Common and Differential Traits of the Membrane Lipidome of Colon Cancer Cell Lines and Their Secreted Vesicles: Impact on Studies Using Cell Lines

Overview

Journal Cancers (Basel)

Publisher MDPI

Specialty Oncology

Date 2020 May 24

PMID 32443825

Citations 9

Authors

Joan Bestard-Escalas

Albert Maimo-Barcelo

Daniel H Lopez

Rebeca Reigada

Francisca Guardiola-Serrano

Jose Ramos-Vivas

Thorsten Hornemann

Toshiro Okazaki

Gwendolyn Barcelo-Coblijn

Affiliations

Soon will be listed here.

Abstract

Colorectal cancer (CRC) is the fourth leading cause of cancer death in the world. Despite the screening programs, its incidence in the population below the 50s is increasing. Therefore, new stratification protocols based on multiparametric approaches are highly needed. In this scenario, the lipidome is emerging as a powerful tool to classify tumors, including CRC, wherein it has proven to be highly sensitive to cell malignization. Hence, the possibility to describe the lipidome at the level of lipid species has renewed the interest to investigate the role of specific lipid species in pathologic mechanisms, being commercial cell lines, a model still heavily used for this purpose. Herein, we characterize the membrane lipidome of five commercial colon cell lines and their extracellular vesicles (EVs). The results demonstrate that both cell and EVs lipidome was able to segregate cells according to their malignancy. Furthermore, all CRC lines shared a specific and strikingly homogenous impact on ether lipid species. Finally, this study also cautions about the need of being aware of the singularities of each cell line at the level of lipid species. Altogether, this study firmly lays the groundwork of using the lipidome as a solid source of tumor biomarkers.

Citing Articles

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References

Bishop J, HAJRA A . Mechanism and specificity of formation of long chain alcohols by developing rat brain. J Biol Chem. 1981; 256(18):9542-50. View

Guinney J, Dienstmann R, Wang X, De Reynies A, Schlicker A, Soneson C . The consensus molecular subtypes of colorectal cancer. Nat Med. 2015; 21(11):1350-6. PMC: 4636487. DOI: 10.1038/nm.3967. View

Abe M, Makino A, Hullin-Matsuda F, Kamijo K, Ohno-Iwashita Y, Hanada K . A role for sphingomyelin-rich lipid domains in the accumulation of phosphatidylinositol-4,5-bisphosphate to the cleavage furrow during cytokinesis. Mol Cell Biol. 2012; 32(8):1396-407. PMC: 3318597. DOI: 10.1128/MCB.06113-11. View

Holcapek M, Liebisch G, Ekroos K . Lipidomic analysis. Anal Bioanal Chem. 2020; 412(10):2187-2189. DOI: 10.1007/s00216-020-02419-9. View

Skotland T, Ekroos K, Kauhanen D, Simolin H, Seierstad T, Berge V . Molecular lipid species in urinary exosomes as potential prostate cancer biomarkers. Eur J Cancer. 2016; 70:122-132. DOI: 10.1016/j.ejca.2016.10.011. View

Fernandez R, Carriel V, Lage S, Garate J, Diez-Garcia J, Ochoa B . Deciphering the Lipid Architecture of the Rat Sciatic Nerve Using Imaging Mass Spectrometry. ACS Chem Neurosci. 2016; 7(5):624-32. DOI: 10.1021/acschemneuro.6b00010. View

Hossain M, Abe Y, Ali F, Youssef M, Honsho M, Fujiki Y . Reduction of Ether-Type Glycerophospholipids, Plasmalogens, by NF-κB Signal Leading to Microglial Activation. J Neurosci. 2017; 37(15):4074-4092. PMC: 6596592. DOI: 10.1523/JNEUROSCI.3941-15.2017. View

Hossain M, Ifuku M, Take S, Kawamura J, Miake K, Katafuchi T . Plasmalogens rescue neuronal cell death through an activation of AKT and ERK survival signaling. PLoS One. 2013; 8(12):e83508. PMC: 3869814. DOI: 10.1371/journal.pone.0083508. View

Melo S, Luecke L, Kahlert C, Fernandez A, Gammon S, Kaye J . Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature. 2015; 523(7559):177-82. PMC: 4825698. DOI: 10.1038/nature14581. View

10.

Lydic T, Townsend S, Adda C, Collins C, Mathivanan S, Reid G . Rapid and comprehensive 'shotgun' lipidome profiling of colorectal cancer cell derived exosomes. Methods. 2015; 87:83-95. PMC: 4615275. DOI: 10.1016/j.ymeth.2015.04.014. View

11.

Mapstone M, Cheema A, Fiandaca M, Zhong X, Mhyre T, MacArthur L . Plasma phospholipids identify antecedent memory impairment in older adults. Nat Med. 2014; 20(4):415-8. PMC: 5360460. DOI: 10.1038/nm.3466. View

12.

Wubbolts R, Leckie R, Veenhuizen P, Schwarzmann G, Mobius W, Hoernschemeyer J . Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation. J Biol Chem. 2003; 278(13):10963-72. DOI: 10.1074/jbc.M207550200. View

13.

Planutis A, Holcombe R, Planoutene M, Planoutis K . SW480 colorectal cancer cells that naturally express Lgr5 are more sensitive to the most common chemotherapeutic agents than Lgr5-negative SW480 cells. Anticancer Drugs. 2015; 26(9):942-7. DOI: 10.1097/CAD.0000000000000270. View

14.

Benjamin D, Cozzo A, Ji X, Roberts L, Louie S, Mulvihill M . Ether lipid generating enzyme AGPS alters the balance of structural and signaling lipids to fuel cancer pathogenicity. Proc Natl Acad Sci U S A. 2013; 110(37):14912-7. PMC: 3773741. DOI: 10.1073/pnas.1310894110. View

15.

Doria M, Cotrim C, Simoes C, Macedo B, Domingues P, Domingues M . Lipidomic analysis of phospholipids from human mammary epithelial and breast cancer cell lines. J Cell Physiol. 2012; 228(2):457-68. DOI: 10.1002/jcp.24152. View

16.

Valli A, Rodriguez M, Moutsianas L, Fischer R, Fedele V, Huang H . Hypoxia induces a lipogenic cancer cell phenotype via HIF1α-dependent and -independent pathways. Oncotarget. 2015; 6(4):1920-41. PMC: 4385826. DOI: 10.18632/oncotarget.3058. View

17.

Ferreira da Silva T, Eira J, Lopes A, Malheiro A, Sousa V, Luoma A . Peripheral nervous system plasmalogens regulate Schwann cell differentiation and myelination. J Clin Invest. 2014; 124(6):2560-70. PMC: 4038568. DOI: 10.1172/JCI72063. View

18.

Johnson S, Gulhati P, Rampy B, Han Y, Rychahou P, Doan H . Novel expression patterns of PI3K/Akt/mTOR signaling pathway components in colorectal cancer. J Am Coll Surg. 2010; 210(5):767-76, 776-8. PMC: 2895913. DOI: 10.1016/j.jamcollsurg.2009.12.008. View

19.

Gaposchkin D, Zoeller R . Plasmalogen status influences docosahexaenoic acid levels in a macrophage cell line. Insights using ether lipid-deficient variants. J Lipid Res. 1999; 40(3):495-503. View

20.

Zhou X, Mao J, Ai J, Deng Y, Roth M, Pound C . Identification of plasma lipid biomarkers for prostate cancer by lipidomics and bioinformatics. PLoS One. 2012; 7(11):e48889. PMC: 3495963. DOI: 10.1371/journal.pone.0048889. View