Rapid Movement of Palmitoleic Acid from Phosphatidylcholine to Phosphatidylinositol in Activated Human Monocytes

Overview

Journal Biomolecules

Publisher MDPI

Specialties Biochemistry
Molecular Biology

Date 2024 Jun 27

PMID 38927110

Authors

Miguel A Bermudez

Alvaro Garrido

Laura Pereira

Teresa Garrido

Maria A Balboa

Jesus Balsinde

Affiliations

Soon will be listed here.

Abstract

This work describes a novel route for phospholipid fatty acid remodeling involving the monounsaturated fatty acid palmitoleic acid. When administered to human monocytes, palmitoleic acid rapidly incorporates into membrane phospholipids, notably into phosphatidylcholine (PC). In resting cells, palmitoleic acid remains within the phospholipid pools where it was initially incorporated, showing no further movement. However, stimulation of the human monocytes with either receptor-directed (opsonized zymosan) or soluble (calcium ionophore A23187) agonists results in the rapid transfer of palmitoleic acid moieties from PC to phosphatidylinositol (PI). This is due to the activation of a coenzyme A-dependent remodeling route involving two different phospholipase A enzymes that act on different substrates to generate free palmitoleic acid and lysoPI acceptors. The stimulated enrichment of specific PI molecular species with palmitoleic acid unveils a hitherto-unrecognized pathway for lipid turnover in human monocytes which may play a role in regulating lipid signaling during innate immune activation.

Citing Articles

Bioactive lipid signaling and lipidomics in macrophage polarization: Impact on inflammation and immune regulation.

Rodriguez J, Casas J, Balboa M, Balsinde J Front Immunol. 2025; 16:1550500.

PMID: 40028333 PMC: 11867965. DOI: 10.3389/fimmu.2025.1550500.

References

Yamashita A, Hayashi Y, Nemoto-Sasaki Y, Ito M, Oka S, Tanikawa T . Acyltransferases and transacylases that determine the fatty acid composition of glycerolipids and the metabolism of bioactive lipid mediators in mammalian cells and model organisms. Prog Lipid Res. 2013; 53:18-81. DOI: 10.1016/j.plipres.2013.10.001. View

Fuchs B, Suss R, Teuber K, Eibisch M, Schiller J . Lipid analysis by thin-layer chromatography--a review of the current state. J Chromatogr A. 2010; 1218(19):2754-74. DOI: 10.1016/j.chroma.2010.11.066. View

Rodriguez J, Guijas C, Astudillo A, Rubio J, Balboa M, Balsinde J . Sequestration of 9-Hydroxystearic Acid in FAHFA (Fatty Acid Esters of Hydroxy Fatty Acids) as a Protective Mechanism for Colon Carcinoma Cells to Avoid Apoptotic Cell Death. Cancers (Basel). 2019; 11(4). PMC: 6521239. DOI: 10.3390/cancers11040524. View

Wyatt S, Winters K, Dubbert P . Overweight and obesity: prevalence, consequences, and causes of a growing public health problem. Am J Med Sci. 2006; 331(4):166-74. DOI: 10.1097/00000441-200604000-00002. View

Hayashi D, Mouchlis V, Dennis E . Omega-3 versus Omega-6 fatty acid availability is controlled by hydrophobic site geometries of phospholipase As. J Lipid Res. 2021; 62:100113. PMC: 8551542. DOI: 10.1016/j.jlr.2021.100113. View

Chan K, Pillon N, Sivaloganathan D, Costford S, Liu Z, Theret M . Palmitoleate Reverses High Fat-induced Proinflammatory Macrophage Polarization via AMP-activated Protein Kinase (AMPK). J Biol Chem. 2015; 290(27):16979-88. PMC: 4505442. DOI: 10.1074/jbc.M115.646992. View

Lebrero P, Astudillo A, Rubio J, Fernandez-Caballero L, Kokotos G, Balboa M . Cellular Plasmalogen Content Does Not Influence Arachidonic Acid Levels or Distribution in Macrophages: A Role for Cytosolic Phospholipase Aγ in Phospholipid Remodeling. Cells. 2019; 8(8). PMC: 6721556. DOI: 10.3390/cells8080799. View

Otto A, Gan-Schreier H, Zhu X, Tuma-Kellner S, Staffer S, Ganzha A . Group VIA phospholipase A2 deficiency in mice chronically fed with high-fat-diet attenuates hepatic steatosis by correcting a defect of phospholipid remodeling. Biochim Biophys Acta Mol Cell Biol Lipids. 2019; 1864(5):662-676. DOI: 10.1016/j.bbalip.2019.01.012. View

Lopez S, Bermudez B, Montserrat-de la Paz S, Jaramillo S, Varela L, Ortega-Gomez A . Membrane composition and dynamics: a target of bioactive virgin olive oil constituents. Biochim Biophys Acta. 2014; 1838(6):1638-56. DOI: 10.1016/j.bbamem.2014.01.007. View

10.

Ono T, Yamada K, Chikazawa Y, Ueno M, Nakamoto S, Okuno T . Characterization of a novel inhibitor of cytosolic phospholipase A2alpha, pyrrophenone. Biochem J. 2002; 363(Pt 3):727-35. PMC: 1222525. DOI: 10.1042/0264-6021:3630727. View

11.

Balboa M, Saez Y, Balsinde J . Calcium-independent phospholipase A2 is required for lysozyme secretion in U937 promonocytes. J Immunol. 2003; 170(10):5276-80. DOI: 10.4049/jimmunol.170.10.5276. View

12.

Lands W . Stories about acyl chains. Biochim Biophys Acta. 1999; 1483(1):1-14. DOI: 10.1016/s1388-1981(99)00177-8. View

13.

Astudillo A, Balboa M, Balsinde J . Compartmentalized regulation of lipid signaling in oxidative stress and inflammation: Plasmalogens, oxidized lipids and ferroptosis as new paradigms of bioactive lipid research. Prog Lipid Res. 2022; 89:101207. DOI: 10.1016/j.plipres.2022.101207. View

14.

Balboa M, Balsinde J, Dillon D, Carman G, Dennis E . Proinflammatory macrophage-activating properties of the novel phospholipid diacylglycerol pyrophosphate. J Biol Chem. 1998; 274(1):522-6. DOI: 10.1074/jbc.274.1.522. View

15.

Cao H, Gerhold K, Mayers J, Wiest M, Watkins S, Hotamisligil G . Identification of a lipokine, a lipid hormone linking adipose tissue to systemic metabolism. Cell. 2008; 134(6):933-44. PMC: 2728618. DOI: 10.1016/j.cell.2008.07.048. View

16.

Ntambi J, Miyazaki M . Regulation of stearoyl-CoA desaturases and role in metabolism. Prog Lipid Res. 2003; 43(2):91-104. DOI: 10.1016/s0163-7827(03)00039-0. View

17.

Chakravarthy M, Lodhi I, Yin L, Malapaka R, Xu H, Turk J . Identification of a physiologically relevant endogenous ligand for PPARalpha in liver. Cell. 2009; 138(3):476-88. PMC: 2725194. DOI: 10.1016/j.cell.2009.05.036. View

18.

BLIGH E, Dyer W . A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959; 37(8):911-7. DOI: 10.1139/o59-099. View

19.

Gijon M, Spencer D, Siddiqi A, Bonventre J, Leslie C . Cytosolic phospholipase A2 is required for macrophage arachidonic acid release by agonists that Do and Do not mobilize calcium. Novel role of mitogen-activated protein kinase pathways in cytosolic phospholipase A2 regulation. J Biol Chem. 2000; 275(26):20146-56. DOI: 10.1074/jbc.M908941199. View

20.

Dernini S, Berry E . Mediterranean Diet: From a Healthy Diet to a Sustainable Dietary Pattern. Front Nutr. 2015; 2:15. PMC: 4518218. DOI: 10.3389/fnut.2015.00015. View