Limonene Exerts Antiproliferative Effects and Increases Nitric Oxide Levels on a Lymphoma Cell Line by Dual Mechanism of the ERK Pathway: Relationship with Oxidative Stress

REFERENCES

• Hursting, S.D.; Perkins, S.N.; Haines, D.C.; Ward, J.M.; Phang, J.M. Chemoprevention of spontaneous tumorigenesis in p-53 knockout mice. Cancer Res 1995, 55, 3949–3953.
   PubMed Web of Science ®Google Scholar
• Elegbede, J.A.; Elson, C.E.; Qureshi, A.; Tanner, M.A.; Gould, M.N. Inhibition of DMBA-induced mammary cancer by monoterpene D-limonene. Carcinogenesis 1984, 5, 661–665.
   PubMed Web of Science ®Google Scholar
• Haag, J.D.; Lindstrom, M.J.; Gould, M.N. Limonene-induced regression of mammary carcinomas. Cancer Res 1992, 52, 4021–4026.
   PubMed Web of Science ®Google Scholar
• Manuele, M.G.; Ferraro, G.; Anesini, C. Effect of Tilia x viridis flowers on the proliferation of a lymphoma cell line and on normal murine lymphocytes: participation of monoterpenes specially limonene. Phytother Res 2008, 22, 1520–1526.
   PubMed Web of Science ®Google Scholar
• Manuele, M.G.; Barreiro Arcos, M.L.; Davicino, R.; Ferraro, G.; Cremaschi, G.; Anesini, C. Mechanism of the antiproliferative action of limonene on a lymphoma cell line: participation of nitric oxide. Phytother Res 20081011–1017.
   Web of Science ®Google Scholar
• Davicino, R.; Manuele, M.G.; Ferraro, G.; Micalizzi, Blas.; Anesini, C. Modulatory effect of hydrogen peroxide on tumoral lymphocytes proliferation. Immunopharmacol Immunotoxicol 2009, 31, 130–139.
   PubMedGoogle Scholar
• Su, T.T.; Chang, H.L.; Shyue, S.K.; Hsu, S.L. Emodin induces apoptosis in human lung adenocarcinoma cells through a reactive oxygen species-dependent mitochondrial signaling pathway. Biochem Pharmacol 2005, 70, 229–241.
   PubMed Web of Science ®Google Scholar
• Kondo, K.; Nakamura, H.; Masutami, H.; Yodoi, J. Redox regulation of human thioredoxin network. Antioxid Redox Signal 2006, 8, 1881–1890.
   PubMed Web of Science ®Google Scholar
• Anesini, C.; Genaro, A.; Cremaschi, G.; Sterin Borda, L.; Cazaux, C.; Borda, E. Immunomodulatory activity of Larrea divaricata Cav. Fitoterapia 1996, 67, 329–333.
   Google Scholar
• Manuele, M.G.; Ferraro, G.; Barreiro Arcos, M.L.; López, P.; Cremaschi, G.; Anesini, C. Comparative immunomodulatory effect of scopoletin on tumoral and normal lymphocytes. Life Sci 2006, 79, 2043–2048.
   PubMed Web of Science ®Google Scholar
• Becherel, P.A.; Chosidow, O.; LeGoff, L.; Frances, C.; Debre, P.; Mossalayi, M.D.; Arock, M. Inducible nitric oxide synthase and proinflammatory cytokine expression by human keratinocytes during acute urticaria. Mol Med 1997, 3, 686–694.
   PubMed Web of Science ®Google Scholar
• Gorelik, G.; Barreiro Arcos, M.L.; Klecha, A.J.; Cremaschi, G.A. Differential expression of protein kinase C isoenzymes related to high nitric oxide synthase activity in a T lymphoma cell line. Biochim Biophys Acta 2002, 1588, 179–188.
   PubMed Web of Science ®Google Scholar
• Carrillo, M.C.; Kanai, S.; Nokubo, M.; Kitani, K. Derprenyl induces activities of both superoxide dismutase and catalase but not glutathione peroxidase in the striatum of young male rats. Life Sci 1991, 48, 517–521.
   PubMed Web of Science ®Google Scholar
• Herzog, V.; Fahimi, H.D. A new sensitive colorimetric assay for peroxidase using 3,3′ diaminobenzidine as hydrogen donors. Anal Biochem 1973, 55, 554–562.
   PubMed Web of Science ®Google Scholar
• Schopf, R.E.; Mattar, J.; Meyenburg, W.; Scheiner, O.; Hammann, K.P.; Lemmei, E.M. Measurement of the respiratory burst in human monocytes and polymorphonuclear leukocytes by nitroblue tetrazolium reduction and chemiluminescence. J Immunol Methods 1984, 67, 109–117.
   PubMed Web of Science ®Google Scholar
• Dunnett, C.W. New tables of multiples comparisons with control. Biometrics 1964, 20, 482–491.
   Web of Science ®Google Scholar
• Wattenberg, L.W.; Sparnins, V.L.; Barany, G. Inhibition of N-nitrosodiethylamine carcinogenesis in mice by naturally occurring organosulfur compounds and monoterpenes. Cancer Res 1989, 49, 2689–2694.
   PubMed Web of Science ®Google Scholar
• Shoff, S.M.; Grummer, M.; Yatvin, M.B.; Elson, C.E. Concentration-dependent increase of murine p388 and B16 population doubling time by the acyclic monoterpene geraniol. Cancer Res 1991, 51, 37–42.
   PubMed Web of Science ®Google Scholar
• Del Toro-Arreola, S.; Flores-Torales, E.; Torres-Lozano, C.; Del Toro-Arreola, A.; Tostado-Pelayo, K.; Ramirez-Duenas, M.G.; Daneri-Navarro, A. Effect of D-limonene on immune response in BALB/c mice with lymphoma. Int Immunopharmacol 2005, 5, 829–838.
   PubMed Web of Science ®Google Scholar
• Zhang, Y.; Zhao, W.; Zhang, H.J.; Domann, F.E.; Oberley, L.W. Overexpression of copper zinc superoxide dismutase suppresses human glioma cell growth. Cancer Res 2002, 62, 1205–1212.
   PubMed Web of Science ®Google Scholar
• Pervin, S.; Singh, R.; Chaudhuri, G. Nitric oxide-induced cytostasis and cell cycle arrest of a human breast cancer cell line (MDA_MB-231): potential role of cyclin D1. Proc Natl Acad Sci USA 2001, 98, 3583–3588.
   PubMed Web of Science ®Google Scholar
• Crowell, P.L.; Chang, R.R.; Ren, Z.; Elson, C.E.; Gould, M.N. Selective inhibition of isoprenylation of 21–26 kDa proteins by anticarcinogen D-limonene and its metabolites. J Biol Chem 1991, 266, 17679–17685.
   PubMed Web of Science ®Google Scholar
• Gelb, M.H.; Tamanoi, F.; Yokoyama, K.; Ghomashchi, F.; Esson, K.; Gould, M.N. The inhibition of protein prenyltransferases by oxygenated metabolites of limonene and perillyl alcohol. Cancer Lett 1995, 91, 169–175.
   PubMed Web of Science ®Google Scholar
• Ruch, R.J.; Singler, K. Growth inhibition of rat liver epithelial tumor cells by monoterpenes does not involve Ras plasma membrane association. Carcinogenesis 1994, 15, 787–789.
   PubMed Web of Science ®Google Scholar
• Uedo, N.; Tatsuta, M.; Hiroyasu, L.; Miyako, B.; Noriko, S.; Hiroyuki, Y.; Toru, O. Inhibition by D-limonene of gastric carcinogenesis induced by N-methyl-N′-nitroso-N-nitrosoguanidine in Wistar rats. Cancer Lett 1999, 137, 131–136.
   PubMed Web of Science ®Google Scholar
• Wang Clay, C.C.; Yi-Ming, Chiang; Shu-Chiao, Sung.; Ya-Ling, Hsu.; Jiunn-Kae, Chang.; Po-Lin, Kuo Plumbagin induces cell cycle arrest and apoptosis through reactive oxygen species/c-Jun N-terminal kinase pathways in human melanoma A 375.S2 cells. Cancer Lett 2008, 259, 82–98.
   PubMed Web of Science ®Google Scholar
• Wang, W.; Macaulary, R. J. B. Apoptosis of medulloblastoma cells in vitro follows inhibition of farnesylation using manumycin A. Int J Cancer 1999, 82, 430–434.
   PubMed Web of Science ®Google Scholar
• Bolick, S. C. E.; Landowski, T.H.; Boulware, M.; Oshiro, M.; Ohkanda, J.; Hamilton, A.D.; Sebti, S.M.; Dalton, W.S. The farnesyl transferase inhibitor, FTI-277, inhibits growth and induces apoptosis in drug-resistant myeloma tumor cells. Leukemia 2003, 17, 451–457.
   PubMed Web of Science ®Google Scholar
• Lerner, E.C.; Zhang, T.T.; Knowles, D.B.; Qian, Y.; Hamilton, A.D.; Sebti, S.M. Inhibition of the prenylation of K-Ras but not H or N-Ras is highly resistant to CAAX peptidomimetics and requires both a farnesyl transferase and a geranyl transferase I inhibitor in human tumor cell lines. Oncogene 1997, 15, 1283–1288.
   PubMed Web of Science ®Google Scholar
• Williams, J.G.; Drugan, J.K.; Yi, G.S.; Clark, G.J.; Der, C.J.; Campbell, S.L. Elucidation of binding determinants and functional consequences of Ras/Raf-cysteine-rich domain interactions. J Biol Chem 2000, 275, 22172–22179. .
   PubMed Web of Science ®Google Scholar
• Laezza, C.; Fiorentino, L.; Pisanti, S.; Gazzero, P.; Caraglia, M.; Portella, G.; Vitale, M.; Bifulco, M. Lovastatin induces apoptosis of k-Ras-transformed thyroid cells via inhibition of Ras farnesylation and by modulating redox state. J Mol Med 2008, 86, 1341–1351.
   PubMed Web of Science ®Google Scholar
• Hortelano, S.; Alvarez, A.M.; Bosca, L. Nitric oxide induces tyrosine nitration and release of cytochrome c preceding an increase of mitochondrial transmembrane potential in macrophages. FASEB J 1999, 13, 2311–2317.
   PubMed Web of Science ®Google Scholar
• Peng, H.B.; Spiecker, M.; Liao, J.K. Inducible nitric oxide: an autoregulatory feedback inhibitor of vascular inflammation. J Immunol 1998, 161, 1970–1976.
   PubMed Web of Science ®Google Scholar
• Patel, R.P.; Moellering, D.; Murphy-Ullrich, J.; Jo, H.; Beckman, J.S. Cell signaling by reactive nitrogen and oxygen species in artherosclerosis. Free Radic Biol Med 2000, 28, 1780–1794.
   PubMed Web of Science ®Google Scholar
• Tripathi, P.; Tripathi, P.; Kashyap, L.; Singh, V. The role of nitric oxide in inflammatory reactions. FEMS Immunol Med Microbiol 2007, 51, 443–452.
   PubMed Web of Science ®Google Scholar
• Peng, H.B.; Libby, P.; Llao, J.K. Induction and stabilization of Ikappa B alpha by nitric oxide mediates inhibition of NF-Kappa B. J Biol Chem 1995, 270, 14214–14219.
   PubMed Web of Science ®Google Scholar
• Chen, F.; Kuhn, D.C.; Sun, S.C.; Gaydos, L.J.; Demers, L.M. Dependence and reversal of nitric oxide production on NF-Kappa B in silica and lipopolysaccharide-induced macrophages. Biochem Biophys Res Commun 1995, 214, 839–846.
   PubMed Web of Science ®Google Scholar
• Togashi, H.; Sasaki, M.; Frohman, E.; Taira, E.; Ratan, R.; Dawson, T.M.; Dawson, V.L. Neuronal (type I) nitric oxide synthase regulates nuclear factor Kappa B activity and immunologic (type II) nitric oxide synthase expression. Proc Natl Acad Sci USA 1997, 94, 2676–2680.
   PubMed Web of Science ®Google Scholar
• Mathews, J.R.; Bottong, C.H.; Panico, M.; Morris, H.R.; Hay, R.T. Inhibition of NF-Kappa B DNA binding by nitric oxide. Nucleic Acid Res 1996, 24, 2236–2242.
   PubMed Web of Science ®Google Scholar
• Wang, Z.; Brecher, P. Salicylate inhibition of extracellular signal-regulated kinases and inducible nitric oxide synthase. Hypertension 1999, 34, 1259–1264.
   PubMed Web of Science ®Google Scholar
• Riobó, N.A.; Melani, M.; Sanjuan, N.; Fiszman, M.L.; Gravielle, M.C.; Carreras, M.C.; Cadenas, E.; Poderoso, J.J. The modulation of mitochondrial nitric oxide synthase activity in rat brain development. J Biol Chem 2002, 277, 42447–42455.
   PubMed Web of Science ®Google Scholar
• Stalker, T.J.; Lefer, A.M.; Scalia, R. A new HMG-CoA reductase inhibitor, rosuvastatinh exerts anti-inflammatory effects on the microvascular endothelium: the role of mevalonic acid. Br J Pharmacol 2001, 133, 406–412.
   PubMed Web of Science ®Google Scholar
• Riganti, C.; Orecchia, S.; Pescarmona, G.; Betta, P.G.; Ghigo, D.; Bosia, A. Statins revert doxorubicin resistance via nitric oxide in malignant mesothelioma. Int J Cancer 2006, 119, 17–27.
   Google Scholar
• Jimenez, L.A.; Zanella, C.; Fung, H.; Janssen, Y.M.; Vacek, P.; Charland, C.; Goldberg, J.; Mossman, B.T. Role of extracellular signal-regulated protein kinases in apoptosis by asbestos and H2O2. Am J Physiol 1997, 273, 1029–1035.
   PubMed Web of Science ®Google Scholar
• Wenzel, U.; Nickel, A.; Kuntz, S.; Daniel, H. Ascorbic acid supresses drug-induced apoptosis in human colon cancer cells by scavenging mitochondrial superoxide anions. Carcinogenesis 2004, 25, 703–712.
   PubMed Web of Science ®Google Scholar
• Nomura, K.; Imai, H.; Koumura, T.; Arai, M.; Nakagawa, Y. Mitochondrial phospholipid hydroperoxide glutathione peroxidase suppresses apoptosis mediated by a mitochondrial death pathway. J Biol Chem 1999, 274, 29294–29302.
   PubMed Web of Science ®Google Scholar
• Takahashi, A.; Masuda, A.; Sun, M.; Centonze, V.E.; Herman, B. Oxidative stress-induced apoptosis is associated with alterations in mitochondrial caspase activity and Bcl-2-dependent alterations in mitochondrial pH (pHm). Brain Res Bull 2004, 62, 497–504.
   PubMed Web of Science ®Google Scholar