The anti-inflammatory effect of dimethyl trisulfide in experimental acute pancreatitis.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
05 10 2023
05 10 2023
Historique:
received:
12
09
2022
accepted:
27
09
2023
medline:
2
11
2023
pubmed:
6
10
2023
entrez:
5
10
2023
Statut:
epublish
Résumé
Various organosulfur compounds, such as dimethyl trisulfide (DMTS), display anti-inflammatory properties. We aimed to examine the effects of DMTS on acute pancreatitis (AP) and its mechanism of action in both in vivo and in vitro studies. AP was induced in FVB/n mice or Wistar rats by caerulein, ethanol-palmitoleic acid, or L-ornithine-HCl. DMTS treatments were administered subcutaneously. AP severity was assessed by pancreatic histological scoring, pancreatic water content, and myeloperoxidase activity measurements. The behaviour of animals was followed. Pancreatic heat shock protein 72 (HSP72) expression, sulfide, and protein persulfidation were measured. In vitro acinar viability, intracellular Ca
Identifiants
pubmed: 37798377
doi: 10.1038/s41598-023-43692-9
pii: 10.1038/s41598-023-43692-9
pmc: PMC10556037
doi:
Substances chimiques
dimethyl trisulfide
3E691T3NL1
Sulfides
0
Antioxidants
0
Anti-Inflammatory Agents
0
Ceruletide
888Y08971B
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
16813Informations de copyright
© 2023. Springer Nature Limited.
Références
Peery, A. F. et al. Burden and cost of gastrointestinal, liver, and pancreatic diseases in the United States: Update 2018. Gastroenterology 156, 254-272.e11 (2019).
pubmed: 30315778
doi: 10.1053/j.gastro.2018.08.063
Roberts, S. E. et al. The incidence and aetiology of acute pancreatitis across Europe. Pancreatology 17, 155–165 (2017).
pubmed: 28159463
doi: 10.1016/j.pan.2017.01.005
Banks, P. A. et al. Classification of acute pancreatitis–2012: revision of the Atlanta classification and definitions by international consensus. Gut 62, 102–111 (2013).
pubmed: 23100216
doi: 10.1136/gutjnl-2012-302779
Forsmark, C. E., Vege, S. S. & Wilcox, C. M. Acute pancreatitis. New Engl J Medicine 375, 1972–1981 (2016).
doi: 10.1056/NEJMra1505202
Pallagi, P., Madácsy, T., Varga, Á. & Maléth, J. Intracellular Ca2+ signalling in the pathogenesis of acute pancreatitis: Recent advances and translational perspectives. Int J Mol Sci 21, 4005 (2020).
pubmed: 32503336
pmcid: 7312053
doi: 10.3390/ijms21114005
Saluja, A., Dudeja, V., Dawra, R. & Sah, R. P. Early intra-acinar events in pathogenesis of pancreatitis. Gastroenterology 156, 1979–1993 (2019).
pubmed: 30776339
doi: 10.1053/j.gastro.2019.01.268
Barreto, S. G. et al. Critical thresholds: key to unlocking the door to the prevention and specific treatments for acute pancreatitis. Gut 70, 194–203 (2021).
pubmed: 32973069
doi: 10.1136/gutjnl-2020-322163
Sendler, M. et al. Cathepsin B-mediated activation of trypsinogen in endocytosing macrophages increases severity of pancreatitis in mice. Gastroenterology 154, 704-718.e10 (2018).
pubmed: 29079517
doi: 10.1053/j.gastro.2017.10.018
Crockett, S. D. et al. American gastroenterological association institute guideline on initial management of acute pancreatitis. Gastroenterology 154, 1096–1101 (2018).
pubmed: 29409760
doi: 10.1053/j.gastro.2018.01.032
Rose, P., Moore, P. K. & Zhu, Y.-Z. Garlic and gaseous mediators. Trends Pharmacol Sci 39, 624–634 (2018).
pubmed: 29706261
doi: 10.1016/j.tips.2018.03.009
Koike, S., Ogasawara, Y., Shibuya, N., Kimura, H. & Ishii, K. Polysulfide exerts a protective effect against cytotoxicity caused by t-buthylhydroperoxide through Nrf2 signaling in neuroblastoma cells. Febs Lett 587, 3548–3555 (2013).
pubmed: 24055470
doi: 10.1016/j.febslet.2013.09.013
Wang, H., Shi, X., Qiu, M., Lv, S. & Liu, H. Hydrogen sulfide plays an important protective role through influencing endoplasmic reticulum stress in diseases. Int J Biol Sci 16, 264–271 (2020).
pubmed: 31929754
pmcid: 6949148
doi: 10.7150/ijbs.38143
Wallace, J. L. & Wang, R. Hydrogen sulfide-based therapeutics: exploiting a unique but ubiquitous gasotransmitter. Nat Rev Drug Discov 14, 329–345 (2015).
pubmed: 25849904
doi: 10.1038/nrd4433
Zanardo, R. C. O. et al. Hydrogen sulfide is an endogenous modulator of leukocyte-mediated inflammation. Faseb J 20, 2118–2120 (2006).
pubmed: 16912151
doi: 10.1096/fj.06-6270fje
Bhatia, M. & Gaddam, R. R. Hydrogen sulfide in inflammation: A novel mediator and therapeutic target. Antioxid Redox Sign 34, 1368–1377 (2021).
doi: 10.1089/ars.2020.8211
Marimuthu, M. K., Moorthy, A. & Ramasamy, T. Diallyl disulfide attenuates STAT3 and NF-κB pathway through PPAR-γ activation in cerulein-induced acute pancreatitis and associated lung injury in mice. Inflammation 45, 45–58 (2022).
pubmed: 35061151
doi: 10.1007/s10753-021-01527-7
Kumar, M. M. & Tamizhselvi, R. Protective effect of diallyl disulfide against cerulein-induced acute pancreatitis and associated lung injury in mice. Int Immunopharmacol 80, 106136 (2020).
doi: 10.1016/j.intimp.2019.106136
Sidhapuriwala, J. N., Hegde, A., Ang, A. D., Zhu, Y. Z. & Bhatia, M. Effects of S-propargyl-cysteine (SPRC) in caerulein-induced acute pancreatitis in mice. Plos One 7, e32574 (2012).
pubmed: 22396778
pmcid: 3291555
doi: 10.1371/journal.pone.0032574
Bhatia, M., Sidhapuriwala, J. N., Sparatore, A. & Moore, P. K. Treatment with h2s-releasing diclofenac protects mice against acute pancreatitis-associated lung injury. Shock 29, 84–88 (2008).
pubmed: 17621252
doi: 10.1097/shk.0b013e31806ec26
Dong, X., Kiss, L., Petrikovics, I. & Thompson, D. E. Reaction of dimethyl trisulfide with hemoglobin. Chem Res Toxicol 30, 1661–1663 (2017).
pubmed: 28809548
doi: 10.1021/acs.chemrestox.7b00181
Pozsgai, G. et al. Analgesic effect of dimethyl trisulfide in mice is mediated by TRPA1 and sst4 receptors. Nato Sci S A Lif Sci 65, 10–21 (2017).
Petrikovics, I. et al. Antidotal efficacies of the cyanide antidote candidate dimethyl trisulfide alone and in combination with cobinamide derivatives. Toxicol Mech Method 29, 1–24 (2019).
doi: 10.1080/15376516.2019.1585504
Bátai, I. Z. et al. Investigation of the role of the TRPA1 Ion channel in conveying the effect of dimethyl trisulfide on vascular and histological changes in serum-transfer arthritis. Pharm 15, 671 (2022).
Kissm, L. et al. From the cover. In vitro and in vivo blood-brain barrier penetration studies with the novel cyanide antidote candidate dimethyl trisulfide in mice. Toxicol Sci 160, 398–407 (2017).
doi: 10.1093/toxsci/kfx190
Ceppa, E. et al. Transient receptor potential ion channels V4 and A1 contribute to pancreatitis pain in mice. Am J Physiol-gastr L 299, G556–G571 (2010).
Kusiak, A. A. et al. Activation of pancreatic stellate cells attenuates intracellular Ca2+ signals due to downregulation of TRPA1 and protects against cell death induced by alcohol metabolites. Cell Death Dis 13, 744 (2022).
pubmed: 36038551
pmcid: 9421659
doi: 10.1038/s41419-022-05186-w
Kalyanaraman, B. et al. Measuring reactive oxygen and nitrogen species with fluorescent probes: Challenges and limitations. Free Radical Bio Med 52, 1–6 (2012).
doi: 10.1016/j.freeradbiomed.2011.09.030
Criddle, D. N. et al. Menadione-induced reactive oxygen species generation via redox cycling promotes apoptosis of murine pancreatic acinar cells*. J Biol Chem 281, 40485–40492 (2006).
pubmed: 17088248
doi: 10.1074/jbc.M607704200
Silva, D. D. et al. Intravascular residence time determination for the cyanide antidote dimethyl trisulfide in rat by using liquid-liquid extraction coupled with high performance liquid chromatography. J Anal Methods Chem 2016, 6546475 (2016).
pubmed: 28053802
pmcid: 5174746
doi: 10.1155/2016/6546475
Dong, Z. et al. Sulforaphane protects pancreatic acinar cell injury by modulating Nrf2-mediated oxidative stress and NLRP3 inflammatory pathway. Oxid Med Cell Longev 2016, 7864150 (2016).
pubmed: 27847555
pmcid: 5101394
doi: 10.1155/2016/7864150
Whiteman, M. et al. The effect of hydrogen sulfide donors on lipopolysaccharide-induced formation of inflammatory mediators in macrophages. Antioxid Redox Sign 12, 1147–1154 (2010).
doi: 10.1089/ars.2009.2899
Pálinkás, Z. et al. Interactions of hydrogen sulfide with myeloperoxidase. Brit J Pharmacol 172, 1516–1532 (2015).
doi: 10.1111/bph.12769
Faller, S. et al. Inhaled hydrogen sulfide protects against ventilator-induced lung injury. Anesthesiology 113, 104–115 (2010).
pubmed: 20574227
doi: 10.1097/ALN.0b013e3181de7107
Kui, B. et al. Recent advances in the investigation of pancreatic inflammation induced by large doses of basic amino acids in rodents. Lab Invest 94, 138–149 (2014).
pubmed: 24365745
doi: 10.1038/labinvest.2013.143
Rakonczay, Z. et al. A new severe acute necrotizing pancreatitis model induced by l-ornithine in rats. Crit Care Med 36, 2117–2127 (2008).
pubmed: 18594222
pmcid: 6624069
doi: 10.1097/CCM.0b013e31817d7f5c
Rakonczay, Z., Takács, T., Boros, I. & Lonovics, J. Heat shock proteins and the pancreas. J Cell Physiol 195, 383–391 (2003).
pubmed: 12704647
doi: 10.1002/jcp.10268
Bliksøen, M., Kaljusto, M.-L., Vaage, J. & Stensløkken, K.-O. Effects of hydrogen sulphide on ischaemia–reperfusion injury and ischaemic preconditioning in the isolated, perfused rat heart. Eur J Cardio-thorac 34, 344–349 (2008).
doi: 10.1016/j.ejcts.2008.03.017
Rakonczay, Z. et al. Nontoxic heat shock protein coinducer BRX-220 protects against acute pancreatitis in rats. Free Radical Bio Med 32, 1283–1292 (2002).
doi: 10.1016/S0891-5849(02)00833-X
Párniczky, A. et al. Prospective, multicentre, nationwide clinical data from 600 cases of acute pancreatitis. Plos One 11, e0165309 (2016).
pubmed: 27798670
pmcid: 5087847
doi: 10.1371/journal.pone.0165309
Salameh, E. et al. Chronic colitis-induced visceral pain is associated with increased anxiety during quiescent phase. Am J Physiol-gastr L 316, G692–G700 (2019).
Zhang, M.-M. et al. Effects of NB001 and gabapentin on irritable bowel syndrome-induced behavioral anxiety and spontaneous pain. Mol Brain 7, 47 (2014).
pubmed: 24935250
pmcid: 4071154
doi: 10.1186/1756-6606-7-47
Durst, M. et al. Analysis of pain and analgesia protocols in acute cerulein-induced pancreatitis in male C57BL/6 mice. Front Physiol 12, 744638 (2021).
pubmed: 34880773
pmcid: 8645955
doi: 10.3389/fphys.2021.744638
Michalski, C. W. et al. Cannabinoids ameliorate pain and reduce disease pathology in cerulein-induced acute pancreatitis. Gastroenterology 132, 1968–1978 (2007).
pubmed: 17484889
doi: 10.1053/j.gastro.2007.02.035
Baskin, S. I. et al. In vitro and in vivo comparison of sulfur donors as antidotes to acute cyanide intoxication. J Appl Toxicol 19, 173–183 (1999).
pubmed: 10362268
doi: 10.1002/(SICI)1099-1263(199905/06)19:3<173::AID-JAT556>3.0.CO;2-2
Kumar, M., Arora, P. & Sandhir, R. Hydrogen sulfide reverses LPS-induced behavioral deficits by suppressing microglial activation and promoting M2 polarization. J Neuroimmune Pharm 16, 483–499 (2021).
doi: 10.1007/s11481-020-09920-z
Dingenen, J. V., Pieters, L., Vral, A. & Lefebvre, R. A. The H2S-releasing naproxen derivative ATB-346 and the slow-release H2S Donor GYY4137 reduce intestinal inflammation and restore transit in postoperative ileus. Front Pharmacol 10, 116 (2019).
pubmed: 30842737
pmcid: 6391894
doi: 10.3389/fphar.2019.00116
Silva-Islas, C. A. et al. Diallyl trisulfide protects rat brain tissue against the damage induced by ischemia-reperfusion through the Nrf2 pathway. Antioxidants 8, 410 (2019).
pubmed: 31540440
pmcid: 6770608
doi: 10.3390/antiox8090410
Koike, S., Nishimoto, S. & Ogasawara, Y. Cysteine persulfides and polysulfides produced by exchange reactions with H2S protect SH-SY5Y cells from methylglyoxal-induced toxicity through Nrf2 activation. Redox Biol 12, 530–539 (2017).
pubmed: 28371750
pmcid: 5377440
doi: 10.1016/j.redox.2017.03.020
Dóka, É. et al. Control of protein function through oxidation and reduction of persulfidated states. Sci Adv 6, eaax8358 (2020).
pubmed: 31911946
pmcid: 6938701
doi: 10.1126/sciadv.aax8358
Zivanovic, J. et al. Selective persulfide detection reveals evolutionarily conserved antiaging effects of S-sulfhydration. Cell Metab 30, 1152-1170.e13 (2019).
pubmed: 31735592
pmcid: 7185476
doi: 10.1016/j.cmet.2019.10.007
Erdélyi, K. et al. Reprogrammed transsulfuration promotes basal-like breast tumor progression via realigning cellular cysteine persulfidation. Proc National Acad Sci 118, e2100050118 (2021).
doi: 10.1073/pnas.2100050118
Czikora, Á. et al. Cystathionine β-synthase overexpression drives metastatic dissemination in pancreatic ductal adenocarcinoma via inducing epithelial-to-mesenchymal transformation of cancer cells. Redox Biol 57, 102505 (2022).
pubmed: 36279629
pmcid: 9594639
doi: 10.1016/j.redox.2022.102505
Gerasimenko, J. V., Petersen, O. H. & Gerasimenko, O. V. SARS-CoV-2 S protein subunit 1 elicits Ca2+ influx: Dependent Ca2+ signals in pancreatic stellate cells and macrophages in situ. Function 3, zqac002 (2022).
pubmed: 35284826
pmcid: 8903325
doi: 10.1093/function/zqac002
Gerasimenko, J. V. & Gerasimenko, O. V. The role of Ca2+ signalling in the pathology of exocrine pancreas. Cell Calcium 112, 102740 (2023).
pubmed: 37058923
doi: 10.1016/j.ceca.2023.102740
Powell, C. R., Dillon, K. M. & Matson, J. B. A review of hydrogen sulfide (H2S) donors: Chemistry and potential therapeutic applications. Biochem Pharmacol 149, 110–123 (2018).
pubmed: 29175421
doi: 10.1016/j.bcp.2017.11.014
Armstrong, J. A. et al. Oxidative stress alters mitochondrial bioenergetics and modifies pancreatic cell death independently of cyclophilin D, resulting in an apoptosis-to-necrosis shift. J Biol Chem 293, 8032–8047 (2018).
pubmed: 29626097
pmcid: 5971444
doi: 10.1074/jbc.RA118.003200
Criddle, D. N. Reactive oxygen species, Ca2+ stores and acute pancreatitis; a step closer to therapy?. Cell Calcium 60, 180–189 (2016).
pubmed: 27229361
doi: 10.1016/j.ceca.2016.04.007
Pérez, S., Pereda, J., Sabater, L. & Sastre, J. Redox signaling in acute pancreatitis. Redox Biol 5, 1–14 (2015).
pubmed: 25778551
pmcid: 4360040
doi: 10.1016/j.redox.2015.01.014
Petersen, O. H., Gerasimenko, J. V., Gerasimenko, O. V., Gryshchenko, O. & Peng, S. The roles of calcium and ATP in the physiology and pathology of the exocrine pancreas. Physiol Rev 101, 1691–1744 (2021).
pubmed: 33949875
doi: 10.1152/physrev.00003.2021
Iciek, M., Bilska-Wilkosz, A. & Górny, M. Sulfane sulfur: new findings on an old topic. Acta Biochim Pol 66, 533–544 (2019).
pubmed: 31883321
Zhang, F. et al. Diallyl trisulfide suppresses oxidative stress-induced activation of hepatic stellate cells through production of hydrogen sulfide. Oxid Med Cell Longev 2017, 1406726 (2017).
pubmed: 28303169
pmcid: 5337887
doi: 10.1155/2017/1406726
Kang, J. S., Kim, G.-Y., Kim, B. W. & Choi, Y. H. Antioxidative effects of diallyl trisulfide on hydrogen peroxide-induced cytotoxicity through regulation of nuclear factor-E2-related factor-mediated thioredoxin reductase 1 expression in C2C12 skeletal muscle myoblast cells. Gen Physiol Biophys 36, 129–139 (2017).
pubmed: 28218609
doi: 10.4149/gpb_2016042
Gryshchenko, O., Gerasimenko, J. V., Petersen, O. H. & Gerasimenko, O. V. Calcium signaling in pancreatic immune cells in situ. Funct 2, zqaa026 (2020).
doi: 10.1093/function/zqaa026
Mishanina, T. V., Libiad, M. & Banerjee, R. Biogenesis of reactive sulfur species for signaling by hydrogen sulfide oxidation pathways. Nat Chem Biol 11, 457–464 (2015).
pubmed: 26083070
pmcid: 4818113
doi: 10.1038/nchembio.1834
Paul, B. D. & Snyder, S. H. H2S signalling through protein sulfhydration and beyond. Nat Rev Mol Cell Bio 13, 499–507 (2012).
doi: 10.1038/nrm3391
Mustafa, A. K. et al. H2S signals through protein s-sulfhydration. Sci Signal 2, ra72 (2009).
pubmed: 19903941
pmcid: 2998899
doi: 10.1126/scisignal.2000464
Nagy, P. Chapter one mechanistic chemical perspective of hydrogen sulfide signaling. Methods Enzymol 554, 3–29 (2015).
pubmed: 25725513
doi: 10.1016/bs.mie.2014.11.036
Faro, M. L. L., Fox, B., Whatmore, J. L., Winyard, P. G. & Whiteman, M. Hydrogen sulfide and nitric oxide interactions in inflammation. Nato Sci S A Lif Sci 41, 38–47 (2014).
Ditrói, T. et al. Comprehensive analysis of how experimental parameters affect H2S measurements by the monobromobimane method. Free Radical Bio Med 136, 146–158 (2019).
doi: 10.1016/j.freeradbiomed.2019.04.006
Nagy, P., Dóka, É., Ida, T. & Akaike, T. Measuring reactive sulfur species and thiol oxidation states: Challenges and cautions in relation to alkylation-based protocols. Antioxid Redox Sign 33, 1174–1189 (2020).
doi: 10.1089/ars.2020.8077
Bogdándi, V. et al. Speciation of reactive sulfur species and their reactions with alkylating agents: Do we have any clue about what is present inside the cell?. Brit J Pharmacol 176, 646–670 (2019).
doi: 10.1111/bph.14394
Dombi, Á. et al. Dimethyl trisulfide diminishes traumatic neuropathic pain acting on TRPA1 receptors in mice. Int J Mol Sci 22, 3363 (2021).
pubmed: 33806000
pmcid: 8036544
doi: 10.3390/ijms22073363
Wang, Q. et al. TRPA1 regulates macrophages phenotype plasticity and atherosclerosis progression. Atherosclerosis 301, 44–53 (2020).
pubmed: 32325260
doi: 10.1016/j.atherosclerosis.2020.04.004
Miyamoto, R. et al. Polysulfides (H2Sn) produced from the interaction of hydrogen sulfide (H2S) and nitric oxide (NO) activate TRPA1 channels. Sci Rep-uk 7, 45995 (2017).
doi: 10.1038/srep45995
du Sert, N. P. et al. The ARRIVE guidelines 20: Updated guidelines for reporting animal research. Plos Biol 18, e3000410 (2020).
doi: 10.1371/journal.pbio.3000410
Fűr, G. et al. Mislocalization of CFTR expression in acute pancreatitis and the beneficial effect of VX-661 + VX-770 treatment on disease severity. J Physiology 599, 4955–4971 (2021).
doi: 10.1113/JP281765
Bálint, E. R. et al. Fentanyl but not morphine or buprenorphine improves the severity of necrotizing acute pancreatitis in rats. Int J Mol Sci 23, 1192 (2022).
pubmed: 35163111
pmcid: 8835441
doi: 10.3390/ijms23031192
Huang, W. et al. Fatty acid ethyl ester synthase inhibition ameliorates ethanol-induced Ca2+-dependent mitochondrial dysfunction and acute pancreatitis. Gut 63, 1313 (2014).
pubmed: 24162590
doi: 10.1136/gutjnl-2012-304058
Balla, Z. et al. Kynurenic acid and its analogue SZR-72 ameliorate the severity of experimental acute necrotizing pancreatitis. Front Immunol 12, 702764 (2021).
pubmed: 34745090
pmcid: 8567016
doi: 10.3389/fimmu.2021.702764
Williams, J. A. Isolation of rodent pancreatic acinar cells and acini by collagenase digestion. Pancreapedia https://doi.org/10.3998/panc.2010.18 (2010).
doi: 10.3998/panc.2010.18
Akaike, T. et al. Cysteinyl-tRNA synthetase governs cysteine polysulfidation and mitochondrial bioenergetics. Nat Commun 8, 1177 (2017).
pubmed: 29079736
pmcid: 5660078
doi: 10.1038/s41467-017-01311-y
Faul, F., Erdfelder, E., Buchner, A. & Lang, A.-G. Statistical power analyses using G*Power 3.1: Tests for correlation and regression analyses. Behav Res Methods 41, 1149–1160 (2009).
pubmed: 19897823
doi: 10.3758/BRM.41.4.1149