Berberine improves intestinal motility and visceral pain in the mouse models mimicking diarrhea-predominant irritable bowel syndrome (IBS-D) symptoms in an opioid-receptor dependent manner

PLoS ONE

Volumn 10, Issue 12, 2015, Pages

  Chen, Chunqiu ^a   Lu, Meiling ^a   Pan, Qiuhui ^a   Fichna, Jakub ^b   Zheng, Lijun ^a   Wang, Kesheng ^a   Yu, Zhen ^a   Li, Yongyu ^a   Li, Kun ^a   Song, Aihong ^a   Liu, Zhongchen ^a   Song, Zhenshun ^a   Kreis, Martin ^c  

^a TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

^b MEDICAL UNIVERSITY OF LODZ   (Poland)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BERBERINE; DELTA OPIATE RECEPTOR; MU OPIATE RECEPTOR; OPIATE RECEPTOR; MESSENGER RNA;

ABDOMINAL PAIN; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; BRAIN CELL; CONTROLLED STUDY; DRUG MECHANISM; FEMALE; INTESTINAL DYSMOTILITY; INTESTINAL SECRETION; INTESTINE MOTILITY; INTESTINE TRANSIT TIME; IRRITABLE COLON; MALE; MOUSE; NOCICEPTION; NONHUMAN; PROTEIN EXPRESSION; VISCERAL PAIN; ANIMAL; BAGG ALBINO MOUSE; COMPLICATION; DIARRHEA; DISEASE MODEL; DRUG EFFECTS; GASTROINTESTINAL MOTILITY; GENETICS; IRRITABLE BOWEL SYNDROME; METABOLISM; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT;

ANIMALS; BERBERINE; DIARRHEA; DISEASE MODELS, ANIMAL; FEMALE; GASTROINTESTINAL MOTILITY; IRRITABLE BOWEL SYNDROME; MALE; MICE; MICE, INBRED BALB C; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, OPIOID; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; VISCERAL PAIN;

EID: 84957561127     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0145556     Document Type: Article

References (40)

1. Tang QL, Lai ML, Zhong YF, Wang AM, Su JK, Zhang MQ (2013) Antinociceptive effectof berberine on visceral hypersensitivity in rats. World J Gastroenterol 19:4582-4589. doi: 10.3748/wjg.v19.i28.4582 PMID: 23901236
2. Mo C, Wang L, Zhang J, Numazawa S, Tang H, Tang X, et al. (2014) The crosstalk between Nrf2and AMPK signal pathways is important for the anti-inflammatory effectof berberine in LPS-stimulated macrophages and endotoxin-shocked mice. Antioxid Redox Signal 20:574-588. doi: 10.1089/ars.2012. 5116 PMID: 23875776
3. Tan W, Li Y, Chen M, Wang Y (2011) Berberine hydrochloride: anticancer activity and nanoparticulate delivery system. Int J Nanomedicine 6:1773-1777. doi: 10.2147/IJN. S22683 PMID: 21931477
4. Hsu YY, Tseng YT, Lo YC (2013) Berberine, a natural antidiabetes drug, attenuates glucose neurotoxicity and promotes Nrf2-related neurite outgrowth. Toxicol Appl Pharmacol 272:787-796. doi: 10. 1016/j.taap. 2013.08.008 PMID: 23954465
5. Dong H, Zhao Y, Zhao L, Lu F (2013) The effects of berberine on blood lipids: a systemic review and meta-analysis of randomized controlled trials. Planta Med 79:437-446. doi: 10.1055/s-0032-1328321 PMID: 23512497
6. Derosa G, Maffioli P, Cicero AF (2012) Berberine on metabolic and cardiovascular risk factors: an analysis from preclinical evidences to clinical trials. Expert Opin BiolTher 12:1113-1124. doi: 10.1517/14712598.2012.704014 PMID: 22780092
7. Bhutada P, Mundhada Y, Bansod K, Tawari S, Patil S, Dixit P, et al. (2011) Protection of cholinergic and antioxidant system contributes to the effect of berberine ameliorating memory dysfunction in rat model of streptozotocin-induced diabetes. Behav Brain Res 220:30-41. doi: 10.1016/j.bbr.2011.01. 022 PMID: 21262264
8. Peng WH, Lo KL, Lee YH, Hung TH, Lin YC (2007) Berberine produces antidepressant-like effects in the forced swim test and in the tail suspension test in mice. Life Sci 81:933-938. PMID: 17804020
9. Kulkarni SK, Dhir A (2010) Berberine: a plant alkaloid with therapeutic potential for central nervous system disorders. PhytotherRes 24:317-324. doi: 10.1002/ptr.2968 PMID: 19998323
10. Chen DP, Xiong YJ, Lv BC, Liu FF, Wang L, Tang ZY, et al. (2013) Effects of berberine on rat jejunal motility. J Pharm Pharmacol 65:734-744. doi: 10.1111/jphp. 12026 PMID: 23600391
11. Chen C, Yu Z, Li Y, Fichna J, Storr M (2014) Effects of berberine in the gastrointestinal tract-a review of actions and therapeutic implications. Am J Chin Med 42:1053-1070. doi: 10.1142/S0192415X14500669 PMID: 25183302
12. Feng Y, Li Y, Chen C, Lin X, Yang Y, Cai H, et al. (2013) Inhibiting roles of berberine in gut movement of rodents are related to activation of the endogenous opioid system. Phytother Res 27:1564-1571. doi: 10.1002/ptr.4926 PMID: 23339028
13. Ide S, Sora I, Ikeda K, Minami M, Uhl GR, Ishihara K (2010) Reduced emotional and corticosterone responses to stress in mu-opioid receptor knockout mice. Neuropharmacology 58:241-247. doi: 10. 1016/j.neuropharm.2009.07.005 PMID: 19596019
14. Filliol D, Ghozland S, Chluba J, Martin M, Matthes HW, Simonin F, et al. (2000) Mice deficient for deltaand mu-opioid receptors exhibit opposing alterations of emotional responses. Nat Genet 25:195-200. PMID: 10835636
15. Corazziari E (1999) Role of opioid ligands in the irritable bowel syndrome. Can J Gastroenterol 13 Suppl A: 71A-75A. PMID: 10202212
16. Dahan A, Olofsen E, Niesters M (2015) Pharmacotherapy for pain: efficacy and safety issues examined by subgroup analyses. Pain 156 Suppl 1:S119-S126. doi: 10.1016/j.pain. 0000000000000023 PMID: 25789429
17. Pradhan AA, Befort K, Nozaki C, Gaveriaux-Ruff C, Kieffer BL (2011) The delta opioid receptor: an evolving target for the treatment of brain disorders. Trends Pharmacol Sci 32:581-590. doi: 10.1016/j. tips.2011.06.008 PMID: 21925742
18. Fichna J, Lapointe T, Chapman K, Janecka A, Vergnolle N, AltierC, et al. (2012) Newneostigminebased behavioral mouse model of abdominal pain. Pharmacol Rep 64:1146-1154. PMID: 23238471
19. Xu SY, Wu YM, Ji Z, GaoXY, Pan SY (2012) A modified technique for culturing primary fetal rat cortical neurons. J Biomed Biotechnol 2012:803930. doi: 10.1155/2012/803930 PMID: 23193366
20. Wagner JJ, Etemad LR, Thompson AM (2001) Opioid-mediated facilitation of long-term depression in rat hippocampus. J Pharmacol Exp Ther 296:776-781. PMID: 11181906
21. Ito D, Komatsu T, Gohara K (2013) Measurement of saturation processes in glutamatergicand GABAergic synapse densities during long-term development of cultured rat cortical networks. Brain Res 1534:22-32. doi: 10.1016/j.brainres.2013.08.004 PMID: 23948099
22. Jerndal P, Ringstrom G, Agerforz P, Karpefors M, Akkermans LM, Bayati A, et al. (2010) Gastrointestinal-specific anxiety: an important factor for severity of GI symptoms and quality of life in IBS. Neurogastroenterol Motil 22:646-e179. doi: 10.1111/j.1365-2982.2010.01493.x PMID: 20367800
23. Bray BD, Nicol F, Penman ID, Ford MJ (2006) Symptom interpretation and quality of life in patients with irritable bowel syndrome. Br J Gen Pract 56:122-126. PMID: 16464326
24. Ong EW, Cahill CM (2014) Molecular Perspectives for mu/delta Opioid Receptor Heteromers as Distinct, Functional Receptors. Cells 3:152-179. doi: 10.3390/cells3010152 PMID: 24709907
25. He SQ, Zhang ZN, Guan JS, Liu HR, Zhao B, Wang HB, et al. (2011) Facilitation of mu-opioid receptor activity by preventing delta-opioid receptor-mediated codegradation. Neuron 69:120-131. doi: 10. 1016/j.neuron. 2010.12.001 PMID: 21220103
26. Zhang X, Bao L, Li S (2015) Opioid receptor trafficking and interaction in nociceptors. BrJ Pharmacol 172:364-374. doi: 10.1111/bph.12653 PMID: 24611685
27. Bodnar RJ (2013) Endogenous opiates and behavior: 2012. Peptides 50:55-95. doi: 10.1016/j. peptides.2013.10.001 PMID: 24126281
28. Martini C, van VM, Drewes A, Aarts L, Dahan A, Niesters M (2015) A Randomized Controlled Trial on the Effect of Tapentadol and Morphine on Conditioned Pain Modulation in Healthy Volunteers. PLoS One 10:e0128997. doi: 10.1371/journal.pone.0128997 PMID: 26076171
29. Werner MU, Pereira MP, Andersen LP, Dahl JB (2015) Endogenous opioid antagonism in physiological experimental pain models: a systematic review. PLoS One 10:e0125887. doi: 10.1371/journal.pone. 0125887 PMID: 26029906
30. Scherrer G, Imamachi N, Cao YQ, ContetC, Mennicken F, O'Donnell D, et al. (2009) Dissociation of the opioid receptor mechanisms that control mechanical and heat pain. Cell 137:1148-1159. doi: 10. 1016/j.cell.2009.04.019 PMID: 19524516
31. Matsumoto K, Narita M, Muramatsu N, Nakayama T, Misawa K, Kitajima M, et al. (2014) Orally active opioid mu/delta dual agonist MGM-16, a derivative of the indole alkaloid mitragynine, exhibits potent antiallodynic effect on neuropathic pain in mice. J Pharmacol Exp Ther 348:383-392. doi: 10.1124/jpet.113.208108 PMID: 24345467
32. Normandin A, Luccarini P, Molat JL, Gendron L, Dallel R (2013) Spinal mu and delta opioids inhibit both thermal and mechanical pain in rats. J Neurosci 33:11703-11714. doi: 10.1523/JNEUROSCI.1631-13.2013 PMID: 23843537
33. Sobczak M, Pilarczyk A, Jonakowski M, Jarmuz A, SalagaM, Lipkowski AW, et al. (2014) Anti-inflammatory and antinociceptive action of the dimeric enkephalin peptide biphalin in the mouse model of colitis: new potential treatment of abdominal pain associated with inflammatory bowel diseases. Peptides 60:102-106. doi: 10.1016/j.peptides.2014.08.005 PMID: 25151037
34. Zielinska M, Chen C, Mokrowiecka A, Cygankiewicz AI, Zakrzewski PK, Salaga M, et al. (2015) Orally administered novel cyclic pentapeptide P-317 alleviates symptoms of diarrhoea-predominant irritable bowel syndrome. J Pharm Pharmacol 67:244-254. doi: 10.1111/jphp. 12335 PMID: 25515402
35. Kabli N, Nguyen T, Balboni G, O'Dowd BF, George SR (2014) Antidepressant-likeandanxiolytic-like effects following activation of the mu-delta opioid receptor heteromer in the nucleus accumbens. Mol Psychiatry 19:986-994. doi: 10.1038/mp. 2013.115 PMID: 24061495
36. Sauriyal DS, Jaggi AS, Singh N (2011) Extending pharmacological spectrum of opioids beyond analgesia: multifunctional aspects in different pathophysiological states. Neuropeptides 45:175-188. doi: 10. 1016/j.npep. 2010.12.004 PMID: 21208657
37. Brocardo PS, Budni J, Lobato KR, Santos AR, Rodrigues AL (2009) Evidence for the involvement of the opioid system in the antidepressant-like effect of folic acid in the mouse forced swimming test. Behav Brain Res 200:122-127. doi: 10.1016/j.bbr.2009.01.004 PMID: 19162083
38. Saitoh A, Yamada M (2012) Antidepressant-like Effects of delta Opioid Receptor Agonists in Animal Models. Curr Neuropharmacol 10:231-238. doi: 10.2174/157015912803217314 PMID: 23449756
39. Altarifi AA, Rice KC, Negus SS (2015) Effects of mu-opioid receptor agonists in assays of acute painstimulated and pain-depressed behavior in male rats: role of mu-agonist efficacy and noxious stimulus intensity. J Pharmacol ExpTher 352:208-217. doi: 10.1124/jpet.114.219873 PMID: 25406170
40. Nozaki C, Nagase H, Nemoto T, Matifas A, Kieffer BL, Gaveriaux-Ruff C (2014) In vivo properties of KNT-127, a novel delta opioid agonist: receptor internalisation, antihyperalgesia and antidepressant effects in mice. Br J Pharmacol. 171:5376-5386. doi: 10.1111/bph.12852 PMID: 25048778