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Inflammopharmacology

, Volume 27, Issue 1, pp 5–13 | Cite as

Black pepper and its bioactive constituent piperine: promising therapeutic strategies for oral lichen planus

  • Jing-Ya Yang
  • Jing Zhang
  • Gang ZhouEmail author
Review
  • 105 Downloads

Abstract

Oral lichen planus (OLP) is a common T cell-mediated chronic inflammatory disease with malignant potential and unclear etiology. The present study suggests that antigen-specific mechanisms in which dentritic cells, T lymphocytes and NF-κB signaling pathway play critical roles, are involved in the pathogenesis of OLP. Additionally, it has been indicated that altered expression of cyclooxygenase 2 (COX-2) and imbalanced oxidant-antioxidant status as well as psychological issue may act as promoters to the development of OLP. Therapies for OLP are primarily aimed to control symptoms and a specific cure is not yet available. Black pepper and its principle bioactive compound piperine have been reported to possess remarkable pharmacological activities. Not only has piperine been evidenced to exhibit repressive effects on the maturation of dentritic cells, the proliferation, activation and function of T lymphocytes as well as the NF-κB signaling pathway, but also to suppress the overproduction of COX-2 and weaken the oxidative stress. Furthermore, piperine might be a possible agent for alleviating psychological disorders and preventing carcinogenesis. Given all these into consideration, piperine may be a novel and effective therapeutic strategy for OLP.

Keywords

Black pepper Piperine Oral lichen planus 

Notes

Acknowledgement

This work was supported by grants from the National Natural Science Foundation of China (nos. 81771080, 81371147) to Gang Zhou.

Compliance with ethical standards

Conflict of interest

All authors declare no conflict of interest regarding the publication of this paper.

References

  1. Abdel HRM, Fawzy MM, Metwally D et al (2012) DNA polymorphisms and tissue cyclooxygenase-2 expression in oral lichen planus: a case–control study. J Eur Acad Dermatol Venereol 26(9):1122–1126Google Scholar
  2. Abdolsamadi H, Rafieian N, Goodarzi MT et al (2014) Levels of salivary antioxidant vitamins and lipid peroxidation in patients with oral lichen planus and healthy individuals. Chonnam Med J. 50(2):58–62Google Scholar
  3. Agha-Hosseini F, Mirzaii-Dizgah I, Mikaili S, Abdollahi M (2009) Increased salivary lipid peroxidation in human subjects with oral lichen planus. Int J Dent Hyg. 7(4):246–250Google Scholar
  4. Alrashdan MS, Cirillo N, McCullough M (2016) Oral lichen planus: a literature review and update. Arch Dermatol Res 308(8):539–551Google Scholar
  5. Alshahrani S, Baccaglini L (2014) Psychological screening test results for stress, depression, and anxiety are variably associated with clinical severity of recurrent aphthous stomatitis and oral lichen planus. J Evid Based Dent Pract. 14(4):206–208Google Scholar
  6. Alves MG, Do Carmo Carvalho BF, Balducci I, Cabral LA, Nicodemo D, Almeida JD (2015) Emotional assessment of patients with oral lichen planus. Int J Dermatol 54(1):29–32Google Scholar
  7. Amirchaghmaghi M, Hashemy SI, Alirezaei B et al (2016) Evaluation of plasma isoprostane in patients with oral lichen planus. J Dent (Shiraz). 17(1):21–25Google Scholar
  8. Azizi A, Farshchi F (2012) Comparison of salivary and plasma antioxidant levels in lichen planus patients and healthy subjects. J Oral Pathol Med 41(7):524–526Google Scholar
  9. Bae GS, Kim MS, Jung WS et al (2010) Inhibition of lipopolysaccharide-induced inflammatory responses by piperine. Eur J Pharmacol 642(1–3):154–162Google Scholar
  10. Bae GS, Kim JJ, Park KC et al (2012) Piperine inhibits lipopolysaccharide-induced maturation of bone-marrow-derived dendritic cells through inhibition of ERK and JNK activation. Phytother Res. 26(12):1893–1897Google Scholar
  11. Balkwill F, Mantovani A (2001) Inflammation and cancer: back to Virchow. Lancet 357(9255):539–545Google Scholar
  12. Bang JS, Oh DH, Choi HM et al (2009) Anti-inflammatory and antiarthritic effects of piperine in human interleukin 1beta-stimulated fibroblast-like synoviocytes and in rat arthritis models. Arthritis Res Ther. 11(2):R49Google Scholar
  13. Barrett AW, Cruchley AT, Williams DM (1996) Oral mucosal Langerhans’ cells. Crit Rev Oral Biol Med 7(1):36–58Google Scholar
  14. Battino M, Greabu M, Totan A et al (2008) Oxidative stress markers in oral lichen planus. BioFactors 33(4):301–310Google Scholar
  15. Bayer AL, Pugliese A, Malek TR (2013) The IL-2/IL-2R system: from basic science to therapeutic applications to enhance immune regulation. Immunol Res 57(1–3):197–209Google Scholar
  16. Buczko P, Zalewska A, Szarmach I (2015) Saliva and oxidative stress in oral cavity and in some systemic disorders. J Physiol Pharmacol 66(1):3–9Google Scholar
  17. Butt MS, Pasha I, Sultan MT, Randhawa MA, Saeed F, Ahmed W (2013) Black pepper and health claims: a comprehensive treatise. Crit Rev Food Sci Nutr 53(9):875–886Google Scholar
  18. Chen Y, Zhang W, Geng N, Tian K, Jack WL (2008) MMPs, TIMP-2, and TGF-beta1 in the cancerization of oral lichen planus. Head Neck 30(9):1237–1245Google Scholar
  19. Chuchawankul S, Khorana N, Poovorawan Y (2012) Piperine inhibits cytokine production by human peripheral blood mononuclear cells. Genet Mol Res 11(1):617–627Google Scholar
  20. Cortés-Ramírez DA, Rodríguez-Tojo MJ, Gainza-Cirauqui ML, Martínez-Conde R, Aguirre-Urizar JM (2010) Overexpression of cyclooxygenase-2 as a biomarker in different subtypes of the oral lichenoid disease. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 110(6):738–743Google Scholar
  21. Crincoli V, Di BMB, Scivetti M, Lucchese A, Tecco S, Festa F (2011) Oral lichen planus: update on etiopathogenesis, diagnosis and treatment. Immunopharmacol Immunotoxicol 33(1):11–20Google Scholar
  22. Danielsson K, Ebrahimi M, Wahlin YB, Nylander K, Boldrup L (2012) Increased levels of COX-2 in oral lichen planus supports an autoimmune cause of the disease. J Eur Acad Dermatol Venereol 26(11):1415–1419Google Scholar
  23. Darczuk D, Krzysciak W, Vyhouskaya P et al (2016) Salivary oxidative status in patients with oral lichen planus. J Physiol Pharmacol 67(6):885–894Google Scholar
  24. Deng Y, Sriwiriyajan S, Tedasen A, Hiransai P, Graidist P (2016) Anti-cancer effects of Piper nigrum via inducing multiple molecular signaling in vivo and in vitro. J Ethnopharmacol 188:87–95Google Scholar
  25. Derosa G, Maffioli P, Sahebkar A (2016) Piperine and its role in chronic diseases. Adv Exp Med Biol 928:173–184Google Scholar
  26. Doucette CD, Greenshields AL, Liwski RS, Hoskin DW (2015a) Piperine blocks interleukin-2-driven cell cycle progression in CTLL-2 T lymphocytes by inhibiting multiple signal transduction pathways. Toxicol Lett 234(1):1–12Google Scholar
  27. Doucette CD, Rodgers G, Liwski RS, Hoskin DW (2015b) Piperine from black pepper inhibits activation-induced proliferation and effector function of T lymphocytes. J Cell Biochem 116(11):2577–2588Google Scholar
  28. Edwards PC, Kelsch R (2002) Oral lichen planus: clinical presentation and management. J Can Dent Assoc 68(8):494–499Google Scholar
  29. El-Rifaie AA, Rashed LA, Doss RW (2015) The role of cyclooxygenase-2 and prostaglandin E2 in the pathogenesis of cutaneous lichen planus. Clin Exp Dermatol 40(8):903–907Google Scholar
  30. Farthing PM, Matear P, Cruchley AT (1990) The activation of Langerhans cells in oral lichen planus. J Oral Pathol Med 19(2):81–85Google Scholar
  31. Federico A, Morgillo F, Tuccillo C, Ciardiello F, Loguercio C (2007) Chronic inflammation and oxidative stress in human carcinogenesis. Int J Cancer 121(11):2381–2386Google Scholar
  32. Fitzpatrick SG, Hirsch SA, Gordon SC (2014) The malignant transformation of oral lichen planus and oral lichenoid lesions: a systematic review. J Am Dent Assoc 145(1):45–56Google Scholar
  33. Gavic L, Cigic L, Biocina LD, Gruden V, Gruden PJS (2014) The role of anxiety, depression, and psychological stress on the clinical status of recurrent aphthous stomatitis and oral lichen planus. J Oral Pathol Med 43(6):410–417Google Scholar
  34. Girardi C, Luz C, Cherubini K, de Figueiredo MA, Nunes ML, Salum FG (2011) Salivary cortisol and dehydroepiandrosterone (DHEA) levels, psychological factors in patients with oral lichen planus. Arch Oral Biol 56(9):864–868Google Scholar
  35. Hritcu L, Noumedem JA, Cioanca O, Hancianu M, Postu P, Mihasan M (2015) Anxiolytic and antidepressant profile of the methanolic extract of Piper nigrum fruits in beta-amyloid (1-42) rat model of Alzheimer’s disease. Behav Brain Funct 11:13Google Scholar
  36. Huang W, Chen Z, Wang Q et al (2013) Piperine potentiates the antidepressant-like effect of trans-resveratrol: involvement of monoaminergic system. Metab Brain Dis 28(4):585–595Google Scholar
  37. Hwang YP, Yun HJ, Kim HG et al (2011) Suppression of phorbol-12-myristate-13-acetate-induced tumor cell invasion by piperine via the inhibition of PKCα/ERK1/2-dependent matrix metalloproteinase-9 expression. Toxicol Lett 203(1):9–19Google Scholar
  38. Ivanovski K, Nakova M, Warburton G et al (2005) Psychological profile in oral lichen planus. J Clin Periodontol 32(10):1034–1040Google Scholar
  39. Jungell P (1991) Oral lichen planus. A review. Int J Oral Maxillofac Surg. 20(3):129–135Google Scholar
  40. Kannan A, Huang W, Huang F, August A (2012) Signal transduction via the T cell antigen receptor in naïve and effector/memory T cells. Int J Biochem Cell Biol 44(12):2129–2134Google Scholar
  41. Kawanishi S, Hiraku Y, Pinlaor S, Ma N (2006) Oxidative and nitrative DNA damage in animals and patients with inflammatory diseases in relation to inflammation-related carcinogenesis. Biol Chem 387(4):365–372Google Scholar
  42. Kesarwala AH, Krishna MC, Mitchell JB (2016) Oxidative stress in oral diseases. Oral Dis 22(1):9–18Google Scholar
  43. Khom S, Strommer B, Schöffmann A et al (2013) GABAA receptor modulation by piperine and a non-TRPV1 activating derivative. Biochem Pharmacol 85(12):1827–1836Google Scholar
  44. Kim HG, Han EH, Jang WS et al (2012) Piperine inhibits PMA-induced cyclooxygenase-2 expression through downregulating NF-κB, C/EBP and AP-1 signaling pathways in murine macrophages. Food Chem Toxicol 50(7):2342–2348Google Scholar
  45. Koleva II, van Beek TA, Soffers AE, Dusemund B, Rietjens IM (2012) Alkaloids in the human food chain–natural occurrence and possible adverse effects. Mol Nutr Food Res 56(1):30–52Google Scholar
  46. Kong LD, Cheng CH, Tan RX (2004) Inhibition of MAO A and B by some plant-derived alkaloids, phenols and anthraquinones. J Ethnopharmacol 91(2–3):351–355Google Scholar
  47. Koray M, Dülger O, Ak G et al (2003) The evaluation of anxiety and salivary cortisol levels in patients with oral lichen planus. Oral Dis 9(6):298–301Google Scholar
  48. Kumar S, Singhal V, Roshan R, Sharma A, Rembhotkar GW, Ghosh B (2007) Piperine inhibits TNF-alpha induced adhesion of neutrophils to endothelial monolayer through suppression of NF-kappaB and IkappaB kinase activation. Eur J Pharmacol 575(1–3):177–186Google Scholar
  49. Lai LH, Fu QH, Liu Y et al (2012) Piperine suppresses tumor growth and metastasis in vitro and in vivo in a 4T1 murine breast cancer model. Acta Pharmacol Sin 33(4):523–530Google Scholar
  50. Lee SA, Hong SS, Han XH et al (2005) Piperine from the fruits of Piper longum with inhibitory effect on monoamine oxidase and antidepressant-like activity. Chem Pharm Bull (Tokyo). 53(7):832–835Google Scholar
  51. Lee SH, Kim HY, Back SY, Han HK (2018) Piperine-mediated drug interactions and formulation strategy for piperine: recent advances and future perspectives. Expert Opin Drug Metab Toxicol. 14(1):43–57Google Scholar
  52. Li TJ, Cui J (2013) COX-2, MMP-7 expression in oral lichen planus and oral squamous cell carcinoma. Asian Pac J Trop Med. 6(8):640–643Google Scholar
  53. Li S, Wang C, Li W, Koike K, Nikaido T, Wang MW (2007a) Antidepressant-like effects of piperine and its derivative, antiepilepsirine. J Asian Nat Prod Res 9(3–5):421–430Google Scholar
  54. Li S, Wang C, Wang M, Li W, Matsumoto K, Tang Y (2007b) Antidepressant like effects of piperine in chronic mild stress treated mice and its possible mechanisms. Life Sci 80(15):1373–1381Google Scholar
  55. Liu Y, Yadev VR, Aggarwal BB, Nair MG (2010) Inhibitory effects of black pepper (Piper nigrum) extracts and compounds on human tumor cell proliferation, cyclooxygenase enzymes, lipid peroxidation and nuclear transcription factor-kappa-B. Nat Prod Commun 5(8):1253–1257Google Scholar
  56. Lodi G, Scully C, Carrozzo M, Griffiths M, Sugerman PB, Thongprasom K (2005) Current controversies in oral lichen planus: report of an international consensus meeting. Part 1. Viral infections and etiopathogenesis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 100(1):40–51Google Scholar
  57. Lu R, Zhou G, Du G, Xu X, Yang J, Hu J (2011) Expression of T-bet and GATA-3 in peripheral blood mononuclear cells of patients with oral lichen planus. Arch Oral Biol 56(5):499–505Google Scholar
  58. Lu R, Zhang J, Sun W, Du G, Zhou G (2015) Inflammation-related cytokines in oral lichen planus: an overview. J Oral Pathol Med 44(1):1–14Google Scholar
  59. Lu Y, Liu J, Li H, Gu L (2016) Piperine ameliorates lipopolysaccharide-induced acute lung injury via modulating NF-κB signaling pathways. Inflammation. 39(1):303–308Google Scholar
  60. Lundqvist EN, Wahlin YB, Bergdahl M, Bergdahl J (2006) Psychological health in patients with genital and oral erosive lichen planus. J Eur Acad Dermatol Venereol 20(6):661–666Google Scholar
  61. Lysitsa S, Samson J, Gerber-Wicht C, Lang U, Lombardi T (2008) COX-2 expression in oral lichen planus. Dermatology 217(2):150–155Google Scholar
  62. Manayi A, Nabavi SM, Setzer WN, Jafari S (2017) Piperine as a potential anti-cancer agent: a review on preclinical studies. Curr Med Chem.  https://doi.org/10.2174/0929867324666170523120656 Google Scholar
  63. Mao QQ, Xian YF, Ip SP, Che CT (2011) Involvement of serotonergic system in the antidepressant-like effect of piperine. Prog Neuropsychopharmacol Biol Psychiatry 35(4):1144–1147Google Scholar
  64. Mao QQ, Huang Z, Zhong XM, Xian YF, Ip SP (2014a) Brain-derived neurotrophic factor signalling mediates the antidepressant-like effect of piperine in chronically stressed mice. Behav Brain Res 261:140–145Google Scholar
  65. Mao QQ, Huang Z, Zhong XM, Xian YF, Ip SP (2014b) Piperine reverses chronic unpredictable mild stress-induced behavioral and biochemical alterations in rats. Cell Mol Neurobiol 34(3):403–408Google Scholar
  66. Maraskovsky E, Chen WF, Shortman K (1989) IL-2 and IFN-gamma are two necessary lymphokines in the development of cytolytic T cells. J Immunol. 143(4):1210–1214Google Scholar
  67. Meghwal M, Goswami TK (2013) Piper nigrum and piperine: an update. Phytother Res. 27(8):1121–1130Google Scholar
  68. Mignogna MD, Fedele S, Lo RL, Lo ML, Bucci E (2004) Immune activation and chronic inflammation as the cause of malignancy in oral lichen planus: is there any evidence. Oral Oncol 40(2):120–130Google Scholar
  69. Misra S, Sharma K (2014) COX-2 signaling and cancer: new players in old arena. Curr Drug Targets 15(3):347–359Google Scholar
  70. Mittal R, Gupta RL (2000) In vitro antioxidant activity of piperine. Methods Find Exp Clin Pharmacol 22(5):271–274Google Scholar
  71. Myers LK, Kang AH, Postlethwaite AE et al (2000) The genetic ablation of cyclooxygenase 2 prevents the development of autoimmune arthritis. Arthritis Rheum 43(12):2687–2693Google Scholar
  72. Nadendla LK, Meduri V, Paramkusam G, Pachava KR (2014) Association of salivary cortisol and anxiety levels in lichen planus patients. J Clin Diagn Res. 8(12):ZC01–ZC03Google Scholar
  73. Nagler RM, Klein I, Zarzhevsky N, Drigues N, Reznick AZ (2002) Characterization of the differentiated antioxidant profile of human saliva. Free Radic Biol Med. 32(3):268–277Google Scholar
  74. Nogueira PA, Carneiro S, Ramos-e-Silva M (2015) Oral lichen planus: an update on its pathogenesis. Int J Dermatol 54(9):1005–1010Google Scholar
  75. Payeras MR, Cherubini K, Figueiredo MA, Salum FG (2013) Oral lichen planus: focus on etiopathogenesis. Arch Oral Biol 58(9):1057–1069Google Scholar
  76. Peng Q, Zhang J, Ye X, Zhou G (2017) Tumor-like microenvironment in oral lichen planus: evidence of malignant transformation. Expert Rev Clin Immunol. 13(6):635–643Google Scholar
  77. Pippi R, Patini R, Ghiciuc CM et al (2014) Diurnal trajectories of salivary cortisol, salivary α-amylase and psychological profiles in oral lichen planus patients. J Biol Regul Homeost Agents 28(1):147–156Google Scholar
  78. Pippi R, Romeo U, Santoro M, Del VA, Scully C, Petti S (2016) Psychological disorders and oral lichen planus: matched case-control study and literature review. Oral Dis 22(3):226–234Google Scholar
  79. Pradeep CR, Kuttan G (2004) Piperine is a potent inhibitor of nuclear factor-kappaB (NF-kappaB), c-Fos, CREB, ATF-2 and proinflammatory cytokine gene expression in B16F-10 melanoma cells. Int Immunopharmacol 4(14):1795–1803Google Scholar
  80. Prolo P, Chiappelli F, Cajulis E et al (2002) Psychoneuroimmunology in oral biology and medicine: the model of oral lichen planus. Ann N Y Acad Sci 966:429–440Google Scholar
  81. Rauscher FM, Sanders RA, Watkins JB (2000) Effects of piperine on antioxidant pathways in tissues from normal and streptozotocin-induced diabetic rats. J Biochem Mol Toxicol 14(6):329–334Google Scholar
  82. Rekha VR, Sunil S, Rathy R (2017) Evaluation of oxidative stress markers in oral lichen planus. J Oral Maxillofac Pathol. 21(3):387–393Google Scholar
  83. Rodgers G, Doucette CD, Soutar DA, Liwski RS, Hoskin DW (2016) Piperine impairs the migration and T cell-activating function of dendritic cells. Toxicol Lett 242:23–33Google Scholar
  84. Roopashree MR, Gondhalekar RV, Shashikanth MC, George J, Thippeswamy SH, Shukla A (2010) Pathogenesis of oral lichen planus–a review. J Oral Pathol Med 39(10):729–734Google Scholar
  85. Scrobotă I, Mocan T, Cătoi C, Bolfă P, Mureşan A, Băciuţ G (2011) Histopathological aspects and local implications of oxidative stress in patients with oral lichen planus. Rom J Morphol Embryol 52(4):1305–1309Google Scholar
  86. Sezer E, Ozugurlu F, Ozyurt H, Sahin S, Etikan I (2007) Lipid peroxidation and antioxidant status in lichen planus. Clin Exp Dermatol 32(4):430–434Google Scholar
  87. Shah B, Ashok L, Sujatha GP (2009) Evaluation of salivary cortisol and psychological factors in patients with oral lichen planus. Indian J Dent Res. 20(3):288–292Google Scholar
  88. Shirzad A, Pouramir M, Seyedmajidi M, Jenabian N, Bijani A, Motallebnejad M (2014) Salivary total antioxidant capacity and lipid peroxidation in patients with erosive oral lichen planus. J Dent Res Dent Clin Dent Prospects. 8(1):35–39Google Scholar
  89. Singh P, Grover J, Byatnal AA, Guddattu V, Radhakrishnan R, Solomon MC (2017) Elucidating the role of Cyclooxygenase-2 in the pathogenesis of oral lichen planus—an immunohistochemical study with supportive histochemical analysis. J Oral Pathol Med 46(5):381–386Google Scholar
  90. Sloberg K, Jonsson R, Jontell M (1984) Assessment of Langerhans’ cells in oral lichen planus using monoclonal antibodies. J Oral Pathol 13(5):516–524Google Scholar
  91. Smith WL, Garavito RM, DeWitt DL (1996) Prostaglandin endoperoxide H synthases (cyclooxygenases)-1 and -2. J Biol Chem 271(52):33157–33160Google Scholar
  92. Srinivasan K (2007) Black pepper and its pungent principle-piperine: a review of diverse physiological effects. Crit Rev Food Sci Nutr 47(8):735–748Google Scholar
  93. Sugerman PB, Satterwhite K, Bigby M (2000) Autocytotoxic T-cell clones in lichen planus. Br J Dermatol 142(3):449–456Google Scholar
  94. Sugerman PB, Savage NW, Walsh LJ et al (2002) The pathogenesis of oral lichen planus. Crit Rev Oral Biol Med 13(4):350–365Google Scholar
  95. Suzuki J, Ogawa M, Futamatsu H, Kosuge H, Tanaka H, Isobe M (2006) A cyclooxygenase-2 inhibitor alters Th1/Th2 cytokine balance and suppresses autoimmune myocarditis in rats. J Mol Cell Cardiol 40(5):688–695Google Scholar
  96. Tadakamadla J, Kumar S, Lalloo R, Johnson NW (2017) Qualitative analysis of the impact of oral potentially malignant disorders on daily life activities. PLoS One 12(4):e0175531Google Scholar
  97. Tvarijonaviciute A, Aznar-Cayuela C, Rubio CP, Ceron JJ, López-Jornet P (2017) Evaluation of salivary oxidate stress biomarkers, nitric oxide and C-reactive protein in patients with oral lichen planus and burning mouth syndrome. J Oral Pathol Med 46(5):387–392Google Scholar
  98. Uma PK, Geervani P, Eggum BO (1993) Common Indian spices: nutrient composition, consumption and contribution to dietary value. Plant Foods Hum Nutr 44(2):137–148Google Scholar
  99. Upadhyay RB, Carnelio S, Shenoy RP, Gyawali P, Mukherjee M (2010) Oxidative stress and antioxidant defense in oral lichen planus and oral lichenoid reaction. Scand J Clin Lab Invest 70(4):225–228Google Scholar
  100. Upadhyay J, Upadhyay RB, Agrawal P, Jaitley S, Shekhar R (2013) Langerhans cells and their role in oral mucosal diseases. N Am J Med Sci. 5(9):505–514Google Scholar
  101. Vaibhav K, Shrivastava P, Javed H et al (2012) Piperine suppresses cerebral ischemia-reperfusion-induced inflammation through the repression of COX-2, NOS-2, and NF-κB in middle cerebral artery occlusion rat model. Mol Cell Biochem 367(1–2):73–84Google Scholar
  102. Vallejo MJ, Huerta G, Cerero R, Seoane JM (2001) Anxiety and depression as risk factors for oral lichen planus. Dermatology 203(4):303–307Google Scholar
  103. van der Waal I (2009) Potentially malignant disorders of the oral and oropharyngeal mucosa; terminology, classification and present concepts of management. Oral Oncol 45(4–5):317–323Google Scholar
  104. Vardell E (2015) Natural Medicines: a Complementary and Alternative Medicines Tool Combining Natural Standard and the Natural Medicines Comprehensive Database. Med Ref Serv Q. 34(4):461–470Google Scholar
  105. Verma A, Kushwaha HN, Srivastava AK et al (2017) Piperine attenuates UV-R induced cell damage in human keratinocytes via NF-kB, Bax/Bcl-2 pathway: an application for photoprotection. J Photochem Photobiol, B 172:139–148Google Scholar
  106. Vijayakumar RS, Surya D, Nalini N (2004) Antioxidant efficacy of black pepper (Piper nigrum L.) and piperine in rats with high fat diet induced oxidative stress. Redox Rep. 9(2):105–110Google Scholar
  107. Vlková B, Stanko P, Minárik G et al (2012) Salivary markers of oxidative stress in patients with oral premalignant lesions. Arch Oral Biol 57(12):1651–1656Google Scholar
  108. Wattanathorn J, Chonpathompikunlert P, Muchimapura S, Priprem A, Tankamnerdthai O (2008) Piperine, the potential functional food for mood and cognitive disorders. Food Chem Toxicol 46(9):3106–3110Google Scholar
  109. Ying X, Chen X, Cheng S, Shen Y, Peng L, Xu HZ (2013a) Piperine inhibits IL-β induced expression of inflammatory mediators in human osteoarthritis chondrocyte. Int Immunopharmacol 17(2):293–299Google Scholar
  110. Ying X, Yu K, Chen X et al (2013b) Piperine inhibits LPS induced expression of inflammatory mediators in RAW 264.7 cells. Cell Immunol. 285(1–2):49–54Google Scholar
  111. Zaugg J, Baburin I, Strommer B, Kim HJ, Hering S, Hamburger M (2010) HPLC-based activity profiling: discovery of piperine as a positive GABA(A) receptor modulator targeting a benzodiazepine-independent binding site. J Nat Prod 73(2):185–191Google Scholar
  112. Zhai WJ, Zhang ZB, Xu NN et al (2016) Piperine plays an anti-inflammatory role in staphylococcus aureus endometritis by inhibiting activation of NF-κB and MAPK pathways in mice. Evid Based Complement Alternat Med. 2016:8597208Google Scholar
  113. Zhang L, Bertucci AM, Smith KA, Xu L, Datta SK (2007) Hyperexpression of cyclooxygenase 2 in the lupus immune system and effect of cyclooxygenase 2 inhibitor diet therapy in a murine model of systemic lupus erythematosus. Arthritis Rheum 56(12):4132–4141Google Scholar
  114. Zhang J, Zhu X, Li H et al (2015) Piperine inhibits proliferation of human osteosarcoma cells via G2/M phase arrest and metastasis by suppressing MMP-2/-9 expression. Int Immunopharmacol 24(1):50–58Google Scholar
  115. Zhou XJ, Sugerman PB, Savage NW, Walsh LJ (2001) Matrix metalloproteinases and their inhibitors in oral lichen planus. J Cutan Pathol 28(2):72–82Google Scholar
  116. Zhou G, Xia K, Du GF et al (2009) Activation of nuclear factor-kappa B correlates with tumor necrosis factor-alpha in oral lichen planus: a clinicopathologic study in atrophic-erosive and reticular form. J Oral Pathol Med 38(7):559–564Google Scholar
  117. Zhou G, Zhang J, Ren XW, Hu JY, Du GF, Xu XY (2012) Increased B7-H1 expression on peripheral blood T cells in oral lichen planus correlated with disease severity. J Clin Immunol 32(4):794–801Google Scholar

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© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.The State Key Laboratory Breeding Base of Basic Science of Stomatology (HubeiMOST) and Key Laboratory of Oral Biomedicine Ministry of EducationSchool and Hospital of Stomatology, Wuhan UniversityWuhanPeople’s Republic of China
  2. 2.Department of Oral MedicineSchool and Hospital of Stomatology, Wuhan UniversityWuhanPeople’s Republic of China

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