In vivo modulation of iNOS pathway in hepatocellular carcinoma by Nigella sativa

Environmental Health and Preventive Medicine

Volumn 18, Issue 5, 2013, Pages 377-385

  Fathy, Moustafa ^a,b   Nikaido, Toshio ^a  

^a UNIVERSITY OF TOYAMA   (Japan)

^b Minia University   (Egypt)

Author keywords

Hepatocellular carcinoma; Inducible nitric oxide synthase; Nigella sativa ethanolic extract; Nitric oxide; Tumor necrosis factor alpha

Indexed keywords

ALPHA FETOPROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; MESSENGER RNA; NIGELLA SATIVA EXTRACT; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BLACK CUMIN; CONTROLLED STUDY; DRUG EFFECT; DRUG EFFICACY; ENZYME ACTIVITY; ENZYME BLOOD LEVEL; ENZYME REGULATION; HISTOPATHOLOGY; IN VIVO STUDY; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; LIVER HISTOLOGY; MALE; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING;

NIGELLA SATIVA; RATTUS;

ALKYLATING AGENTS; ALPHA-FETOPROTEINS; ANIMALS; ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; CYTOKINES; DIETHYLNITROSAMINE; DNA, COMPLEMENTARY; ENZYME-LINKED IMMUNOSORBENT ASSAY; LIVER NEOPLASMS, EXPERIMENTAL; MALE; NIGELLA SATIVA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PLANT EXTRACTS; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEEDS;

EID: 84884974691     PISSN: 1342078X     EISSN: 13474715     Source Type: Journal    
DOI: 10.1007/s12199-013-0336-8     Document Type: Article

References (65)

1. Alderton WK, Cooper CE, Knowles RG. Nitric oxide synthases: structure, function and inhibition. Biochem J. 2001;357:593-615.
2. Schwentker A, Vodovotz Y, Weller R, Billiar TR. Nitric oxide and wound repair: role of cytokines? Nitric Oxide. 2002;7:1-10.
3. Stamler JS, Lamas S, Fang FC. Nitrosylation. The prototypic redox-based signaling mechanism. Cell. 2001;106:675-83.
4. Dedon PC, Tannenbaum SR. Reactive nitrogen species in the chemical biology of inflammation. Arch Biochem Biophys. 2004;423:12-22.
5. Ohshima H, Tatemichi M, Sawa T. Chemical basis of inflammation-induced carcinogenesis. Arch Biochem Biophys. 2003;417:3-11.
6. Crowell JA, Steele VE, Sigman CC, Fay JR. Is inducible nitric oxide synthase a target for chemoprevention? Mol Cancer Ther. 2003;2:815-23.
7. Hofseth LJ, Hussain SP, Wogan GN, Harris CC. Nitric oxide in cancer and chemoprevention. Free Radic Biol Med. 2003;34:955-68.
8. Jaiswal M, LaRusso NF, Gores GJ. Nitric oxide in gastrointestinal epithelial cell carcinogenesis: linking inflammation to oncogenesis. Am J Physiol Gastrointest Liver Physiol. 2001;281:G626-34.
9. Wu J, Akaike T, Hayashida K, Okamoto T, Okuyama A, Maeda H. Enhanced vascular permeability in solid tumor involving peroxynitrite and matrix metalloproteinases. Jpn J Cancer Res. 2001;92:439-51.
10. Aurello P, Rossi Del Monte S, D'Angelo F, Cicchini C, Ciardi A, Bellagamba R, et al. Vascular endothelial growth factor C and microvessel density in gastric carcinoma: correlation with clinicopathological factors. Our experience and review of the literature. Oncol Res. 2009;17:405-11.
11. Ishii Y, Ogura T, Tatemichi M, Fujisawa H, Otsuka F, Esumi H. Induction of matrix metalloproteinase gene transcription by nitric oxide and mechanisms of MMP-1 gene induction in human melanoma cell lines. Int J Cancer. 2003;103:161-8.
12. Ribes J, Cleries R, Esteban L, Moreno V, Bosch FX. The influence of alcohol consumption and hepatitis B and C infections on the risk of liver cancer in Europe. J Hepatol. 2008;49:233-42.
13. Parkin DM, Bray F, Ferlay J, Pisani P. Estimating the world cancer burden: Globocan 2000. Int J Cancer. 2001;94:153-6.
14. D'Alessandro N, Poma P, Montalto G. Multifactorial nature of hepatocellular carcinoma drug resistance: could plant polyphenols be helpful? World J Gastroenterol. 2007;13:2037-43.
15. Ikeguchi M, Ueta T, Yamane Y, Hirooka Y, Kaibara N. Inducible nitric oxide synthase and survivin messenger RNA expression in hepatocellular carcinoma. Clin Cancer Res. 2002;8:3131-6.
16. Rahman MA, Dhar DK, Yamaguchi E, Maruyama S, Sato T, Hayashi H, et al. Coexpression of inducible nitric oxide synthase and COX-2 in hepatocellular carcinoma and surrounding liver: possible involvement of COX-2 in the angiogenesis of hepatitis C virus-positive cases. Clin Cancer Res. 2001;7:1325-32.
17. Mohammed NA, Abd El-Aleem S, Appleton I, Maklouf MM, Said M, McMahon RF. Expression of nitric oxide synthase isoforms in human liver cirrhosis. J Pathol. 2003;200:647-55.
18. Gardner CR, Laskin JD, Dambach DM, Sacco M, Durham SK, Bruno MK, et al. Reduced hepatotoxicity of acetaminophen in mice lacking inducible nitric oxide synthase: potential role of tumor necrosis factor-alpha and interleukin-10. Toxicol Appl Pharmacol. 2002;184:27-36.
19. McKim SE, Gabele E, Isayama F, Lambert JC, Tucker LM, Wheeler MD, et al. Inducible nitric oxide synthase is required in alcohol-induced liver injury: studies with knockout mice. Gastroenterology. 2003;125:1834-44.
20. Sanz-Cameno P, Medina J, Garcia-Buey L, Garcia-Sanchez A, Borque MJ, Martin-Vilchez S, et al. Enhanced intrahepatic inducible nitric oxide synthase expression and nitrotyrosine accumulation in primary biliary cirrhosis and autoimmune hepatitis. J Hepatol. 2002;37:723-9.
21. Wei CL, Khoo HE, Lee KH, Hon WM. Differential expression and localization of nitric oxide synthases in cirrhotic livers of bile duct-ligated rats. Nitric Oxide. 2002;7:91-102.
22. Balkwill F. Tumor necrosis factor or tumor promoting factor? Cytokine Growth Factor Rev. 2002;13:135-41.
23. Balkwill F, Charles KA, Mantovani A. Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell. 2005;7:211-7.
24. Aggarwal BB, Shishodia S, Sandur SK, Pandey MK, Sethi G. Inflammation and cancer: how hot is the link? Biochem Pharmacol. 2006;72:1605-21.
25. Aviello G, Romano B, Borrelli F, Capasso R, Gallo L, Piscitelli F, et al. Chemopreventive effect of the non-psychotropic phytocannabinoid cannabidiol on experimental colon cancer. J Mol Med (Berl). 2012. doi: 10.1007/s00109-011-0856- x.
26. Huang FY, Chan AO, Rashid A, Wong DK, Cho CH, Yuen MF. Helicobacter pylori induces promoter methylation of E-cadherin via interleukin-1beta activation of nitric oxide production in gastric cancer cells. Cancer. 2012;118:4969-80.
27. Li CF, Fang FM, Wang JM, Tzeng CC, Tai HC, Wei YC, et al. EGFR nuclear import in gallbladder carcinoma: nuclear phosphorylated EGFR upregulates iNOS expression and confers independent prognostic impact. Ann Surg Oncol. 2012;19:443-54.
28. Li TW, Yang H, Peng H, Xia M, Mato JM, Lu SC. Effects of S-adenosylmethionine and methylthioadenosine on inflammation-induced colon cancer in mice. Carcinogenesis. 2012;33:427-35.
29. Ma N, Thanan R, Kobayashi H, Hammam O, Wishahi M, El Leithy T, et al. Nitrative DNA damage and Oct3/4 expression in urinary bladder cancer with Schistosoma haematobium infection. Biochem Biophys Res Commun. 2011;414:344-9.
30. Murata M, Thanan R, Ma N, Kawanishi S. Role of nitrative and oxidative DNA damage in inflammation-related carcinogenesis. J Biomed Biotechnol. 2012;2012:623019.
31. Piplani H, Vaish V, Sanyal SN. Dolastatin 15, a mollusk linear peptide, and Celecoxib, a selective cyclooxygenase-2 inhibitor, prevent preneoplastic colonic lesions and induce apoptosis through inhibition of the regulatory transcription factor NF-kappaB and an inflammatory protein, iNOS. Eur J Cancer Prev. 2012;21:511-22.
32. Vaish V, Sanyal SN. Role of Sulindac and Celecoxib in the regulation of angiogenesis during the early neoplasm of colon: exploring PI3-K/PTEN/Akt pathway to the canonical Wnt/beta-catenin signaling. Biomed Pharmacother. 2012;66:354-67.
33. Abdel-Hamid NM, El-Moselhy MA, El-Baz A. Hepatocyte lysosomal membrane stabilization by olive leaves against chemically induced hepatocellular neoplasia in rats. Int J Hepatol. 2011;2011:736581.
34. Randhawa MA, Alghamdi MS. Anticancer activity of Nigella sativa (black seed) - a review. Am J Chin Med. 2011;39:1075-91.
35. Ashraf SS, Rao MV, Kaneez FS, Qadri S, Al-Marzouqi AH, Chandranath IS, et al. Nigella sativa extract as a potent antioxidant for petrochemical-induced oxidative stress. J Chromatogr Sci. 2011;49:321-6.
36. Ali BH, Blunden G. Pharmacological and toxicological properties of Nigella sativa. Phytother Res. 2003;17:299-305.
37. Salem ML. Immunomodulatory and therapeutic properties of the Nigella sativa L. seed. Int Immunopharmacol. 2005;5:1749-70.
38. Padhye S, Banerjee S, Ahmad A, Mohammad R, Sarkar FH. From here to eternity - the secret of Pharaohs: therapeutic potential of black cumin seeds and beyond. Cancer Ther. 2008;6:495-510.
39. el Ammar SM, Gameil NM, Shawky NM, Nader MA. Comparative evaluation of anti-inflammatory properties of thymoquinone and curcumin using an asthmatic murine model. Int Immunopharmacol. 2011;11:2232-6.
40. Ibrahim ZS, Ishizuka M, Soliman M, ElBohi K, Sobhy W, Muzandu K, et al. Protection by Nigella sativa against carbon tetrachloride-induced downregulation of hepatic cytochrome P450 isozymes in rats. Jpn J Vet Res. 2008;56:119-28.
41. Kanter M. Effects of Nigella sativa seed extract on ameliorating lung tissue damage in rats after experimental pulmonary aspirations. Acta Histochem. 2009;111:393-403.
42. Kanter M. Thymoquinone attenuates lung injury induced by chronic toluene exposure in rats. Toxicol Ind Health. 2011;27:387-95.
43. Kanter M. Thymoquinone reestablishes spermatogenesis after testicular injury caused by chronic toluene exposure in rats. Toxicol Ind Health. 2011;27:155-66.
44. Michel CG, El-Sayed NS, Moustafa SF, Ezzat SM, Nesseem DI, El-Alfy TS. Phytochemical and biological investigation of the extracts of Nigella sativa L. seed waste. Drug Test Anal. 2011;3:245-54.
45. Sayed-Ahmed MM, Aleisa AM, Al-Rejaie SS, Al-Yahya AA, Al-Shabanah OA, Hafez MM, et al. Thymoquinone attenuates diethylnitrosamine induction of hepatic carcinogenesis through antioxidant signaling. Oxid Med Cell Longev. 2010;3:254-61.
46. Singh S, Gupta AK. Nitric oxide: role in tumour biology and iNOS/NO-based anticancer therapies. Cancer Chemother Pharmacol. 2011;67:1211-24.
47. Giantonio BJ, Catalano PJ, Meropol NJ, O'Dwyer PJ, Mitchell EP, Alberts SR, et al. Bevacizumab in combination with oxaliplatin, fluorouracil, and leucovorin (FOLFOX4) for previously treated metastatic colorectal cancer: results from the Eastern Cooperative Oncology Group Study E3200. J Clin Oncol. 2007;25:1539-44.
48. Ichinoe M, Mikami T, Shiraishi H, Okayasu I. High microvascular density is correlated with high VEGF, iNOS and COX-2 expression in penetrating growth-type early gastric carcinomas. Histopathology. 2004;45:612-8.
49. Nakamura Y, Yasuoka H, Tsujimoto M, Yang Q, Tsukiyama A, Imabun S, et al. Clinicopathological significance of vascular endothelial growth factor-C in breast carcinoma with long-term follow-up. Mod Pathol. 2003;16:309-14.
50. Ahn B, Ohshima H. Suppression of intestinal polyposis in Apc(Min/+) mice by inhibiting nitric oxide production. Cancer Res. 2001;61:8357-60.
51. Kisley LR, Barrett BS, Bauer AK, Dwyer-Nield LD, Barthel B, Meyer AM, et al. Genetic ablation of inducible nitric oxide synthase decreases mouse lung tumorigenesis. Cancer Res. 2002;62:6850-6.
52. Rao CV, Indranie C, Simi B, Manning PT, Connor JR, Reddy BS. Chemopreventive properties of a selective inducible nitric oxide synthase inhibitor in colon carcinogenesis, administered alone or in combination with celecoxib, a selective cyclooxygenase-2 inhibitor. Cancer Res. 2002;62:165-70.
53. Scott DJ, Hull MA, Cartwright EJ, Lam WK, Tisbury A, Poulsom R, et al. Lack of inducible nitric oxide synthase promotes intestinal tumorigenesis in the Apc(Min/+) mouse. Gastroenterology. 2001;121:889-99.
54. Boyault S, Rickman DS, de Reynies A, Balabaud C, Rebouissou S, Jeannot E, et al. Transcriptome classification of HCC is related to gene alterations and to new therapeutic targets. Hepatology. 2007;45:42-52.
55. Khan MS, Halagowder D, Devaraj SN. Methylated chrysin induces co-ordinated attenuation of the canonical Wnt and NF-κB signaling pathway and upregulates apoptotic gene expression in the early hepatocarcinogenesis rat model. Chem Biol Interact. 2011;193:12-21.
56. Iddamaldeniya SS, Thabrew MI, Wickramasinghe SM, Ratnatunge N, Thammitiyagodage MG. A long-term investigation of the anti-hepatocarcinogenic potential of an indigenous medicine comprised of Nigella sativa, Hemidesmus indicus and Smilax glabra. J Carcinog. 2006;5:11.
57. Iddamaldeniya SS, Wickramasinghe N, Thabrew I, Ratnatunge N, Thammitiyagodage MG. Protection against diethylnitrosoamine-induced hepatocarcinogenesis by an indigenous medicine comprised of Nigella sativa, Hemidesmus indicus and Smilax glabra: a preliminary study. J Carcinog. 2003;2:6.
58. Al-Ali A, Alkhawajah AA, Randhawa MA, Shaikh NA. Oral and intraperitoneal LD50 of thymoquinone, an active principle of Nigella sativa, in mice and rats. J Ayub Med Coll Abbottabad. 2008;20:25-7.
59. Mansour MA, Ginawi OT, El-Hadiyah T, El-Khatib AS, Al-Shabanah OA, Al-Sawaf HA. Effects of volatile oil constituents of Nigella sativa on carbon tetrachloride-induced hepatotoxicity in mice: evidence for antioxidant effects of thymoquinone. Res Commun Mol Pathol Pharmacol. 2001;110:239-51.
60. Mansour MA, Al-Ismaeel H, Al-Rikabi AC, Al-Shabanah OA. Comparison of angiotensin converting enzyme inhibitors and angiotensin II type 1 receptor blockade for the prevention of premalignant changes in the liver. Life Sci. 2011;89:188-94.
61. Nakagawa T, Takeishi S, Kameyama A, Yagi H, Yoshioka T, Moriwaki K, et al. Glycomic analyses of glycoproteins in bile and serum during rat hepatocarcinogenesis. J Proteome Res. 2010;9:4888-96.
62. Taha MM, Abdul AB, Abdullah R, Ibrahim TA, Abdelwahab SI, Mohan S. Potential chemoprevention of diethylnitrosamine-initiated and 2-acetylaminofluorene-promoted hepatocarcinogenesis by zerumbone from the rhizomes of the subtropical ginger (Zingiber zerumbet). Chem Biol Interact. 2010;186:295-305.
63. Singh BN, Singh BR, Sarma BK, Singh HB. Potential chemoprevention of N-nitrosodiethylamine-induced hepatocarcinogenesis by polyphenolics from Acacia nilotica bark. Chem Biol Interact. 2009;181:20-8.
64. Lee J, Lim KT. Preventive effect of phytoglycoprotein (38 kDa) on expression of alpha-fetoprotein and matrix metalloproteinase-9 in diethylnitrosamine-treated ICR mice. Drug Chem Toxicol. 2011;35(3):277-84.
65. Machida K, Tsukamoto H, Liu JC, Han YP, Govindarajan S, Lai MM, et al. c-Jun mediates hepatitis C virus hepatocarcinogenesis through signal transducer and activator of transcription 3 and nitric oxide-dependent impairment of oxidative DNA repair. Hepatology. 2010;52:480-92.