Docosahexaenoic Acid Incorporation Is Not Affected by Doxorubicin Chemotherapy in either Whole Cell or Lipid Raft Phospholipids of Breast Cancer Cells in vitro and Tumor Phospholipids in vivo.
Analytical Techniques
Cancer
Docosahexaenoic acid
Fatty acid analysis
Nutrition
Phospholipid analysis
Physiology
Specific lipids
n-3 Fatty acids
Journal
Lipids
ISSN: 1558-9307
Titre abrégé: Lipids
Pays: United States
ID NLM: 0060450
Informations de publication
Date de publication:
09 2020
09 2020
Historique:
received:
13
04
2020
revised:
04
05
2020
accepted:
06
05
2020
pubmed:
27
6
2020
medline:
3
8
2021
entrez:
27
6
2020
Statut:
ppublish
Résumé
To better understand how docosahexaenoic acid (DHA) improves the effects of doxorubicin (DOX), we examined DHA ± DOX on changes in whole cell and lipid raft phospholipids (PL) of MDA-MB-231 and MCF-7 breast cancer cells. We sought to confirm whether the relative changes in PL DHA content of MDA-MB-231 cells could be extended to PL from MDA-MB-231 tumors grown in mice fed a DHA supplemented diet ±DOX. Treatment with DHA did not change PL composition yet DOX increased the proportion of phosphatidylserine in MCF-7 cell lipid rafts by two-fold (p < 0.001). Regardless of DOX, the relative percent incorporation of DHA was higher in MDA-MB-231 cells compared to MCF-7 cells in phosphatidylserine, phosphatidylethanolamine, and phosphatidylcholine (whole cell and lipid rafts); and higher in phosphatidylethanolamine vs. phosphatidylcholine (4.4-fold in MCF-7 and 6-fold in MDA-MB-231 cells respectively). DHA treatment increased eicosapentaenoic acid and docosapentaenoic acid in MDA-MB-231 cells but not MCF-7 cells. Increased DHA content in MDA-MB-231 cells, MCF-7 cells, and MDA-MB-231 tumors in all PL moieties (except sphingomyelin) corresponded with reduced arachidonic acid (p < 0.05). Feeding mice 2.8% (w/w of fat) DHA ± DOX increased tumor necrotic regions (p < 0.05). This study established differential incorporation of DHA into whole cell and lipid rafts between human breast cancer cell lines. However, within each cell line, this incorporation was not altered by DOX confirming that DOX does not change membrane lipid composition. Furthermore, our findings indicate that membrane changes observed in vitro are translatable to in vivo changes and that DHA + DOX could contribute to the anticancer effects through increased necrosis.
Substances chimiques
Membrane Lipids
0
Phospholipids
0
Docosahexaenoic Acids
25167-62-8
Doxorubicin
80168379AG
Eicosapentaenoic Acid
AAN7QOV9EA
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
549-565Subventions
Organisme : CIHR
ID : 155908
Pays : Canada
Informations de copyright
© 2020 AOCS.
Références
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. The International Journal of Biochemistry & Cell Biology, 38:196-208. https://doi.org/10.1016/j.biocel.2005.08.015
Barnhart, B. C., Alappat, E. C., & Peter, M. E. (2003) The CD95 type I/type II model. Seminars in Immunology, 15:185-193.
Berquin, I. M., Edwards, I. J., & Chen, Y. Q. (2008) Multi-targeted therapy of cancer by omega-3 fatty acids. Cancer Letters, 269:363-377.
Biondo, P. D., Brindley, D. N., Sawyer, M. B., & Field, C. J. (2008) The potential for treatment with dietary long-chain polyunsaturated n-3 fatty acids during chemotherapy. Journal of Nutritional Biochemistry, 19:787-796. https://doi.org/10.1016/j.jnutbio.2008.02.003
Bougnoux, P., Hajjaji, N., Ferrasson, M. N., Giraudeau, B., Couet, C., & Le, F. O. (2009) Improving outcome of chemotherapy of metastatic breast cancer by docosahexaenoic acid: A phase II trial. British Journal of Cancer, 101:1978-1985. https://doi.org/10.1038/sj.bjc.6605441
Chajes, V., Sattler, W., Stranzl, A., & Kostner, G. M. (1995) Influence of n-3 fatty acids on the growth of human breast cancer cells in vitro: Relationship to peroxides and vitamin-E. Breast Cancer Research and Treatment, 34:199-212. https://doi.org/10.1007/bf00689711
Chapkin, R. S., Wang, N., Fan, Y. Y., Lupton, J. R., & Prior, I. A. (2008) Docosahexaenoic acid alters the size and distribution of cell surface microdomains. Biochimica et Biophysica Acta, 1778:466-471. https://doi.org/10.1016/j.bbamem.2007.11.003
Chen, X., Li, W., Ren, J., Huang, D., He, W., Song, Y., … Han, J. (2013) Translocation of mixed lineage kinase domain-like protein to plasma membrane leads to necrotic cell death. Cell Research, 24:105-121. https://doi.org/10.1038/cr.2013.171
Conklin, K. A. (2004) Chemotherapy-associated oxidative stress: Impact on chemotherapeutic effectiveness. Integrative Cancer Therapies, 3:294-300. https://doi.org/10.1177/1534735404270335
Corsetto, P. A., Montorfano, G., 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 in Health and Disease, 10:73.
Cruz-Hernandez, C., Goeuriot, S., Giuffrida, F., Thakkar, S. K., & Destaillats, F. (2013) Direct quantification of fatty acids in human milk by gas chromatography. Journal of Chromatography. A, 1284:174-179. https://doi.org/10.1016/j.chroma.2013.01.094
Das, U. N. (1999) Essential fatty acids and their metabolites and cancer. Nutrition, 15:239-240.
D'Eliseo, D., & Velotti, F. (2016) Omega-3 fatty acids and cancer cell cytotoxicity: Implications for multi-targeted cancer therapy. Journal of Clinical Medicine, 5:15.
DeRuiter, F. E., & Dwyer, J. (2002) Consumer acceptance of irradiated foods: Dawn of a new era? Food Service Technology, 2:47-58. https://doi.org/10.1046/j.1471-5740.2002.00031.x
Escribá, P. V., González-Ros, J. M., Goñi, F. M., Kinnunen, P. K. J., Vigh, L., Sánchez-Magraner, L., … Barceló-Coblijn, G. (2008) Membranes: A meeting point for lipids, proteins and therapies. Journal of Cellular and Molecular Medicine, 12:829-875. https://doi.org/10.1111/j.1582-4934.2008.00281.x
Ewaschuk, J. B., Newell, M., & Field, C. J. (2012) Docosahexanoic acid improves chemotherapy efficacy by inducing CD95 translocation to lipid rafts in ER(−) breast cancer cells. Lipids, 47:1019-1030. https://doi.org/10.1007/s11745-012-3717-7
Field, C. J., Ryan, E. A., Thomson, A. B., & Clandinin, M. T. (1988) Dietary fat and the diabetic state alter insulin binding and the fatty acyl composition of the adipocyte plasma membrane. Biochemical Journal, 253:417-424. https://doi.org/10.1042/bj2530417
Folch, J., Lees, M., & Sloane Stanley, G. H. (1957) A simple method for the isolation and purification of total lipides from animal tissues. Journal of Biological Chemistry, 226:497-509.
Foster, L. J., De Hoog, C. L., & Mann, M. (2003) Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proceedings of the National Academy of Sciences of the United States of America, 100:5813-5818.
Gaba, R. C., Emmadi, R., Parvinian, A., & Casadaban, L. C. (2016) Correlation of doxorubicin delivery and tumor necrosis after drug-eluting bead Transarterial chemoembolization of rabbit VX2 liver tumors. Radiology, 280:752-761. https://doi.org/10.1148/radiol.2016152099
Germain, E., Chajes, 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. International Journal of Cancer, 75:578-583.
Gu, Z., Wu, J., Wang, S., Suburu, J., Chen, H., Thomas, M. J., … Chen, Y. Q. (2013) Polyunsaturated fatty acids affect the localization and signaling of PIP3/AKT in prostate cancer cells. Carcinogenesis, 34:1968-1975. https://doi.org/10.1093/carcin/bgt147
He, M., Guo, S., & Li, Z. (2015) In situ characterizing membrane lipid phenotype of breast cancer cells using mass spectrometry profiling. Scientific Reports, 5:11298-11298. https://doi.org/10.1038/srep11298
Higuchi, Y. (2003) Chromosomal DNA fragmentation in apoptosis and necrosis induced by oxidative stress. Biochemical Pharmacology, 66:1527-1535. https://doi.org/10.1016/s0006-2952(03)00508-2
Holliday, D. L., & Speirs, V. (2011) Choosing the right cell line for breast cancer research. Breast Cancer Research, 13:215. https://doi.org/10.1186/bcr2889
Kang, K. S., Wang, P., Yamabe, N., Fukui, M., Jay, T., & Zhu, B. T. (2010) Docosahexaenoic acid induces apoptosis in MCF-7 cells in vitro and in vivo via reactive oxygen species formation and caspase 8 activation. PLoS One, 5:e10296. https://doi.org/10.1371/journal.pone.0010296
Kim, W., Fan, Y. Y., Barhoumi, R., Smith, R., McMurray, D. N., & Chapkin, R. S. (2008) n-3 polyunsaturated fatty acids suppress the localization and activation of signaling proteins at the immunological synapse in murine CD4+ T cells by affecting lipid raft formation. Journal of Immunology, 181:6236-6243. https://doi.org/10.4049/jimmunol.181.9.6236
Lee, E. J., Yun, U. J., Koo, H. K., Sung, J. Y., Shim, J., Ye, S. K., … Kim, Y. N. (2013) Down-regulation of lipid raft-associated onco-proteins via cholesterol-dependent lipid raft internalization in doxosahexaenoic acid-induced apoptosis. Biochimica et Biophysica Acta, 1841:190-203.
Liu, J., & Ma, D. W. (2014) The role of n-3 polyunsaturated fatty acids in the prevention and treatment of breast cancer. Nutrients, 6:5184-5223. https://doi.org/10.3390/nu6115184
Ma, D. W. L., Seo, J., Davidson, L. A., Callaway, E. S., Fan, Y., Lupton, J. R., & Chapkin, R. S. (2004) n-3 PUFA alter caveolae lipid composition and resident protein localization in mouse colon. The FASEB Journal, 18:1040-1042. https://doi.org/10.1096/fj.03-1430fje
Magtanong, L., Ko, P. J., & Dixon, S. J. (2016) Emerging roles for lipids in non-apoptotic cell death. Cell Death and Differentiation, 23:1099-1109. https://doi.org/10.1038/cdd.2016.25
Maheo, K., Vibet, S., Steghens, J. P., Dartigeas, C., Lehman, M., Bougnoux, P., & Gore, J. (2005) Differential sensitization of cancer cells to doxorubicin by DHA: A role for lipoperoxidation. Free Radical Biology & Medicine, 39:742-751.
Menendez, J. A., Lupu, R., & Colomer, R. (2005) Exogenous supplementation with omega-3 polyunsaturated fatty acid docosahexaenoic acid (DHA; 22:6n-3) synergistically enhances taxane cytotoxicity and downregulates Her-2/neu (c-erbB-2) oncogene expression in human breast cancer cells. European Journal of Cancer Prevention, 14:263-270.
Merendino, N., Costantini, L., Manzi, L., Molinari, R., D'Eliseo, D., & Velotti, F. (2013) Dietary omega-3 polyunsaturated fatty acid DHA: A potential adjuvant in the treatment of cancer. BioMed Research International, 2013:11. https://doi.org/10.1155/2013/310186
Newell, M., Baker, K., Postovit, L. M., & Field, C. J. (2017) A critical review on the effect of docosahexaenoic acid (DHA) on cancer cell cycle progression. International Journal of Molecular Sciences, 18:1784. https://doi.org/10.3390/ijms18081784
Newell, M., Brun, M., & Field, C. J. (2019a) Treatment with DHA modifies the response of MDA-MB-231 breast cancer cells and tumors from nu/nu mice to doxorubicin through apoptosis and cell cycle arrest. The Journal of Nutrition, 149:46-56. https://doi.org/10.1093/jn/nxy224
Newell, M., Goruk, S., Mazurak, V., Postovit, L., & Field, C. J. (2019b) Role of docosahexaenoic acid in enhancement of docetaxel action in patient-derived breast cancer xenografts. Breast Cancer Research and Treatment, 177:357-367. https://doi.org/10.1007/s10549-019-05331-8
Oda, K., Matsuoka, Y., Funahashi, A., & Kitano, H. (2005) A comprehensive pathway map of epidermal growth factor receptor signaling. Molecular Systems Biology, 1. https://doi.org/10.1038/msb4100014
Ozben, T. (2007) Oxidative stress and apoptosis: Impact on cancer therapy. Journal of Pharmaceutical Sciences, 96:2181-2196. https://doi.org/10.1002/jps.20874
Pizato, N., Luzete, B. C., Kiffer, L. F. M. V., Corrêa, L. H., Santos, I. O., Assumpção, J. A. F., … Magalhães, K. G. (2018) Omega-3 docosahexaenoic acid induces pyroptosis cell death in triple-negative breast cancer cells. Scientific Reports, 8:1952. https://doi.org/10.1038/s41598-018-20422-0
Plourde, M., Chouinard-Watkins, R., Vandal, M., Zhang, Y., Lawrence, P., Brenna, T. J., & Cunanne, S. C. (2011) Plasma incorporation, apparent retroconversion and β-oxidation of 13C-docosahexaenoic acid in the elderly. Nutrition and Metabolism, 8:5. https://doi.org/10.1186/1743-7075-8-5
Ridgway, N. D. (2013) The role of phosphatidylcholine and choline metabolites to cell proliferation and survival. Critical Reviews in Biochemistry and Molecular Biology, 48:20-38. https://doi.org/10.3109/10409238.2012.735643
Robinson, L. E., & Field, C. J. (1998) Dietary long-chain (n-3) fatty acids facilitate immune cell activation in sedentary, but not exercise-trained rats. The Journal of Nutrition, 128:498-504. https://doi.org/10.1093/jn/128.3.498
Rogers, K. R., Kikawa, K. D., Mouradian, M., Hernandez, K., McKinnon, K. M., Ahwah, S. M., & Pardini, R. S. (2010) Docosahexaenoic acid alters epidermal growth factor receptor-related signaling by disrupting its lipid raft association. Carcinogenesis, 31:1523-1530. https://doi.org/10.1093/carcin/bgq111
Rose, D. P., Connolly, J. M., Rayburn, J., & Coleman, M. (1995) Influence of diets containing eicosapentaenoic or docosahexaenoic acid on growth and metastasis of breast cancer cell in nude mice. Journal of the National Cancer Institute, 87:587-592.
Sauer, L. A., & Dauchy, R. T. (1990) Tumour-host metabolic interrelationships. Biochemical Society Transactions, 18:80-82. https://doi.org/10.1042/bst0180080
Schley, P. D., Brindley, D. N., & Field, C. J. (2007) (n-3) PUFA alter raft lipid composition and decrease epidermal growth factor receptor levels in lipid rafts of human breast cancer cells. Journal of Nutrition, 137:548-553.
Seibert, K., Shafie, S. M., Triche, T. J., Whang-Peng, J. J., O'Brien, S. J., Toney, J. H., … Lippman, M. E. (1983) Clonal variation of MCF-7 breast cancer cells in vitro and in athymic nude mice. Cancer Research, 43:2223-2239.
Sezgin, E., Levental, I., Mayor, S., & Eggeling, C. (2017) The mystery of membrane organization: Composition, regulation and roles of lipid rafts. Nature Reviews. Molecular Cell Biology, 18:361-374. https://doi.org/10.1038/nrm.2017.16
Shaw, A. S. (2006) Lipid rafts: Now you see them, now you don't. Nature Immunology, 7:1139-1142.
Simons, K., & Toomre, D. (2000) Lipid rafts and signal transduction. Nature Reviews. Molecular Cell Biology, 1:31-39.
Sinha, B. K., Mimnaugh, E. G., Rajagopalan, S., & Myers, C. E. (1989) Adriamycin activation and oxygen free radical formation in human breast tumor cells: Protective role of glutathione peroxidase in Adriamycin resistance. Cancer Research, 49:3844-3848.
Stillwell, W., & Wassall, S. R. (2003) Docosahexaenoic acid: Membrane properties of a unique fatty acid. Chemistry and Physics of Lipids, 126:1-27. https://doi.org/10.1016/s0009-3084(03)00101-4
Stillwell, W., Shaikh, S. R., Zerouga, M., Siddiqui, R., & Wassall, S. R. (2005) Docosahexaenoic acid affects cell signaling by altering lipid rafts. Reproduction Nutrition Development, 45:559-579. https://doi.org/10.1051/rnd:2005046
Subedi, K., Yu, H. M., Newell, M., Weselake, R. J., Meesapyodsuk, D., Qiu, X., … Field, C. J. (2015) Stearidonic acid-enriched flax oil reduces the growth of human breast cancer in vitro and in vivo. Breast Cancer Research and Treatment, 149:17-29. https://doi.org/10.1007/s10549-014-3212-3
Tacar, O., Sriamornsak, P., & Dass, C. R. (2013) Doxorubicin: An update on anticancer molecular action, toxicity and novel drug delivery systems. The Journal of Pharmacy and Pharmacology, 65:157-170. https://doi.org/10.1111/j.2042-7158.2012.01567.x
Turk, H. F., & Chapkin, R. S. (2013) Membrane lipid raft organization is uniquely modified by n-3 polyunsaturated fatty acids. Prostaglandins, Leukotrienes, and Essential Fatty Acids, 88:43-47. https://doi.org/10.1016/j.plefa.2012.03.008
Verkleij, A. J., Zwaal, R. F., Roelofsen, B., Comfurius, P., Kastelijn, D., & van Deenen, L. L. (1973) The asymmetric distribution of phospholipids in the human red cell membrane. A combined study using phospholipases and freeze-etch electron microscopy. Biochimica et Biophysica Acta, 323:178-193. https://doi.org/10.1016/0005-2736(73)90143-0
Wei, L., Surma, M., Gough, G., Shi, S., Lambert-Cheatham, N., Chang, J., & Shi, J. (2015) Dissecting the mechanisms of doxorubicin and oxidative stress-induced cytotoxicity: The involvement of Actin cytoskeleton and ROCK1. PLoS One, 10:e0131763. https://doi.org/10.1371/journal.pone.0131763
Xiong, Y., Zhao, Y.-Y., Goruk, S., Oilund, K., Field, C. J., Jacobs, R. L., & Curtis, J. M. (2012) Validation of an LC-MS/MS method for the quantification of choline-related compounds and phospholipids in foods and tissues. Journal of Chromatography B, 911:170-179. https://doi.org/10.1016/j.jchromb.2012.10.038
Yu, H.-M., Newell, M., Subedi, K., Weselake, R. J., Mazurak, V., & Field, C. J. (2015) Bypassing the D6-desaturase enzyme and directly providing n-3 and n-6 PUFA pathway intermediates reduces the survival of two human breast cancer cell lines. European Journal of Lipid Science Technology, 117:1378-1390.
Zerouga, M., Stillwell, W., Stone, J., Powner, A., & Jenski, L. J. (1996) Phospholipid class as a determinant in docosahexaenoic acid's effect on tumor cell viability. Anticancer Research, 16:2863-2868.