Skip to main content

Advertisement

SpringerLink
Log in

Low-dose curcumin reduced TNBS-associated mucin depleted foci in mice by scavenging superoxide anion and lipid peroxides, rebalancing matrix NO synthase and aconitase activities, and recoupling mitochondria

  • Original Article
  • Published:
Inflammopharmacology Aims and scope Submit manuscript

Abstract

Background

The role of mitochondrial dysfunction in the pathogenesis of inflammatory bowel diseases (IBD) is still being investigated. This study evaluated the therapeutic effect of curcumin (Cur), a polyphenolic electrophile in 2,4,6-trinitrobenzene sulfonic acid (TNBS)-induced chronic colitis and mitochondrial dysfunction, in mice.

Methods

Colitis was induced by rectal instillation to mice of 30 mg kg−1 TNBS, alone or followed by daily intraperitoneal injections of Cur 25 mg kg−1. Animals were euthanized at days 3, 7, and 14, post TNBS challenge. Colon mitochondria of control mice were treated with 5 µM Cur, and TNBS (50, 100 µM)-toxicity was evaluated by measuring swelling, respiration, and aconitase and fumarase activities. Redox status was evaluated in colon mucosa and in mitochondria.

Results

In vitro, a short-term Cur treatment controlled the dose and time dependent mitochondrial toxicity induced by TNBS, by collapsing the generation of superoxide anion and hydroperoxy lipids, rebalancing nitric oxide synthase and aconitase activities, and recoupling mitochondria. In vivo, a daily low-dose Cur abolished mice mortality which reached 27% in model group. Cur improved in a time dependent manner mucosal redox homeostasis, cell apoptosis, mucin depleted crypts and crypt abscesses by controlling prooxidant activity of myeloperoxidase and NO synthase associated to phagocytes influx, quenching hydroperoxy lipids, and reboosting GSH levels.

Conclusion

Cur, by quenching intra and extra mitochondrial ROS generation, rebalancing aconitase/fumarase and MDA/GSH ratios, and recoupling mitochondria, may support mithormesis priming and remitting in IBD.

Graphic abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

CD:

Crohn’s disease

Cul3:

Cullin3-based Cullin-RING E3 ubiquitin ligase

Cur:

Curcumin

ARE/EpRE:

Antioxidant response element/electrophile response element

ETC:

Electron transfer chain; GSH, reduced glutathione

IBD:

Inflammatory bowel diseases

I(O)MM:

Inner (outer) mitochondrial membrane

iNOS:

Inducible NO synthase

Keap1:

Kelch-like ECH associated protein 1

MDA:

Malondialdehyde

MPO:

Myeloperoxidase

mPTP:

Mitochondrial permeability transition pore

NO:

Nitric oxide

NOX2:

NADPH Oxidase2

O2·− :

Superoxide anion

NRF2:

Nuclear factor (erythroid-derived 2)-like 2

OxPhos:

Oxidative phosphorylation

mt:

Mitochondria

PN:

Neutrophils

ROS:

Reactive oxygen species

TNBS:

2,4,6-Trinitrobenzene sulfonic acid

References

  • Aggarwal BB, Gupta SC, Sung B (2013) Curcumin: an orally bioavailable blocker of TNF and other pro-inflammatory biomarkers. Br J Pharmacol 169:1672–1692

    CAS  PubMed  PubMed Central  Google Scholar 

  • Aggarwal BB, Deb L, Prasad S (2015) Curcumin differs from tetrahydrocurcumin for molecular targets, signaling pathways and cellular responses. Molecules 20:185–205

    Google Scholar 

  • Aviello G, Knaus UG (2016) ROS in gastrointestinal inflammation: rescue ? Br J Pharmacol 174:1704–1718

    PubMed  PubMed Central  Google Scholar 

  • Awasthi S, Pandya U, Singhal SS, Lin JT, Thiviyanathan V, Seifert WE et al (2000) Curcumin-glutathione interactions and the role of human glutathione S-transferase P1–1. Chem-Biol Interact 128:19–38

    CAS  PubMed  Google Scholar 

  • Balogun E, Hoque M, Gong P, Killeen E, Green CJ, Foresti R et al (2003) Curcumin activates the haemoxygenase-1gene via regulation of Nrf2 and the antioxidant-responsive element. Biochem J 371:887–895

    CAS  PubMed  PubMed Central  Google Scholar 

  • Beltrán B, Nos P, Dasi F, Iborra M, Bastida G, Martínez M et al (2010) Mitochondrial dysfunction, persistent oxidative damage, and catalase inhibition in immune cells of naïve and treated Crohn’s disease. Inflamm Bowel Dis 16:76–86

    PubMed  Google Scholar 

  • Bernardi P, Rasola A, Forte M, Lippe G (2015) The mitochondrial permeability transition pore: channel formation by F-ATP synthase, integration in signal transduction, and role in pathophysiology. Physiol Rev 95(4):1111–1155

    PubMed  PubMed Central  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of proteins utilizing the protein-dye binding. Anal Biochem 72:248–252

    CAS  Google Scholar 

  • Brand MD (2016) Mitochondrial generation of superoxide and hydrogen peroxide as the source of mitochondrial redox signaling. Free Radic Biol Med 100:14–31

    CAS  PubMed  Google Scholar 

  • Brown GC, Borutaite V (2004) Inhibition of mitochondrial respiratory complex I by nitricoxide, peroxynitrite and S-nitrosothiols. Biochim Biophys Acta 1658:44–54

    CAS  PubMed  Google Scholar 

  • Capasso R, Borrelli F, Cascio MG, Aviello G, Huben K, Zjawiony JK et al (2008) Inhibitory effect of salvinorin A, from Salvia divinorum, on ileitis-induced hypermotility: cross-talk between kappa-opioid and cannabinoid CB(1) receptors. Br J Pharmacol. 155(5):681–689

    CAS  PubMed  PubMed Central  Google Scholar 

  • Capasso R, Orlando P, Pagano E, Aveta T, Buono L, Borrelli F et al (2014) Palmitoylethanolamide normalizes intestinal motility in a model of post-inflammatory accelerated transit: involvement of CB1 receptors and TRPV1 channels. Br J Pharmacol 171(17):4026–4037

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chamulitrat W (1999) Desulfonation of a colitis inducer 2,4,6-trinitrobenzene sulfonic acid produces sulfite radical. Biochim Biophys Acta 1472(1–2):368–375

    CAS  PubMed  Google Scholar 

  • Chen JJ, Yu BP (1994) Alterations in mitochondrial membrane fluidity by lipid peroxidation products. Free Radic Biol Med 17:411–418

    CAS  PubMed  Google Scholar 

  • Chen XJ, Wang X, Kaufman BA, Butow RA (2005) Aconitase couples metabolic regulation to mitochondrial DNA maintenance. Science 307:714–717

    CAS  PubMed  Google Scholar 

  • Chen W, Luo S, Xie P, Hou T, Yu T, Fu X (2018) Overexpressed UCP2 regulates mitochondrial flashes and reverses lipopolysaccharide-induced cardiomyocytes injury. Am J Transl Res 10(5):1347–1356

    CAS  PubMed  PubMed Central  Google Scholar 

  • Circu ML, Aw TY (2011) Redox biology of the intestine. Free Radic Res 45:1245–1266

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cox AG, Winterbourn CC, Hampton MB (2009) Mitochondrial peroxiredoxin involvement in antioxidant defence and redox signalling. Biochem J 425:313–325

    PubMed  Google Scholar 

  • Dinkova-Kostova AT, Holtzclaw WD, Wakabayashi N (2005) Keap1, the sensor for electrophiles and oxidants that regulates the phase 2 response, is a zinc metalloprotein. Biochemistry 44:6889–6899

    CAS  PubMed  Google Scholar 

  • Edwards RL, Luis PB, Varuzza PV, Joseph AI, Presley SH, Chaturvedi R, Schneider C (2017) The anti-inflammatory activity of curcumin is mediated by its oxidative metabolites. J Biol Chem 292:21243–21252

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ellman G (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82(1):70–77

    CAS  PubMed  Google Scholar 

  • Fedorak R, Empey L, Walker K (1992) Verapamil alters eicosanoid synthesis and accelerates healing during experimental colitis in rats. Gastroenterology 102:1229–1235

    CAS  PubMed  Google Scholar 

  • Femia AP, Bendinelli B, Giannini A, Salvadori M, Pinzani P, Dolara P, Caderni G (2005) Mucin-depleted foci have b-catenin genes mutations, altered expression of its protein and are dose-and time-dependent in the colon of 1,2-dimethylhydrazine-treated rats. Int J Cancer 116(1):9–15

    CAS  PubMed  Google Scholar 

  • Forman N, Wilson D (1982) Energetics and stoichiometry of oxidative phosphorylation from NADH to cytochrome c in isolated rat liver mitochondria. J Biol Chem 25:12908–12915

    Google Scholar 

  • Forman HJ, Davies KJA, Fulvio Ursini F (2014) How do nutritional antioxidants really work: nucleophilic tone and para-hormesis versus free radical scavenging in vivo. Free Radic Biol Med 66:24–25

    CAS  PubMed  Google Scholar 

  • Glebov OK, Rodriguez LM, Nakahara K, Jenkins J, Cliatt J, Humbyrd CJ et al (2003) Distinguishing right from left colon by the pattern of gene expression. Cancer Epidemiol Biomarkers Prev 12:755–762

    CAS  PubMed  Google Scholar 

  • Green LC, Wagner DA, Glogowski J, Skiper PL, Wishnock JS, Tannenbaum SR (1982) Analysis of nitrate, nitrite and [15 N] nitrate in biological fluids. Anal Biochem 126:131–138

    CAS  PubMed  Google Scholar 

  • Grisham MB, Volkmer C, Tso P, Yamada T (1991) Metabolism of trinitrobenzene sulfonic acid by the rat colon produces reactive oxygen species. Gastroenterology 101:540–547

    CAS  PubMed  Google Scholar 

  • Grossi V, Hyams JS, Glidden NC, Knight BE, Young EE (2019) Characterizing clinical features and creating a gene expression profile associated with pain burden in children with inflammatory bowel disease. Inflamm Bowel Dis. https://doi.org/10.1093/ibd/izz240

    Article  PubMed  Google Scholar 

  • Handy DE, Loscalzo J (2012) Redox regulation of mitochondrial function. Antioxid Redox Signal 16(11):1323–1367

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hausladen A, Firdovich I (1996) Measuring nitric oxide and superoxide: rate constants for aconitase reactivity. Met Enzymol 269:37–41

    CAS  Google Scholar 

  • Heger M, van Golen RF, Broekgaarden M, Michel MC (2013) The molecular basis for the pharmacokinetics and pharmacodynamics of curcumin and its metabolites in relation to cancer. Pharmacol Rev 66:222–307

    PubMed  Google Scholar 

  • Hennig P, Garstkiewicz M, Grossi S, Michela Di Filippo M, French LE, Beer HD (2018) The crosstalk between Nrf2 and inflammasomes. Int J Mol Sci 19:562

    PubMed Central  Google Scholar 

  • Hölttä V, Klemetti P, Sipponen T, Westerholm-Ormio M, Kociubinski G, Salo H et al (2008) IL-23/IL-17 immunity as a hallmark of Crohn's disease. Inflamm Bowel Dis 14(9):1175–1184

    PubMed  Google Scholar 

  • Houten SM, Wanders RJA (2010) A general introduction to the biochemistry of mitochondrial fatty acid β-oxidation. J Inherit Metab Dis 33:469–477

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huang J, Peng W, Zheng Y, Hao H, Li S, Yao Y, et al (2019) Upregulation of UCP2 expression protects against lps-induced oxidative stress and apoptosis in cardiomyocytes. Oxidat Med Cellular Longev 2019:articleID 2758262

  • Izem-Meziane I, Djerdjouri B, Rimbaud S, Caffin F, Fortin D, Garnier A et al (2012) Catecholamine-induced cardiac mitochondrial dysfunction and mPTP opening: protective effect of curcumin. Am J Physiol Heart Circ Physiol 302:H665–H674

    CAS  PubMed  Google Scholar 

  • Jiao Y, Wilkinson J, Pietsch CE, BussJ L, Wang W, Planalp R et al (2006) Iron chelation in the biological activity of curcumin. Free Radic Biol Med 40:1152–1160

    CAS  PubMed  Google Scholar 

  • Kanai AJ, Pearce LL, Clemens PR, Birder LA, Van Bibber MM, Choi SY et al (2001) Identification of a neuronal nitric oxide synthase in isolated cardiac mitochondria using electrochemical detection. Proc Natl Acad Sci USA 98(24):14126–14131

    CAS  PubMed  Google Scholar 

  • Kaulmann A, Bohn T (2016) Bioactivity of polyphenols: preventive and adjuvant strategies toward reducing inflammatory bowel diseases-promises, perspectives and pitfalls. Oxid Med Cell Longev 2016:9346470

    PubMed  PubMed Central  Google Scholar 

  • Krawisz JE, Sharon P, Stenson WF (1984) Quantification assay for acute intestinal inflammation based on myeloperoxidase activity. Gastroenterology 87:1344–1350

    CAS  PubMed  Google Scholar 

  • Kunnumakkara AB, Bordoloi D, Padmavathi G, Monisha J, Roy NK, Prasad S, Aggarwal BB (2017) Curcumin, the golden nutraceutical: multi targeting for multiple chronic diseases. Br J Pharmacol 174(11):1325–1348

    CAS  PubMed  Google Scholar 

  • Kuznetsov A, Gnaiger E (2003) Complex I (NADH: Ubiquinone oxidoreductase, EC 1.6.5.3) mitochondrial membrane enzyme. MiT Net 8(15):1–8

    Google Scholar 

  • Lewis K, McKay DM (2009) Metabolic stress evokes decreases in epithelial barrier function. Ann NY Acad Sci USA 1165:327–337

    Google Scholar 

  • Li W, Kong AN (2009) Molecular mechanisms of Nrf2-mediated antioxidant response. Mol Carcinog 48:91–104

    CAS  PubMed  PubMed Central  Google Scholar 

  • Luis PB, Gordon ON, Nakashima F, Joseph AI, Shibata T, Uchida K et al (2017) Oxidative metabolism of curcumin-glucuronide by peroxidases and isolated human leukocytes. Biochem. Pharmacol 132:143–149

    CAS  PubMed  PubMed Central  Google Scholar 

  • Masubuchi Y, Nakayama S, Horie T (2002) Role of mitochondrial permeability transition in diclofenac–induced hepatocyte injury in rats. Hepatology 35:544–551

    CAS  PubMed  Google Scholar 

  • Millar SA, Stone NL, Bellman ZD, Yates AS, England TJ, O'Sullivan SE (2019) A systematic review of cannabidiol dosing in clinical populations. Br J Clin Pharmacol 85:1888–1900

    CAS  PubMed  PubMed Central  Google Scholar 

  • Morris GP, Beck PL, Herridge MS, Depew WT, Szewczuk MR, Wallace JL (1989) Hapten-induced model of chronic inflammation and ulceration in the rat colon. Gastroenterology 96:795–803

    CAS  PubMed  Google Scholar 

  • Mouzaoui S, Rahim I, Djerdjouri B (2012) Aminoguanidine and curcumin attenuated tumor necrosis factor (TNF)-α-induced oxidative stress, colitis and hepatotoxicity in mice. Int Immunopharmacol 12:302–311

    CAS  PubMed  Google Scholar 

  • Murphy MP (2009) How mitochondria produce reactive oxygen species. Biochem J 417(1):1–13

    CAS  PubMed  Google Scholar 

  • Nazli A, Yang PC, Jury J, Howe K, Watson JL, Söderholm JD et al (2004) Epithelia under metabolic stress perceive commensal bacteria as a threat. Am J Pathol 164:947–957

    PubMed  PubMed Central  Google Scholar 

  • Neurath M, Fuss I, Kelasall B, Stuber E, Strober W (1995) Antibodies to interleukin-12 abrogate established experimental colitis in mice. J Exp Med 182:1281–1290

    CAS  PubMed  Google Scholar 

  • Novak EA, Mollen KP (2015) Mitochondrial dysfunction in inflammatory bowel disease. Front Cell Dev Biol 3:62

    PubMed  PubMed Central  Google Scholar 

  • Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358

    CAS  Google Scholar 

  • Ohtani H, Katoh H, Tanaka T, Saotome M, Urushida T, Satoh H et al (2012) Effects of nitric oxide on mitochondrial permeability transition pore and thiol mediated responses in cardiac myocytes. Nitric Oxide 26:95–101

    CAS  PubMed  Google Scholar 

  • Packiriswamy N, Coulson KF, Holcombe SJ, Sordillo LM (2017) Oxidative stress-induced mitochondrial dysfunction in a normal colon epithelial cell line. World J Gastroenterol 23(19):3427–3439

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pagano E, Capasso R, Piscitelli F, Romano B, Parisi OA, Finizio S et al (2016) An orally active cannabis extract with high content in cannabidiol attenuates chemically-induced intestinal inflammation and hypermotility in the mouse. Front Pharmacol 4(7):341

    Google Scholar 

  • Pagano E, Romano B, Iannotti FA, Parisi OA, D'Armiento M, Pignatiello S et al (2019) The non-euphoric phytocannabinoid cannabidivarin counteracts intestinal inflammation in mice and cytokine expression in biopsies from UC pediatric patients. Pharmacol Res 22:104464

    Google Scholar 

  • Peng Y, Junliang PuJ, Tang C, Wu Z (2017) Curcumin inhibits heat-induced apoptosis by suppressing NADPH oxidase 2 and activating the Akt/mTOR signaling pathway in bronchial epithelial cells. Cell Physiol Biochem 41:2091–2103

    CAS  PubMed  Google Scholar 

  • Pfeiffer K, Gohil V, Stuart RA, Hunte C, Brandt U, Greenberg ML, Schagger H (2003) Cardiolipin stabilizes respiratory chain supercomplexes. J Biol Chem 278:52873–52880

    CAS  PubMed  Google Scholar 

  • Priyadarsini KI, Maity DK, Naik GH, Kumar MS, Unnikrishnan MK, Satav JG, Mohan H (2003) Role of phenolic OH and methylene hydrogen on the free radical reactions and antioxidant activity of curcumin. Free Radic Biol Med 35:475–484

    CAS  PubMed  Google Scholar 

  • Racker E (1950) Spectrophotometric measurements of the enzymatic formation of fumaric and cis-aconitic acids. Biochim Biophys Acta 4(1–3):211–214

    CAS  PubMed  Google Scholar 

  • Saha S, Adhikarya A, Bhattacharyya P, Das T, Sa G (2012) Death by design: where curcumin sensitizes drug-resistant tumours. Anticancer Res 32(7):2567–2584

    CAS  PubMed  Google Scholar 

  • Sakai E, Morioka T, Yamada E, Ohkubo H, Higurashi T, Hosono K et al (2012) Identification of preneoplastic lesions as mucin-depleted foci in patients with sporadic colorectal cancer. Cancer Sci 103:144–149

    CAS  PubMed  Google Scholar 

  • Sharpley MS, Shannon RJ, Draghi F, Hirst J (2006) Interactions between phospholipids and NADH:ubiquinone oxidoreductase (complex I) from bovine mitochondria. Biochemistry 45:241–248

    CAS  PubMed  Google Scholar 

  • Sifroni KG, Damiani CR, Stoffel C, Cardoso MR, Ferreira IC, Rezin GT et al (2010) Mitochondrial respiratory chain in the colonic mucosal of patients with ulcerative colitis. Mol Cell Biochem 342:111–115

    CAS  PubMed  Google Scholar 

  • Spinelli JB, Haigis MC (2018) The multifaceted contributions of mitochondria to cellular metabolism. Nat Cell Biol 20(7):745–754

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun Y, Mironova V, Chen Y, Lundh EPF, Zhang Q, Cai Y, et al (2020) Molecular pathway analysis indicates a distinct metabolic phenotype in women with right-sided colon cancer. Trans Onc 13(1):42–56

  • Szebeni GJ, Nagy LI, Berkó A, Hoffmann A, Fehér LZ, Bagyánszki M et al (2019) The anti-inflammatory role of mannich curcuminoids: special focus on colitis. Molecules 24:1546. https://doi.org/10.3390/molecules24081546beni

    Article  CAS  PubMed Central  Google Scholar 

  • Titov DV, Cracan V, Goodman RP, Peng J, Grabarek Z, Mootha VK (2016) Complementation of mitochondrial electron transport chain by manipulation of the NAD+/NADH ratio. Science 352:231–235

    CAS  PubMed  PubMed Central  Google Scholar 

  • Towers N, Dixon H, Kellerman G, Linnane A (1972) Biogenesis of mitochondria. The sensitivity of rat liver mitochondria to antibiotics; a phylogenetics difference between a mammalian system and yeast. Anal Biochem Biophys 151:361–369

    CAS  Google Scholar 

  • Tu L, Chen J, Xu D, Xie Z, Yu B, Tao Y, Shi G, Duan L (2017) IL-33-induced alternatively activated macrophage attenuates the development of TNBS-induced colitis. Oncotarget 8(17):27704–27714

    PubMed  PubMed Central  Google Scholar 

  • Ukil A, Maity S, Karmakar S, Datta N, Vedasiromoni JR, Das PK (2003) Curcumin, the major component of food flavour turmeric, reduces mucosal injury in trinitrobenzene sulphonic acid-induced colitis. Br J Pharm 139:209–218

    CAS  Google Scholar 

  • Vozza A, Parisi G, De Leonardis F et al (2014) UCP2 transports C4 metabolites out of mitochondria, regulating glucose and glutamine oxidation. Proc Nat Acad Sci USA 111(3):960–965

    CAS  PubMed  Google Scholar 

  • Wang J, Pan MH, Cheng AL, Lin LI, Ho YS, Hsieh CY, Lin JK (1997) Stability of curcumin in buffer solutions and characterization of its degradation products. J Pharm Biomed Anal 15:1867–1876

    CAS  PubMed  Google Scholar 

  • Wang A, Keita AV, Phan V, McKay CM, Schoultz I, Lee J et al (2014) Targeting mitochondria-derived reactive oxygen species to reduce epithelial barrier dysfunction and colitis. Am J Pathol 184:2516–2527

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wei QY, Chen WF, Zhou B, YangL LZL (2006) Inhibition of lipid peroxidation and protein oxidation in rat liver mitochondria by curcumin and its analogues. Biochim Biophys Acta 1760:70–77

    CAS  PubMed  Google Scholar 

  • Wong HS, Dighe PA, Mezera V, Monternier PA, Brand MD (2017) Production of superoxide and hydrogen peroxide from specific mitochondrial sites under different bioenergetic conditions. J Biol Chem 292:16804–16809

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaoka T, Yan F, Hanwei C, Hobbs S, Dise RS, Tong W, Polik DB (2008) Transactivation of EGF receptor and ErbB2 protects intestinal epithelial cells from TNF-induced apoptosis. Proc Natl Acad Sci USA 105:11772–11777

    CAS  PubMed  Google Scholar 

  • Yin H, Zhu M (2012) Free radical oxidation of cardiolipin: chemical mechanisms, detection and implication in apoptosis, mitochondrial dysfunction and human diseases. Free Radic Res 46(8):959–974

    CAS  PubMed  Google Scholar 

  • Zádor F, Wollemann M (2015) Receptome: interactions between three pain-related receptors or the “Triumvirate” of cannabinoid, opioid and TRPV1 receptors. Pharmacol Res 102:254–263

    PubMed  Google Scholar 

  • Zorov DB, Juhaszova M, Sollott SJ (2014) Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol Rev 94(3):909–950

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are grateful to Dr Dang MC and Dr El Benna J from “the Laboratoire d'Excellence Inflamex”, Faculté de Médecine, Site Xavier Bichat, Paris, France, for the kind gift of TNBS.

Author information

Authors and Affiliations

  1. Laboratory of Cellular and Molecular Biology, Faculty of Biological Sciences, University of Sciences and Technology Houari Boumediene, Bab Ezzouar, Algiers, Algeria

    Souad Mouzaoui & Bahia Djerdjouri

  2. Department of Biology, Middle East Technical University, Ankara, Turkey

    Sreeparna Banerjee

Authors
  1. Souad Mouzaoui
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sreeparna Banerjee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bahia Djerdjouri
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bahia Djerdjouri.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mouzaoui, S., Banerjee, S. & Djerdjouri, B. Low-dose curcumin reduced TNBS-associated mucin depleted foci in mice by scavenging superoxide anion and lipid peroxides, rebalancing matrix NO synthase and aconitase activities, and recoupling mitochondria. Inflammopharmacol 28, 949–965 (2020). https://doi.org/10.1007/s10787-019-00684-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10787-019-00684-4

Keywords

Search

Navigation