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Oxidative Medicine and Cellular Longevity
Volume 2016, Article ID 7864150, 12 pages
http://dx.doi.org/10.1155/2016/7864150
Research Article

Sulforaphane Protects Pancreatic Acinar Cell Injury by Modulating Nrf2-Mediated Oxidative Stress and NLRP3 Inflammatory Pathway

1State Key Laboratory of Food Science and Technology, School of Food Science and Technology, Jiangnan University, Wuxi 214122, China
2Jiangnan University School of Medicine, Wuxi 214122, China
3Shanghai Key Laboratory of Bioactive Small Molecules and Department of Pharmacology, School of Pharmacy, Fudan University, Shanghai 201203, China
4Inflammation Research Group, Department of Pathology, University of Otago, Christchurch, 2 Riccarton Avenue, P.O. Box 4345, Christchurch 8140, New Zealand

Received 16 June 2016; Accepted 3 October 2016

Academic Editor: Débora Villaño Valencia

Copyright © 2016 Zhaojun Dong et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. V. Schick, J. A. Scheiber, F. C. Mooren et al., “Effect of magnesium supplementation and depletion on the onset and course of acute experimental pancreatitis,” Gut, vol. 63, no. 9, pp. 1469–1480, 2014. View at Publisher · View at Google Scholar · View at Scopus
  2. N. Zyromski and M. M. Murr, “Evolving concepts in the pathophysiology of acute pancreatitis,” Surgery, vol. 133, no. 3, pp. 235–237, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. S. J. Pandol, A. K. Saluja, C. W. Imrie, and P. A. Banks, “Acute pancreatitis: bench to the bedside,” Gastroenterology, vol. 132, no. 3, pp. 1127–1151, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Escobar, J. Pereda, A. Arduini et al., “Cross-talk between oxidative stress and pro-inflammatory cytokines in acute pancreatitis: a key role for protein phosphatases,” Current Pharmaceutical Design, vol. 15, no. 26, pp. 3027–3042, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. M. H. Schoenberg, M. Buchler, M. Gaspar et al., “Oxygen free radicals in acute pancreatitis of the rat,” Gut, vol. 31, no. 10, pp. 1138–1143, 1990. View at Publisher · View at Google Scholar · View at Scopus
  6. K. Tsai, S.-S. Wang, T.-S. Chen et al., “Oxidative stress: an important phenomenon with pathogenetic significance in the progression of acute pancreatitis,” Gut, vol. 42, no. 6, pp. 850–855, 1998. View at Publisher · View at Google Scholar · View at Scopus
  7. P. Talalay, A. T. Dinkova-Kostova, and W. D. Holtzclaw, “Importance of phase 2 gene regulation in protection against electrophile and reactive oxygen toxicity and carcinogenesis,” Advances in Enzyme Regulation, vol. 43, pp. 121–134, 2003. View at Publisher · View at Google Scholar · View at Scopus
  8. C. D. Fisher, L. M. Augustine, J. M. Maher et al., “Induction of drug-metabolizing enzymes by garlic and allyl sulfide compounds via activation of constitutive androstane receptor and nuclear factor E2-related factor 2,” Drug Metabolism and Disposition, vol. 35, no. 6, pp. 995–1000, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Dabrowski, S. J. Konturek, J. W. Konturek, and A. Gabryelewicz, “Role of oxidative stress in the pathogenesis of caerulein-induced acute pancreatitis,” European Journal of Pharmacology, vol. 377, no. 1, pp. 1–11, 1999. View at Publisher · View at Google Scholar · View at Scopus
  10. T. Hackert and J. Werner, “Antioxidant therapy in acute pancreatitis: experimental and clinical evidence,” Antioxidants and Redox Signaling, vol. 15, no. 10, pp. 2767–2777, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. C. Niederau, M. Niederau, F. Borchard et al., “Effects of antioxidants and free radical scavengers in three different models of acute pancreatitis,” Pancreas, vol. 7, no. 4, pp. 486–496, 1992. View at Publisher · View at Google Scholar · View at Scopus
  12. J.-D. Ren, J. Ma, J. Hou et al., “Hydrogen-rich saline inhibits NLRP3 inflammasome activation and attenuates experimental acute pancreatitis in mice,” Mediators of Inflammation, vol. 2014, Article ID 930894, 9 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  13. H. Liu and P. Talalay, “Relevance of anti-inflammatory and antioxidant activities of exemestane and synergism with sulforaphane for disease prevention,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 47, pp. 19065–19070, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. Y.-H. Ahn, Y. Hwang, H. Liu et al., “Electrophilic tuning of the chemoprotective natural product sulforaphane,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 21, pp. 9590–9595, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Yanaka, J. W. Fahey, A. Fukumoto et al., “Dietary sulforaphane-rich broccoli sprouts reduce colonization and attenuate gastritis in Helicobacter pylori–infected mice and humans,” Cancer Prevention Research, vol. 2, no. 4, pp. 353–360, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. A. E. Wagner, O. Will, C. Sturm, S. Lipinski, P. Rosenstiel, and G. Rimbach, “DSS-induced acute colitis in C57BL/6 mice is mitigated by sulforaphane pre-treatment,” Journal of Nutritional Biochemistry, vol. 24, no. 12, pp. 2085–2091, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. Y. Zheng, S. Tao, F. Lian et al., “Sulforaphane prevents pulmonary damage in response to inhaled arsenic by activating the Nrf2-defense response,” Toxicology and Applied Pharmacology, vol. 265, no. 3, pp. 292–299, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. A. J. Greaney, N. K. Maier, S. H. Leppla, and M. Moayeri, “Sulforaphane inhibits multiple inflammasomes through an nrf2-independent mechanism,” Journal of Leukocyte Biology, vol. 99, no. 1, pp. 189–199, 2016. View at Publisher · View at Google Scholar · View at Scopus
  19. R. Hoque, M. Sohail, A. Malik et al., “TLR9 and the NLRP3 inflammasome link acinar cell death with inflammation in acute pancreatitis,” Gastroenterology, vol. 141, no. 1, pp. 358–369, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. G. Kallifatidis, S. Labsch, V. Rausch et al., “Sulforaphane increases drug-mediated cytotoxicity toward cancer stem-like cells of pancreas and prostate,” Molecular Therapy, vol. 19, no. 1, pp. 188–195, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Sharma, X. Tao, A. Gopal et al., “Protection against acute pancreatitis by activation of protease-activated receptor-2,” American Journal of Physiology-Gastrointestinal and Liver Physiology, vol. 288, no. 2, pp. G388–G395, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Bhatia and A. Hegde, “Treatment with antileukinate, a CXCR2 chemokine receptor antagonist, protects mice against acute pancreatitis and associated lung injury,” Regulatory Peptides, vol. 138, no. 1, pp. 40–48, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. V. P. Singh, A. K. Saluja, L. Bhagat et al., “Phosphatidylinositol 3-kinase-dependent activation of trypsinogen modulates the severity of acute pancreatitis,” Journal of Clinical Investigation, vol. 108, no. 9, pp. 1387–1395, 2001. View at Publisher · View at Google Scholar · View at Scopus
  24. W. G. Niehaus Jr. and B. Samuelsson, “Formation of malonaldehyde from phospholipid arachidonate during microsomal lipid peroxidation,” European Journal of Biochemistry, vol. 6, no. 1, pp. 126–130, 1968. View at Publisher · View at Google Scholar · View at Scopus
  25. K. H. Jung, S.-W. Hong, H.-M. Zheng et al., “Melatonin ameliorates cerulein-induced pancreatitis by the modulation of nuclear erythroid 2-related factor 2 and nuclear factor-kappaB in rats,” Journal of Pineal Research, vol. 48, no. 3, pp. 239–250, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. J. Gout, R. M. Pommier, D. F. Vincent et al., “Isolation and culture of mouse primary pancreatic acinar cells,” Journal of Visualized Experiments, no. 78, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. R. Tamizhselvi, Y.-H. Koh, J. Sun, H. Zhang, and M. Bhatia, “Hydrogen sulfide induces ICAM-1 expression and neutrophil adhesion to caerulein-treated pancreatic acinar cells through NF-κB and Src-family kinases pathway,” Experimental Cell Research, vol. 316, no. 9, pp. 1625–1636, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Gibbs, J. Schwartzman, V. Deng, and J. Alumkal, “Sulforaphane destabilizes the androgen receptor in prostate cancer cells by inactivating histone deacetylase 6,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 39, pp. 16663–16668, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. K.-W. Zeng, Q. Yu, F.-J. Song et al., “Deoxysappanone B, a homoisoflavone from the Chinese medicinal plant Caesalpinia sappan L., protects neurons from microglia-mediated inflammatory injuries via inhibition of IκB kinase (IKK)-NF-κB and p38/ERK MAPK pathways,” European Journal of Pharmacology, vol. 748, pp. 18–29, 2015. View at Publisher · View at Google Scholar · View at Scopus
  30. H. Huang, Y. Liu, J. Daniluk et al., “Activation of nuclear factor-κB in acinar cells increases the severity of pancreatitis in mice,” Gastroenterology, vol. 144, no. 1, pp. 202–210, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. V. Hornung and E. Latz, “Critical functions of priming and lysosomal damage for NLRP3 activation,” European Journal of Immunology, vol. 40, no. 3, pp. 620–623, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Paolini, P. Perocco, D. Canistro et al., “Induction of cytochrome P450, generation of oxidative stress and in vitro cell-transforming DNA-damaging activities by glucoraphanin, the bioprecursor of the chemopreventive agent sulforaphane found in broccoli,” Carcinogenesis, vol. 25, no. 1, pp. 61–67, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. Y.-S. Keum, T. Oo Khor, W. Lin et al., “Pharmacokinetics and pharmacodynamics of broccoli sprouts on the suppression of prostate cancer in transgenic adenocarcinoma of mouse prostate (TRAMP) Mice: implication of induction of Nrf2, HO-1 and apoptosis and the suppression of Akt-dependent kinase pathway,” Pharmaceutical Research, vol. 26, no. 10, pp. 2324–2331, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. Y. Li, T. Zhang, X. Li, P. Zou, S. J. Schwartz, and D. Sun, “Kinetics of sulforaphane in mice after consumption of sulforaphane-enriched broccoli sprout preparation,” Molecular Nutrition and Food Research, vol. 57, no. 12, pp. 2128–2136, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. J. D. Clarke, A. Hsu, D. E. Williams et al., “Metabolism and tissue distribution of sulforaphane in Nrf2 knockout and wild-type mice,” Pharmaceutical Research, vol. 28, no. 12, pp. 3171–3179, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. G. V. Bricker, K. M. Riedl, R. A. Ralston, K. L. Tober, T. M. Oberyszyn, and S. J. Schwartz, “Isothiocyanate metabolism, distribution, and interconversion in mice following consumption of thermally processed broccoli sprouts or purified sulforaphane,” Molecular Nutrition and Food Research, vol. 58, no. 10, pp. 1991–2000, 2014. View at Publisher · View at Google Scholar · View at Scopus
  37. P. Singh, R. Sharma, K. McElhanon et al., “Sulforaphane protects the heart from doxorubicin-induced toxicity,” Free Radical Biology and Medicine, vol. 86, pp. 90–101, 2015. View at Publisher · View at Google Scholar · View at Scopus
  38. L. Wang, Z. Tian, Q. Yang et al., “Sulforaphane inhibits thyroid cancer cell growth and invasiveness through the reactive oxygen species-dependent pathway,” Oncotarget, vol. 6, no. 28, pp. 25917–25931, 2015. View at Publisher · View at Google Scholar · View at Scopus
  39. N. V. Matusheski and E. H. Jeffery, “Comparison of the bioactivity of two glucoraphanin hydrolysis products found in broccoli, sulforaphane and sulforaphane nitrile,” Journal of Agricultural and Food Chemistry, vol. 49, no. 12, pp. 5743–5749, 2001. View at Publisher · View at Google Scholar · View at Scopus
  40. C. Xu, M.-T. Huang, G. Shen et al., “Inhibition of 7,12-Dimethylbenz(a)anthracene-induced skin tumorigenesis in C57BL/6 mice by sulforaphane is mediated by nuclear factor E2–related factor 2,” Cancer Research, vol. 66, no. 16, pp. 8293–8296, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. L. Elbling, R.-M. Weiss, O. Teufelhofer et al., “Green tea extract and (−)-epigallocatechin-3-gallate, the major tea catechin, exert oxidant but lack antioxidant activities,” The FASEB Journal, vol. 19, no. 7, pp. 807–809, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Enomoto, K. Itoh, E. Nagayoshi et al., “High sensitivity of Nrf2 knockout mice to acetaminophen hepatotoxicity associated with decreased expression of ARE-regulated drug metabolizing enzymes and antioxidant genes,” Toxicological Sciences, vol. 59, no. 1, pp. 169–177, 2001. View at Publisher · View at Google Scholar · View at Scopus
  43. K. H. Chan, M. K. C. Ng, and R. Stocker, “Haem oxygenase-I and cardiovascular disease: mechanisms and therapeutic potential,” Clinical Science, vol. 120, no. 12, pp. 493–504, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. L. Cheng, Z. Jin, R. Zhao, K. Ren, C. Deng, and S. Yu, “Resveratrol attenuates inflammation and oxidative stress induced by myocardial ischemia-reperfusion injury: role of Nrf2/ARE pathway,” International Journal of Clinical and Experimental Medicine, vol. 8, no. 7, pp. 10420–10428, 2015. View at Google Scholar · View at Scopus
  45. H. Guo, M.-J. Li, Q.-Q. Liu et al., “Danhong injection attenuates ischemia/reperfusion-induced brain damage which is associating with Nrf2 levels in vivo and in vitro,” Neurochemical Research, vol. 39, no. 9, pp. 1817–1824, 2014. View at Publisher · View at Google Scholar · View at Scopus
  46. Y.-Z. Wang, Y.-C. Zhang, J.-S. Cheng et al., “Protective effects of BML-111 on cerulein-induced acute pancreatitis-associated lung injury via activation of Nrf2/ARE signaling pathway,” Inflammation, vol. 37, no. 4, pp. 1120–1133, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. L. Chen, L. Wang, X. Zhang et al., “The protection by Octreotide against experimental ischemic stroke: up-regulated transcription factor Nrf2, HO-1 and down-regulated NF-κB expression,” Brain Research, vol. 1475, pp. 80–87, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. B. Li, W. Cui, J. Liu et al., “Sulforaphane ameliorates the development of experimental autoimmune encephalomyelitis by antagonizing oxidative stress and Th17-related inflammation in mice,” Experimental Neurology, vol. 250, pp. 239–249, 2013. View at Publisher · View at Google Scholar · View at Scopus
  49. P. Santofimia-Castaño, D. Clea Ruy, L. Garcia-Sanchez et al., “Melatonin induces the expression of Nrf2-regulated antioxidant enzymes via PKC and Ca2+ influx activation in mouse pancreatic acinar cells,” Free Radical Biology and Medicine, vol. 87, pp. 226–236, 2015. View at Publisher · View at Google Scholar · View at Scopus
  50. M.-Y. Song, E.-K. Kim, W.-S. Moon et al., “Sulforaphane protects against cytokine- and streptozotocin-induced β-cell damage by suppressing the NF-κB pathway,” Toxicology and Applied Pharmacology, vol. 235, no. 1, pp. 57–67, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. M. Bhatia, M. Brady, S. Shokuhi, S. Christmas, J. P. Neoptolemos, and J. Slavin, “Inflammatory mediators in acute pancreatitis,” The Journal of Pathology, vol. 190, no. 2, pp. 117–125, 2000. View at Publisher · View at Google Scholar · View at Scopus
  52. D. Altavilla, C. Famulari, M. Passaniti et al., “Attenuated cerulein-induced pancreatitis in nuclear factor-κB-deficient mice,” Laboratory Investigation, vol. 83, no. 12, pp. 1723–1732, 2003. View at Publisher · View at Google Scholar · View at Scopus
  53. W. Jin, H. Wang, W. Yan et al., “Disruption of Nrf2 enhances upregulation of nuclear factor-κB activity, proinflammatory cytokines, and intercellular adhesion molecule-1 in the brain after traumatic brain injury,” Mediators of Inflammation, vol. 2008, Article ID 725174, 7 pages, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. R. K. Thimmulappa, H. Lee, T. Rangasamy et al., “Nrf2 is a critical regulator of the innate immune response and survival during experimental sepsis,” The Journal of Clinical Investigation, vol. 116, no. 4, pp. 984–995, 2006. View at Publisher · View at Google Scholar · View at Scopus
  55. H. S. Youn, Y. S. Kim, Z. Y. Park et al., “Sulforaphane suppresses oligomerization of TLR4 in a thiol-dependent manner,” The Journal of Immunology, vol. 184, no. 1, pp. 411–419, 2010. View at Publisher · View at Google Scholar · View at Scopus