back to reference Duca FA, Côté CD, Rasmussen BA, Zadeh-Tahmasebi M, Rutter GA, Filippi BM, et al. Metformin activates a duodenal Ampk-dependent pathway to lower hepatic glucose production in rats. Nat Med. 2015;21:506–11.CrossRefPubMed Duca FA, Côté CD, Rasmussen BA, Zadeh-Tahmasebi M, Rutter GA, Filippi BM, et al. Metformin activates a duodenal Ampk-dependent pathway to lower hepatic glucose production in rats. Nat Med. 2015;21:506–11.CrossRefPubMed
53.
go back to reference Zhang Z, Chen Y, Xiang L, Wang Z, Xiao GG, Hu J. Effect of curcumin on the diversity of gut microbiota in ovariectomized rats. Nutrients. 2017;9:1146. Zhang Z, Chen Y, Xiang L, Wang Z, Xiao GG, Hu J. Effect of curcumin on the diversity of gut microbiota in ovariectomized rats. Nutrients. 2017;9:1146.
54.
go back to reference Shen L, Liu L, Ji HF. Regulative effects of curcumin spice administration on gut microbiota and its pharmacological implications. Food Nutr Res. 2017;61:1361780.CrossRefPubMedPubMedCentral Shen L, Liu L, Ji HF. Regulative effects of curcumin spice administration on gut microbiota and its pharmacological implications. Food Nutr Res. 2017;61:1361780.CrossRefPubMedPubMedCentral
55.
go back to reference Feng W, Wang H, Zhang P, Gao C, Tao J, Ge Z, et al. Modulation of gut microbiota contributes to curcumin-mediated attenuation of hepatic steatosis in rats. Biochim Biophys Acta. 1861;2017:1801–12. Feng W, Wang H, Zhang P, Gao C, Tao J, Ge Z, et al. Modulation of gut microbiota contributes to curcumin-mediated attenuation of hepatic steatosis in rats. Biochim Biophys Acta. 1861;2017:1801–12.
56.
go back to reference McFadden RM, Larmonier CB, Shehab KW, Midura-Kiela M, Ramalingam R, Harrison CA, et al. The role of curcumin in modulating colonic microbiota during colitis and colon cancer prevention. Inflamm Bowel Dis. 2015;21:2483–94.CrossRefPubMedPubMedCentral McFadden RM, Larmonier CB, Shehab KW, Midura-Kiela M, Ramalingam R, Harrison CA, et al. The role of curcumin in modulating colonic microbiota during colitis and colon cancer prevention. Inflamm Bowel Dis. 2015;21:2483–94.CrossRefPubMedPubMedCentral
57.
go back to reference Horta-Baas G, Romero-Figueroa MDS, Montiel-Jarquín AJ, Pizano-Zárate ML, García-Mena J, Ramírez-Durán N. Intestinal dysbiosis and rheumatoid arthritis: a link between gut microbiota and the pathogenesis of rheumatoid arthritis. J Immunol Res. 2017;2017:4835189.CrossRefPubMedPubMedCentral Horta-Baas G, Romero-Figueroa MDS, Montiel-Jarquín AJ, Pizano-Zárate ML, García-Mena J, Ramírez-Durán N. Intestinal dysbiosis and rheumatoid arthritis: a link between gut microbiota and the pathogenesis of rheumatoid arthritis. J Immunol Res. 2017;2017:4835189.CrossRefPubMedPubMedCentral
58.
go back to reference Pianta A, Arvikar S, Strle K, Drouin EE, Wang Q, Costello CE, et al. Evidence of the immune relevance of Prevotella copri, a gut microbe, in patients with rheumatoid arthritis. Arthritis Rheumatol. 2017;69(5):964–75.CrossRefPubMed Pianta A, Arvikar S, Strle K, Drouin EE, Wang Q, Costello CE, et al. Evidence of the immune relevance of Prevotella copri, a gut microbe, in patients with rheumatoid arthritis. Arthritis Rheumatol. 2017;69(5):964–75.CrossRefPubMed
59.
go back to reference Maeda Y, Takeda K. Role of gut microbiota in rheumatoid arthritis. J Clin Med. 2017;6. Maeda Y, Takeda K. Role of gut microbiota in rheumatoid arthritis. J Clin Med. 2017;6.
Metadata
Title
Curcumin attenuates collagen-induced inflammatory response through the “gut-brain axis”
Authors
Yannong Dou
Jinque Luo
Xin Wu
Zhifeng Wei
Bei Tong
Juntao Yu
Ting Wang
Xinyu Zhang
Yan Yang
Xusheng Yuan
Peng Zhao
Yufeng Xia
Huijuan Hu
Yue Dai
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Journal of Neuroinflammation / Issue 1/2018
Electronic ISSN: 1742-2094
DOI
https://doi.org/10.1186/s12974-017-1047-7

Other articles of this Issue 1/2018

Journal of Neuroinflammation 1/2018 Go to the issue