Sulforaphane Inhibits Prostaglandin E2 Synthesis by Suppressing Microsomal Prostaglandin E Synthase 1

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Zhou, Jiping ^a   Joplin, Denise G ^a   Cross, Janet V ^a   Templeton, Dennis J ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOOXYGENASE 2; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PROSTAGLANDIN E SYNTHASE 1; PROSTAGLANDIN E2; SULFORAPHANE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CONTROLLED STUDY; ENZYME INHIBITION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; LUNG CARCINOMA; MICROSOME; MOUSE; NONHUMAN; PROMOTER REGION; PROSTAGLANDIN SYNTHESIS; PROTEIN EXPRESSION; TUMOR XENOGRAFT;

ANIMALS; CELL LINE, TUMOR; DINOPROSTONE; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INTRAMOLECULAR OXIDOREDUCTASES; MICE; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RNA, MESSENGER; THIOCYANATES; TRANSPLANTATION, HETEROLOGOUS;

MUS;

EID: 84869205212     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049744     Document Type: Article

References (63)

1. Park JY, Pillinger MH, Abramson SB, (2006) Prostaglandin E2 synthesis and secretion: the role of PGE2 synthases. Clin Immunol 119: 229-240.
2. Murakami M, Kudo I, (2002) Phospholipase A2. J Biochem 131: 285-292.
3. Smith WL, (1989) The eicosanoids and their biochemical mechanisms of action. Biochem J 259: 315-324.
4. Davies P, Bailey PJ, Goldenberg MM, Ford-Hutchinson AW, (1984) The role of arachidonic acid oxygenation products in pain and inflammation. Annu Rev Immunol 2: 335-357.
5. Bianchi A, Moulin D, Sebillaud S, Koufany M, Galteau MM, et al. (2005) Contrasting effects of peroxisome-proliferator-activated receptor (PPAR)gamma agonists on membrane-associated prostaglandin E2 synthase-1 in IL-1beta-stimulated rat chondrocytes: evidence for PPARgamma-independent inhibition by 15-deoxy-Delta12,14prostaglandin J2. Arthritis Res Ther 7: R1325-1337.
6. Kudo I, Murakami M, (2005) Prostaglandin e synthase, a terminal enzyme for prostaglandin E2 biosynthesis. J Biochem Mol Biol 38: 633-638.
7. Funk CD, (2001) Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294: 1871-1875.
8. Rainsford KD, (2007) Anti-inflammatory drugs in the 21st century. Subcell Biochem 42: 3-27.
9. Iyer JP, Srivastava PK, Dev R, Dastidar SG, Ray A, (2009) Prostaglandin E(2) synthase inhibition as a therapeutic target. Expert Opin Ther Targets 13: 849-865.
10. Ambrosone CB, McCann SE, Freudenheim JL, Marshall JR, Zhang Y, et al. (2004) Breast cancer risk in premenopausal women is inversely associated with consumption of broccoli, a source of isothiocyanates, but is not modified by GST genotype. J Nutr 134: 1134-1138.
11. Zhao B, Seow A, Lee EJ, Poh WT, Teh M, et al. (2001) Dietary isothiocyanates, glutathione S-transferase-M1,-T1 polymorphisms and lung cancer risk among Chinese women in Singapore. Cancer Epidemiol Biomarkers Prev 10: 1063-1067.
12. Zhang Y, Talalay P, (1994) Anticarcinogenic activities of organic isothiocyanates: chemistry and mechanisms. Cancer Res 54: 1976s-1981s.
13. Fahey JW, Talalay P, (1999) Antioxidant functions of sulforaphane: a potent inducer of Phase II detoxication enzymes. Food Chem Toxicol 37: 973-979.
14. Maheo K, Morel F, Langouet S, Kramer H, Le Ferrec E, et al. (1997) Inhibition of cytochromes P-450 and induction of glutathione S-transferases by sulforaphane in primary human and rat hepatocytes. Cancer Res 57: 3649-3652.
15. Gamet-Payrastre L, Li P, Lumeau S, Cassar G, Dupont MA, et al. (2000) Sulforaphane, a naturally occurring isothiocyanate, induces cell cycle arrest and apoptosis in HT29 human colon cancer cells. Cancer Res 60: 1426-1433.
16. Gamet-Payrastre L, Lumeau S, Gasc N, Cassar G, Rollin P, et al. (1998) Selective cytostatic and cytotoxic effects of glucosinolates hydrolysis products on human colon cancer cells in vitro. Anticancer Drugs 9: 141-148.
17. Choi S, Lew KL, Xiao H, Herman-Antosiewicz A, Xiao D, et al. (2007) D,L-Sulforaphane-induced cell death in human prostate cancer cells is regulated by inhibitor of apoptosis family proteins and Apaf-1. Carcinogenesis 28: 151-162.
18. Gingras D, Gendron M, Boivin D, Moghrabi A, Theoret Y, et al. (2004) Induction of medulloblastoma cell apoptosis by sulforaphane, a dietary anticarcinogen from Brassica vegetables. Cancer Lett 203: 35-43.
19. Jackson SJ, Singletary KW, (2004) Sulforaphane: a naturally occurring mammary carcinoma mitotic inhibitor, which disrupts tubulin polymerization. Carcinogenesis 25: 219-227.
20. Chiao JW, Chung FL, Kancherla R, Ahmed T, Mittelman A, et al. (2002) Sulforaphane and its metabolite mediate growth arrest and apoptosis in human prostate cancer cells. Int J Oncol 20: 631-636.
21. Shen G, Xu C, Chen C, Hebbar V, Kong AN, (2006) p53-independent G1 cell cycle arrest of human colon carcinoma cells HT-29 by sulforaphane is associated with induction of p21CIP1 and inhibition of expression of cyclin D1. Cancer Chemother Pharmacol 57: 317-327.
22. Jackson SJ, Singletary KW, Venema RC, (2007) Sulforaphane suppresses angiogenesis and disrupts endothelial mitotic progression and microtubule polymerization. Vascul Pharmacol 46: 77-84.
23. Bertl E, Bartsch H, Gerhauser C, (2006) Inhibition of angiogenesis and endothelial cell functions are novel sulforaphane-mediated mechanisms in chemoprevention. Mol Cancer Ther 5: 575-585.
24. Heiss E, Herhaus C, Klimo K, Bartsch H, Gerhauser C, (2001) Nuclear factor kappa B is a molecular target for sulforaphane-mediated anti-inflammatory mechanisms. J Biol Chem 276: 32008-32015.
25. Cross JV, Rady JM, Foss Jr FW, Lyons C, Macdonald TL, et al. (2009) Nutrient isothiocyanates covalently modify and inhibit the inflammatory cytokine macrophage migration inhibitory factor (MIF). Biochem J.
26. Maxwell PH, (2005) The HIF pathway in cancer. Semin Cell Dev Biol 16: 523-530.
27. Semenza GL, (2003) Targeting HIF-1 for cancer therapy. Nat Rev Cancer 3: 721-732.
28. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, et al. (1999) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399: 271-275.
29. Brown JM, (2002) Tumor microenvironment and the response to anticancer therapy. Cancer Biol Ther 1: 453-458.
30. Moeller BJ, Cao Y, Li CY, Dewhirst MW, (2004) Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: role of reoxygenation, free radicals, and stress granules. Cancer Cell 5: 429-441.
31. Apte RN, Dotan S, Elkabets M, White MR, Reich E, et al. (2006) The involvement of IL-1 in tumorigenesis, tumor invasiveness, metastasis and tumor-host interactions. Cancer Metastasis Rev 25: 387-408.
32. Hellwig-Burgel T, Rutkowski K, Metzen E, Fandrey J, Jelkmann W, (1999) Interleukin-1beta and tumor necrosis factor-alpha stimulate DNA binding of hypoxia-inducible factor-1. Blood 94: 1561-1567.
33. Stiehl DP, Jelkmann W, Wenger RH, Hellwig-Burgel T, (2002) Normoxic induction of the hypoxia-inducible factor 1alpha by insulin and interleukin-1beta involves the phosphatidylinositol 3-kinase pathway. FEBS Lett 512: 157-162.
34. Sinha P, Clements VK, Fulton AM, Ostrand-Rosenberg S, (2007) Prostaglandin E2 promotes tumor progression by inducing myeloid-derived suppressor cells. Cancer Res 67: 4507-4513.
35. Lin W, Wu RT, Wu T, Khor TO, Wang H, et al. (2008) Sulforaphane suppressed LPS-induced inflammation in mouse peritoneal macrophages through Nrf2 dependent pathway. Biochem Pharmacol 76: 967-973.
36. Cheung KL, Khor TO, Kong AN, (2009) Synergistic effect of combination of phenethyl isothiocyanate and sulforaphane or curcumin and sulforaphane in the inhibition of inflammation. Pharm Res 26: 224-231.
37. Mohammed SI, Coffman K, Glickman NW, Hayek MG, Waters DJ, et al. (2001) Prostaglandin E2 concentrations in naturally occurring canine cancer. Prostaglandins Leukot Essent Fatty Acids 64: 1-4.
38. Hanaka H, Pawelzik SC, Johnsen JI, Rakonjac M, Terawaki K, et al. (2009) Microsomal prostaglandin E synthase 1 determines tumor growth in vivo of prostate and lung cancer cells. Proc Natl Acad Sci U S A 106: 18757-18762.
39. Deems R, Buczynski MW, Bowers-Gentry R, Harkewicz R, Dennis EA, (2007) Detection and quantitation of eicosanoids via high performance liquid chromatography-electrospray ionization-mass spectrometry. Methods Enzymol 432: 59-82.
40. Stichtenoth DO, Thoren S, Bian H, Peters-Golden M, Jakobsson PJ, et al. (2001) Microsomal prostaglandin E synthase is regulated by proinflammatory cytokines and glucocorticoids in primary rheumatoid synovial cells. J Immunol 167: 469-474.
41. Cheng S, Afif H, Martel-Pelletier J, Pelletier JP, Li X, et al. (2004) Activation of peroxisome proliferator-activated receptor gamma inhibits interleukin-1beta-induced membrane-associated prostaglandin E2 synthase-1 expression in human synovial fibroblasts by interfering with Egr-1. J Biol Chem 279: 22057-22065.
42. Naraba H, Yokoyama C, Tago N, Murakami M, Kudo I, et al. (2002) Transcriptional regulation of the membrane-associated prostaglandin E2 synthase gene. Essential role of the transcription factor Egr-1. J Biol Chem 277: 28601-28608.
43. Lee JJ, Natsuizaka M, Ohashi S, Wong GS, Takaoka M, et al. (2010) Hypoxia activates the cyclooxygenase-2-prostaglandin E synthase axis. Carcinogenesis 31: 427-434.
44. Cho SJ, Kang MJ, Homer RJ, Kang HR, Zhang X, et al. (2006) Role of early growth response-1 (Egr-1) in interleukin-13-induced inflammation and remodeling. J Biol Chem 281: 8161-8168.
45. Egerod FL, Bartels A, Fristrup N, Borre M, Orntoft TF, et al. (2009) High frequency of tumor cells with nuclear Egr-1 protein expression in human bladder cancer is associated with disease progression. BMC Cancer 9: 385.
46. Komatsu DE, Hadjiargyrou M, (2004) Activation of the transcription factor HIF-1 and its target genes, VEGF, HO-1, iNOS, during fracture repair. Bone 34: 680-688.
47. Swirnoff AH, Milbrandt J, (1995) DNA-binding specificity of NGFI-A and related zinc finger transcription factors. Mol Cell Biol 15: 2275-2287.
48. Christy B, Nathans D, (1989) DNA binding site of the growth factor-inducible protein Zif268. Proc Natl Acad Sci U S A 86: 8737-8741.
49. Mabjeesh NJ, Escuin D, LaVallee TM, Pribluda VS, Swartz GM, et al. (2003) 2ME2 inhibits tumor growth and angiogenesis by disrupting microtubules and dysregulating HIF. Cancer Cell 3: 363-375.
50. Woo KJ, Kwon TK, (2007) Sulforaphane suppresses lipopolysaccharide-induced cyclooxygenase-2 (COX-2) expression through the modulation of multiple targets in COX-2 gene promoter. Int Immunopharmacol 7: 1776-1783.
51. Williams CS, Mann M, DuBois RN, (1999) The role of cyclooxygenases in inflammation, cancer, and development. Oncogene 18: 7908-7916.
52. Ding Y, Tong M, Liu S, Moscow JA, Tai HH, (2005) NAD+-linked 15-hydroxyprostaglandin dehydrogenase (15-PGDH) behaves as a tumor suppressor in lung cancer. Carcinogenesis 26: 65-72.
53. Graham DJ, Campen D, Hui R, Spence M, Cheetham C, et al. (2005) Risk of acute myocardial infarction and sudden cardiac death in patients treated with cyclo-oxygenase 2 selective and non-selective non-steroidal anti-inflammatory drugs: nested case-control study. Lancet 365: 475-481.
54. Clyman RI, Mauray F, Rudolph AM, Heymann MA, (1980) Age-dependent sensitivity of the lamb ductus arteriosus to indomethacin and prostaglandins. J Pediatr 96: 94-98.
55. Miller AM, Rayburn WF, Smith CV, (1991) Patterns of uterine activity after intravaginal prostaglandin E2 during preinduction cervical ripening. Am J Obstet Gynecol 165: 1006-1009.
56. Gomez-Hernandez A, Martin-Ventura JL, Sanchez-Galan E, Vidal C, Ortego M, et al. (2006) Overexpression of COX-2, Prostaglandin E synthase-1 and prostaglandin E receptors in blood mononuclear cells and plaque of patients with carotid atherosclerosis: regulation by nuclear factor-kappaB. Atherosclerosis 187: 139-149.
57. Li X, Afif H, Cheng S, Martel-Pelletier J, Pelletier JP, et al. (2005) Expression and regulation of microsomal prostaglandin E synthase-1 in human osteoarthritic cartilage and chondrocytes. J Rheumatol 32: 887-895.
58. Thornton RD, Lane P, Borghaei RC, Pease EA, Caro J, et al. (2000) Interleukin 1 induces hypoxia-inducible factor 1 in human gingival and synovial fibroblasts. Biochem J 350 Pt 1: 307-312.
59. Grimmer C, Pfander D, Swoboda B, Aigner T, Mueller L, et al. (2007) Hypoxia-inducible factor 1alpha is involved in the prostaglandin metabolism of osteoarthritic cartilage through up-regulation of microsomal prostaglandin E synthase 1 in articular chondrocytes. Arthritis Rheum 56: 4084-4094.
60. Banning A, Florian S, Deubel S, Thalmann S, Muller-Schmehl K, et al. (2008) GPx2 counteracts PGE2 production by dampening COX-2 and mPGES-1 expression in human colon cancer cells. Antioxid Redox Signal 10: 1491-1500.
61. Nishikawa T, Tsuno NH, Okaji Y, Sunami E, Shuno Y, et al. (2010) The inhibition of autophagy potentiates anti-angiogenic effects of sulforaphane by inducing apoptosis. Angiogenesis 13: 227-238.
62. Bert AG, Grepin R, Vadas MA, Goodall GJ, (2006) Assessing IRES activity in the HIF-1αlpha and other cellular 5′ UTRs. RNA 12: 1074-1083.
63. Lang KJ, Kappel A, Goodall GJ, (2002) Hypoxia-inducible factor-1alpha mRNA contains an internal ribosome entry site that allows efficient translation during normoxia and hypoxia. Mol Biol Cell 13: 1792-1801.