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Current Pharmaceutical Biotechnology

Author(s): Mehdi Zobeiri, Saeideh Momtaz, Fatemeh Parvizi, Devesh Tewari, Mohammad H. Farzaei* and Seyed M. Nabavi

DOI: 10.2174/1389201021666191216122555

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Targeting Mitogen-Activated Protein Kinases by Natural Products: A Novel Therapeutic Approach for Inflammatory Bowel Diseases

Page: [1342 - 1353] Pages: 12

  • * (Excluding Mailing and Handling)

Abstract

An increase in the prevalence of Inflammatory Bowel Diseases (IBD) as a multifactorial intestinal chronic inflammation as well as the absence of a certain cure, has created an innovative era in the management of IBD by molecule/pathway-based anti-inflammatory approaches. There are credible documentations that demonstrate Mitogen-Activated Protein Kinases (MAPK) acts as IBD regulator. Upon the activation of MAPK signalling pathway, the transcription and expression of various encoding inflammatory molecules implicated in IBD are altered, thereby exacerbating the inflammation development. The current pharmacological management of IBD, including drug and biological therapies are expensive, possess temporary relief and some adverse effects. In this context, a variety of dietary fruits or medicinal herbs have received worldwide attention versus the development of IBD. Infact, natural ingredients, such as Flavaglines, Fisetin, Myricitrin, Cardamonin, Curcumin, Octacosanol and Mangiferin possess protective and therapeutic effects against IBD via modulation of different segments of MAPK signaling pathway. This review paper calls attention to the role of MAPK signaling triggered by natural products in the prevention and treatment of IBD.

Keywords: Natural product, IBD, MAPK, natural dietary supplement, ulcerative colitis, therapeutic target.

Graphical Abstract

[1]
Khor, B.; Gardet, A.; Xavier, R.J. Genetics and pathogenesis of inflammatory bowel disease. Nature, 2011, 474(7351), 307-317.
[http://dx.doi.org/10.1038/nature10209] [PMID: 21677747]
[2]
Rapozo, D.C.; Bernardazzi, C.; de Souza, H.S. Diet and microbiota in inflammatory bowel disease: The gut in disharmony. World J. Gastroenterol., 2017, 23(12), 2124-2140.
[http://dx.doi.org/10.3748/wjg.v23.i12.2124] [PMID: 28405140]
[3]
Ananthakrishnan, A.N. Epidemiology and risk factors for IBD. Nat. Rev. Gastroenterol. Hepatol., 2015, 12(4), 205-217.
[http://dx.doi.org/10.1038/nrgastro.2015.34] [PMID: 25732745]
[4]
Legaki, E.; Gazouli, M. Influence of environmental factors in the development of inflammatory bowel diseases. World J. Gastrointest. Pharmacol. Ther., 2016, 7(1), 112-125.
[http://dx.doi.org/10.4292/wjgpt.v7.i1.112] [PMID: 26855817]
[5]
Matricon, J.; Barnich, N.; Ardid, D. Immunopathogenesis of inflammatory bowel disease. Self Nonself, 2010, 1(4), 299-309.
[http://dx.doi.org/10.4161/self.1.4.13560] [PMID: 21487504]
[6]
Katsanos, K.H.; Papadakis, K.A. Inflammatory bowel disease: updates on molecular targets for biologics. Gut Liver, 2017, 11(4), 455-463.
[http://dx.doi.org/10.5009/gnl16308] [PMID: 28486793]
[7]
Rogler, G. Where are we heading to in pharmacological IBD therapy? Pharmacol. Res., 2015, 100, 220-227.
[http://dx.doi.org/10.1016/j.phrs.2015.07.005] [PMID: 26277232]
[8]
Garg, N.; Luzzatto-Knaan, T.; Melnik, A.V.; Caraballo-Rodríguez, A.M.; Floros, D.J.; Petras, D.; Gregor, R.; Dorrestein, P.C.; Phelan, V.V. Natural products as mediators of disease. Nat. Prod. Rep., 2017, 34(2), 194-219.
[http://dx.doi.org/10.1039/C6NP00063K] [PMID: 27874907]
[9]
Farzaei, M.H.; El-Senduny, F.F.; Momtaz, S.; Parvizi, F.; Iranpanah, A.; Tewari, D.; Naseri, R.; Abdolghaffari, A.H.; Rezaei, N. An update on dietary consideration in inflammatory bowel disease: anthocyanins and more. Expert Rev. Gastroenterol. Hepatol., 2018, 12(10), 1007-1024.
[http://dx.doi.org/10.1080/17474124.2018.1513322] [PMID: 30136591]
[10]
Farzaei, M.H.; Bahramsoltani, R.; Abdolghaffari, A.H.; Sodagari, H.R.; Esfahani, S.A.; Rezaei, N. A mechanistic review on plant-derived natural compounds as dietary supplements for prevention of inflammatory bowel disease. Expert Rev. Gastroenterol. Hepatol., 2016, 10(6), 745-758.
[http://dx.doi.org/10.1586/17474124.2016.1145546] [PMID: 26799847]
[11]
Debnath, T.; Kim, D.H.; Lim, B.O. Natural products as a source of anti-inflammatory agents associated with inflammatory bowel disease. Molecules, 2013, 18(6), 7253-7270.
[http://dx.doi.org/10.3390/molecules18067253] [PMID: 23783459]
[12]
Santino, A.; Scarano, A.; De Santis, S.; De Benedictis, M.; Giovinazzo, G.; Chieppa, M. Gut microbiota modulation and anti-inflammatory properties of dietary polyphenols in IBD: New and consolidated perspectives. Curr. Pharm. Des., 2017, 23(16), 2344-2351.
[http://dx.doi.org/10.2174/1381612823666170207145420] [PMID: 28176667]
[13]
Yuan, G.; Wahlqvist, M.L.; He, G.; Yang, M.; Li, D. Natural products and anti-inflammatory activity. Asia Pac. J. Clin. Nutr., 2006, 15(2), 143-152.
[PMID: 16672197]
[14]
Pearson, G.; Robinson, F.; Beers Gibson, T.; Xu, B.E.; Karandikar, M.; Berman, K.; Cobb, M.H. Mitogen-Activated Protein (MAP) kinase pathways: Regulation and physiological functions. Endocr. Rev., 2001, 22(2), 153-183.
[PMID: 11294822]
[15]
Cuadrado, A.; Nebreda, A.R. Mechanisms and functions of p38 MAPK signalling. Biochem. J., 2010, 429(3), 403-417.
[http://dx.doi.org/10.1042/BJ20100323] [PMID: 20626350]
[16]
Waetzig, G.H.; Seegert, D.; Rosenstiel, P.; Nikolaus, S.; Schreiber, S. p38 mitogen-activated protein kinase is activated and linked to TNF-α signaling in inflammatory bowel disease. J. Immunol., 2002, 168(10), 5342-5351.
[http://dx.doi.org/10.4049/jimmunol.168.10.5342] [PMID: 11994493]
[17]
Tas, S.W.; Maracle, C.X.; Balogh, E.; Szekanecz, Z. Targeting of proangiogenic signalling pathways in chronic inflammation. Nat. Rev. Rheumatol., 2016, 12(2), 111-122.
[http://dx.doi.org/10.1038/nrrheum.2015.164] [PMID: 26633288]
[18]
Broom, O.J.; Widjaya, B.; Troelsen, J.; Olsen, J.; Nielsen, O.H. Mitogen activated protein kinases: A role in inflammatory bowel disease? Clin. Exp. Immunol., 2009, 158(3), 272-280.
[http://dx.doi.org/10.1111/j.1365-2249.2009.04033.x] [PMID: 19793335]
[19]
Zhao, X.; Kang, B.; Lu, C.; Liu, S.; Wang, H.; Yang, X.; Chen, Y.; Jiang, B.; Zhang, J.; Lu, Y.; Zhi, F. Evaluation of p38 MAPK pathway as a molecular signature in ulcerative colitis. J. Proteome Res., 2011, 10(5), 2216-2225.
[http://dx.doi.org/10.1021/pr100969w] [PMID: 21428429]
[20]
Hanai, H.; Iida, T.; Takeuchi, K.; Watanabe, F.; Maruyama, Y.; Andoh, A.; Tsujikawa, T.; Fujiyama, Y.; Mitsuyama, K.; Sata, M.; Yamada, M.; Iwaoka, Y.; Kanke, K.; Hiraishi, H.; Hirayama, K.; Arai, H.; Yoshii, S.; Uchijima, M.; Nagata, T.; Koide, Y. Curcumin maintenance therapy for ulcerative colitis: Randomized, multicenter, double-blind, placebo-controlled trial. Clin. Gastroenterol. Hepatol., 2006, 4(12), 1502-1506.
[http://dx.doi.org/10.1016/j.cgh.2006.08.008] [PMID: 17101300]
[21]
Jeong, J.J.; Jang, S.E.; Hyam, S.R.; Han, M.J.; Kim, D.H. Mangiferin ameliorates colitis by inhibiting IRAK1 phosphorylation in NF-κB and MAPK pathways. Eur. J. Pharmacol., 2014, 740, 652-661.
[http://dx.doi.org/10.1016/j.ejphar.2014.06.013] [PMID: 24972244]
[22]
Qian, Z.; Wu, Z.; Huang, L.; Qiu, H.; Wang, L.; Li, L.; Yao, L.; Kang, K.; Qu, J.; Wu, Y.; Luo, J.; Liu, J.J.; Yang, Y.; Yang, W.; Gou, D. Mulberry fruit prevents LPS-induced NF-κB/pERK/ MAPK signals in macrophages and suppresses acute colitis and colorectal tumorigenesis in mice. Sci. Rep., 2015, 5, 17348.
[http://dx.doi.org/10.1038/srep17348] [PMID: 26615818]
[23]
Mehta, M.; Ahmed, S.; Dryden, G. Immunopathophysiology of inflammatory bowel disease: How genetics link barrier dysfunction and innate immunity to inflammation. Innate Immun., 2017, 23(6), 497-505.
[http://dx.doi.org/10.1177/1753425917722206] [PMID: 28770665]
[24]
Sharma, R.; Young, C.; Neu, J. Molecular modulation of intestinal epithelial barrier: Contribution of microbiota. BioMed Res. Int., 2010.
[http://dx.doi.org/10.1155/2010/305879]
[25]
Geremia, A.; Biancheri, P.; Allan, P.; Corazza, G.R.; Di Sabatino, A. Innate and adaptive immunity in inflammatory bowel disease. Autoimmun. Rev., 2014, 13(1), 3-10.
[http://dx.doi.org/10.1016/j.autrev.2013.06.004] [PMID: 23774107]
[26]
Kobayashi, T.; Okamoto, S.; Hisamatsu, T.; Kamada, N.; Chinen, H.; Saito, R.; Kitazume, M.T.; Nakazawa, A.; Sugita, A.; Koganei, K.; Isobe, K.; Hibi, T. IL23 differentially regulates the Th1/Th17 balance in ulcerative colitis and Crohn’s disease. Gut, 2008, 57(12), 1682-1689.
[http://dx.doi.org/10.1136/gut.2007.135053] [PMID: 18653729]
[27]
Cătană, C.S.; Berindan Neagoe, I.; Cozma, V.; Magdaş, C.; Tăbăran, F.; Dumitraşcu, D.L. Contribution of the IL-17/IL-23 axis to the pathogenesis of inflammatory bowel disease. World J. Gastroenterol., 2015, 21(19), 5823-5830.
[http://dx.doi.org/10.3748/wjg.v21.i19.5823] [PMID: 26019446]
[28]
Coskun, M.; Vermeire, S.; Nielsen, O.H. Novel targeted therapies for inflammatory bowel disease. Trends Pharmacol. Sci., 2017, 38(2), 127-142.
[http://dx.doi.org/10.1016/j.tips.2016.10.014] [PMID: 27916280]
[29]
Pérez-Jeldres, T.; Tyler, C.J.; Boyer, J.D.; Karuppuchamy, T.; Bamias, G.; Dulai, P.S.; Boland, B.S.; Sandborn, W.J.; Patel, D.R.; Rivera-Nieves, J. Cell trafficking interference in inflammatory bowel disease: Therapeutic interventions based on basic pathogenesis concepts. Inflamm. Bowel Dis., 2019, 25(2), 270-282.
[http://dx.doi.org/10.1093/ibd/izy269] [PMID: 30165490]
[30]
Zhu, H.; Li, Y.R. Oxidative stress and redox signaling mechanisms of inflammatory bowel disease: Updated experimental and clinical evidence. Exp. Biol. Med. (Maywood), 2012, 237(5), 474-480.
[http://dx.doi.org/10.1258/ebm.2011.011358] [PMID: 22442342]
[31]
Piechota-Polanczyk, A.; Fichna, J. Review article: The role of oxidative stress in pathogenesis and treatment of inflammatory bowel diseases. Naunyn Schmiedebergs Arch. Pharmacol., 2014, 387(7), 605-620.
[http://dx.doi.org/10.1007/s00210-014-0985-1] [PMID: 24798211]
[32]
Bhattacharyya, A.; Chattopadhyay, R.; Mitra, S.; Crowe, S.E. Oxidative stress: An essential factor in the pathogenesis of gastrointestinal mucosal diseases. Physiol. Rev., 2014, 94(2), 329-354.
[http://dx.doi.org/10.1152/physrev.00040.2012] [PMID: 24692350]
[33]
Zuo, L.; Sypert, D.C.; Clark, A.D.; Xu, Z.; Garrison, D.E.; He, F. Redox mechanism of reactive oxygen species in gastrointestinal tract diseases. Gastrointestinal Tissue; Academic Press, 2017, pp. 21-27.
[http://dx.doi.org/10.1016/B978-0-12-805377-5.00002-3]
[34]
Mylonas, C.; Kouretas, D. Lipid peroxidation and tissue damage. In Vivo, 1999, 13(3), 295-309.
[PMID: 10459507]
[35]
Fontani, F.; Domazetovic, V.; Marcucci, T.; Vincenzini, M.T.; Iantomasi, T. MMPs, ADAMs and their natural inhibitors in inflammatory bowel disease: Involvement of oxidative stress. J. Clin. Gastroenterol. Hepatol., 2017, 3, 039.
[36]
Gottschalk, R.A.; Martins, A.J.; Angermann, B.R.; Dutta, B.; Ng, C.E.; Uderhardt, S.; Tsang, J.S.; Fraser, I.D.; Meier-Schellersheim, M.; Germain, R.N. Distinct NF-κB and MAPK activation thresholds uncouple steady-state microbe sensing from anti-pathogen inflammatory responses. Cell Syst., 2016, 2(6), 378-390.
[http://dx.doi.org/10.1016/j.cels.2016.04.016] [PMID: 27237739]
[37]
Topcu-Tarladacalisir, Y.; Akpolat, M.; Uz, Y.H.; Kizilay, G.; Sapmaz-Metin, M.; Cerkezkayabekir, A.; Omurlu, I.K. Effects of curcumin on apoptosis and oxidoinflammatory regulation in a rat model of acetic acid-induced colitis: The roles of c-Jun N-terminal kinase and p38 mitogen-activated protein kinase. J. Med. Food, 2013, 16(4), 296-305.
[http://dx.doi.org/10.1089/jmf.2012.2550] [PMID: 23566056]
[38]
Coskun, M.; Olsen, J.; Seidelin, J.B.; Nielsen, O.H. MAP kinases in inflammatory bowel disease. Clin. Chim. Acta, 2011, 412(7-8), 513-520.
[http://dx.doi.org/10.1016/j.cca.2010.12.020] [PMID: 21185271]
[39]
Sánchez-Fidalgo, S.; Villegas, I.; Rosillo, M.Á.; Aparicio-Soto, M.; de la Lastra, C.A. Dietary squalene supplementation improves DSS-induced acute colitis by downregulating p38 MAPK and NFkB signaling pathways. Mol. Nutr. Food Res., 2015, 59(2), 284-292.
[http://dx.doi.org/10.1002/mnfr.201400518] [PMID: 25387687]
[40]
Zundler, S.; Neurath, M.F. Integrating immunologic signaling networks: The JAK/STAT pathway in colitis and colitis-associated cancer. Vaccines (Basel), 2016, 4(1), 5.
[http://dx.doi.org/10.3390/vaccines4010005] [PMID: 26938566]
[41]
Coskun, M.; Salem, M.; Pedersen, J.; Nielsen, O.H. Involvement of JAK/STAT signaling in the pathogenesis of inflammatory bowel disease. Pharmacol. Res., 2013, 76, 1-8.
[http://dx.doi.org/10.1016/j.phrs.2013.06.007] [PMID: 23827161]
[42]
Banerjee, S.; Biehl, A.; Gadina, M.; Hasni, S.; Schwartz, D.M. JAK–STAT signaling as a target for inflammatory and autoimmune diseases: Current and future prospects. Drugs, 2017, 77(5), 521-546.
[http://dx.doi.org/10.1007/s40265-017-0701-9] [PMID: 28255960]
[43]
Kalla, R.; Ventham, N.T.; Kennedy, N.A.; Quintana, J.F.; Nimmo, E.R.; Buck, A.H.; Satsangi, J. MicroRNAs: New players in IBD. Gut, 2015, 64(3), 504-517.
[http://dx.doi.org/10.1136/gutjnl-2014-307891] [PMID: 25475103]
[44]
Chen, W.X.; Ren, L.H.; Shi, R.H. Implication of miRNAs for inflammatory bowel disease treatment: Systematic review. World J. Gastrointest. Pathophysiol., 2014, 5(2), 63-70.
[http://dx.doi.org/10.4291/wjgp.v5.i2.63] [PMID: 24891977]
[45]
Mijan, M.A.; Lim, B.O. Diets, functional foods, and nutraceuticals as alternative therapies for inflammatory bowel disease: Present status and future trends. World J. Gastroenterol., 2018, 24(25), 2673-2685.
[http://dx.doi.org/10.3748/wjg.v24.i25.2673] [PMID: 29991873]
[46]
Rastegarpanah, M.; Malekzadeh, R.; Vahedi, H.; Mohammadi, M.; Elahi, E.; Chaharmahali, M.; Safarnavadeh, T.; Abdollahi, M. A randomized, double blinded, placebo-controlled clinical trial of silymarin in ulcerative colitis. Chin. J. Integr. Med., 2015, 21(12), 902-906.
[http://dx.doi.org/10.1007/s11655-012-1026-x] [PMID: 22528757]
[47]
Rastegarpanah, M.; Omidzohour, N.; Vahedi, H.; Malekzadeh, R.; Hashemian, F.; Safarnavadeh, T.; Abdollahi, M. Management of human ulcerative colitis by SaturexTM: A randomized controlled trial. Int. J. Pharmacol., 2011, 7(4), 516-521.
[http://dx.doi.org/10.3923/ijp.2011.516.521]
[48]
Kamali, M.; Tavakoli, H.; Khodadoost, M.; Daghaghzadeh, H.; Kamalinejad, M.; Gachkar, L.; Mansourian, M.; Adibi, P. Efficacy of the Punica granatum peels aqueous extract for symptom management in ulcerative colitis patients. A randomized, placebo-controlled, clinical trial. Complement. Ther. Clin. Pract., 2015, 21(3), 141-146.
[http://dx.doi.org/10.1016/j.ctcp.2015.03.001] [PMID: 26256131]
[49]
Langhorst, J.; Varnhagen, I.; Schneider, S.B.; Albrecht, U.; Rueffer, A.; Stange, R.; Michalsen, A.; Dobos, G.J. Randomised clinical trial: A herbal preparation of myrrh, chamomile and coffee charcoal compared with mesalazine in maintaining remission in ulcerative colitis--a double-blind, double-dummy study. Aliment. Pharmacol. Ther., 2013, 38(5), 490-500.
[http://dx.doi.org/10.1111/apt.12397] [PMID: 23826890]
[50]
Faghfoori, Z.; Navai, L.; Shakerhosseini, R.; Somi, M.H.; Nikniaz, Z.; Norouzi, M.F. Effects of an oral supplementation of germinated barley foodstuff on serum tumour necrosis factor-α, interleukin-6 and -8 in patients with ulcerative colitis. Ann. Clin. Biochem., 2011, 48(Pt 3), 233-237.
[http://dx.doi.org/10.1258/acb.2010.010093] [PMID: 21367884]
[51]
Langmead, L.; Feakins, R.M.; Goldthorpe, S.; Holt, H.; Tsironi, E.; De Silva, A.; Jewell, D.P.; Rampton, D.S. Randomized, double-blind, placebo-controlled trial of oral Aloe vera gel for active ulcerative colitis. Aliment. Pharmacol. Ther., 2004, 19(7), 739-747.
[http://dx.doi.org/10.1111/j.1365-2036.2004.01902.x] [PMID: 15043514]
[52]
Ben-Arye, E.; Goldin, E.; Wengrower, D.; Stamper, A.; Kohn, R.; Berry, E. Wheat grass juice in the treatment of active distal ulcerative colitis: A randomized double-blind placebo-controlled trial. Scand. J. Gastroenterol., 2002, 37(4), 444-449.
[http://dx.doi.org/10.1080/003655202317316088] [PMID: 11989836]
[53]
Fernández-Bañares, F.; Hinojosa, J.; Sánchez-Lombraña, J.L.; Navarro, E.; Martínez-Salmerón, J.F.; García-Pugés, A.; González-Huix, F.; Riera, J.; González-Lara, V.; Domínguez-Abascal, F.; Giné, J.J.; Moles, J.; Gomollón, F.; Gassull, M.A. Spanish Group for the Study of Crohn’s Disease and Ulcerative Colitis (GETECCU). Randomized clinical trial of Plantago ovata seeds (dietary fiber) as compared with mesalamine in maintaining remission in ulcerative colitis. Am. J. Gastroenterol., 1999, 94(2), 427-433.
[PMID: 10022641]
[54]
Gong, Y.; Zha, Q.; Li, L.; Liu, Y.; Yang, B.; Liu, L.; Lu, A.; Lin, Y.; Jiang, M. Efficacy and safety of Fufangkushen colon-coated capsule in the treatment of ulcerative colitis compared with mesalazine: A double-blinded and randomized study. J. Ethnopharmacol., 2012, 141(2), 592-598.
[http://dx.doi.org/10.1016/j.jep.2011.08.057] [PMID: 21911045]
[55]
Tang, T.; Targan, S.R.; Li, Z.S.; Xu, C.; Byers, V.S.; Sandborn, W.J. Randomised clinical trial: herbal extract HMPL-004 in active ulcerative colitis - a double-blind comparison with sustained release mesalazine. Aliment. Pharmacol. Ther., 2011, 33(2), 194-202.
[http://dx.doi.org/10.1111/j.1365-2036.2010.04515.x] [PMID: 21114791]
[56]
Madisch, A.; Miehlke, S.; Eichele, O.; Mrwa, J.; Bethke, B.; Kuhlisch, E.; Bästlein, E.; Wilhelms, G.; Morgner, A.; Wigginghaus, B.; Stolte, M. Boswellia serrata extract for the treatment of collagenous colitis. A double-blind, randomized, placebo-controlled, multicenter trial. Int. J. Colorectal Dis., 2007, 22(12), 1445-1451.
[http://dx.doi.org/10.1007/s00384-007-0364-1] [PMID: 17764013]
[57]
Arthur, J.S.; Ley, S.C. Mitogen-activated protein kinases in innate immunity. Nat. Rev. Immunol., 2013, 13(9), 679-692.
[http://dx.doi.org/10.1038/nri3495] [PMID: 23954936]
[58]
Kim, E.K.; Choi, E.J. Compromised MAPK signaling in human diseases: An update. Arch. Toxicol., 2015, 89(6), 867-882.
[http://dx.doi.org/10.1007/s00204-015-1472-2] [PMID: 25690731]
[59]
Peti, W.; Page, R. Molecular basis of MAP kinase regulation. Protein Sci., 2013, 22(12), 1698-1710.
[http://dx.doi.org/10.1002/pro.2374] [PMID: 24115095]
[60]
Turjanski, A.G.; Vaqué, J.P.; Gutkind, J.S. MAP kinases and the control of nuclear events. Oncogene, 2007, 26(22), 3240-3253.
[http://dx.doi.org/10.1038/sj.onc.1210415] [PMID: 17496919]
[61]
Thouverey, C.; Caverzasio, J. Focus on the p38 MAPK signaling pathway in bone development and maintenance. Bonekey Rep., 2015, 4, 711.
[http://dx.doi.org/10.1038/bonekey.2015.80] [PMID: 26131361]
[62]
Zarubin, T.; Han, J. Activation and signaling of the p38 MAP kinase pathway. Cell Res., 2005, 15(1), 11-18.
[http://dx.doi.org/10.1038/sj.cr.7290257] [PMID: 15686620]
[63]
Sabio, G.; Davis, R.J. TNF and MAP kinase signalling pathways. Semin. Immunol., 2014, 26(3), 237-245.
[http://dx.doi.org/10.1016/j.smim.2014.02.009] [PMID: 24647229]
[64]
O’Callaghan, C.; Fanning, L.J.; Barry, O.P. p38δ MAPK: Emerging roles of a neglected isoform. Int. J. Biochem. Cell., 2014, 2014272689
[65]
Torii, S.; Yamamoto, T.; Tsuchiya, Y.; Nishida, E. ERK MAP kinase in G cell cycle progression and cancer. Cancer Sci., 2006, 97(8), 697-702.
[http://dx.doi.org/10.1111/j.1349-7006.2006.00244.x] [PMID: 16800820]
[66]
Nithianandarajah-Jones, G.N.; Wilm, B.; Goldring, C.E.; Müller, J.; Cross, M.J. ERK5: Structure, regulation and function. Cell. Signal., 2012, 24(11), 2187-2196.
[http://dx.doi.org/10.1016/j.cellsig.2012.07.007] [PMID: 22800864]
[67]
Rovida, E.; Di Maira, G.; Tusa, I.; Cannito, S.; Paternostro, C.; Navari, N.; Vivoli, E.; Deng, X.; Gray, N.S.; Esparís-Ogando, A.; David, E.; Pandiella, A.; Dello Sbarba, P.; Parola, M.; Marra, F. The mitogen-activated protein kinase ERK5 regulates the development and growth of hepatocellular carcinoma. Gut, 2015, 64(9), 1454-1465.
[http://dx.doi.org/10.1136/gutjnl-2014-306761] [PMID: 25183205]
[68]
Takeda, K.; Naguro, I.; Nishitoh, H.; Matsuzawa, A.; Ichijo, H. Apoptosis signaling kinases: From stress response to health outcomes. Antioxid. Redox Signal., 2011, 15(3), 719-761.
[http://dx.doi.org/10.1089/ars.2010.3392] [PMID: 20969480]
[69]
Chang, L.; Karin, M. Mammalian MAP kinase signalling cascades. Nature, 2001, 410(6824), 37-40.
[http://dx.doi.org/10.1038/35065000] [PMID: 11242034]
[70]
Keshet, Y.; Seger, R. The MAP kinase signaling cascades: A system of hundreds of components regulates a diverse array of physiological functions. Methods Mol. Biol., 2010, 661, 3-38.
[http://dx.doi.org/10.1007/978-1-60761-795-2_1] [PMID: 20811974]
[71]
Kyriakis, J.M.; Avruch, J. Mammalian MAPK signal transduction pathways activated by stress and inflammation: A 10-year update. Physiol. Rev., 2012, 92(2), 689-737.
[http://dx.doi.org/10.1152/physrev.00028.2011] [PMID: 22535895]
[72]
Rincón, M.; Davis, R.J. Regulation of the immune response by stress-activated protein kinases. Immunol. Rev., 2009, 228(1), 212-224.
[http://dx.doi.org/10.1111/j.1600-065X.2008.00744.x] [PMID: 19290930]
[73]
Rose, B.A.; Force, T.; Wang, Y. Mitogen-activated protein kinase signaling in the heart: Angels versus demons in a heart-breaking tale. Physiol. Rev., 2010, 90(4), 1507-1546.
[http://dx.doi.org/10.1152/physrev.00054.2009] [PMID: 20959622]
[74]
Kim, E.K.; Choi, E.J. Pathological roles of MAPK signaling pathways in human diseases. Biochim. Biophys. Acta, 2010, 1802(4), 396-405.
[http://dx.doi.org/10.1016/j.bbadis.2009.12.009] [PMID: 20079433]
[75]
Seki, E.; Brenner, D.A.; Karin, M. A liver full of JNK: Signaling in regulation of cell function and disease pathogenesis, and clinical approaches. Gastroenterology, 2012, 143(2), 307-320.
[http://dx.doi.org/10.1053/j.gastro.2012.06.004] [PMID: 22705006]
[76]
Krens, S.F.; Spaink, H.P.; Snaar-Jagalska, B.E. Functions of the MAPK family in vertebrate-development. FEBS Lett., 2006, 580(21), 4984-4990.
[http://dx.doi.org/10.1016/j.febslet.2006.08.025] [PMID: 16949582]
[77]
Nakamura, K.; Shirai, T.; Morishita, S.; Uchida, S.; Saeki-Miura, K.; Makishima, F. p38 mitogen-activated protein kinase functionally contributes to chondrogenesis induced by growth/differentiation factor-5 in ATDC5 cells. Exp. Cell Res., 1999, 250(2), 351-363.
[http://dx.doi.org/10.1006/excr.1999.4535] [PMID: 10413589]
[78]
Stanton, L.A.; Underhill, T.M.; Beier, F. MAP kinases in chondrocyte differentiation. Dev. Biol., 2003, 263(2), 165-175.
[http://dx.doi.org/10.1016/S0012-1606(03)00321-X] [PMID: 14597193]
[79]
Oh, C.D.; Chang, S.H.; Yoon, Y.M.; Lee, S.J.; Lee, Y.S.; Kang, S.S.; Chun, J.S. Opposing role of mitogen-activated protein kinase subtypes, erk-1/2 and p38, in the regulation of chondrogenesis of mesenchymes. J. Biol. Chem., 2000, 275(8), 5613-5619.
[http://dx.doi.org/10.1074/jbc.275.8.5613] [PMID: 10681543]
[80]
Watanabe, H.; de Caestecker, M.P.; Yamada, Y. Transcriptional cross-talk between Smad, ERK1/2, and p38 mitogen-activated protein kinase pathways regulates transforming growth factor-β-induced aggrecan gene expression in chondrogenic ATDC5 cells. J. Biol. Chem., 2001, 276(17), 14466-14473.
[http://dx.doi.org/10.1074/jbc.M005724200] [PMID: 11278290]
[81]
Gorter, J.A.; Iyer, A.; White, I.; Colzi, A.; van Vliet, E.A.; Sisodiya, S.; Aronica, E. Hippocampal subregion-specific microRNA expression during epileptogenesis in experimental temporal lobe epilepsy. Neurobiol. Dis., 2014, 62, 508-520.
[http://dx.doi.org/10.1016/j.nbd.2013.10.026] [PMID: 24184920]
[82]
Krab, L.C.; Goorden, S.M.; Elgersma, Y. Oncogenes on my mind: ERK and MTOR signaling in cognitive diseases. Trends Genet., 2008, 24(10), 498-510.
[http://dx.doi.org/10.1016/j.tig.2008.07.005] [PMID: 18774199]
[83]
Kumar, V.; Zhang, M.X.; Swank, M.W.; Kunz, J.; Wu, G.Y. Regulation of dendritic morphogenesis by Ras-PI3K-Akt-mTOR and Ras-MAPK signaling pathways. J. Neurosci., 2005, 25(49), 11288-11299.
[http://dx.doi.org/10.1523/JNEUROSCI.2284-05.2005] [PMID: 16339024]
[84]
Chotiner, J.K.; Nielson, J.; Farris, S.; Lewandowski, G.; Huang, F.; Banos, K.; de Leon, R.; Steward, O. Assessment of the role of MAP kinase in mediating activity-dependent transcriptional activation of the immediate early gene Arc/Arg3.1 in the dentate gyrus in vivo. Learn. Mem., 2010, 17(2), 117-129.
[http://dx.doi.org/10.1101/lm.1585910] [PMID: 20154358]
[85]
Nateri, A.S.; Raivich, G.; Gebhardt, C.; Da Costa, C.; Naumann, H.; Vreugdenhil, M.; Makwana, M.; Brandner, S.; Adams, R.H.; Jefferys, J.G.; Kann, O.; Behrens, A. ERK activation causes epilepsy by stimulating NMDA receptor activity. EMBO J., 2007, 26(23), 4891-4901.
[http://dx.doi.org/10.1038/sj.emboj.7601911] [PMID: 17972914]
[86]
de Araújo Herculano, B.; Vandresen-Filho, S.; Martins, W.C.; Boeck, C.R.; Tasca, C.I. NMDA preconditioning protects against quinolinic acid-induced seizures via PKA, PI3K and MAPK/ERK signaling pathways. Behav. Brain Res., 2011, 219(1), 92-97.
[http://dx.doi.org/10.1016/j.bbr.2010.12.025] [PMID: 21185872]
[87]
Crespo-Biel, N.; Canudas, A.M.; Camins, A.; Pallàs, M. Kainate induces AKT, ERK and cdk5/GSK3β pathway deregulation, phosphorylates tau protein in mouse hippocampus. Neurochem. Int., 2007, 50(2), 435-442.
[http://dx.doi.org/10.1016/j.neuint.2006.10.002] [PMID: 17116346]
[88]
Hu, B.; Liu, C.; Bramlett, H.; Sick, T.J.; Alonso, O.F.; Chen, S.; Dietrich, W.D. Changes in trkB-ERK1/2-CREB/Elk-1 pathways in hippocampal mossy fiber organization after traumatic brain injury. J. Cereb. Blood Flow Metab., 2004, 24(8), 934-943.
[http://dx.doi.org/10.1097/01.WCB.0000125888.56462.A1] [PMID: 15362724]
[89]
Pernice, H.F.; Schieweck, R.; Kiebler, M.A.; Popper, B. mTOR and MAPK: From localized translation control to epilepsy. BMC Neurosci., 2016, 17(1), 73.
[http://dx.doi.org/10.1186/s12868-016-0308-1] [PMID: 27855659]
[90]
Keyse, S.M. Protein phosphatases and the regulation of mitogen-activated protein kinase signalling. Curr. Opin. Cell Biol., 2000, 12(2), 186-192.
[http://dx.doi.org/10.1016/S0955-0674(99)00075-7] [PMID: 10712927]
[91]
Schaeffer, H.J.; Weber, M.J. Mitogen-activated protein kinases: specific messages from ubiquitous messengers. Mol. Cell. Biol., 1999, 19(4), 2435-2444.
[http://dx.doi.org/10.1128/MCB.19.4.2435] [PMID: 10082509]
[92]
Sui, X.; Kong, N.; Ye, L.; Han, W.; Zhou, J.; Zhang, Q.; He, C.; Pan, H. p38 and JNK MAPK pathways control the balance of apoptosis and autophagy in response to chemotherapeutic agents. Cancer Lett., 2014, 344(2), 174-179.
[http://dx.doi.org/10.1016/j.canlet.2013.11.019] [PMID: 24333738]
[93]
Han, J.; Lee, J.D.; Bibbs, L.; Ulevitch, R.J. A MAP kinase targeted by endotoxin and hyperosmolarity in mammalian cells. Science, 1994, 265(5173), 808-811.
[http://dx.doi.org/10.1126/science.7914033] [PMID: 7914033]
[94]
Loesch, M.; Chen, G. The p38 MAPK stress pathway as a tumor suppressor or more? Front. Biosci., 2008, 13, 3581-3593.
[http://dx.doi.org/10.2741/2951] [PMID: 18508457]
[95]
Ono, K.; Han, J. The p38 signal transduction pathway: activation and function. Cell. Signal, 2000, 12(1), 1-13.
[http://dx.doi.org/10.1016/S0898-6568(99)00071-6] [PMID: 10676842]
[96]
Cuenda, A.; Rousseau, S. p38 MAP-kinases pathway regulation, function and role in human diseases. Biochim. Biophys. Acta, 2007, 1773(8), 1358-1375.
[http://dx.doi.org/10.1016/j.bbamcr.2007.03.010] [PMID: 17481747]
[97]
Martin, E.D.; Bassi, R.; Marber, M.S. p38 MAPK in cardioprotection - are we there yet? Br. J. Pharmacol., 2015, 172(8), 2101-2113.
[http://dx.doi.org/10.1111/bph.12901] [PMID: 25204838]
[98]
Campbell, J.S.; Argast, G.M.; Yuen, S.Y.; Hayes, B.; Fausto, N. Inactivation of p38 MAPK during liver regeneration. Int. J. Biochem. Cell Biol., 2011, 43(2), 180-188.
[http://dx.doi.org/10.1016/j.biocel.2010.08.002] [PMID: 20708092]
[99]
Tormos, A.M.; Taléns-Visconti, R.; Nebreda, A.R.; Sastre, J. p38 MAPK: a dual role in hepatocyte proliferation through reactive oxygen species. Free Radic. Res., 2013, 47(11), 905-916.
[http://dx.doi.org/10.3109/10715762.2013.821200] [PMID: 23906070]
[100]
Ribeiro, N.; Thuaud, F.; Nebigil, C.; Désaubry, L. Recent advances in the biology and chemistry of the flavaglines. Bioorg. Med. Chem., 2012, 20(6), 1857-1864.
[http://dx.doi.org/10.1016/j.bmc.2011.10.048] [PMID: 22071525]
[101]
Ribeiro, N.; Thuaud, F.; Bernard, Y.; Gaiddon, C.; Cresteil, T.; Hild, A.; Hirsch, E.C.; Michel, P.P.; Nebigil, C.G.; Désaubry, L. Flavaglines as potent anticancer and cytoprotective agents. J. Med. Chem., 2012, 55(22), 10064-10073.
[http://dx.doi.org/10.1021/jm301201z] [PMID: 23072299]
[102]
Han, J.; Zhao, Q.; Basmadjian, C.; Désaubry, L.; Theiss, A.L. Flavaglines ameliorate experimental colitis and protect against intestinal epithelial cell apoptosis and mitochondrial dysfunction. Inflamm. Bowel Dis., 2016, 22(1), 55-67.
[http://dx.doi.org/10.1097/MIB.0000000000000592] [PMID: 26398710]
[103]
Kim, Y.K.; Kim, R.G.; Park, S.J.; Ha, J.H.; Choi, J.W.; Park, H.J.; Lee, K.T. In vitro antiinflammatory activity of kalopanaxsaponin A isolated from Kalopanax pictus in murine macrophage RAW 264.7 cells. Biol. Pharm. Bull., 2002, 25(4), 472-476.
[http://dx.doi.org/10.1248/bpb.25.472] [PMID: 11995927]
[104]
Joh, E.H.; Kim, D.H. Kalopanaxsaponin A ameliorates experimental colitis in mice by inhibiting IRAK-1 activation in the NF-κB and MAPK pathways. Br. J. Pharmacol., 2011, 162(8), 1731-1742.
[http://dx.doi.org/10.1111/j.1476-5381.2010.01195.x] [PMID: 21198552]
[105]
Wang, C.; Dai, Y.; Yang, J.; Chou, G.; Wang, C.; Wang, Z. Treatment with total alkaloids from Radix Linderae reduces inflammation and joint destruction in type II collagen-induced model for rheumatoid arthritis. J. Ethnopharmacol., 2007, 111(2), 322-328.
[http://dx.doi.org/10.1016/j.jep.2006.11.031] [PMID: 17204385]
[106]
Lv, Q.; Qiao, S.M.; Xia, Y.; Shi, C.; Xia, Y.F.; Chou, G.X.; Wang, Z.T.; Dai, Y.; Wei, Z.F. Norisoboldine ameliorates DSS-induced ulcerative colitis in mice through induction of regulatory T cells in colons. Int. Immunopharmacol., 2015, 29(2), 787-797.
[http://dx.doi.org/10.1016/j.intimp.2015.08.040] [PMID: 26363976]
[107]
Telang, M.; Dhulap, S.; Mandhare, A.; Hirwani, R. Therapeutic and cosmetic applications of mangiferin: A patent review. Expert Opin. Ther. Pat., 2013, 23(12), 1561-1580.
[http://dx.doi.org/10.1517/13543776.2013.836182] [PMID: 24066838]
[108]
Dou, W.; Zhang, J.; Ren, G.; Ding, L.; Sun, A.; Deng, C.; Wu, X.; Wei, X.; Mani, S.; Wang, Z. Mangiferin attenuates the symptoms of dextran sulfate sodium-induced colitis in mice via NF-κB and MAPK signaling inactivation. Int. Immunopharmacol., 2014, 23(1), 170-178.
[http://dx.doi.org/10.1016/j.intimp.2014.08.025] [PMID: 25194678]
[109]
Liu, W.; Liu, Y.; Wang, Z.; Yu, T.; Lu, Q.; Chen, H. Suppression of MAPK and NF-κ B pathways by schisandrin B contributes to attenuation of DSS-induced mice model of inflammatory bowel disease. Pharmazie, 2015, 70(9), 598-603.
[PMID: 26492645]
[110]
Zhang, J.; Dou, W.; Zhang, E.; Sun, A.; Ding, L.; Wei, X.; Chou, G.; Mani, S.; Wang, Z. Paeoniflorin abrogates DSS-induced colitis via a TLR4-dependent pathway. Am. J. Physiol. Gastrointest. Liver Physiol., 2014, 306(1), G27-G36.
[http://dx.doi.org/10.1152/ajpgi.00465.2012] [PMID: 24232001]
[111]
Yan, F.; Wang, L.; Shi, Y.; Cao, H.; Liu, L.; Washington, M.K.; Chaturvedi, R.; Israel, D.A.; Cao, H.; Wang, B.; Peek, R.M., Jr; Wilson, K.T.; Polk, D.B. Berberine promotes recovery of colitis and inhibits inflammatory responses in colonic macrophages and epithelial cells in DSS-treated mice. Am. J. Physiol. Gastrointest. Liver Physiol., 2012, 302(5), G504-G514.
[http://dx.doi.org/10.1152/ajpgi.00312.2011] [PMID: 22173918]
[112]
Lee, S.J.; Shin, J.S.; Choi, H.E.; Lee, K.G.; Cho, Y.W.; An, H.J.; Jang, D.S.; Jeong, J.C.; Kwon, O.K.; Nam, J.H.; Lee, K.T. Chloroform fraction of Solanum tuberosum L. cv Jayoung epidermis suppresses LPS-induced inflammatory responses in macrophages and DSS-induced colitis in mice. Food Chem. Toxicol., 2014, 63, 53-61.
[http://dx.doi.org/10.1016/j.fct.2013.10.040] [PMID: 24184733]
[113]
Sánchez-Fidalgo, S.; Sánchez de Ibargüen, L.; Cárdeno, A.; Alarcón de la Lastra, C. Influence of extra virgin olive oil diet enriched with hydroxytyrosol in a chronic DSS colitis model. Eur. J. Nutr., 2012, 51(4), 497-506.
[http://dx.doi.org/10.1007/s00394-011-0235-y] [PMID: 21874330]
[114]
Sánchez-Fidalgo, S.; Cárdeno, A.; Sánchez-Hidalgo, M.; Aparicio-Soto, M.; de la Lastra, C.A. Dietary extra virgin olive oil polyphenols supplementation modulates DSS-induced chronic colitis in mice. J. Nutr. Biochem., 2013, 24(7), 1401-1413.
[http://dx.doi.org/10.1016/j.jnutbio.2012.11.008] [PMID: 23337347]
[115]
Sánchez-Fidalgo, S.; Cárdeno, A.; Sánchez-Hidalgo, M.; Aparicio-Soto, M.; Villegas, I.; Rosillo, M.A.; de la Lastra, C.A. Dietary unsaponifiable fraction from extra virgin olive oil supplementation attenuates acute ulcerative colitis in mice. Eur. J. Pharm. Sci., 2013, 48(3), 572-581.
[http://dx.doi.org/10.1016/j.ejps.2012.12.004] [PMID: 23238173]
[116]
Shin, J.S.; Cho, E.J.; Choi, H.E.; Seo, J.H.; An, H.J.; Park, H.J.; Cho, Y.W.; Lee, K.T. Anti-inflammatory effect of a standardized triterpenoid-rich fraction isolated from Rubus coreanus on dextran sodium sulfate-induced acute colitis in mice and LPS-induced macrophages. J. Ethnopharmacol. 2014, 158(Pt A), 291-300.
[http://dx.doi.org/10.1016/j.jep.2014.10.044] [PMID: 25446582]
[117]
Choi, Y.H.; Bae, J.K.; Chae, H.S.; Choi, Y.O.; Nhoek, P.; Choi, J.S.; Chin, Y.W. Isoliquiritigenin ameliorates dextran sulfate sodium-induced colitis through the inhibition of MAPK pathway. Int. Immunopharmacol., 2016, 31, 223-232.
[http://dx.doi.org/10.1016/j.intimp.2015.12.024] [PMID: 26771170]
[118]
Guo, T.; Lin, Q.; Li, X.; Nie, Y.; Wang, L.; Shi, L.; Xu, W.; Hu, T.; Guo, T.; Luo, F. Octacosanol attenuates inflammation in both RAW264. 7 macrophages and a mouse model of colitis. J. Agric. Food Chem., 2017, 65(18), 3647-3658.
[http://dx.doi.org/10.1021/acs.jafc.6b05465] [PMID: 28122452]
[119]
Almeer, R.S.; Mahmoud, S.M.; Amin, H.K.; Abdel Moneim, A.E. Ziziphus spina-christi fruit extract suppresses oxidative stress and p38 MAPK expression in ulcerative colitis in rats via induction of Nrf2 and HO-1 expression. Food Chem. Toxicol., 2018, 115, 49-62.
[http://dx.doi.org/10.1016/j.fct.2018.03.002] [PMID: 29518435]
[120]
Camacho-Barquero, L.; Villegas, I.; Sánchez-Calvo, J.M.; Talero, E.; Sánchez-Fidalgo, S.; Motilva, V.; Alarcón de la Lastra, C. Curcumin, a Curcuma longa constituent, acts on MAPK p38 pathway modulating COX-2 and iNOS expression in chronic experimental colitis. Int. Immunopharmacol., 2007, 7(3), 333-342.
[http://dx.doi.org/10.1016/j.intimp.2006.11.006] [PMID: 17276891]
[121]
Schwanke, R.C.; Marcon, R.; Meotti, F.C.; Bento, A.F.; Dutra, R.C.; Pizzollatti, M.G.; Calixto, J.B. Oral administration of the flavonoid myricitrin prevents dextran sulfate sodium-induced experimental colitis in mice through modulation of PI3K/Akt signaling pathway. Mol. Nutr. Food Res., 2013, 57(11), 1938-1949.
[http://dx.doi.org/10.1002/mnfr.201300134] [PMID: 23861337]
[122]
Ren, G.; Sun, A.; Deng, C.; Zhang, J.; Wu, X.; Wei, X.; Mani, S.; Dou, W.; Wang, Z. The anti-inflammatory effect and potential mechanism of cardamonin in DSS-induced colitis. Am. J. Physiol. Gastrointest. Liver Physiol., 2015, 309(7), G517-G527.
[http://dx.doi.org/10.1152/ajpgi.00133.2015] [PMID: 26251468]
[123]
Sahu, B.D.; Kumar, J.M.; Sistla, R. Fisetin, a dietary flavonoid, ameliorates experimental colitis in mice: Relevance of NF-κB signaling. J. Nutr. Biochem., 2016, 28, 171-182.
[http://dx.doi.org/10.1016/j.jnutbio.2015.10.004] [PMID: 26878795]
[124]
Yang, X.L.; Guo, T.K.; Wang, Y.H.; Huang, Y.H.; Liu, X.; Wang, X.X.; Li, W.; Zhao, X.; Wang, L.P.; Yan, S.; Wu, D.; Wu, Y.J. Ginsenoside Rd attenuates the inflammatory response via modulating p38 and JNK signaling pathways in rats with TNBS-induced relapsing colitis. Int. Immunopharmacol., 2012, 12(2), 408-414.
[http://dx.doi.org/10.1016/j.intimp.2011.12.014] [PMID: 22227208]
[125]
Sánchez-Fidalgo, S.; Cárdeno, A.; Villegas, I.; Talero, E.; de la Lastra, C.A. Dietary supplementation of resveratrol attenuates chronic colonic inflammation in mice. Eur. J. Pharmacol., 2010, 633(1-3), 78-84.
[http://dx.doi.org/10.1016/j.ejphar.2010.01.025] [PMID: 20132809]