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Mini-Reviews in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1389-5575
ISSN (Online): 1875-5607

Review Article

Therapeutic Potential of Vanillin and its Main Metabolites to Regulate the Inflammatory Response and Oxidative Stress

Author(s): Carlos S.M. Bezerra-Filho, Joice N. Barboza, Marilia T.S. Souza, Peter Sabry, Nasser S.M. Ismail and Damião P. de Sousa*

Volume 19, Issue 20, 2019

Page: [1681 - 1693] Pages: 13

DOI: 10.2174/1389557519666190312164355

Price: $65

Abstract

Many phenolic compounds found in foods and medicinal plants have shown interesting therapeutic potential and have attracted the attention of the pharmaceutical industry as promising pharmacologically active compounds in health promotion and disease prevention. Vanillin is a phenolic aldehyde, widely used as a flavoring agent in the food, pharmaceutical, and cosmetics industries. A variety of pharmacological activities has been attributed to this compound and its main metabolites, vanillic acid and vanillyl alcohol, including their anti-inflammatory ability. The relationship of the anti- inflammatory effects of vanillin, vanillic acid, and vanillyl alcohol and their actions on oxidative stress is well established. Considering that the inflammatory process is related to several pathologies, including new diseases with few therapeutic options, and limited efficiency, the search for effective treatment strategies and discovery of new anti-inflammatory agents capable of modulating inflammation becomes necessary. Therefore, in this review, we discuss the therapeutic potential of vanillin and its main metabolites for the treatment of inflammatory diseases and their actions on redox status. In addition, the molecular docking evaluation of vanillin, its metabolites and isoeugenol were carried out into the phospholipase A2 binding site.

Keywords: Natural products, vanillin, vanillic acid, vanillyl alcohol, anti-inflammatory, antioxidant.

Graphical Abstract
[1]
Blando, F.; Albano, C.; Liu, Y.; Nicoletti, I.; Corradini, D.; Tommasi, N.; Gerardi, C.; Mita, G.; Kitts, D.D. Polyphenolic composition and antioxidant activity of under-utilised Prunus mahaleb L. fruit. J. Sci. Food Agric., 2016, 96(8), 2641-2649.
[2]
Chuang, C.C.; Mclntosh, M.K. Potential mechanisms by which polyphenol-rich grapes prevent obesity-mediated inflammation and metabolic diseases. Annu. Rev. Nutr., 2011, 31, 155-176.
[3]
Leouifoudi, I.; Harnafi, H.; Zyad, A. Olive Mill Waste extracts: polyphenols content, antioxidant and antimicrobial activities. Adv. Pharmacol. Sci., 2015, 2015, 1-11.
[4]
Mezni, F.; Shili, S.; Ali, N.B.; Khouja, M.L. Khaldi, Maaroufi, A. Evaluation of Pistacia lentiscus seed oil and phenolic compounds for in vitro antiproliferative effects against bhk21 cells. Pharm. Biol., 2016, 54(5), 747-751.
[5]
Saini, R.; Dangwall, K.; Singh, H.; Garg, V. Antioxidant and antiproliferative activities of phenolics isolated from fruits of Himalayan yellow raspberry (Rubus ellipticus). J. Food Sci. Technol., 2014, 51(11), 3369-3375.
[6]
Gallage, N.J.; Hansen, E.H.; Kannangara, R.; Olsen, C.E.; Motawia, M.S.; Jørgensen, K.; Inger, H.; Hebelstrup, K.; Grisoni, M.; Møller, B.L. Vanillin formation from ferulic acid in Vanilla planifolia is catalysed by a single enzyme. Nat. Commun., 2014, 5, 4037.
[7]
Yang, W.; Tang, H.; Ni, J.; Wu, Q.; Hua, D.; Tao, F.; Xu, P. Characterization of two Streptomyces enzymes that convert ferulic acid to vanillin. PLoS One, 2013, 8(6)e67339
[8]
Liang, J.A.; Wu, S.L.; You, H.Y.; School, C.Y.; Ho, T.Y. Vanillin inhibits matrix metalloproteinase-9 expression through down-regulation of nuclear factor-κB signaling pathway in human hepatocellular carcinoma cells. Mol. Pharmacol., 2009, 75, 151-157.
[9]
Lirdprapamongkol, K.; Sakurai, H.; Suzuki, S.; Koizumi, K.; Prangsaengtong, O.; Viriyaroj, A.; Ruchirawat, S.; Svasti, J.; Saiki, I. Albany Adult School I. Vanillin enhances TRAIL-induced apoptosis in cancer cells through stage of NF-κB activation. In Vivo, 2010, 24(4), 501-506.
[10]
Dhanalakshmi, C.; Manivasagam, T.; Nataraj, J.; Justin Thenmozhi, A.; This, M. Neurosupportive role of vanillin, the natural phenolic compound, on rotenone induced neurotoxicity in SH-SY5Y neuroblastoma cells. Evid. Based Complement. Alternat. Med., 2015, 2015, 1-11.
[11]
Murakami, Y.; Hirata, A.; Ito, S.; Shoji, M.; Tanaka, S.; Yasui, T.; Machino, M.; Fujisawa, S. Re-evaluation of cyclooxygenase-2-inhibiting activity of vanillin and guaiacol in macrophages stimulated with lipopolysaccharide. Anticancer Res., 2007, 27(2), 801-807.
[12]
Tai, A.; Sawano, T.; Yazama, F.; Ito, H. Evaluation of the antioxidant activity of vanillin by using multiple antioxidant assays. Biochim. Biophys. Acta, 2011, 1810(2), 170-177.
[13]
Bezerra, D.P.; Soares, A.K.; de Sousa, D.P. Overview of the role of vanillin on redox status and cancer development. Oxid. Med. Cell. Longev., 2016, 20169734816
[14]
Kumar, V.; Abbas, A.; Aster, J.C. Robbins & Cotran Pathologic Patologia-Bases of Diseases, 9th ed; Elsevier: Rio de Janeiro, Brazil, 2013, pp. 29-32.
[15]
Fischer, R.; Maier, O. Interrelation of oxidative stress and inflammation in neurodegenerative disease: Role of TNF. Oxid. Med. Cell. Longev., 2015, 2015610813
[16]
Smallwood, M.J.; Nissim, A.; Knight, A.R.; Whiteman, M.; Haigh, R.; Winyard, P.G. Oxidative stress in autoimmune rheumatic diseases. Free Radic. Biol. Med., 2018, 2018, S0891-S5849.
[17]
Ayala-Fontánez, N.; Soler, D.C.; McCormick, T.S. Current knowledge on psoriasis and autoimmune diseases. Psoriasis (Auckl), 2016, 6, 7-32.
[18]
Bel, E.H.; Brinke, A.T. New anti-eosinophil drugs for asthma and COPD: Targeting the trait! Chest, 2017, 152(6), 1276-1282.
[19]
Thomson, A.B.; Gupta, M.; Freeman, J. Use of tumor necrosis factor-blockers for Crohn’s disease. World J. Gastroenterol., 2012, 18(35), 4823-4854.
[20]
Zhai, K.F.; Duan, H.; Luo, L.; Cao, W.G.; Han, F.K.; Shan, L.L.; Fang, X.M. Protective effects of paeonol on inflammatory response in IL-1β-induced human fibroblast-like Synoviocytes and rheumatoid arthritis progression via modulating NF-κB pathway. Inflammopharmacology, 2017, 25(5), 523-532.
[21]
Pisoschi, A.M.; Pop, A. The role of antioxidants in the chemistry of oxidative stress: A review. Eur. J. Med. Chem., 2015, 97, 55-74.
[22]
Sies, H. Oxidative stress: From basic research clinical application. Am. J. Med., 1991, 91(3), S31-S38.
[23]
Sies, H. Oxidative stress: A concept in redox biology and medicine. Redox Biol., 2015, 4, 180-183.
[24]
Moniruzzaman, M.; Lee, G.; Bose, S.; Choi, M.; Jung, J.K.; Lee, H.; Cho, J. Antioxidant and Anti-inflammatory activities of N-((3, 4-dihydro-2H-benzo [h] chromene-2-yl) methyl)-4-methoxyaniline in LPS-induced BV2 Microglial Cells. Biol. Pharm. Bull., 2015, 38(12), 1831-1835.
[25]
Gutiérrez-Grijalva, E.P.; Picos-Salas, M.A.; Leyva-López, N.; Criollo-Mendoza, M.S.; Vazquez-Olivo, G.; Heredia, J.B. Flavonoids and Phenolic Acids from Oregano: Occurrence, Biological Activity and Health Benefits. Plants, 2017, 7(1), 2.
[26]
Lesjak, M.; Nataša, I.B.; Pintać, S.D.; Majkić, T.; Bekvalac, K.; Orčić, D.; Neda Dukić, N.M. Antioxidant and anti-inflammatory activities of quercetin and its derivatives. J. Funct. Foods, 2018, 40, 68-75.
[27]
Jang, Y.W.; Lee, J.Y.; Kim, C.J. Anti-cannibalistic activity of phenolic compounds from the roots of Gastrodia elata Bl. Int. Immunopharmacol., 2010, 10(2), 147-154.
[28]
Wu, S.L.; Chen, J.C.; Li, C.C.; So, H.Y.; Ho, T.Y.; School, C.Y. Vanillin improves and prevents trinitrobenzene sulfonic acid-induced colitis in mice. J. Pharmacol. Exp. Ther., 2009, 330(2), 370-376.
[29]
Wojdasiewicz, P.; Poniatowski, Ł. Szukiewicz, D. The role of inflammatory and anti-inflammatory cytokines in the pathogenesis of osteoarthritis. Mediators Inflamm., 2014, 2014, 1-19.
[30]
Arab, H.H.; Salama, S.A.; Omar, H.A.; Arafa, E.S.A.; Principe, I.A. Diosmin protects against ethanol-induced gastric injury in rats: novel anti-ulcer actions. PLoS One, 2015, 10(3)e0122417
[31]
Sarkar, N.; Purkayastha, S.; Sarkar, B.; Guha, D. Modulation of gastric mucosal mast cell population: Role of vestibulo cerebellar lesion. Indian J. Exp. Biol., 2006, 44, 627-634.
[32]
Thomas, D.; Govindhan, S.; Baiju, E.C.; Arjun, G.; Kunnumakkara, A.B.; Padikkala, J. Cyperus rotundus L. prevents non-steroidal anti-inflammatory drug-induced gastric mucosal damage by inhibiting oxidative stress. J. Basic Clin. Physiol. Pharmacol., 2015, 26(5), 485-490.
[33]
Al-Asmari, A.; Al Shahrani, H.; Al Masri, N.; Al Faraidi, A.; Elfaki, I.; Arshaduddin, M. Vanillin abrogates ethanol-induced gastric injury in rats via modulation of gastric secretion, oxidative stress and inflammation. Toxicol. Rep., 2016, 3, 105-113.
[34]
Molderings, G.J.; Meis, K.; Kolck, U.W.; Homann, J.; Frieling, T. Comparative analysis of mutation of kit tyrosine kinase in mast cells from patients with systemic mast cell activation syndrome and healthy subjects. Immunogenetics, 2010, 62(11-12), 721-727.
[35]
An, S.M.; Park, C.H.; Heo, J.C.; Park, J.Y.; Woo, S.U.; Seo, J.H.; Lee, S.H. Gastrodia Elata Blume protects against stress-induced gastric mucosal lesions in mice. Int. J. Mol. Med., 2007, 20(2), 209-215.
[36]
Park, S.; Kim, D.S.; Kang, S. Gastrodia Elata Blume water extracts improve insulin resistance by decreasing body fat in diet-induced obese rats: vanillin and 4-hydroxybenzaldehyde are the bioactive candidates. Eur. J. Nutr., 2011, 50(2), 107-118.
[37]
Makni, M.; Chtourou, Y.; Fetoui, H.; Garoui, E.M.; Boudawara, T.; Zeghal, N. Evaluation of the antioxidant, anti-inflammatory and hepatoprotective properties of vanillin in carbon fumigants-treated rats. Eur. J. Pharmacol., 2011, 668(1-2), 133-139.
[38]
Galgani, J.E.; Núñez, B.; Videla, L.A. Vanillin suppresses Kupffer cell-related carbon colloidal-induced respiratory burst activity in isolated perfused rat liver: Anti-inflammatory implications. Food Funct., 2012, 3, 1319-1323.
[39]
Kanegae, M.P.; Fonseca, L.M.; Brunetti, I.L.; Silva, S.O.; Ximenes, V.F. The reactivity of ortho-methoxy-substituted catechol radicals with sulfhydryl groups: contribution for the comprehension of the mechanism of stage of NADPH oxidase by apocynin. Biochem. Pharmacol., 2007, 74(3), 457-464.
[40]
Saad, H.B.; Driss, D.; Amara, I.B.; Boudawara, O.; Boudawara, T.; Chaabouni, S.E.; Zeghal, K.M.; Hakim, A. Altered hepatic mRNA expression of immune response‐associated DNA damage in mice liver induced by potassium bromate: Protective role of vanillin. Environ. Toxicol., 2016, 31(12), 1796-1807.
[41]
Li, S.; Tan, H.Y.; Wang, N.; Zhang, Z.J.; Lao, L.; Wong, C.W.; Feng, Y. The role of oxidative stress and antioxidants in liver diseases. Int. J. Mol. Sci., 2015, 16(11), 26087-26124.
[42]
Lam, P.; Cheung, F.; Tan, H.Y.; Wang, N.; Yuen, M.F.; Feng, Y. Hepatoprotective effects of Chinese medicinal herbs: The focus on anti-inflammatory and anti-oxidative activities. Int. J. Mol. Sci., 2016, 17(4), 465.
[43]
Pabla, N.; Dong, Z. Cisplatin nephrotoxicity: Mechanisms and renoprotective strategies. Kidney Int., 2008, 73(9), 994-1007.
[44]
Alhoshani, A.R.; Hafez, M.; Husain, S.; Al-Sheikh, A.M.; Alotaibi, M.R.; Al-Rejaie, S.S.; Al-Shabanah, O.A. Protective effect of rutin supplementation against cisplatin-induced nephrotoxicity in rats. BMC Nephrol., 2017, 18(1), 194-203.
[45]
Lee, H.; Lee, G.; Kim, H.; Bae, H. Paeonol, the major compound of moutan cortex, attenuates cisplatin-induced nephrotoxicity in mice. Evid. Based Complement. Alternat. Med., 2013, 2013, 1-7.
[46]
Elseweidy, M.; Askar, M.E.; Elswefy, S.E.; Shawky, M. The new modulator Vanillin candidate renal injury induced by cisplatin in experimental rats. Cytokine, 2017, 99, 260-265.
[47]
Fouad, A.A.; Al-Melhim, W.N. Vanillin mitigates the adverse impact of cisplatin and methotrexate on rat kidneys. Hum. Exp. Toxicol., 2017, 2017, 1-7.
[48]
Makni, M.; Chtourou, Y.; Garoui, E.M.; Boudawara, T.; Fetoui, H. Fumigants Carbon-induced nephrotoxicity and DNA damage in rats: protective role of vanillin. Hum. Exp. Toxicol., 2012, 31(8), 844-852.
[49]
Ho, K.; Yazan, L.S.; Ismail, N.; Ismail, M. Toxicology study of vanillin on rats orally and intra-peritoneal administration. Food Chem. Toxicol., 2011, 49(1), 25-30.
[50]
Lin, L.C.; Chen, Y.F.; Lee, W.C.; Wu, Y.T.; Tsai, T.H. Pharmacokinetics of gastrodin and its metabolite p-hydroxybenzyl alcohol in rat blood, brain and bile by microdialysis coupled to LC-MS/ MS. J. Pharm. Biomed. Anal., 2008, 48(3), 909-917.
[51]
Saad, H.; Kharrat, N.; Driss, D.; Gargouri, M.; Marrakchi, R.; Jammoussi, K.; Hakim, A. Effects of vanillin on potassium bromate-induced neurotoxicity in adult mice: Impact on behavior, oxidative stress, inflammation and gene expression, fatty acid composition. Arch. Physiol. Biochem., 2017, 123(3), 165-174.
[52]
Tsai, C.F.; Huang, C.L.; Lin, Y.L.; Lee, Y.C.; Yang, Y.C.; Huang, N.K. The neuroprotective effects of an extract of Gastrodia Elata. J. Ethnopharmacol., 2011, 138(1), 119-125.
[53]
Tansey, M.G.; Goldberg, M.S. Neuroinflammation in Parkinson’s disease: Its role in neuronal death and implications for therapeutic intervention. Neurobiol. Dis., 2010, 37(3), 510-518.
[54]
Virgilio, A.; Greco, A.; Fabbrini, G.; Inghilleri, M.; Rizzo, M.I.; Gallo, A.; Vincentiis, M. Parkinson’s disease: Autoimmunity and neuroinflammation. Autoimmun. Rev., 2016, 15(10), 1005-1011.
[55]
Yan, X.; Liu, D.F.; Zhang, X.Y.; Liu, D.; Xu, S.Y.; Chen, G.X.; Liu, J.X. Vanillin protects dopaminergic neurons against inflammation-mediated cell death by inhibiting ERK1/2, p38 and the NF-κB signaling pathway. Int. J. Mol. Sci., 2017, 18(2), 389.
[56]
Dhanalakshmi, C.; Janakiraman, U.; Manivasagam, T.; Thenmozhi, A.J.; Essa, M.; Kalandar, A.; Guillemin, G.J. Vanillin attenuated behavioral impairments, neurochemical deficts, oxidative stress and apoptosis against rotenone induced rat model of Parkinson’s disease. Neurochem. Res., 2016, 41(8), 1899-1910.
[57]
Cheng, H.M.; Chen, F.Y.; Li, C.C.; So, H.Y.; Liao, Y.F.; Ho, T.Y.; School, C.Y. Oral administration of Vanillin Improves Imiquimod-Induced Psoriatic Skin Inflammation in mice. J. Agric. Food Chem., 2017, 65(47), 10233-10242.
[58]
Lim, E.J.; Kang, H.J.; Jung, H.J.; Song, Y.S.; Lim, C.J.; Park, E.H. Anti-angiogenic, anti-inflammatory and anti-nociceptive activities of vanillin in ICR mice. Biomol. Ther. , 2008, 16, 132-136.
[59]
He, F.; Duan, X.; Dai, R.; Wang, W.; Yang, C.; Lin, Q. Protective Effects of ethyl acetate extraction from Gastrodia Elata blume on blood-brain barrier in cerebral focal ischemia reperfusion. Afr. J. Tradit. Complement. Altern. Med., 2016, 13(4), 199-209.
[60]
Strand, L.P.; Scheline, R.R. The metabolism of vanillin and isovanillin in the rat. Xenobiotica, 1975, 5(1), 49-63.
[61]
Chao, W.W.; Hong, Y.H.; Chen, M.L.; Lin, B.F. Inhibitory effects of Angelica sinensis ethyl acetate extract and major compounds on NF-κB trans-activation activity and LPS-induced inflammation. J. Ethnopharmacol., 2010, 129(2), 244-249.
[62]
Hua, Y.; Xue, W.; Zhang, M.; Wei, Y.; Ji, P. Metabonomics study on the hepatoprotective effect of polysaccharides from different preparations of Angelica sinensis. J. Ethnopharmacol., 2014, 151(3), 1090-1099.
[63]
Bunel, V.; Antoine, M.H.; Nortier, J.; Duez, P.; Stévigny, C. Nephroprotective effects of ferulic acid, Z-ligustilide and E-ligustilide isolated from Angelica sinensis against cisplatin toxicity in vitro. Toxicol. In Vitro, 2015, 29(3), 458-467.
[64]
Nbalagan, V.; Raju, K.; Shanmugam, S. Manoharan. Assessment of Lipid Peroxidation and Antioxidant Status in Vanillic Acid Treated 7, 12-Dimethylbenz [a] anthracene Induced Hamster Buccal Pouch Carcinogenesis. J. Clin. Diagn. Res: JCDR, 2017, 11(3), BF01-BF04.
[65]
Chou, T.H.; Ding, H.Y.; Hung, W.J.; Liang, C.H. Antioxidative characteristics and inhibition of α‐melanocyte‐stimulating hormone‐stimulated melanogenesis of vanillin and vanillic acid from Origanum vulgare. Exp. Dermatol., 2010, 19(8), 742-750.
[66]
Prince, P.S.M.; Rajakumar, S.; Dhanasekar, K. Protective effects of vanillic acid on electrocardiogram, lipid peroxidation, antioxidants, proinflammatory markers and histopathology in isoproterenol induced cardiotoxic rats. Eur. J. Pharmacol., 2011, 668(1-2), 233-240.
[67]
Kim, S.J.; Kim, M.C.; Um, J.Y.; Hong, S.H. The beneficial effect of vanillic acid on ulcerative colitis. Molecules, 2010, 15(10), 7208-7217.
[68]
Kim, M.C.; Kim, S.J.; Kim, D.S.; Jeon, Y.D.; Park, S.J.; Lee, H.S.; Um, J.Y.; Hong, S.H. Vanillic acid inhibits inflammatory mediators by suppressing NF-κB in lipopolysaccharide-stimulated peritoneal mouse macrophages. Immunopharmacol. Immunotoxicol., 2011, 33(3), 525-532.
[69]
Itoh, A.; Isoda, K.; Kondoh, M.; Kawase, M.; Kobayashi, M.; Tamesada, M.; Yagi, K. Hepatoprotective effect of syringic acid and vanillic acid on concanavalin a-induced liver injury. Biol. Pharm. Bull., 2009, 32(7), 1215-1219.
[70]
Itoh, A.; Isoda, K.; Kondoh, M.; Kawase, M.; Watari, A.; Kobayashi, M.; Yagi, K. Hepatoprotective effect of syringic acid and vanillic acid on CCl4-induced liver injury. Biol. Pharm. Bull., 2010, 33(6), 983-987.
[71]
Kakalij, M.R.; Tejaswini, G.; Patil, M.A.; Dinesh, K.B.; Diwan, P.V. Vanillic acid ameliorates cationic bovine serum albumin induced immune complex glomerulonephritis in BALB/c mice. Drug Dev. Res., 2016, 77(4), 171-179.
[72]
Amin, F.U.; Shah, S.A.; Kim, M.O. Vanillic acid attenuates Aβ 1-42-induced oxidative stress and cognitive impairment in mice. Sci. Rep., 2017, 7, 40753.
[73]
Huang, S.H.; Lin, C.M.; Chiang, B.H. Protective effects of Angelica sinensis extract on amyloid β-peptide-induced neurotoxicity. Phytomedicine, 2008, 15(9), 710-721.
[74]
Zhan, H.D.; Zhou, H.Y.; Sui, Y.P.; Du, X.L.; Wang, W.H.; Dai, L.; Jiang, T.L. The rhizome of Gastrodia elata Blume-An ethnopharmacological review. J. Ethnopharmacol., 2016, 18(9), 361-385.
[75]
Kim, I.S.; Choi, D.K.; Jung, H.J. Neuroprotective effects of vanillyl alcohol in Gastrodia elata Blume through suppression of oxidative stress and anti-apoptotic activity in toxin-induced dopaminergic MN9D cells. Molecules, 2011, 16(7), 5349-5361.
[76]
An, H.; Kim, I.S.; Koppula, S.; Kim, B.W.; Park, P.J.; Lim, B.O.; Choi, D.K. Protective effects of Gastrodia elata Blume on MPP+-induced cytotoxicity in human dopaminergic SH-SY5Y cells. J. Ethnopharmacol., 2010, 130(2), 290-298.
[77]
Jung, H.J.; Song, Y.S.; Lim, C.J.; Park, E.H. Anti-angiogenic, anti-inflammatory and anti-nociceptive activities of vanillyl alcohol. Arch. Pharm. Res., 2008, 31(10), 1275-1279.
[78]
Murakami, M.; Kudo, I. Phospholipase A2. J. Biochem., 2002, 131(3), 285-292.
[79]
Dileep, K.V.; Remya, C.; Cerezo, J.; Fassihi, A.; Pérez-Sánchez, H.; Sadasivan, C. Comparative studies on the inhibitory activities of selected benzoic acid derivatives against secretory phospholipase A2, a key enzyme involved in the inflammatory pathway. Mol. Biosyst., 2015, 11(7), 1973-1979.
[80]
Yamada, M.; Okada, Y.; Yoshida, T.; Nagasawa, T. Biotransformation of isoeugenol to vanillin by Pseudomonas putida IE27 cells. Appl. Microbiol. Biotechnol., 2007, 73(5), 1025-1030.
[81]
Zhao, L.Q.; Sun, Z.H.; Zheng, P.; Zhu, L.L. Biotransformation of isoeugenol to vanillin by a novel strain of Bacillus fusiformis. Biotechnol. Lett., 2005, 27(19), 1505-1509.
[82]
Berman, H.M.; Westbrook, J.; Feng, Z.; Gilliand, G.; Bhat, T.N.; Weissig, H.; Bourne, P.E. The Protein Data Bank. Nucleic Acids Res., 2000, 28(1), 235-242.
[83]
Van Den Heuvel, R.H.; Fraaije, M.W.; Mattevi, A.; Van Berkel, W.J. Asp-170 is crucial for the redox properties of vanillyl-alcohol oxidase. J. Biol. Chem., 2000, 275(20), 14799-14808.
[84]
Janssen, M.J.; Van Der Wiel, W.A.; Beiboer, S.H.; Van Kampen, M.D.; Verheji, H.M.; Slotboom, A.J.; Egmond, M.R. Catalytic role of the active site histidine of porcine pancreatic phospholipase A2 probed by the variants H48Q, H48N and H48K. Protein Eng., 1999, 12(6), 497-503.
[85]
Tatulian, S.A. Structural effects of covalent inhibition of phospholipase A2 suggest allosteric coupling between membrane binding and catalytic sites. Biophys. J., 2003, 84(3), 1773-1783.
[86]
Shukla, P.K.; Gautam, L.; Sinha, M.; Kaur, P.; Sharma, S.; Singh, T.P. Structures and binding studies of the complexes of phospholipase A2 with five inhibitors. Biochim. Biophys. Acta, 2015, 1854(4), 269-27.

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