Inhibition of fatty acid amide hydrolase activates Nrf2 signalling and induces heme oxygenase 1 transcription in breast cancer cells

British Journal of Pharmacology

Volumn 170, Issue 3, 2013, Pages 489-505

  Li, H ^a   Wood, J T ^b   Whitten, K M ^b   Vadivel, S K ^b   Seng, S ^a   Makriyannis, A ^b   Avraham, H K ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b NORTHEASTERN UNIVERSITY   (United States)

Author keywords

breast cancer; endocannabinoids; FAAH enzyme; heme oxygenase 1; Nrf2; oxidative stress

Indexed keywords

ANANDAMIDE; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CYCLOHEXYLCARBAMIC ACID 3' CARBAMOYLBIPHENYL 3 YL ESTER; FATTY ACID AMIDASE; HEME OXYGENASE 1; KELCH LIKE ECH ASSOCIATED PROTEIN 1; MESSENGER RNA; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NRF2; VANILLOID RECEPTOR 1;

ANTIOXIDANT ACTIVITY; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CANCER CELL CULTURE; CELL IMMORTALIZATION; CELL STRAIN MCF 7; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

BREAST CANCER; ENDOCANNABINOIDS; FAAH ENZYME; HEME OXYGENASE 1; NRF2; OXIDATIVE STRESS;

ACTIVE TRANSPORT, CELL NUCLEUS; AMIDOHYDROLASES; ANTINEOPLASTIC AGENTS; ARACHIDONIC ACIDS; BENZAMIDES; BREAST NEOPLASMS; CARBAMATES; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCANNABINOIDS; ENZYME INDUCTION; ENZYME INHIBITORS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HEME OXYGENASE-1; HUMANS; MCF-7 CELLS; NF-E2-RELATED FACTOR 2; POLYUNSATURATED ALKAMIDES; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TRANSFECTION;

EID: 84884553627     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12111     Document Type: Article

References (73)

1. Abadji V, Lin S, Taha G, Griffin G, Stevenson LA, Pertwee RG, et al. (1994). (R)-methanandamide: a chiral novel anandamide possessing higher potency and metabolic stability. J Med Chem 37: 1889-1893.
2. Alpini G, Demorrow S, (2009). Changes in the endocannabinoid system may give insight into new and effective treatments for cancer. Vitam Horm 81: 469-485.
3. Benhar M, Engelberg D, Levitzki A, (2002). ROS, stress-activated kinases and stress signaling in cancer. EMBO Rep 3: 420-425.
4. Berberat PO, Katori M, Kaczmarek E, Anselmo D, Lassman C, Ke B, et al. (2003). Heavy chain ferritin acts as an antiapoptotic gene that protects livers from ischemia reperfusion injury. FASEB J 17: 1724-1726.
5. Bisogno T, Ligresti A, Di Marzo V, (2005). The endocannabinoid signalling system: biochemical aspects. Pharmacol Biochem Behav 81: 224-238.
6. Chatterjee S, Kundu S, Sengupta S, Bhattacharyya A, (2009). Divergence to apoptosis from ROS induced cell cycle arrest: effect of cadmium. Mutat Res 663: 22-31.
7. Clapper JR, Mangieri RA, Piomelli D, (2009). The endocannabinoid system as a target for the treatment of cannabis dependence. Neuropharmacology 56 (Suppl. 1): 235-243.
8. De Petrocellis L, Melck D, Palmisano A, Bisogno T, Laezza C, Bifulco M, et al. (1998). The endogenous cannabinoid anandamide inhibits human breast cancer cell proliferation. Proc Natl Acad Sci U S A 95: 8375-8380.
9. Di Marzo V, Melck D, Orlando P, Bisogno T, Zagoory O, Bifulco M, et al. (2001). Palmitoylethanolamide inhibits the expression of fatty acid amide hydrolase and enhances the anti-proliferative effect of anandamide in human breast cancer cells. Biochem J 358 (Pt 1): 249-255.
10. Doi K, Akaike T, Fujii S, Tanaka S, Ikebe N, Beppu T, et al. (1999). Induction of haem oxygenase-1 nitric oxide and ischaemia in experimental solid tumours and implications for tumour growth. Br J Cancer 80: 1945-1954.
11. Durante W, (2003). Heme oxygenase-1 in growth control and its clinical application to vascular disease. J Cell Physiol 195: 373-382.
12. Egertova M, Michael GJ, Cravatt BF, Elphick MR, (2004). Fatty acid amide hydrolase in brain ventricular epithelium: mutually exclusive patterns of expression in mouse and rat. J Chem Neuroanat 28: 171-181.
13. Ewing P, Wilke A, Eissner G, Holler E, Andreesen R, Gerbitz A, (2005). Expression of heme oxygenase-1 protects endothelial cells from irradiation-induced apoptosis. Endothelium 12: 113-119.
14. Eyssen-Hernandez R, Ladoux A, Frelin C, (1996). Differential regulation of cardiac heme oxygenase-1 and vascular endothelial growth factor mRNA expressions by hemin, heavy metals, heat shock and anoxia. FEBS Lett 382: 229-233.
15. Fang J, Sawa T, Akaike T, Akuta T, Sahoo SK, Khaled G, et al. (2003). In vivo antitumor activity of pegylated zinc protoporphyrin: targeted inhibition of heme oxygenase in solid tumor. Cancer Res 63: 3567-3574.
16. Fang J, Sawa T, Akaike T, Greish K, Maeda H, (2004). Enhancement of chemotherapeutic response of tumor cells by a heme oxygenase inhibitor, pegylated zinc protoporphyrin. Int J Cancer 109: 1-8.
17. Folch J, Lees M, Sloane Stanley G, (1957). A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497-509.
18. Furukawa M, Xiong Y, (2005). BTB protein Keap1 targets antioxidant transcription factor Nrf2 for ubiquitination by the Cullin 3-Roc1 ligase. Mol Cell Biol 25: 162-171.
19. Gobbi G, Bambico FR, Mangieri R, Bortolato M, Campolongo P, Solinas M, et al. (2005). Antidepressant-like activity and modulation of brain monoaminergic transmission by blockade of anandamide hydrolysis. Proc Natl Acad Sci U S A 102: 18620-18625.
20. Goodman AI, Choudhury M, da Silva JL, Schwartzman ML, Abraham NG, (1997). Overexpression of the heme oxygenase gene in renal cell carcinoma. Proc Soc Exp Biol Med 214: 54-61.
21. Grimaldi C, Pisanti S, Laezza C, Malfitano AM, Santoro A, Vitale M, et al. (2006). Anandamide inhibits adhesion and migration of breast cancer cells. Exp Cell Res 312: 363-373.
22. Guindon J, Hohmann AG, (2009). The endocannabinoid system and pain. CNS Neurol Disord Drug Targets 8: 403-421.
23. Hart S, Fischer OM, Ullrich A, (2004). Cannabinoids induce cancer cell proliferation via tumor necrosis factor alpha-converting enzyme (TACE/ADAM17)-mediated transactivation of the epidermal growth factor receptor. Cancer Res 64: 1943-1950.
24. Hill M, Pereira V, Chauveau C, Zagani R, Remy S, Tesson L, et al. (2005). Heme oxygenase-1 inhibits rat and human breast cancer cell proliferation: mutual cross inhibition with indoleamine 2,3-dioxygenase. FASEB J 19: 1957-1968.
25. Jozkowicz A, Was H, Dulak J, (2007). Heme oxygenase-1 in tumors: is it a false friend? Antioxid Redox Signal 9: 2099-2117.
26. 9-tetrahydrocannabinol in BV-2 microglial cells. Br J Pharmacol 165: 2512-2528.
27. Kaspar JW, Niture SK, Jaiswal AK, (2009). Nrf2:INrf2 (Keap1) signaling in oxidative stress. Free Radic Biol Med 47: 1304-1309.
28. Kathuria S, Gaetani S, Fegley D, Valino F, Duranti A, Tontini A, et al. (2003). Modulation of anxiety through blockade of anandamide hydrolysis. Nat Med 9: 76-81.
29. Kim HJ, So HS, Lee JH, Park C, Park SY, Kim YH, et al. (2006). Heme oxygenase-1 attenuates the cisplatin-induced apoptosis of auditory cells via down-regulation of reactive oxygen species generation. Free Radic Biol Med 40: 1810-1819.
30. Kobayashi A, Tong KI, (2006). [Oxidative/electrophilic stress sensor Keap1 regulates the rapid turnover of transcripition factor Nrf2]. Tanpakushitsu Kakusan Koso 51 (10 Suppl.): 1304-1308.
31. Kobayashi M, Yamamoto M, (2005). Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid Redox Signal 7: 385-394.
32. Kobayashi M, Yamamoto M, (2006). Nrf2-Keap1 regulation of cellular defense mechanisms against electrophiles and reactive oxygen species. Adv Enzyme Regul 46: 113-140.
33. Laezza C, Pisanti S, Crescenzi E, Bifulco M, (2006). Anandamide inhibits Cdk2 and activates Chk1 leading to cell cycle arrest in human breast cancer cells. FEBS Lett 580: 6076-6082.
34. Lautier D, Luscher P, Tyrrell RM, (1992). Endogenous glutathione levels modulate both constitutive and UVA radiation/hydrogen peroxide inducible expression of the human heme oxygenase gene. Carcinogenesis 13: 227-232.
35. Lee JS, Surh YJ, (2005). Nrf2 as a novel molecular target for chemoprevention. Cancer Lett 224: 171-184.
36. Lee JM, Li J, Johnson DA, Stein TD, Kraft AD, Calkins MJ, et al. (2005). Nrf2, a multi-organ protector? FASEB J 19: 1061-1066.
37. Lin CW, Shen SC, Hou WC, Yang LY, Chen YC, (2008). Heme oxygenase-1 inhibits breast cancer invasion via suppressing the expression of matrix metalloproteinase-9. Mol Cancer Ther 7: 1195-1206.
38. Lin HY, Shen SC, Chen YC, (2005). Anti-inflammatory effect of heme oxygenase 1: glycosylation and nitric oxide inhibition in macrophages. J Cell Physiol 202: 579-590.
39. Lin HY, Shen SC, Lin CW, Yang LY, Chen YC, (2007). Baicalein inhibition of hydrogen peroxide-induced apoptosis via ROS-dependent heme oxygenase 1 gene expression. Biochim Biophys Acta 1773: 1073-1086.
40. Liu H, Nowak R, Chao W, Bloch KD, (2003). Nerve growth factor induces anti-apoptotic heme oxygenase-1 in rat pheochromocytoma PC12 cells. J Neurochem 86: 1553-1563.
41. McAllister SD, Glass M, (2002). CB(1) and CB(2) receptor-mediated signalling: a focus on endocannabinoids. Prostaglandins Leukot Essent Fatty Acids 66: 161-171.
42. Maines MD, (1988). Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J 2: 2557-2568.
43. Maines MD, Abrahamsson PA, (1996). Expression of heme oxygenase-1 (HSP32) in human prostate: normal, hyperplastic, and tumor tissue distribution. Urology 47: 727-733.
44. Martin D, Rojo AI, Salinas M, Diaz R, Gallardo G, Alam J, et al. (2004). Regulation of heme oxygenase-1 expression through the phosphatidylinositol 3-kinase/Akt pathway and the Nrf2 transcription factor in response to the antioxidant phytochemical carnosol. J Biol Chem 279: 8919-8929.
45. Melck D, Rueda D, Galve-Roperh I, De Petrocellis L, Guzman M, Di Marzo V, (1999). Involvement of the cAMP/protein kinase A pathway and of mitogen-activated protein kinase in the anti-proliferative effects of anandamide in human breast cancer cells. FEBS Lett 463: 235-240.
46. Motterlini R, Foresti R, Bassi R, Calabrese V, Clark JE, Green CJ, (2000). Endothelial heme oxygenase-1 induction by hypoxia. Modulation by inducible nitric-oxide synthase and S-nitrosothiols. J Biol Chem 275: 13613-13620.
47. Nasser MW, Qamri Z, Deol YS, Smith D, Shilo K, Zou X, et al. (2011). Crosstalk between chemokine receptor CXCR4 and cannabinoid receptor CB2 in modulating breast cancer growth and invasion. Plos One 6: e23901.
48. Nioi P, McMahon M, Itoh K, Yamamoto M, Hayes JD, (2003). Identification of a novel Nrf2-regulated antioxidant response element (ARE) in the mouse NAD(P)H:quinone oxidoreductase 1 gene: reassessment of the ARE consensus sequence. Biochem J 374 (Pt 2): 337-348.
49. Nishie A, Ono M, Shono T, Fukushi J, Otsubo M, Onoue H, et al. (1999). Macrophage infiltration and heme oxygenase-1 expression correlate with angiogenesis in human gliomas. Clin Cancer Res 5: 1107-1113.
50. Nowis D, Legat M, Grzela T, Niderla J, Wilczek E, Wilczynski GM, et al. (2006). Heme oxygenase-1 protects tumor cells against photodynamic therapy-mediated cytotoxicity. Oncogene 25: 3365-3374.
51. O'Sullivan SE, (2007). Cannabinoids go nuclear: evidence for activation of peroxisome proliferator-activated receptors. Br J Pharmacol 152: 576-582.
52. Oesch S, Gertsch J, (2009). Cannabinoid receptor ligands as potential anticancer agents-high hopes for new therapies? J Pharm Pharmacol 61: 839-853.
53. Otterbein LE, Soares MP, Yamashita K, Bach FH, (2003). Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol 24: 449-455.
54. Pae HO, Chung HT, (2009). Heme oxygenase-1: its therapeutic roles in inflammatory diseases. Immune Netw 9: 12-19.
55. Pae HO, Choi BM, Oh GS, Lee MS, Ryu DG, Rhew HY, et al. (2004). Roles of heme oxygenase-1 in the antiproliferative and antiapoptotic effects of nitric oxide on Jurkat T cells. Mol Pharmacol 66: 122-128.
56. Pi J, Leung L, Xue P, Wang W, Hou Y, Liu D, et al. (2010). Deficiency in the nuclear factor E2-related factor-2 transcription factor results in impaired adipogenesis and protects against diet-induced obesity. J Biol Chem 285: 9292-9300.
57. Piomelli D, Tarzia G, Duranti A, Tontini A, Mor M, Compton TR, et al. (2006). Pharmacological profile of the selective FAAH inhibitor KDS-4103 (URB597). CNS Drug Rev 12: 21-38.
58. Qamri Z, Preet A, Nasser MW, Bass CE, Leone G, Barsky SH, et al. (2009). Synthetic cannabinoid receptor agonists inhibit tumor growth and metastasis of breast cancer. Mol Cancer Ther 8: 3117-3129.
59. Rajesh M, Mukhopadhyay P, Hasko G, Liaudet L, Mackie K, Pacher P, (2010). Cannabinoid-1 receptor activation induces reactive oxygen species-dependent and -independent mitogen-activated protein kinase activation and cell death in human coronary artery endothelial cells. Br J Pharmacol 160: 688-700.
60. Rizzardini M, Zappone M, Villa P, Gnocchi P, Sironi M, Diomede L, et al. (1998). Kupffer cell depletion partially prevents hepatic heme oxygenase 1 messenger RNA accumulation in systemic inflammation in mice: role of interleukin 1beta. Hepatology 27: 703-710.
61. Ross RA, (2003). Anandamide and vanilloid TRPV1 receptors. Br J Pharmacol 140: 790-801.
62. Sander CS, Chang H, Hamm F, Elsner P, Thiele JJ, (2004). Role of oxidative stress and the antioxidant network in cutaneous carcinogenesis. Int J Dermatol 43: 326-335.
63. Siegmund SV, Uchinami H, Osawa Y, Brenner DA, Schwabe RF, (2005). Anandamide induces necrosis in primary hepatic stellate cells. Hepatology 41: 1085-1095.
64. Siegmund SV, Seki E, Osawa Y, Uchinami H, Cravatt BF, Schwabe RF, (2006). Fatty acid amide hydrolase determines anandamide-induced cell death in the liver. J Biol Chem 281: 10431-10438.
65. Stuhlmeier KM, (2000). Activation and regulation of Hsp32 and Hsp70. Eur J Biochem 267: 1161-1167.
66. Sunamura M, Duda DG, Ghattas MH, Lozonschi L, Motoi F, Yamauchi J, et al. (2003). Heme oxygenase-1 accelerates tumor angiogenesis of human pancreatic cancer. Angiogenesis 6: 15-24.
67. Tanaka S, Akaike T, Fang J, Beppu T, Ogawa M, Tamura F, et al. (2003). Antiapoptotic effect of haem oxygenase-1 induced by nitric oxide in experimental solid tumour. Br J Cancer 88: 902-909.
68. Terry CM, Clikeman JA, Hoidal JR, Callahan KS, (1998). Effect of tumor necrosis factor-alpha and interleukin-1 alpha on heme oxygenase-1 expression in human endothelial cells. Am J Physiol 274 (3 Pt 2): H883-H891.
69. Torisu-Itakura H, Furue M, Kuwano M, Ono M, (2000). Co-expression of thymidine phosphorylase and heme oxygenase-1 in macrophages in human malignant vertical growth melanomas. Jpn J Cancer Res 91: 906-910.
70. Walpole CS, Bevan S, Bovermann G, Boelsterli JJ, Breckenridge R, Davies JW, et al. (1994). The discovery of capsazepine, the first competitive antagonist of the sensory neuron excitants capsaicin and resiniferatoxin. J Med Chem 37: 1942-1954.
71. Wang Z, Zhang J, Liu H, Huang H, Wang C, Shen Y, et al. (2009). Melatonin, a potent regulator of hemeoxygenase-1, reduces cardiopulmonary bypass-induced renal damage in rats. J Pineal Res 46: 248-254.
72. Wei Y, Wang X, Wang L, (2009). Presence and regulation of cannabinoid receptors in human retinal pigment epithelial cells. Mol Vis 15: 1243-1251.
73. Williams J, Wood J, Pandarinathan L, Karanian DA, Bahr BA, Vouros P, et al. (2007). Quantitative method for the profiling of the endocannabinoid metabolome by LC-atmospheric pressure chemical ionization-MS. Anal Chem 79: 5582-5593.