Ovarian Tumours of Different Histologic Type and Clinical Stage Induce Similar Changes in Lipid Metabolism

Overview

Journal Br J Cancer

Specialty Oncology

Date 2018 Oct 9

PMID 30293997

Citations 18

Authors

Riikka Johanna Niemi

Elena Ioana Braicu

Hagen Kulbe

Kaisa Maria Koistinen

Jalid Sehouli

Ulla Puistola

Johanna Unelma Maenpaa

Mika Hilvo

Affiliations

Soon will be listed here.

Abstract

Background: Previous results obtained from serum samples of late-stage, high-grade serous ovarian carcinoma patients showed large alterations in lipid metabolism. To validate and extend the results, we studied lipidomic changes in early-stage ovarian tumours. In addition to serous ovarian cancer, we investigated whether these changes occur in mucinous and endometrioid histological subtypes as well.

Methods: Altogether, 354 serum or plasma samples were collected from three centres, one from Germany and two from Finland. We performed lipidomic analysis of samples from patients with malignant (N = 138) or borderline (N = 25) ovarian tumours, and 191 controls with benign pathology. These results were compared to previously published data.

Results: We found 39 lipids that showed consistent alteration both in early- and late-stage ovarian cancer patients as well as in pre- and postmenopausal women. Most of these changes were already significant at an early stage and progressed with increasing stage. Furthermore, 23 lipids showed similar alterations in all investigated histological subtypes.

Conclusions: Changes in lipid metabolism due to ovarian cancer occur in early-stage disease but intensify with increasing stage. These changes occur also in other histological subtypes besides high-grade serous carcinoma. Understanding lipid metabolism in ovarian cancer may lead to new therapeutic and diagnostic alternatives.

Citing Articles

Expression of lipid-metabolism genes is correlated with immune microenvironment and predicts prognosis of hepatocellular carcinoma.

Hao L, Li S, Hu X Sci Rep. 2024; 14(1):25705.

PMID: 39463421 PMC: 11514195. DOI: 10.1038/s41598-024-76578-5.

Serum Lipidome Profiling Reveals a Distinct Signature of Ovarian Cancer in Korean Women.

Sah S, Bifarin O, Moore S, Gaul D, Chung H, Kwon S Cancer Epidemiol Biomarkers Prev. 2024; 33(5):681-693.

PMID: 38412029 PMC: 11061607. DOI: 10.1158/1055-9965.EPI-23-1293.

LncRNA RPARP-AS1 promotes the progression of osteosarcoma cells through regulating lipid metabolism.

Cai F, Liu L, Bo Y, Yan W, Tao X, Peng Y BMC Cancer. 2024; 24(1):166.

PMID: 38308235 PMC: 10835925. DOI: 10.1186/s12885-024-11901-x.

The Contribution of Lipidomics in Ovarian Cancer Management: A Systematic Review.

Tzelepi V, Gika H, Begou O, Timotheadou E Int J Mol Sci. 2023; 24(18).

PMID: 37762264 PMC: 10531399. DOI: 10.3390/ijms241813961.

Peripheral Blood Serum NMR Metabolomics Is a Powerful Tool to Discriminate Benign and Malignant Ovarian Tumors.

Nunes S, Sousa J, Silva F, Silveira M, Guimaraes A, Serpa J Metabolites. 2023; 13(9).

PMID: 37755269 PMC: 10537270. DOI: 10.3390/metabo13090989.

References

Shayesteh L, Lu Y, Kuo W, Baldocchi R, Godfrey T, Collins C . PIK3CA is implicated as an oncogene in ovarian cancer. Nat Genet. 1999; 21(1):99-102. DOI: 10.1038/5042. View

Pyragius C, Fuller M, Ricciardelli C, Oehler M . Aberrant lipid metabolism: an emerging diagnostic and therapeutic target in ovarian cancer. Int J Mol Sci. 2013; 14(4):7742-56. PMC: 3645713. DOI: 10.3390/ijms14047742. View

Weir J, Wong G, Barlow C, Greeve M, Kowalczyk A, Almasy L . Plasma lipid profiling in a large population-based cohort. J Lipid Res. 2013; 54(10):2898-908. PMC: 3770102. DOI: 10.1194/jlr.P035808. View

Gupta D, Lis C . Role of CA125 in predicting ovarian cancer survival - a review of the epidemiological literature. J Ovarian Res. 2009; 2:13. PMC: 2764643. DOI: 10.1186/1757-2215-2-13. View

Zhang Y, Liu Y, Li L, Wei J, Xiong S, Zhao Z . High resolution mass spectrometry coupled with multivariate data analysis revealing plasma lipidomic alteration in ovarian cancer in Asian women. Talanta. 2016; 150:88-96. DOI: 10.1016/j.talanta.2015.12.021. View

Gaul D, Mezencev R, Long T, Jones C, Benigno B, Gray A . Highly-accurate metabolomic detection of early-stage ovarian cancer. Sci Rep. 2015; 5:16351. PMC: 4647115. DOI: 10.1038/srep16351. View

Zhao Z, Cai Q, Xu Y . The Lipidomic Analyses in Low and Highly Aggressive Ovarian Cancer Cell Lines. Lipids. 2015; 51(2):179-87. DOI: 10.1007/s11745-015-4108-7. View

Zhang T, Wu X, Yin M, Fan L, Zhang H, Zhao F . Discrimination between malignant and benign ovarian tumors by plasma metabolomic profiling using ultra performance liquid chromatography/mass spectrometry. Clin Chim Acta. 2012; 413(9-10):861-8. DOI: 10.1016/j.cca.2012.01.026. View

Odunsi K, Wollman R, Ambrosone C, Hutson A, McCann S, Tammela J . Detection of epithelial ovarian cancer using 1H-NMR-based metabonomics. Int J Cancer. 2004; 113(5):782-8. DOI: 10.1002/ijc.20651. View

10.

Wigger L, Cruciani-Guglielmacci C, Nicolas A, Denom J, Fernandez N, Fumeron F . Plasma Dihydroceramides Are Diabetes Susceptibility Biomarker Candidates in Mice and Humans. Cell Rep. 2017; 18(9):2269-2279. DOI: 10.1016/j.celrep.2017.02.019. View

11.

Segui B, Andrieu-Abadie N, Jaffrezou J, Benoist H, Levade T . Sphingolipids as modulators of cancer cell death: potential therapeutic targets. Biochim Biophys Acta. 2006; 1758(12):2104-20. DOI: 10.1016/j.bbamem.2006.05.024. View

12.

Laaksonen R, Ekroos K, Sysi-Aho M, Hilvo M, Vihervaara T, Kauhanen D . Plasma ceramides predict cardiovascular death in patients with stable coronary artery disease and acute coronary syndromes beyond LDL-cholesterol. Eur Heart J. 2016; 37(25):1967-76. PMC: 4929378. DOI: 10.1093/eurheartj/ehw148. View

13.

Furuya H, Shimizu Y, Kawamori T . Sphingolipids in cancer. Cancer Metastasis Rev. 2011; 30(3-4):567-76. DOI: 10.1007/s10555-011-9304-1. View

14.

Ke C, Hou Y, Zhang H, Fan L, Ge T, Guo B . Large-scale profiling of metabolic dysregulation in ovarian cancer. Int J Cancer. 2014; 136(3):516-26. DOI: 10.1002/ijc.29010. View

15.

Denkert C, Budczies J, Kind T, Weichert W, Tablack P, Sehouli J . Mass spectrometry-based metabolic profiling reveals different metabolite patterns in invasive ovarian carcinomas and ovarian borderline tumors. Cancer Res. 2006; 66(22):10795-804. DOI: 10.1158/0008-5472.CAN-06-0755. View

16.

Braicu E, Darb-Esfahani S, Schmitt W, Koistinen K, Heiskanen L, Poho P . High-grade ovarian serous carcinoma patients exhibit profound alterations in lipid metabolism. Oncotarget. 2017; 8(61):102912-102922. PMC: 5732699. DOI: 10.18632/oncotarget.22076. View

17.

Li H, Zhao Z, Wei G, Yan L, Wang D, Zhang H . Group VIA phospholipase A2 in both host and tumor cells is involved in ovarian cancer development. FASEB J. 2010; 24(10):4103-16. PMC: 2996900. DOI: 10.1096/fj.10-161356. View

18.

Sutphen R, Xu Y, Wilbanks G, Fiorica J, Grendys Jr E, Lapolla J . Lysophospholipids are potential biomarkers of ovarian cancer. Cancer Epidemiol Biomarkers Prev. 2004; 13(7):1185-91. View

19.

Vinayavekhin N, Sueajai J, Chaihad N, Panrak R, Chokchaisiri R, Sangvanich P . Serum lipidomics analysis of ovariectomized rats under Curcuma comosa treatment. J Ethnopharmacol. 2016; 192:273-282. DOI: 10.1016/j.jep.2016.07.054. View

20.

Folch J, Lees M, SLOANE STANLEY G . A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem. 1957; 226(1):497-509. View