Blood oxylipin profiles as a marker of the pathogenesis of oncological diseases

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Abstract

Oxylipins are signal lipids derived from polyunsaturated fatty acids (PUFAs), which are formed by polyenzymatic multi-acid pathways of danger (cyclooxygenase, lipoxygenase, epoxygenase, anandamide), as well as non-enzymatically. These PUFA transformation pathways are activated in parallel, forming a mixture of active inclusions. Although the combination of oxylipins with tumor secretions was performed a long time ago, the methods of instrumental analysis have only recently been improved, measurements of oxylipins of different classes (profiles) have been compared. The review considers approaches to obtaining the profile of oxylipins by HPLC-MS/MS. The profiles of oxylipins in samples of patients with oncological diseases (breast cancer, colorectal cancer, ovarian cancer, lung cancer, prostate cancer, liver cancer) were compared. The conclusion is made about the possible possibilities of using the profile of blood oxylipins as markers of oncological diseases. Understanding the high level of exceeding the level of PUFAs and the physiological activity of oxylipin mixtures will be accompanied by the perfection of early diagnosis and prediction of the course of tumor diseases.

About the authors

D. V Chistyakov

Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University

Email: chistyakof@gmail.com
119992 Moscow, Russia

L. V Kovalenko

Surgut State University

Email: chistyakof@gmail.com
628412 Ugra, Surgut, Russia

M. Y Donnikov

Surgut State University

Email: chistyakof@gmail.com
628412 Ugra, Surgut, Russia

M. G Sergeeva

Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University

Email: chistyakof@gmail.com
119992 Moscow, Russia

References

  1. Сергеева М. Г., Варфоломеева А. Т. (2006) Каскад арахидоновой кислоты, Народное образование, Москва.
  2. Gabbs, M., Leng, S., Devassy, J. G., Monirujjaman, M., and Aukema, H. M. (2015) Advances in our understanding of oxylipins derived from dietary PUFAs, Adv. Nutr., 6, 513-540, doi: 10.3945/an.114.007732.
  3. Hajeyah, A. A., Griffiths, W. J., Wang, Y., Finch, A. J., and O'Donnell, V. B. (2020) The biosynthesis of enzymatically oxidized lipids, Front. Endocrinol., 11, 591819, doi: 10.3389/FENDO.2020.591819.
  4. Генрихс Е. Е., Бобров М. Ю., Андрианова Е. Л., Грецкая Н. М., Лыжин А. А., Блаженова А. В., Фрумкина Л. Е., Безуглов В. В., Хаспеков Л. Г. (2010) Модуляторы эндогенной каннабиноидной системы как нейропротекторы, Анналы клин. эксп. неврол., 4, 37-42.
  5. Buczynski, M. W., Dumlao, D. S., and Dennis, E. A. (2009) An integrated omics analysis of eicosanoid biology, J. Lipid Res., 50, 1015-1038, doi: 10.1194/jlr.R900004-JLR200.
  6. Johnson, A. M., Kleczko, E. K., and Nemenoff, R. A. (2020) Eicosanoids in cancer: new roles in immunoregulation, Front. Pharmacol., 11, 595498, doi: 10.3389/FPHAR.2020.595498.
  7. Dennis, E. A., and Norris, P. C. (2015) Eicosanoid storm in infection and inflammation, Nat. Rev. Immunol., 15, 511-523, doi: 10.1038/nri3859.
  8. Serhan, C. N. (2014) Pro-resolving lipid mediators are leads for resolution physiology, Nature, 510, 92-101, doi: 10.1038/nature13479.
  9. Furman, D., Campisi, J., Verdin, E., Carrera-Bastos, P., Targ, S., Franceschi, C., Gilroy, D., Fasano, A., Miller, G., Miller, A., Mantovani, A., Weyand, C., Barzilai, N., Goronzy, J., Rando, T., Effros, R., Lucia, A., Kleinstreuer, N., and Slavich, G. (2019) Chronic inflammation in the etiology of disease across the life span, Nat. Med., 25, 1822-1832, doi: 10.1038/S41591-019-0675-0.
  10. Medzhitov, R. (2021) The spectrum of inflammatory responses, Science, 374, 1070-1075, doi: 10.1126/SCIENCE.ABI5200.
  11. Medzhitov, R. (2008) Origin and physiological roles of inflammation, Nature, 454, 428-435, doi: 10.1038/nature07201.
  12. Van Praet, L., Jacques, P., Van den Bosch, F., and Elewaut, D. (2012) The transition of acute to chronic bowel inflammation in spondyloarthritis, Nat. Rev. Rheumatol., 8, 288-295, doi: 10.1038/nrrheum.2012.42.
  13. Hanahan, D., and Weinberg, R. A. (2011) Hallmarks of cancer: the next generation, Cell, 144, 646-674, doi: 10.1016/J.CELL.2011.02.013.
  14. Coussens, L. M., and Werb, Z. (2002) Inflammation and cancer, Nature, 420, 860-867, doi: 10.1038/nature01322.
  15. Акимов М. Г., Бобров М. Ю., Безуглов В. В., Коновалов C. С. (2009) Липиды и рак: очерки липидологии онкологического процесса, Прайм-Еврознак.
  16. Schebb, N. H., Kühn, H., Kahnt, A. S., Rund, K. M., O'Donnell, V. B., Flamand, N., Peters-Golden, M., Jakobsson, P., Weylandt, K. H., Rohwer, N., Murphy, R. C., Geisslinger, G., FitzGerald, G. A., Hanson, J., Dahlgren, C., Alnouri, M. W., Offermanns, S., and Steinhilber, D. (2022) Formation, signaling and occurrence of specialized pro-resolving lipid mediators-what is the evidence so far? Front. Pharmacol., 13, 838782, doi: 10.3389/FPHAR.2022.838782.
  17. Burla B., Arita M., Arita M., Bendt, A. K, Cazenave-Gassiot, A., Dennis, E. A., Ekroos, K., Han, X., Ikeda, K., Liebisch, G., Lin, M. K., Loh, T. P., Meikle, P. J., Orešič, M., Quehenberger, O., Shevchenko, A., Torta, F., Wakelam, M. J. O, Wheelock, C. E., and Wenk, M. R. (2018) MS-based lipidomics of human blood plasma: a community-initiated position paper to develop accepted guidelines, J. Lipid Res., 59, 2001-2017, doi: 10.1194/jlr.S087163.
  18. Morris, J. K., Piccolo, B. D., John, C. S., Green, Z. D., Thyfault, J. P., and Adams, S. H. (2019) Oxylipin profiling of Alzheimer's disease in nondiabetic and type 2 diabetic elderly, Metabolites, 9, 177, doi: 10.3390/metabo9090177.
  19. Gao, B., Lang, S., Duan, Y., Wang, Y., Shawcross, D. L., Louvet, A., Mathurin, P., Ho, S. B., Stärkel, P., and Schnabl, B. (2019) Serum and fecal oxylipins in patients with alcohol-related liver disease, Digest. Dis. Sci., 64, 1878-1892, doi: 10.1007/s10620-019-05638-y.
  20. Quehenberger, O., Armando, A. M., Brown, A. H., Milne, S. B., Myers, D. S., Merrill, A. H., Bandyopadhyay, S., Jones, K. N., Kelly, S., Shaner, R. L., Sullards, C. M., Wang, E., Murphy, R. C., Barkley, R. M., Leiker, T. J., Raetz, C. R., Guan, Z., Laird, G. M., Six, D. A., Russell, D. W., McDonald, J. G., Subramaniam, S., Fahy, E., and Dennis, E. A. (2010) Lipidomics reveals a remarkable diversity of lipids in human plasma, J. Lipid Res., 51, 3299-3305, doi: 10.1194/JLR.M009449.
  21. Huynh, K., Barlow, C. K., Jayawardana, K. S., Weir, J. M., Mellett, N. A., Cinel, M., Magliano, D. J., Shaw, J. E., Drew, B. G., and Meikle, P. J. (2019) High-throughput plasma lipidomics: detailed mapping of the associations with cardiometabolic risk factors, Cell Chem. Biol., 26, 71-84.e4, doi: 10.1016/J.CHEMBIOL.2018.10.008.
  22. Lam, S. M., Tian, H., and Shui, G. (2017) Lipidomics, en route to accurate quantitation, Biochim. Biophys. Acta Mol. Cell Biol. Lipids, 1862, 752-761, doi: 10.1016/J.BBALIP.2017.02.008.
  23. Bowden, J. A., Heckert, A., Ulmer, C. Z., Jones, C. M., Koelmel, J. P., Abdullah, L., Ahonen, L., Alnouti, Y., Armando, A. M., Asara, J. M., Bamba, T., Barr, J. R., Bergquist, J., Borchers, C. H., Brandsma, J., Breitkopf, S. B., Cajka, T., Cazenave-Gassiot, A., Checa, A., Cinel, M. A., Colas, R. A., Cremers, S., Dennis, E. A., Evans, J. E., Fauland, A., Fiehn, O., Gardner, M. S., Garrett, T. J., Gotlinger, K. H., Han, J., Huang, Y., Neo, A. H., Hyötyläinen, T., Izumi, Y., Jiang, H., Jiang, H., Jiang, J., Kachman, M., Kiyonami, R., Klavins, K., Klose, C., Köfeler, H. C., Kolmert, J., Koal, T., Koster, G., Kuklenyik, Z., Kurland, I. J., Leadley, M., Lin, K., Maddipati, K. R., McDougall, D., Meikle, P. J., Mellett, N. A., Monnin, C., Moseley, M. A., Nandakumar, R., Oresic, M., Patterson, R., Peake, D., Pierce, J. S., Post, M., Postle, A. D., Pugh, R., Qiu, Y., Quehenberger, O., Ramrup, P., Rees, J., Rembiesa, B., Reynaud, D., Roth, M. R., Sales, S., Schuhmann, K., Schwartzman, M. L., Serhan, C. N., Shevchenko, A., Somerville, S. E., St John-Williams, L., Surma, M. A., Takeda, H., Thakare, R., Thompson, J. W., Torta, F., Triebl, A., Trötzmüller, M., Ubhayasekera, S. J. K., Vuckovic, D., Weir, J. M., Welti, R., Wenk, M. R., Wheelock, C. E., Yao, L., Yuan, M., Zhao, X. H., and Zhou, S. (2017) Harmonizing lipidomics: NIST interlaboratory comparison exercise for lipidomics using SRM 1950-metabolites in frozen human plasma, J. Lipid Res., 58, 2275-2288, doi: 10.1194/JLR.M079012.
  24. Mainka, M., Dalle, C., Pétéra, M., Dalloux-Chioccioli, J., Kampschulte, N., Ostermann, A. I., Rothe, M., Bertrand-Michel, J., Newman, J. W., Gladine, C., and Schebb, N. H. (2020) Harmonized procedures lead to comparable quantification of total oxylipins across laboratories, J. Lipid Res., 61, 1424-1436, doi: 10.1194/jlr.RA120000991.
  25. Koch, E., Mainka, M., Dalle, C., Ostermann, A. I., Rund, K. M., Kutzner, L., Froehlich, L. F., Bertrand-Michel, J., Gladine, C., and Schebb, N. H. (2020) Stability of oxylipins during plasma generation and long-term storage, Talanta, 217, 121074, doi: 10.1016/j.talanta.2020.121074.
  26. Liakh, I., Pakiet, A., Sledzinski, T., and Mika, A. (2020) Methods of the analysis of oxylipins in biological samples, Molecules, 25, 349, doi: 10.3390/molecules25020349.
  27. Frezza, C. (2020) Metabolism and cancer: the future is now, Br. J. Cancer, 122, 133-135, doi: 10.1038/s41416-019-0667-3.
  28. Koundouros, N., and Poulogiannis, G. (2020) Reprogramming of fatty acid metabolism in cancer, Br. J. Cancer, 122, 4-22, doi: 10.1038/S41416-019-0650-Z.
  29. Butler, L. M., Perone, Y., Dehairs, J., Lupien, L. E., de Laat, V., Talebi, A., Loda, M., Kinlaw, W. B., and Swinnen, J. V. (2020) Lipids and cancer: emerging roles in pathogenesis, diagnosis and therapeutic intervention, Adv. Drug Deliv. Rev., 159, 245-293, doi: 10.1016/j.addr.2020.07.013.
  30. Pakiet, A., Kobiela, J., Stepnowski, P., Sledzinski, T., and Mika, A. (2019) Changes in lipids composition and metabolism in colorectal cancer: a review, Lipids Health Dis., 18, 29, doi: 10.1186/S12944-019-0977-8.
  31. Wang, D., and DuBois, R. N. (2018) Role of prostanoids in gastrointestinal cancer, J. Clin. Invest., 128, 2732-2742, doi: 10.1172/JCI97953.
  32. Patrignani, P., Sacco, A., Sostres, C., Bruno, A., Dovizio, M., Piazuelo, E., Di Francesco, L., Contursi, A., Zucchelli, M., Schiavone, S., Tacconelli, S., Patrono, C., and Lanas, A. (2017) Low-dose aspirin acetylates cyclooxygenase-1 in human colorectal mucosa: implications for the chemoprevention of colorectal cancer, Clin. Pharmacol. Ther., 102, 52-61, doi: 10.1002/CPT.639.
  33. Edin, M. L., Duval, C., Zhang, G., and Zeldin, D. C. (2020) Role of linoleic acid-derived oxylipins in cancer, Cancer Metastasis Rev., 39, 581-582, doi: 10.1007/s10555-020-09904-8.
  34. Azrad, M., Turgeon, C., and Demark-Wahnefried, W. (2013) Current evidence linking polyunsaturated fatty acids with cancer risk and progression, Front. Oncol., 3, 224, doi: 10.3389/FONC.2013.00224.
  35. Markosyan, N., Chen, E. P., and Smyth, E. M. (2014) Targeting COX-2 abrogates mammary tumorigenesis: breaking cancer-associated suppression of immunosurveillance, Oncoimmunology, 3, e29287, doi: 10.4161/ONCI.29287.
  36. Schneider, C., and Pozzi, A. (2011) Cyclooxygenases and lipoxygenases in cancer, Cancer Metastasis Rev., 30, 277-294, doi: 10.1007/S10555-011-9310-3.
  37. Catalano, A., and Procopio, A. (2005) New aspects on the role of lipoxygenases in cancer progression, Histol. Histopathol., 20, 969-975, doi: 10.14670/HH-20.969.
  38. Wang, Q., Morris, R. J., Bode, A. M., and Zhang, T. (2022) Prostaglandin pathways: opportunities for cancer prevention and therapy, Cancer Res., 82, 949-965, doi: 10.1158/0008-5472.CAN-21-2297.
  39. Luo, Y., and Liu, J. Y. (2020) Pleiotropic functions of cytochrome p450 monooxygenase-derived eicosanoids in cancer, Front. Pharmacol., 11, 580897, doi: 10.3389/FPHAR.2020.580897.
  40. Mahapatra, A. D., Choubey, R., and Datta, B. (2020) Small molecule soluble epoxide hydrolase inhibitors in multitarget and combination therapies for inflammation and cancer, Molecules, 25, 5488, doi: 10.3390/MOLECULES25235488.
  41. Bruno, R. D., and Njar, V. C. O. (2007) Targeting cytochrome P450 enzymes: a new approach in anti-cancer drug development, Bioorg. Med. Chem., 15, 5047-5060, doi: 10.1016/J.BMC.2007.05.046.
  42. Laezza, C., Pagano, C., Navarra, G., Pastorino, O., Proto, M. C., Fiore, D., Piscopo, C., Gazzerro, P., and Bifulco, M. (2020) The endocannabinoid system: a target for cancer treatment, Int. J. Mol. Sci., 21, 747, doi: 10.3390/IJMS21030747.
  43. Chocholoušková, M., Jirásko, R., Vrána, D., Gatěk, J., Melichar, B., and Holčapek, M. (2019) Reversed phase UHPLC/ESI-MS determination of oxylipins in human plasma: a case study of female breast cancer, Anal. Bioanal. Chem., 411, 1239-1251, doi: 10.1007/s00216-018-1556-y.
  44. Chistyakov, D. V., Guryleva, M. V., Stepanova, E. S., Makarenkova, L. M., Ptitsyna, E. V., Goriainov, S. V., Nikolskaya, A. I., Astakhova, A. A., Klimenko, A. S., Bezborodova, O. A., Rasskazova, E. A., Potanina, O. G., Abramovich, R. A., Nemtsova, E. R., and Sergeeva, M. G. (2022) Multi-omics approach points to the importance of oxylipins metabolism in early-stage breast cancer, Cancers, 14, 2041, doi: 10.3390/cancers14082041.
  45. Zheng, J., Zheng, Y., Li, W., Zhi, J., Huang, X., Zhu, W., Liu, Z., and Gong, L. (2022) Combined metabolomics with transcriptomics reveals potential plasma biomarkers correlated with non-small-cell lung cancer proliferation through the Akt pathway, Clin. Chim. Acta, 530, 66-73, doi: 10.1016/J.CCA.2022.02.018.
  46. Zhang, J., Yang, Q., Li, J., Zhong, Y., Zhang, L., Huang, Q., Chen, B., Mo, M., Shen, S., Zhong, Q., Liu, H., and Cai, C. (2017) Distinct differences in serum eicosanoids in healthy, enteritis and colorectal cancer individuals, Metabolomics, 14, 4, doi: 10.1007/S11306-017-1293-9.
  47. Guo, J., Pan, Y., Chen, J., Jin, P., Tang, S., Wang, H., Su, H., Wang, Q., Chen, C., Xiong, F., Liu, K., Li, Y., Su, M., Tang, T., He, Y., and Sheng, J. (2023) Serum metabolite signatures in normal individuals and patients with colorectal adenoma or colorectal cancer using UPLC-MS/MS method, J. Proteomics, 270, 104741, doi: 10.1016/J.JPROT.2022.104741.
  48. Zhang, L. J., Chen, B., Zhang, J. J., Li, J., Yang, Q., Zhong, Q. S., Zhan, S., Liu, H., and Cai, C. (2017) Serum polyunsaturated fatty acid metabolites as useful tool for screening potential biomarker of colorectal cancer, Prostaglandins Leukot. Essent. Fatty Acids, 120, 25-31, doi: 10.1016/J.PLEFA.2017.04.003.
  49. Liu, J., Mazzone, P. J., Cata, J. P., Kurz, A., Bauer, M., Mascha, E. J., and Sessler, D. I. (2014) Serum free fatty acid biomarkers of lung cancer, Chest, 146, 670-679, doi: 10.1378/CHEST.13-2568.
  50. Fitian, A. I., Nelson, D. R., Liu, C., Xu, Y., Ararat, M., and Cabrera, R. (2014) Integrated metabolomic profiling of hepatocellular carcinoma in hepatitis C cirrhosis through GC/MS and UPLC/MS-MS, Liver Int., 34, 1428-1444, doi: 10.1111/LIV.12541.
  51. Gong, Z. G., Zhao, W., Zhang, J., Wu, X., Hu, J., Yin, G. C., and Xu, Y. J. (2017) Metabolomics and eicosanoid analysis identified serum biomarkers for distinguishing hepatocellular carcinoma from hepatitis B virus-related cirrhosis, Oncotarget, 8, 63890-63900, doi: 10.18632/ONCOTARGET.19173.
  52. Rodríguez-Blanco, G., Burgers, P. C., Dekker, L. J. M., Ijzermans, J. J. N., Wildhagen, M. F., Schenk-Braat, E. A. M., Bangma, C. H., Jenster, G., and Luider, T. M. (2014) Serum levels of arachidonic acid metabolites change during prostate cancer progression, Prostate, 74, 618-627, doi: 10.1002/PROS.22779.
  53. Pruimboom, W. M., Bac, D. J., van Dijk, A. P. M., Garrelds, I. M., Tak, C. J., Bonta, I. L., Wilson, J. H., and Zijlstra, F. J. (1995) Levels of soluble intercellular adhesion molecule 1, eicosanoids and cytokines in ascites of patients with liver cirrhosis, peritoneal cancer and spontaneous bacterial peritonitis, Int. J. Immunopharmacol., 17, 375-384, doi: 10.1016/0192-0561(95)00015-T.
  54. Hada, M., Edin, M. L., Hartge, P., Lih, F. B., Wentzensen, N., Zeldin, D. C., and Trabert, B. (2019) Prediagnostic serum levels of fatty acid metabolites and risk of ovarian cancer in the prostate, lung, colorectal, and ovarian (PLCO) cancer screening trial, Cancer Epidemiol. Biomarkers Prev., 28, 189-197, doi: 10.1158/1055-9965.EPI-18-0392.
  55. Wu, C. C., Gupta, T., Garcia, V., Ding, Y., and Schwartzman, M. L. (2014) 20-HETE and blood pressure regulation: clinical implications, Cardiol. Rev., 22, 1-12, doi: 10.1097/CRD.0B013E3182961659.
  56. Murakami, M., Sato, H., and Taketomi, Y. (2020) Updating phospholipase A2 biology, Biomolecules, 10, 1-33, doi: 10.3390/BIOM10101457.
  57. Nagarajan, S. R., Butler, L. M., and Hoy, A. J. (2021) The diversity and breadth of cancer cell fatty acid metabolism, Cancer Metab., 9, 2, doi: 10.1186/s40170-020-00237-2.
  58. Yeung, J., Hawley, M., and Holinstat, M. (2017) The expansive role of oxylipins on platelet biology, J. Mol. Med., 95, 575-588, doi: 10.1007/s00109-017-1542-4.
  59. Lone, A. M., and Taskén, K. (2013) Proinflammatory and immunoregulatory roles of eicosanoids in T cells, Front. Immunol., 4, 130, doi: 10.3389/FIMMU.2013.00130.
  60. Bogatcheva, N. V., Sergeeva, M. G., Dudek, S. M., and Verin, A. D. (2005) Arachidonic acid cascade in endothelial pathobiology, Microvasc. Res., 69, 107-127, doi: 10.1016/j.mvr.2005.01.007.

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