DOI QR코드

DOI QR Code

Eryngium foetidum Suppresses Inflammatory Mediators Produced by Macrophages

  • Published : 2012.02.29

Abstract

Objective: This study assessed anti-inflammatory and antioxidant activities of $E.$ $foetidum$ leaf extract on LPS-activated murine macrophages. Methods: RAW264.7 cells were pretreated with or without $E.$ $foetidum$ extract for 1 h prior to incubation with LPS for 24 h. Anti-inflammatory activity was evaluated with reference to iNOS, COX-2, TNF-${\alpha}$ and IL-6 gene expression. In addition, NO and intracellular ROS generation were determined by Griess method and fluorescence intensity and activation of MAPKs and $I{\kappa}B$ by Western blotting. Results: Prior treatment with $E.$ $foetidum$ leaf extract inhibited elevation of IL-6, TNF-${\alpha}$, iNOS and COX-2, together with their cognate mRNAs in a dose-dependent manner. NO and intracellular ROS contents were similarly reduced. These effects were due to inhibition of LPS-induced phosphorylation of JNK and p38 as well as $I{\kappa}B$. $E.$ $foetidum$ ethanol extract were shown to contain lutein, ${\beta}$-carotene, chlorogenic acid, kaempferol and caffeic acid, compounds known to exert these bioactive properties. Conclusions: $E.$ $foetidum$ leaf extract possesses suppressive effects against pro-inflammatory mediators. Thus, $E.$ $foetidum$ has a high potential to be used as a food supplement to reduce risk of cancer associated with inflammation.

Keywords

References

  1. Aggarwal BB (2004). Nuclear factor-[kappa]B: The enemy within. Cancer Cell, 6, 203-8. https://doi.org/10.1016/j.ccr.2004.09.003
  2. Aggarwal BB, Kunnumakkara AB, Harikumar KB, et al (2008). Potential of spice-derived phytochemicals for cancer prevention. Planta Med, 74, 1560-9. https://doi.org/10.1055/s-2008-1074578
  3. Aggarwal BB, Shishodia S (2006). Molecular targets of dietary agents for prevention and therapy of cancer. Biochem Pharmacol, 71, 1397-421. https://doi.org/10.1016/j.bcp.2006.02.009
  4. Aggarwal BB, Shishodia S, Sandur SK, et al (2006). Inflammation and cancer: How hot is the link? Biochem Pharmacol, 72, 1605-21. https://doi.org/10.1016/j.bcp.2006.06.029
  5. Aggarwal BB, Van Kuiken ME, Iyer LH, et al (2009). Molecular targets of nutraceuticals derived from dietary spices: potential role in suppression of inflammation and tumorigenesis. Exp Biol Med, 234, 825-49. https://doi.org/10.3181/0902-MR-78
  6. Ahmed M, Salahy E, Fayed S, et al (2001). Human papillomavirus infection among Egyptian females with cervical carcinoma: relationship to spontaneous apoptosis and TNF-$\alpha$. Clin Biochem, 34, 491-8. https://doi.org/10.1016/S0009-9120(01)00243-0
  7. Ancrile B, Lim KH, Counter C (2007). Oncogenic Ras-induced secretion of IL6 is required for tumorigenesis. Genes Dev, 21, 1714-9. https://doi.org/10.1101/gad.1549407
  8. Arnoldussen YJ, Saatcioglu F (2009). Dual specificity phosphatases in prostate cancer. Mol Cell Endocrinol, 309, 1-7. https://doi.org/10.1016/j.mce.2009.05.019
  9. Arnott C, Scott K, Moore R, et al (2004). Expression of both TNF-$\alpha$ receptor subtypes is essential for optimal skin tumour development. Oncogene, 23, 1902-10. https://doi.org/10.1038/sj.onc.1207317
  10. Babbar N, Casero RJ (2006). Tumor necrosis factor-alpha increases reactive oxygen species by inducing spermine oxidase in human lung epithelial cells: a potential mechanism for inflammation-induced carcinogenesis. Cancer Res, 66, 11125-30. https://doi.org/10.1158/0008-5472.CAN-06-3174
  11. Bai S, Lee S, Na H, et al (2005). Beta-Carotene inhibits inflammatory gene expression in lipopolysaccharidestimulated macrophages by suppressing redox-based NF-kB activation. Exp Mol Med, 37, 323-34. https://doi.org/10.1038/emm.2005.42
  12. Baron J, Cole B, Sandler R, et al (2003). A randomized trial of aspirin to prevent colorectal adenomas. N Engl J Med, 348, 891-9. https://doi.org/10.1056/NEJMoa021735
  13. Bertagnolli M, Eagle C, Zauber A, et al (2006). Celecoxib for the prevention of sporadic colorectal adenomas. N Engl J Med, 355, 873-84. https://doi.org/10.1056/NEJMoa061355
  14. Bingle L, Brown NJ, Lewis CE (2002). The role of tumourassociated macrophages in tumour progression: implications for new anticancer therapies. J Pathol, 196, 254-65. https://doi.org/10.1002/path.1027
  15. Bollrath J, Phesse TJ, Burstin VA, et al (2009). gp130-mediated Stat3 activation in enterocytes regulates cell survival and cell-cycle progression during colitis-associated tumorigenesis. Cancer Cell, 15, 91-102. https://doi.org/10.1016/j.ccr.2009.01.002
  16. Bosca L, Zeini M, Traves PG, et al (2005). Nitric oxide and cell viability in inflammatory cells: a role for NO in macrophage function and fate. Toxicol, 208, 249-58. https://doi.org/10.1016/j.tox.2004.11.035
  17. Burstein E, Duckett C (2003). Dying for NF${\kappa}B$? Control of cell death by transcriptional regulation of the apoptotic machinery. Curr Opin Cell Biol, 15, 732-7. https://doi.org/10.1016/j.ceb.2003.10.005
  18. Campos A, Molognoni F, Melo F, et al (2007). Oxidative stress modulate DNA methylation during melanocyte anchorage blockade associated with malignant transformation. Neoplasia, 9, 1111-21. https://doi.org/10.1593/neo.07712
  19. Chanwitheesuk A, Teerawutgulrag A, Rakariyatham N (2005). Screening of antioxidant activity and antioxidant compounds of some edible plants of Thailand. Food Chem, 92, 491-7. https://doi.org/10.1016/j.foodchem.2004.07.035
  20. Chao P-c, Hsu C-c, Yin M-c (2009). Anti-inflammatory and anti-coagulatory activities of caffeic acid and ellagic acid in cardiac tissue of diabetic mice. Nutr Metab, 6, 33-?. https://doi.org/10.1186/1743-7075-6-33
  21. Chen C, Peng W, Tsai K, et al (2007). Luteolin suppresses inflammation-associated gene expression by blocking NF- [kappa]B and AP-1 activation pathway in mouse alveolar macrophages. Life Sci, 81, 1602-14. https://doi.org/10.1016/j.lfs.2007.09.028
  22. Chen L, Park S, Tumanov A, et al (2010). CD95 promotes tumour growth. Nature, 465, 492-6. https://doi.org/10.1038/nature09075
  23. Cheng S, Xing B, Li J, et al (2007). Interferon gamma regulation of TNFalpha-induced matrix metalloproteinase 3 expression and migration of human glioma T98G cells. Int J Cancer, 121, 1190-6. https://doi.org/10.1002/ijc.22729
  24. Ching S, Ingram D, Hahnel R, et al (2002). Serum levels of micronutrients, antioxidants and total antioxidant status predict risk of breast cancer in a case control study. J Nutr, 132, 303-6. https://doi.org/10.1093/jn/132.2.303
  25. Chung Y, Chang Y (2003). Serum interleukin-6 levels reflect the disease status of colorectal cancer. J Surg Oncol, 83, 222-6. https://doi.org/10.1002/jso.10269
  26. Cilloni D, Martinelli G, Messa F, et al (2007). Nuclear factor- ${\kappa}B$ as a target for new drug development in myeloid malignancies. Haematologica, 92, 1224-9. https://doi.org/10.3324/haematol.11199
  27. Dickinson SE, Olson ER, Zhang J, et al (2011). p38 MAP kinase plays a functional role in UVB-Induced mouse skin carcinogenesis. Mol Carcinog, 50, 469-78. https://doi.org/10.1002/mc.20734
  28. Donkena K, Young C, Tindall D (2010). Oxidative stress and DNA methylation in prostate cancer. Obstet Gynecol Int, 2010, 1-14.
  29. Dos Santos MD, Almeida MC, Lopes NP, et al (2006). Evaluation of the anti-inflammatory, analgesic and antipyretic activities of the natural polyphenol chlorogenic acid. Biol Pharm Bull, 29, 2236-40. https://doi.org/10.1248/bpb.29.2236
  30. Drachenberg DE, Elgamal A-AA, Rowbotham R, et al (1999). Circulating levels of interleukin-6 in patients with hormone refractory prostate cancer. Prostate, 41, 127-33. https://doi.org/10.1002/(SICI)1097-0045(19991001)41:2<127::AID-PROS7>3.0.CO;2-H
  31. Dunn G, Bruce A, Ikeda H, et al (2002). Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol, 3, 991 - 8. https://doi.org/10.1038/ni1102-991
  32. Dutta J, Fan Y, Gupta N, et al (2006). Current insights into the regulation of programmed cell death by NF${\kappa}B$. Oncogene, 25, 6800-16. https://doi.org/10.1038/sj.onc.1209938
  33. Ekmekcioglu S, Ellerhorst J, Smid C, et al (2000). Inducible nitric oxide synthase and nitrotyrosine in human metastatic melanoma tumors correlate with poor survival. Clin Cancer Res, 6, 4768-75.
  34. Esteve P, Chicoine E, Robledo O, et al (2002). Protein kinase C-zeta regulates transcription of the matrix metalloproteinase-9 gene induced by IL-1 and TNFalpha in glioma cells via NF-kappa B. J Biol Chem, 277, 35150-5. https://doi.org/10.1074/jbc.M108600200
  35. Ferrajoli A, Keating M, Manshouri T, et al (2002). The clinical significance of tumor necrosis factor-alpha plasma level in patients having chronic lymphocytic leukemia. Blood, 100, 1215-9.
  36. Franco R, Schoneveld O, Georgakilas A, et al (2008). Oxidative stress, DNA methylation and carcinogenesis. Cancer Lett, 266, 6-11. https://doi.org/10.1016/j.canlet.2008.02.026
  37. Garcia-Tunon I, Ricote M, Ruiz A, et al (2006). Role of tumor necrosis factor-alpha and its receptors in human benign breast lesions and tumors (in situ and infiltrative). Cancer Sci, 97, 1044-9. https://doi.org/10.1111/j.1349-7006.2006.00277.x
  38. Garcia M, Saenz M, Gomez M, et al (1999). Topical antiinflammatory activity of phytosterols isolated from Eryngium foetidum on chronic and acute inflammation models. Phytother Res, 13, 78-80. https://doi.org/10.1002/(SICI)1099-1573(199902)13:1<78::AID-PTR384>3.0.CO;2-F
  39. Giardiello F, Offerhaus J, Tersmette A, et al (1996). Sulindac induced regression of colorectal adenomas infamilial adenomatous polyposis:evaluation of predictive factors. Gut, 38, 578-81. https://doi.org/10.1136/gut.38.4.578
  40. Giardiello F, Yang V, Hylind L, et al (2002). Primary chemoprevention of familial adenomatous polyposis with sulindac. N Engl J Med, 346, 1054-9. https://doi.org/10.1056/NEJMoa012015
  41. Green LC, Wagner DA, Glogowski J, et al (1982). Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal Biochem, 126, 131-8. https://doi.org/10.1016/0003-2697(82)90118-X
  42. Grivennikov S, Karin E, Terzic J, et al (2009). IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell, 15, 103-13. https://doi.org/10.1016/j.ccr.2009.01.001
  43. Guha M, Mackman N (2001). LPS induction of gene expression in human monocytes. Cell Signal, 13, 85-94. https://doi.org/10.1016/S0898-6568(00)00149-2
  44. Guo L, Guo Y, Xiao S, et al (2005). Protein kinase p-JNK is correlated with the activation of AP-1 and its associated Jun family proteins in hepatocellular carcinoma. Life Sci, 77, 1869-78. https://doi.org/10.1016/j.lfs.2005.03.019
  45. Hajri A, Metzger E, Vallat F, et al (1998). Role of nitric oxide in pancreatic tumour growth: in vivo and in vitro studies. Br J Cancer, 78, 841-9. https://doi.org/10.1038/bjc.1998.591
  46. Hamalainen M, Nieminen R, Vuorela P, et al (2007). Anti- Inflammatory Effects of Flavonoids: Genistein, Kaempferol, Quercetin, and Daidzein Inhibit STAT-1 and NF-B Activations, Whereas Flavone, Isorhamnetin, Naringenin, and Pelargonidin Inhibit only NF-B Activation along with Their Inhibitory Effect on iNOS Expression and NO Production in Activated Macrophages. Mediators Inflamm, 2007, 45673-83.
  47. Higuchi T, Iwama T, Yoshinaga K, et al (2003). A randomized,double-blind,placebo-controlled trial of the effects of rofecoxib,a selective cyclooxygenase-2 inhibitor,on rectal polypsin familial adenomatous polyposis patients. Clin Cancer Res, 9, 4756-60.
  48. Howe L, Chang S, Tolle K, et al (2005). HER2/neu-induced mammary tumorigenesis and angiogenesis are reduced in cyclooxygenase-2 knockout mice. Cancer Res, 65, 10113-9. https://doi.org/10.1158/0008-5472.CAN-05-1524
  49. Jaiswal M, LaRusso NF, Burgart LJ, et al (2000). Inflammatory cytokines induce DNA damage and inhibit DNA repair in cholangiocarcinoma cells by a nitric oxide-dependent mechanism. Cancer Res, 60, 184-90.
  50. Jiwajinda S, Santisopasri V, Murakami A, et al (2002). Suppressive effects of edible Thai plants on superoxide and nitric oxide generation. Asian Pac J Cancer Prev, 3, 215-23.
  51. Jost P, Ruland J (2007). Aberrant $NF{\kappa}B$ signaling in lymphoma:mechanisms, consequences, and therapeutic implications. Blood, 109, 2700-7.
  52. Kai H, Kitadai Y, Kodama M, et al (2005). Involvement of proinflammatory cytokines IL-1beta and IL-6 in progression of human gastric carcinoma. Anti cancer Res, 25, 709-13.
  53. Kaplanski G, Marin V, Montero-Julian F, et al (2003). IL-6: a regulator of the transition from neutrophil to monocyte recruitment during inflammation. Trends Immunol, 24, 25-9. https://doi.org/10.1016/S1471-4906(02)00013-3
  54. Karin M (2006). Nuclear factor-${\kappa}B$ in cancer development and progression. Nature, 441, 431-6. https://doi.org/10.1038/nature04870
  55. Kim G, Chandrasekaran K, Morgan W (2008). Mitochondrial dysfunction, persistently elevated levels of reactive oxygen species and radiation-induced genomic instability: a review. Mutagenesis, 21, 361-8.
  56. Kim J-H, Na H-J, Kim C-K, et al (2008). The non-provitamin A carotenoid, lutein, inhibits NF-[kappa]B-dependent gene expression through redox-based regulation of the phosphatidylinositol 3-kinase/PTEN/Akt and NF-[kappa] B-inducing kinase pathways: Role of H2O2 in NF-[kappa] B activation. Free Radic Biol Med, 45, 885-96. https://doi.org/10.1016/j.freeradbiomed.2008.06.019
  57. Kim JH, Kim DH, Baek SH, et al (2006). Rengyolone inhibits inducible nitric oxide synthase expression and nitric oxide production by down-regulation of NF-${\kappa}B$ and p38 MAP kinase activity in LPS-stimulated RAW 264.7 cells. Biochem Pharmacol, 71, 1198-205. https://doi.org/10.1016/j.bcp.2005.12.031
  58. Klotz T, Bloch W, Volberg C, et al (1998). Selective expression of inducible nitric oxide synthase in human prostate carcinoma. Cancer, 82, 1897-903. https://doi.org/10.1002/(SICI)1097-0142(19980515)82:10<1897::AID-CNCR12>3.0.CO;2-O
  59. Kowalski J, Samojedny A, Paul M, et al (2005). Effect of apigenin, kaempferol and resveratrol on the expression of interleukin-1beta and tumor necrosis factor-alpha genes in J774.2 macrophages. Pharmacol Rep, 57, 390-4.
  60. Kulbe H, Thompson R, Wilson J, et al (2007). The inflammatory cytokine tumor necrosis factor-alpha generates an autocrine tumor-promoting network in epithelial ovarian cancer cells. Cancer Res, 67, 585-92. https://doi.org/10.1158/0008-5472.CAN-06-2941
  61. Kumar S, Boehm J, Lee J (2003). p38 MAP kinases: key signalling molecules as therapeutic targets for inflammatory diseases. Nat Rev Drug Discov, 2, 717-26. https://doi.org/10.1038/nrd1177
  62. Kundu JK, Surh Y-J (2008). Inflammation: Gearing the journey to cancer. Mutat Res, 659, 15-30. https://doi.org/10.1016/j.mrrev.2008.03.002
  63. Lagares-Garcia J, Moore R, Collier B, et al (2001). Nitric oxide synthase as a marker in colorectal carcinoma. Am Surg, 67, 709-13.
  64. Lee EH, Faulhaber D, Hanson KM, et al (2004). Dietary lutein reduces ultraviolet radiation-induced inflammation and immunosuppression. J Investig Dermatol, 122, 510-7. https://doi.org/10.1046/j.0022-202X.2004.22227.x
  65. Lim S, Gu J, Kim M, et al (2008). Epigenetic changes induced by reactive oxygen species in hepatocellular carcinoma: methylation of the E-cadherin promoter. Gastroenterol, 135, 2128-40. https://doi.org/10.1053/j.gastro.2008.07.027
  66. Liu J, Ghanim M, Xue L, et al (2009). Analysis of Drosophila segmentation network identifies a JNK pathway factor overexpressed in kidney cancer. Science, 323, 1218-22. https://doi.org/10.1126/science.1157669
  67. Lucci A, Krishnamurthy S, Singh B, et al (2009). Cyclooxygenase-2 expression in primary breast cancers predicts dissemination of cancer cells to the bone marrow. Breast Cancer Res Treat, 117, 61-8. https://doi.org/10.1007/s10549-008-0135-x
  68. Luo J, Kamata H, Karin M (2005). The anti death machinery in IKK/NF${\kappa}B$ signaling. J Clin Immunol, 25, 541-50. https://doi.org/10.1007/s10875-005-8217-6
  69. Mantovani A, Allavena P, Sica A, et al (2008). Cancer-related inflammation. Nature, 454, 436-44. https://doi.org/10.1038/nature07205
  70. Masri F, Comhair S, Koeck T, et al (2005). Abnormalities in nitric oxide and its derivatives in lung cancer. Am J Respir Crit Care Med, 172, 597-605. https://doi.org/10.1164/rccm.200411-1523OC
  71. Melisi D, Chiao P (2007). NF${\kappa}B$ as a target for cancer therapy. Exp Opin Ther Targ, 11, 133-44. https://doi.org/10.1517/14728222.11.2.133
  72. Merken HM, Beecher GR (2000). Liquid chromatographic method for the separation and quantification of prominent flavonoid aglycones. J Chromatogr A, 897, 177-84. https://doi.org/10.1016/S0021-9673(00)00826-8
  73. Michalaki V, Syrigos K, Charles P, et al (2004). Serum levels of IL-6 and TNF-alpha correlate with clinicopathological features and patient survival in patients with prostate cancer. Br J Cancer, 90, 2312-6. https://doi.org/10.1038/sj.bjc.6601814
  74. Min L, He B, Hui L (2011). Mitogen-activated protein kinases in hepatocellular carcinoma development. Semin Cancer Biol, 21, 10-20. https://doi.org/10.1016/j.semcancer.2010.10.011
  75. Moore R, Owens D, Stamp G, et al (1999). Mice deficient in tumor necrosis factor-alpha are resistant to skin carcinogenesis. Nat Med, 5, 828-31. https://doi.org/10.1038/10552
  76. Muller-Decker K, Neufang G, Berger I, et al (2002). Transgenic cyclooxygenase-2 overexpression sensitizes mouse skin for carcinogenesis. Proc Natl Acad Sci USA, 99, 12483-8. https://doi.org/10.1073/pnas.192323799
  77. Nabors L, Suswam E, Huang Y, et al (2003). Tumor necrosis factor alpha induces angiogenic factor up-regulation in malignant glioma cells: a role for RNA stabilization and HuR. Cancer Res, 63, 4181-7.
  78. Nanasombat S, Teckchuen N (2009). Antimicrobial, antioxidant and anticancer activities of Thai local vegetables. J Med Plant Res, 3, 443-9.
  79. Neufang G, Furstenberger G, Heidt M, et al (2001). Abnormal differentiation of epidermis in transgenic mice constitutively expressing cyclooxygenase-2 in skin. Proc Natl Acad Sci USA, 98, 7629-34. https://doi.org/10.1073/pnas.121574098
  80. Oshima H, Oshima M, Inaba K, et al (2004). Hyperplastic gastric tumors induced by activated macrophages in COX-2/ mPGES-1 transgenic mice. Embo J, 23, 1669-78. https://doi.org/10.1038/sj.emboj.7600170
  81. Oshima M, Dinchuk J, Kargman S, et al (1996). Suppression of intestinalpolyposis in Apc delta716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell, 87, 803-9. https://doi.org/10.1016/S0092-8674(00)81988-1
  82. Pan M-H, Ho C-T (2008). Chemopreventive effects of natural dietary compounds on cancer development. Chem Soc Rev, 37, 2558-74. https://doi.org/10.1039/b801558a
  83. Paul JHA, Seaforth CE, Tikasingh T (2010). Eryngium foetidum L.: A review. Fitoterapia, 82, 302-8.
  84. Pollard J (2004). Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer, 4, 71-8. https://doi.org/10.1038/nrc1256
  85. Popivanova B, Kitamura K, Wu Y, et al (2008). Blocking TNFalpha in mice reduces colorectal carcinogenesis associated with chronic colitis. J Clin Invest, 118, 560-70.
  86. Punturee K, Wild C, Vinitketkumneun U (2004). Thai medicinal plants modulate nitric oxide and tumor necrosis factor- [alpha] in J774.2 mouse macrophages. J Ethnopharmacol, 95, 183-9. https://doi.org/10.1016/j.jep.2004.06.019
  87. Saenz M, Fernandez M, Garcia M (1997). Antiinflammatory and analgesic properties from leaves of Eryngium foetidum L. (Apiaceae). Phytother Res, 11, 380-3. https://doi.org/10.1002/(SICI)1099-1573(199708)11:5<380::AID-PTR116>3.0.CO;2-#
  88. Sandler R, Halabi S, Baron J, et al (2003). A randomized trial of aspirin to prevent colorectal adenomas in patients with previous colorectal cancer. N Engl J Med, 348, 883-90. https://doi.org/10.1056/NEJMoa021633
  89. Shan J, Fu J, Zhao Z, et al (2009). Chlorogenic acid inhibits lipopolysaccharide-induced cyclooxygenase-2 expression in RAW264.7 cells through suppressing NF-[kappa]B and JNK/AP-1 activation. Inter Immunopharmacol, 9, 1042-8. https://doi.org/10.1016/j.intimp.2009.04.011
  90. Shin K-M, Kim I-T, Park Y-M, et al (2004). Anti-inflammatory effect of caffeic acid methyl ester and its mode of action through the inhibition of prostaglandin E2, nitric oxide and tumor necrosis factor-$\alpha$ production. Biochem Pharmacol, 68, 2327-36. https://doi.org/10.1016/j.bcp.2004.08.002
  91. Simon O, Singh N (1986). Demonstration of anticonvulsant properties of an aqueous extract of Spirit Weed (Eryngium foetidum L.). West Indian Med J, 35, 121-5.
  92. Singh S, Gupta A (2011). Nitric oxide: role in tumour biology and iNOS/NO-based anticancer therapies. Cancer Chemother Pharmacol, 67, 1211-24. https://doi.org/10.1007/s00280-011-1654-4
  93. Steinbach G, Lynch P, Phillips R, et al (2000). The effect of celecoxib,a cyclooxygenase-2 inhibitor,in familial adenomatous polyposis. N Engl J Med, 342, 1946-52. https://doi.org/10.1056/NEJM200006293422603
  94. Surh Y-J, Chun K-S, Cha H-H, et al (2001). Molecular mechanisms underlying chemopreventive activities of antiinflammatory phytochemicals: down-regulation of COX-2 and iNOS through suppression of NF-[kappa]B activation. Mutat Res, 480, 243-68. https://doi.org/10.1016/S0027-5107(01)00183-X
  95. Szlosarek P, Grimshaw M, Kulbe H, et al (2006). Expression and regulation of tumor necrosis factor alpha in normal and malignant ovarian epithelium. Mol Cancer Ther, 5, 382-90. https://doi.org/10.1158/1535-7163.MCT-05-0303
  96. Tiano H, Loftin C, Akunda J, et al (2002). Deficiency o feither cyclooxygenase (COX-1) or COX-2 alters epidermal differentiation and reduces mouse skin tumorigenesis. Cancer Res, 62, 3395-401.
  97. The Agricultural Co-operative Federation of Thailand (2006). The amount of food consumption at 95 percentile per capita and eater only. In 'Food consumption Data of Thailand'. Agricultural Cooperatives of Thailand's printing assembly, Bangkok p.173.
  98. Tudek B, Winczura A, Janik J, et al (2010). Involvement of oxidatively damaged DNA and repair in cancer development and aging. Am J Transl Res, 2, 254-84.
  99. Tuntipopipat S, Muangnoi C, Chingsuwanrote P, et al (2011). Anti-inflammatory activities of red curry paste extract on lipopolysaccharide-activated murine macrophage cell line. Nutrition, 27, 479-87. https://doi.org/10.1016/j.nut.2010.04.009
  100. Tuntipopipat S, Muangnoi C, Failla ML (2009). Anti- Inflammatory Activities of Extracts of Thai Spices and Herbs with Lipopolysaccharide-Activated RAW 264.7 Murine Macrophages. J Med Food, 12, 1213-20. https://doi.org/10.1089/jmf.2009.1118
  101. Vane JR, Bakhle YS, Botting RM (1998). Cyclooxygenases 1 and 2. Annu. Rev. Pharmacol Toxicol, 38, 97-120. https://doi.org/10.1146/annurev.pharmtox.38.1.97
  102. Vichai V, Kirtikara K (2006). Sulforhodamine B colorimetric assay for cytotoxicity screening. Nat Protoc, 1, 1112-6. https://doi.org/10.1038/nprot.2006.179
  103. Vivanco I, Palaskas N, Tran C, et al (2007). Identification of the JNK signaling pathway as a functional target of the tumor suppressor PTEN. Cancer Cell, 11, 555-69. https://doi.org/10.1016/j.ccr.2007.04.021
  104. Wang G, Ji B, Wang X, et al (2005). Anti-cancer effect of iNOS inhibitor and its correlation with angiogenesis in gastric cancer. World J Gastroenterol, 11, 3830-3. https://doi.org/10.3748/wjg.v11.i25.3830
  105. Weninger W, Rendl M, Pammer J, et al (1998). Nitric oxide synthases in Kaposi's sarcoma are expressed predominantly by vessels and tissue macrophages. Lab Invest, 78, 949-55.
  106. Wolfe KL, Liu RH (2007). Cellular Antioxidant Activity (CAA) Assay for Assessing Antioxidants, Foods, and Dietary Supplements. J Agric Food Chem, 55, 8896-907. https://doi.org/10.1021/jf0715166
  107. Yang S, Miah A, Sales K, et al (2011). Inhibition of the p38 MAPK pathway sensitises human colon cancer cells to 5-fluorouracil treatment. Int J Oncol , 38, 1695-702.
  108. Zhang X, Huang H, Yang T, et al (2010). Chlorogenic acid protects mice against lipopolysaccharide-induced acute lung injury. Injury, 41, 746-52. https://doi.org/10.1016/j.injury.2010.02.029
  109. Ziech D, Franco R, Pappa A, et al (2010). The role of epigenetics in environmental and occupational carcinogenesis. Chem Biol Interact, 188, 340-9. https://doi.org/10.1016/j.cbi.2010.06.012

Cited by

  1. Anticlastogenic Effect of Eryngium foetidum L. Assessed by Erythrocyte Micronucleus Assay vol.13, pp.7, 2012, https://doi.org/10.7314/APJCP.2012.13.7.3343
  2. Kaempferol suppresses lipid accumulation in macrophages through the downregulation of cluster of differentiation 36 and the upregulation of scavenger receptor class B type I and ATP-binding cassette transporters A1 and G1 vol.31, pp.2, 2013, https://doi.org/10.3892/ijmm.2012.1204
  3. vol.52, pp.3, 2014, https://doi.org/10.3109/13880209.2013.837077
  4. Spiny coriander (Eryngium foetidum L.): a commonly used, neglected spicing-culinary herb of Mizoram, India vol.61, pp.6, 2014, https://doi.org/10.1007/s10722-014-0130-5
  5. Effects of Jeju Citrus unshiu Peel Extracts Before and After Bioconversion with Cytolase on Anti-Inflammatory Activity in RAW264.7 Cells vol.44, pp.3, 2015, https://doi.org/10.3746/jkfn.2015.44.3.331
  6. Linn. Leaves in Mice vol.32, pp.3, 2016, https://doi.org/10.5487/TR.2016.32.3.231
  7. Flavonoids and Phenolic Acids from Oregano: Occurrence, Biological Activity and Health Benefits vol.7, pp.1, 2018, https://doi.org/10.3390/plants7010002