Omega-3 polyunsaturated fatty acids of fish and their role in cancerous cell lines: A review of in-vitro studies

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Abstract

Fish are a major dietary source of n-3 and n-6 polyunsaturated fatty acids (PUFAs) in humans since the human body lacks the necessary enzymes required to synthesize them. Diets rich in fish oil containing n-3 fatty acids have been shown to lower the incidence rates of cancer. They have also been shown to have cytotoxic or anti-proliferative effects on a variety of human cancer cell lines, and they are known to nurture overall human health without any observable side effects. The present review focused on in-vitro research findings regarding the apoptotic and anti-proliferative role of n-3 fatty acids FAs that highlight the important mechanisms and pathways of their action in inhibiting the progression of cancer. A survey of the literature indicated the paucity of information on the use of n-3 FAs in combination with other anticancer substances. Therefore, further research needs to be undertaken on the use of n-3 FAs in combination with other anticancer phytochemicals and drugs, the use of antibodies as specific carriers of n-3 FAs, and different increasing ratios of n-3/n-6 FAs that not only control the side effects of chemotherapy but also enhance its efficacy and selectivity. These FAs might also prove to be a pioneer therapy against cancer.

Ahamad M.S., Siddiqui S., Jafri A., Ahmad S., Afzal M., Arshad M. 2014 - Induction of apoptosis and antiproliferative activity of naringenin in human epidermoid carcinoma cell through ROS generation and cell cycle arrest - PlOS One 9(10): e110003.

Almatsier S. 2003 - Basic Principles of Nutrition - Gramedia Pustaka Utama (in Indonesian).

Arita K., Kobuchi H., Utsumi T., Takehara Y., Akiyama J., Horton A.A., Utsumi K. 2001 - Mechanism of apoptosis in HL-60 cells induced by n-3 and n-6 polyunsaturated fatty acids - Biochem. Pharmacol. 62: 821-828.

Arterburn L.M., Hall E.B., Oken H. 2006 - Distribution, interconversion, and dose response of n-3 fatty acids in humans - Am. J. Clin. Nutr. 83: 1467S-1476S.

Baracos V.E., Mazurak V.C., Ma D.W.L.2004 - n-3 Polyunsaturated fatty acids throughout the cancer trajectory: influence on disease incidence, progression, response to therapy and cancer-associated cachexia - Nutr. Res. Rev. 17: 177-192.

Barascu A., Besson P., Le Floch O., Bougnoux P., Jourdan M.L. 2006 - CDK1-cyclin B1 mediates the inhibition of proliferation induced by omega-3 fatty acids in MDA-MB-231 breast cancer cells - Int. J. Biochem. Cell Biol. 38: 196-208.

Bishop-Bailey D., Calatayud S., Warner T.D., Hla T., Mitchell J.A. 2002 - Prostaglandins and the regulation of tumor growth - J. Environ. Pathol. Toxicol. Oncol. 21: 93-101.

Brett M.T., Müller-Navarra D.C. 1997 - The role of highly unsaturated fatty acids in aquatic foodweb processes - Freshw. Biol. 38: 483-499.

Brown M.D., Hart C.A., Gazi E., Bagley S., Clarke N.W. 2006 - Promotion of prostatic metastatic migration towards human bone marrow stoma by Omega 6 and its inhibition by Omega 3 PUFAs - Brit. J. Cancer 94: 842-853.

Calviello G., Resci F., Serini S., Piccioni E., Toesca A., Boninsegna A., Monego G., Ranelletti F.O., Palozza P. 2007 - Docosahexaenoic acid induces proteasome-dependent degradation of beta-catenin, down-regulation of survivin and apoptosis in human colorectal cancer cells not expressing COX-2 - Carcinogenesis 28: 1202-1209.

Canepa E.T., Scassa M.E., Ceruti J.M., Marazita M.C., Carcagno A.L., Sirkin P.F., Ogara M.F. 2007 - INK4 proteins, a family of mammalian CDK inhibitors with novel biological functions - IUBMB Life 59: 419-426.

Cantrill R.C., Ells G.W., De Marco A.C., Horrobin D.F. 1997 - Mechanism of the selective cytotoxic actions of certain essential fatty acids - In: Eicosanoids and Other Bioactive Lipids in Cancer, Inflammation, and Radiation Injury 2. Part A (Eds) K.V. Honn, S. Nigam, L.J. Marnett, Springer Science+Businnes Media: 539-544.

Çelik M., Diler A., Küçükgülmez A. 2005 - A comparison of the proximate compositions and fatty acid profiles of zander (Sander lucioperca) from two different regions and climatic conditions - Food Chem. 92: 637-641.

Cengiz E.I., Ünlü E., Baçhan M. 2010 - Fatty acid composition of total lipids in muscle tissues of nine freshwater fish from the River Tigris (Turkey) - Turk. J. Biol. 34: 433-438.

Chapkin R.S., Hong M.Y., Fan Y.Y., Davidson L.A., Sanders L.M., Henderson C.E., Barhoumi R., Burghardt R.C., Turner N.D., Lupton J.R. 2002 - Dietary n-3 PUFA alter colonocyte mitochondrial membrane composition and function - Lipids 37: 193-199.

Chapkin R.S., Mc Murray D.N., Lupton J.R. 2007 - Colon cancer, fatty acids and anti-inflammatory compounds - Curr. Opin. Gastroenterol. 23: 48-54.

Chapkin R.S., Seo J., Mc Murray, Lupton J.R. 2008 - Mechanisms by which docosahexaenoic acid and related fatty acids reduce colon cancer risk and inflammatory disorders of the intestine - Chem. Phys. Lipids 153: 14-23.

Chen Z.Y., Istfan N.W. 2000 - Docosahexaenoic acid is a potent inducer of apoptosis in HT-29 colon cancer cells - Prostaglandins Leukot. Essent. Fatty Acids 63: 301-308.

Cheokin R.S., Jiang Y.H., Davidson L., A., Lupton J.R. 1997 - Modulation of intra cellular second messengers by dietary fat during colonic tumour development - Adv. Exp. Med. Biol. 422: 85-96.

Chi T.Y., Chen G.G., Lai P.B. 2004 - Eicosapentaenoic acid induces Fas-mediated apoptosis through a p53-dependent pathway in hepatoma cells - Cancer J.10: 190-200.

Chiu L.C., Wan J.M. 1999 - Induction of apoptosis in HL-60 cells by eicosapentaenoic acid (EPA) is associated with downregulation of bcl-2 expression - Cancer Lett. 145: 17-27.

Collett E.D., Davidson L.A., Fan Y.Y., Lupton J.R., Chapkin R.S. 2001 - n-6 and n-3 polyunsaturated fatty acids differentially modulate oncogenic Ras activation in colonocytes - Am. J. Physiol. Cell Physiol. 280: C1066-C1075.

Collins K., Jacks T., Pavletich N.P. 1997 - The cell cycle and cancer - Proc. Natl. Acad. Sci. USA 94: 2776-2778.

Colomer R., Moreno-Nogueira J.M., Garcia-Luna P.P., García-Peris P., García-de-Lorenzo A., Zarazaga A., Quecedo L., del Llano J., Usán L., Casimiro C. 2007 - n-3 fatty acids, cancer and cachexia: a systematic review of the literature - Brit. J. Nutr. 97: 823-831.

Corsetto P.A., Montorfano G.M., Zava S., Jovenitti I.E., Cremona A., Berra B., Rizzo A.M. 2011 - Effects of n-3 PUFAs on Breast Cancer Cells through their Incorporation in Plasma Membrane - Lipids Health Dis. 10: 73.

Crawford M., Galli C., Visioli F., Renaud S., Simopoulos A.P., Spector A.A. 2000 - Role of plant-derived omega-3 fatty acids in human nutrition - Ann. Nutr. Metab. 44: 263-265.

Crawford M.A. 1993 - The role of essential fatty acids in neural development: implications for perinatal nutrition - Am. J. Clin. Nutr. 57: 703S-710S.

Dai J., Shen J., Pan W., Shen S., Das U.N. 2013 - Effects of Polyunsaturated Fatty Acids on the Growth of Gastric Cancer Cells in-vitro - Lipids Health Dis. 12: 71.

Damtew B., Spagnuolo P.J. 1997 - Tumor cell-endothelial cell interactions: evidence for roles for lipoxygenase products of arachidonic acid in metastasis - Prostaglandins Leukot. Essent. Fatty Acids 56: 295-300.

Danbara N., Yuri T., Tsujita-Kyutoku M., Sato M., Senzaki H., Takada H., Hada T., Miyazawa T., Okazaki K., Tsubura A. 2004 - Conjugated docosahexaenoic acid is a potent inducer of cell cycle arrest and apoptosis and inhibits growth of colo 201 human colon cancer cells - Nutr. Cancer 50: 71-79.

Dannenberg A.J., Altorki N.K., Boyle J.O., Dang C., Howe L.R., Weksler B.B., Subbaramaiah K. 2001 - Cyclooxygenase-2: a pharmacological target for the prevention of cancer - Lancet. Oncol. 2: 544-551.

Das U.N. 1991 - Tumoricidal action of cis-unsaturated fatty acids and its relationship to free radicals and lipid peroxidation - Cancer Lett. 50: 235-243.

Das U.N. 1999 - Essential fatty acids, lipid peroxidation and apoptosis - Prostaglandins Leukot. Essent. Fatty Acids 61: 157-163.

Das U.N., Swamy S.M.K., Tan B.K.H. 2002 - Mechanisms by which docosahexaenoic acid and related fatty acids reduce colon cancer risk and inflammatory disorders of the intestine - Nutrition 18: 348-350.

Delston R.B., Harbour J.W. 2006 - Rb at the interface between cell cycle andapoptotic decisions - Curr. Mol. Med. 6: 713-718.

Denkins Y., Kempf D., Ferniz M., Nileshwar S., Marchetti D. 2005 - Role of omega-3 polyunsaturated fatty acids on cyclooxygenase-2 metabolism in brain-metastatic melanoma - J. Lipid Res. 46: 1278-1284.

Dhaneesh K.V., Noushad K.M., Ajith T.T. 2012 - Nutritional evaluation of commercially important fish species of Lakshadweep Archipelago, India - PLOS One 7: e45439.

Domingo J.L. 2007 - Omega-3 Fatty Acids and the Benefits of Fish Consumption: Is all that Glitters Gold? - Environ. Int. 33: 993-998.

Edwards I.J., Sun H., Hu Y., Berquin I.M., O’Flaherty J.T., Cline J.M., Rudel L.L., Chen Y.Q. 2008 - In vivo and in vitro regulation of syndecan-1 in prostate cells by n-3 polyunsaturated fatty acids - J. Biol. Chem. 283: 18441-18449.

Ehringer W., Belcher D., Wassall S.R., Stillwell W. 1990 - A comparison of the effects of linolenic (18:3Ù3) and docosahexaenoic (22:6Ù3) acids on phospholipid bilayers - Chem. Phys. Lipids 54: 79-88.

Ermert L., Dierkes C., Ermert M. 2003 - Immunohistochemical expression of cyclooxygenase isoenzymes and downstream enzymes in human lung tumors - Clin. Cancer Res. 91: 1604-1610.

Fan Y.Y., Spencer T.E., Wang N., Moyer M.P., Chapkin R.S. 2003 - Chemopreventive n-3 fatty acids activate RXR-alpha in colonocytes - Carcinogenesis 24: 1541-1548.

Field C.J., Schley P.D. 2004 - Evidence for potential mechanisms for the effect of conjugated linoleic acid on tumor metabolism and immune function: lessons from n-3 fatty acids - Am. J. Clin. Nutr.79: 1190-1198.

Foijer F., Riele H.T. 2006 - Check, double check: the G2 barrier to cancer - Cell Cycle 5: 831-836.

Fuchs S.Y., Ougolkov A.V., Spiegelman V.S., Minamoto T. 2005 - Oncogenic beta-catenin signalling networks in colorectal cancer - Cell Cycle 4: 1522-1539.

Fukui M., Kang K.S., Okada K., Zhu B.T. 2013 - EPA, an Omega-3 Fatty Acid, Induces Apoptosis in Human Pancreatic Cancer Cells: Role of ROS Accumulation, Caspase-8 Activation and Autophagy Induction - J. Cell. Biochem. 114: 192-203.

Fulda S. 2009 - Tumor resistance to apoptosis - Int. J. Cancer 124: 511-515.

Funahashi H., Satake M., Hasan S., Sawai H., Newman R.A., Reber H.A., Hines O.J., Eibl G. 2008 - Opposing effects of n-6 and n-3 polyunsaturated fatty acids on pancreatic cancer growth - Pancreas 36: 353-362.

Gerber M. 2012 - Omega-3 fatty acids and cancers: a systematic update review of epidemiological studies - Brit. J. Nutr. 107: S228-S239.

German E., Chajcs V., Cognault S., Lhuillery C., Bougnoux P. 1998 - Enhancement of doxorubicin cytotoxicity by polyunsaturated fatty acids in the human breast tumor cell line MDA-MB-231: relationship to lipid peroxidation - Int. J. Cancer 75: 578-583

Griffiths G., Jones H.E., Eaton C.L., Stobart A.K. 1997 - Effect of n-6 polyunsaturated fatty acids on growth and lipid composition of neoplastic and non-neoplastic canine prostate epithelial cell cultures - The Prostate 31: 29-36.

Grivennikov S.I., Greten F.R., Karin M. 2010 - Immunity, inflammation and cancer - Cell 140: 883-899.

Guffy M.M., North J.A., Burns C.P. 1984 - Effect of cellular fatty acid alteration on adriamycin sensitivity in cultured L1210 murine leukemia cells - Cancer Res. 44: 1863-1866

Guil-Guerrero J.L., Lopez-Martinez J.C., Rincon-Cervera M.A.. Campra-Madrid P. 2007 - One step extraction and concentration of polyunsaturated fatty acids from fish liver - J. Am. Oil Chem. Soc. 84: 357-361.

Halder S., Jena N., Croce C.M. 1995 - Inactivation of BCL-2 by phosphorylation - Proc. Natl. Acad. Sci. USA 92: 4507-4511.

Haliloglu H.Í., Bayir A., Sirkecioglu A.N., Aras N.M. Atamanalp M. 2004 - Comparison of fatty acid composition in some tissues of rainbow trout (Oncorhynchus mykiss) living in seawater and freshwater - Food Chem. 86: 55-59.

Hanahan D., Weinberg R.A. 2000 - The Hallmarks of cancer Review - 100: 57-70.

Hawcroft G., Loadman P.M., Belluzzi A., Hull M.A. 2010 - Effect of eicosapentaenoic acid on E-type prostaglandin synthesis and EP4 receptor signalling in human colorectal cancer cells - Neoplasia 12: 618-627.

Heimli H., Giske C., Naderi S., Drevon C.A., Hollung K. 2002 - Eicosapentaenoic acid promotes apoptosis in Ramos cells via activation of caspase-3 and -9 - Lipids 37: 797-802.

Hershman D.L., Weimer L.H., Wang A., Kranwinkel G., Brafman L., Fuentes D., Awad D., Crew K.D. 2011 - Association between patient reported outcomes and quantitative sensory tests for measuring long-term neurotoxicity in breast cancer survivors treated with adjuvant paclitaxel chemotherapy - Breast Cancer Res. Treat. 125: 767-774.

Higashi S., Murata N. 1993 - An in-vivo Study of Substrate Specificities of Acyl-Lipid Desaturases and Acyl Transferases in Lipid Synthesis in Synechocystis PCC6803- Plant Phyiol. 102: 1275-1278.

Hinz B., Brune K. 2002 - Cyclooxygenase: 2-10 years later - J. Pharmacol. Exp. Ther. 300: 367-375.

Homayooni B., Sahari M.A., Barzegar M. 2014 - Concentrations of omega-3 fatty acids from rainbow sardine fish oil by various methods - Int. Food Res. J. 21: 743-748.

Honn K.V., Cicone B., Skoff A. 1981 - Prostacyclin: a potent anti-metastatic agent -Science 212: 1270-1272.

Hostetler H.A., Petrescu A.D., Kier A.B., Schroeder F. 2005 - Peroxisome proliferator-activated receptor alpha interacts with high affinity and is conformationally responsive to endogenous ligands - J. Biol. Chem. 280: 18667-18682.

Huynh M.D., Kitts D.D., Hu C., Trites A.W. 2007 - Comparison of fatty acid profiles of spawning and non-spawning Pacific herring, Clupea harenguspallasi - Comp. Biochem. Physiol. B Biochem. Mol. Biol. 146: 504-511.

Iqbal B., Ghildiyal A., Sahabjada S.S., Arshad M., Mahdi A.A., Tiwari S. 2016 - Antiproliferative and apoptotic effect of curcumin and TRAIL (TNF related apoptosis inducing ligand) in chronic myeloid leukaemic cells - J. Clin. Diagn. Res. 10(4): XC01-XC05.

Jabeen F., Chaudhry A.S. 2011 - Chemical compositions and fatty acid profiles of three freshwater fish species - Food Chem. 125: 991-996.

Jakhar J.K., Pal A.K., Reddy A.D., Sahu N.P., Venkateshwarlu G., Vardia H.K. 2012 - Fatty Acids Composition of Some selected Indian Fishes - Afr. J. Basic Appl. Sci. 4: 155-160.

Jakobsen C.H, Storvold G.L, Bremseth H., Follestad T., Sand K., Mack M., Olsen K.S., Lundemo A.G., Iversen J.G., Krokan H.E,. Schonberg S.A. 2008 - DHA induces ER stress and growth arrest in human colon cancer cells: associations with cholesterol and calcium homeostasis - J. Lipid Res. 49: 2089-2100.

James M.J., Cleland L.G. 1997 - Dietary n-3 fatty acids and therapy for rheumatoid arthritis - Semin. Arthritis Rheum. 27: 85-97.

Janakiram N.B., Mohammed A., Rao C.V. 2011 - Role of lipoxins, resolvins and other bioactive lipids in colon and pancreatic cancer- Cancer Metastasis Rev. 30: 507-523.

Johnson S., Saikia N., Mathur H.B., Agarwal H.C. 2009 - Fatty acid profile of edible oils and fats in India - Centre for Science and Environment, New Delhi: 3-31.

Jump D.B. 2002 - The biochemistry of n-3 polyunsaturated fatty acids - J. Biol. Chem. 277: 8755-8758.

Kato J., Matsushime H., Hiebert S.W., Ewen M.E., Sherr C.J. 1993 - Direct binding of cyclin D to the retinoblastoma gene product (pRb) and pRb phosphorylation by the cyclin D-dependent kinase CDK4 - Genes Dev. 7: 331-342.

Kinsella J.E. 1988 - Fish and sea foods: nutritional implication and quality issues - Food Technol. 51: 46-50.

Kumar S.G., Das U.N. 1995 - Free radical dependent suppression of growth of mouse myelomia cells by alpha-linolenic and eicosapentaenoic acid in vitro - Cancer Lett. 92: 27-38.

Larsson S.C., Kumlin M., Ingelman-Sundberg M., Wolk A. 2004 - Dietary long-chain n-3 fatty acids for the prevention of cancer: a review of potential mechanisms - Am. J. Clin. Nutr. 79: 935-945.

Latham P., Lund E.K., Brown J.C., Johnson I.T. 2001 - Effects of cellular redox balance on induction of apoptosis by eicosapentaenoic acid in HT29 colorectal adenocarcinoma cells and rat colon in vivo - Gut. 49: 97-105.

Liu X.H., Kirschenbaum A., Yao S., Lee R., Holland J.F., Levine A.C. 2000 - Inhibition of cyclooxygenase-2 suppresses angiogenesis and the growth of prostate cancer in vivo - J. Urol. 164: 820-825.

Ljubojevic D., Trbovic D., Lujic J., Bjelic-Cabrilo O., Kostic D., Novakov N., Cirkovic M. 2013 - Fatty acid composition of fishes from inland waters - Bulg. J. Agric. Sci. 19: 62-71.

Lu I.F., Hasio A.C., Hu M.C., Yang F.M., Su H.M. 2010 - Docosahexaenoic acid induces proteasome-dependent degradation of estrogen receptor alpha and inhibits the downstream signalling target in MCF-7 breast cancer cells - J. Nutr. Biochem. 21: 512-517.

Lu. Y., Nie. D., Witt W.T., Chen Q., Shen M., Xie H., Lai L., Dai Y., Zhang J. 2008 - Expression of the fat-1 gene diminishes prostate cancer growth in-vivo through enhancing apoptosis and inhibiting GSK-3 beta phosphorylation - Mol. Cancer Ther. 7: 3203-3211.

Łuczyńska J., Borejszo Z., Łuczyński M.J. 2008 - The composition of fatty acids in muscles of six freshwater fish species from the Mazurian Great Lakes (Northeastern Poland) - Arch. Pol. Fish. 16: 167-178.

Ma D.W., Seo J., Switzer K.C., Fan Y.Y., McMurray D.N., Lupton J.R., Chapkin R.S. 2004 - n-3 PUFA and membrane microdomains: a new frontier in bioactive lipid research - J. Nutr. Biochem.15: 700-706.

Madhavi N., Das U.N. 1994 - Effect of n-6 and n-3 fatty acids on the survival of Vincristine sensitive and resistant human cervical carcinoma cells in vitro - Cancer Lett. 84: 31-41.

Mahmoud B.S., Kawai Y., Yamazaki K., Miyashita K., Suzuki T. 2007 - Effect of treatment with electrolysed NaCl solutions and essential oil compounds on the proximate composition, amino acid and fatty acid composition of carp fillets - Food Chem. 101: 1492-1498.

Mansara P.P., Deshpande R.A., Vaidya M.M., Kaul-Ghanekar R. 2015 - Differential Ratios of Omega Fatty Acids (AA/EPA+DHA) Modulate Growth, Lipid Peroxidation and Expression of Tumor Regulatory MARBPs in Breast Cancer Cell Lines MCF7 and MDA-MB-231 - PLOS One 10: e0136542.

Morgan D.O. 1995 - Principles of CDK regulation - Nature 374: 134.

Napier J.A. 2002 - Plumbing the depths of PUFA biosynthesis: a novel polyketide synthase-like pathway from marine organisms - Trends Plant Sci. 7: 51-54.

Narayanan B.A., Narayanan N.K., Desai D., Pittman B., Reddy B. S. 2004 - Effects of a combination of docosahexaenoic acid and 1,4-phenylene bis(methylene) selenocyanate on cyclooxygenase 2, inducible nitric oxide synthase and beta-catenin pathways in colon cancer cells - Carcinogenesis 25: 2443-2449.

Narayanan B.A., Narayanan N.K., Reddy B.S. 2001 - Docosahexaenoic acid regulated genes and transcription factors inducing apoptosis in human colon cancer cells - Int. J. Oncol. 19: 1255-1262.

Ng Y., Barhoumi R.,Tjalkens R.B., Fan Y.Y., Kolar S., Wang N., Lupton J.R., Chapkin R.S. 2005 - The role of docosahexaenoic acid in mediating mitochondrial membrane lipid oxidation and apoptosis in colonocytes - Carcinogenesis 26: 1914-1921.

Nobili S., Lippi D., Witort E., Donnini M., Bausi L., Mini E., Capaccioli S. 2009 - Natural compounds for cancer treatment and prevention - Pharmacol. Res. 59: 365-378.

Norris P.C., Dennis E.A. 2012. - Omega-3 fatty acids cause dramatic changes in TLR4 and purinergic eicosanoid signalling - Proc. Natl. Acad. Sci. USA 109: 8517-8522.

Notarnicola M., Messa M., Refolo M.G., Tunio V., Miccolis A., Caruso M.G. 2011 - Polyunsaturated Fatty Acids Reduce Fatty Acid Synthase and Hydroxy-Methyl-Glutaryl CoA-Reductase Gene Expression and Promote Apoptosis in HepG2 Cell Line - Lipids Health Dis. 10: 10.

Okada H., Mak T.W. 2004 - Pathways of apoptotic and non-apoptotic death in tumour cells - Nat. Rev. Cancer 4: 592-603.

Omar M.N., Ahlam N.S., Yusoff M., Zainuddin N.A., Yunus K. 2010 - ю-Fatty acids from Malaysian giant snakehead (Channamicropeltes) fish oil - Orient J. Chem. 26: 01-04.

Osman F., Jaswir I., Khaza’ai H., Hashim R. 2007 - Fatty acid profiles of fin fish in Langwani Island Malaysia - J. Oleo Sci. 56: 107-113.

Osman H., Suriah A.R., Law E.C. 2001 - Fatty acid composition and cholesterol content of selected marine fish in Malaysian waters - Food Chem. 73: 55-60.

Padma M., Das U.N. 1986 - Effect of cis unsaturated fatty acids on cellular antioxidant stress in macrophage tumour (AK-5) cells in vitro - Cancer Lett. 109: 63-75.

Pegram M.D., Konecny G.E., O’Callaghan C., Beryt M., Pietras R., Slamon D.J. 2004 - Rational combinations of trastuzumab with chemotherapeutic drugs used in the treatment of breast cancer - J. Natl. Cancer Inst. 96: 739-749.

Pogash T.J., El-Bayoumy K., Amin S., Gowda K., de Cicco R.L.,Barton M., Su Y., Russo I.H., Himmelberger J.A., Slifker M., Manni A. 2014 - Oxidized Derivative of Docosahexaenoic Acid Preferentially Inhibit Cell Proliferation in Triple Negative Over Luminal Breast Cancer Cells - In Vitro Cell. Dev. Biol.-Anim. 51: 121-127.

Rahimabadi E.Z., Mirdar J., Elahi M.Y., Arshadi M.R. 2009 - The lipid quality assessment of Shizothoraxzarudnyi and Schizocyprisaltidorsalis by fatty acid analysis - Pak. J. Biol. Sci. 12: 1090-1093.

Rahman S.A., Huah T.S., Nassan O., Daud N.M. 1995- Fatty acid composition of some Malaysian freshwater fish - Food Chem. 54: 45-49.

Ramesh G., Das U.N. 1998 - Effect of cis-unsaturated fatty acids on Meth-A ascetic tumour cells in vitro and in vivo - Cancer Lett. 123: 207-214.

Ramesh G., Das U.N., Koratkar R., Padma M., Sagar P.S. 1992 - Effect of essential fatty acids on tumor cells - Nutrition 8: 343-347.

Ratkowsky D.A., Olley J., Jayasinghe J.A.G., Wijesundara R.C. 1996 - A consistent correlation between monounsaturated and n-3 polyunsaturated fatty acids in fresh of fish caught at different latitudes - ASEAN Food J. 11: 43-47.

Roynette C.E., Calder P., Dupertuis Y.M., Pichard C. 2004 - n-3 polyunsaturated fatty acids and colon cancer prevention - Clin. Nutr. 23: 139-151.

Sahena F., Zaidul I.S.M., Jinap S., Saari N., Jahurul H.A., Abbas K.A., Norulaini N.A. 2009 - PUFAs in Fish: Extraction, Fractionation, Importance in Health - Compr. Rev. Food Sci. Food Saf. 8: 59-74.

Saito H., Yamashiro R., Alasalvar C., Konno T. 1999 - Influence of diet on fatty acids of three subtropical fish, subfamily Caesioninae (Caesiodia gramma and C. tile) and family Siganidae (Siganus canaliculatus) - Lipid 34: 1073-1081.

Sangeetha P., Das U.N. 1992 - Cytotoxic action of cis-unsaturated fatty acids on human cervical carcinoma (HeLa) cells: relationship to free radicals and lipid peroxidation and its modulation by calmodulin antagonists - Cancer Lett. 63: 189-198.

Schley P.D., Jijon H.B., Robinson L.E., Field C.J. 2005 - Mechanisms of omega-3 fatty acid-induced growth inhibition in MDA-MB-231 human breast cancer cells - Breast Cancer Res. Treat. 92: 187-195.

Schmitz G., Ecker J. 2008 - The opposing effects of n-3 and n-6 fatty acids -Prog. Lipid Res. 47: 147-155.

Serini S., Trombino S., Oliva F., Piccioni E., Monego G., Resci F., Boninsegna A., Picci N., Ranelletti F.O., Calviello G. 2008 - Docosahexaenoic acid induces apoptosis in lung cancer cells by increasing MKP-1 and down-regulating p-ERK1/2 and p-p38 expression - Apoptosis 13: 1172-1183.

Shaikh S.R., Dumaual A.C., Jenski LJ., Stillwell W. 2001 - Lipid phase separation in phospholipid bilayers and monolayers modeling the plasma membrane - Biochem. Biophys. Acta-Biomembr. 1512: 317-328.

Sharma P., Kumer V., Sinha A.K., Ranjan J., Kithsiri H.M.P., Venkateshwarlu G. 2010 - Comparative fatty acid profiles of wild and farmed tropical freshwater fish rohu (Labeo rohita) - Fish Physiol. Biochem. 36: 411-417.

Sherr C.J., Roberts J.M. 1999 - CDK inhibitors: positive and negative regulators of G1-phase progression - Genes Dev. 13: 1501-1512.

Siddiqui R.A., Harvey K.A., Xu Z., Bammerlin E.M., Walker C., Altenburg J.D. 2011 - Docosahexaenoic acid: a natural powerful adjuvant that improves efficacy for anticancer treatment with no adverse effects - Biofactors 37: 399-412.

Siddiqui R.A., Jenski L.J., Harvey K.A., Wiesehan J.D., Stillwell W., Zaloga G.P. 2003 - Cell-cycle arrest in Jurkat leukaemic cells: a possible role for docosahexaenoic acid - Biochem. J. 371: 621-629.

Siddiqui S., Ahamad M.S., Jafri A., Afzal M., Arshad M. 2017 - Piperine triggers apoptosis of human oral squamous carcinoma through cell cycle arrest and mitochondrial oxidative stress - Nutr. Cancer 69: 791-799.

Simopoulos A.P. 2002 - Omega-3 fatty acids in inflammation and autoimmune diseases - J. Am. Coll. Nutr. 21: 495-505.

Simopoulos A.P. 2002 - The importance of the ratio of omega-6/omega-3 essential fatty acids - Biomed. Pharmacother. 56: 365-379.

Smith W., Murphy R. 2002 - The eicosanoids: cyclooxygenase, lipoxygenase and epoxygenase pathways - In: Biochemistry of Lipids, Lipoproteins and Membranes (Eds) D.E. Vance, J.E. Vance, Elsevier, Amsterdam: 341-372.

Solomon L.Z., Jennings A.M., Sharpe P., Cooper A.J., Birch B.R. 1998 - Intravesical chemotherapy with gamma linolenic acid becomes a realistic prospect in serum-free applications: In vitro cytotoxicity and systemic absorption studies - J. Urol. 160: 2280-2283.

Song K.S., Jing K., Kim J.S., Yun E.J., Shin S., Seo K.S., Park J.H., Heo J.Y., Kang J.X., Suh K.S., Wu T. 2011 - Omega-3- polyunsaturated fatty acids suppress pancreatic cancer cell growth in vitro and in vivo via downregulation of Wnt/Beta-catenin signalling - Pancreatology 11: 574-584.

Stancheva M., Merdzhanova A., Dobreva D.A., Makedonski L. 2014 - Common carp (Cyprinus caprio) and European catfish (Silurus glanis) from the Danube River as sources of fat-soluble vitamins and fatty acids - Czech J. Food Sci. 32: 16-24.

Stillwell W., Jenski L.J., Crump F.T., Ehringer W. 1997 - Effect of docosahexaenoic acid on mouse mitochondrial membrane properties - Lipids 32: 497-506.

Sushchik N.N., Gladyshev M.I., Kalachova G.S. 2007 - Seasonal dynamic of fatty acid content of a common food fish from the Yenisei river, Siberian grayling, Thymallus arcticus - Food Chem. 104: 1353-1358.

Suzuki H., Tamura M., Wada S., Crawford M.A. 1995 - Comparison of docosahexaenoic acid with eicosapentaenoic acid on the lowering effect of endogenous plasma cholesterol in adult mice - Fish. Sci. 61: 525-526.

Szatrowski T.P., Nathan C.F. 1991 - Production of large amounts of hydrogen peroxide by human tumor cells - Cancer Res. 51: 794-798.

Tocher D. 2003 - Metabolism and functions of lipid and fatty acid in Teleost fish - Rev. Fish. Sci. 11: 107-184.

Toit-Kohndu J.L., Louw L., Engelbrecht A.M. 2009 - Docosahexaenoic Acid Induces Apoptosis in Colorectal Carcinoma Cells by Modulating the PI3 Kinase and p38 MAPK Pathways - J. Nutr. Biochem. 20: 106-14.

Trombetta A., Maggiora M., Martinasso G., Cotogni P., Canuto R.A., Muzio G. 2007 - Arachidonic and docosahexaenoic acids reduce the growth of A549 human lung-tumor cells increasing lipid peroxidation and PPARs - Chem. Biol. Interact. 165: 239-250.

Tsujita-Kyutoku M., Yuri T., Danbara N., Senzaki H., Kiyozuka Y., Uehara N., Takada H., Hada T., Miyazawa T., Ogawa Y., Tsubura A. 2004 - Conjugated docosahexaenoic acid suppresses KPL-1 human breast cancer cell growth in vitro and in vivo: potential mechanisms of action - Breast Cancer Res. 6: R291-R299.

Ugoala C., Ndukwe G.I., Audu T.O. 2009 - Fatty acids composition and nutritional quality of some freshwater fishes - Nature Proceedings, Doi:10.1038/npre.32391.1.

Vaughan V.C., Hassing M.R., Lewandowski P.A. 2013 - Marine polyunsaturated fatty acids and cancer therapy - Brit. J. Cancer. 108: 486-92.

Wang D., Lippard S.J. 2005 - Cellular processing of platinum anticancer drugs - Nat. Rev. Drug Discov. 4: 307.

Warner T.D., Mitchell J.A. 2004 - Cyclooxygenases: new forms, new inhibitors, and lessons from the clinic - FASEB J. 18: 790-804.

Yang T., Fang S., Zhang H.X., Xu L.X., Zhang Z.Q., Yuan K.T., Xue C.L., Yu H.L., Zhang S., Li Y.F., Shi H.P. 2013 - n-3 PUFAs have antiproliferative and apoptotic effects on human colorectal cancer stem-like cells in vitro - J. Nutr. Biochem. 24: 744-753.

Zajdel A., Wilczok A., Chodurek E., Gruchlik A., Dzieroewicz Z. 2013 - Polyunsaturated Fatty Acids Inhibit Melanoma Cell Growth In Vitro - Acta Pol. Pharm. 70: 365-369.

Zijlstra J.G., deVries E.G.E., Muskriet F.A.J., Martini I.A., Timmer-Bosscha H., Mulder N.H. 1987 - Influence of docosahexaenoic acid in vitro on intracellular adriamycin concentration in lymphocytes and human adriamycin-sensitive and resistant small-cell lung cancer cell lines, and on cytotoxicity in the tumor cell lines - Int. J. Cancer 90: 850-856.

Fisheries & Aquatic Life

The Journal of Stanislaw Sakowicz Inland Fisheries Institute

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CiteScore 2017: 0.53

SCImago Journal Rank (SJR) 2017: 0.204
Source Normalized Impact per Paper (SNIP) 2017: 0.493

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