Biophysical analysis of the plant-specific GIPC sphingolipids reveals multiple modes of membrane regulation
2021; Elsevier BV; Volume: 296; Linguagem: Inglês
10.1016/j.jbc.2021.100602
ISSN1083-351X
AutoresAdiilah Mamode Cassim, Yotam Navon, Yu Gao, Marion Décossas, Laëtitia Fouillen, Axelle Grélard, Minoru Nagano, Olivier Lambert, Delphine Bahammou, Pierre Van Delft, Lilly Maneta-Peyret, Françoise Simon-Plas, Laurent Heux, Bruno Jean, Giovanna Fragneto, Jenny C. Mortimer, Magali Deleu, Laurence Lins, Sébastien Mongrand,
Tópico(s)Cellular transport and secretion
ResumoThe plant plasma membrane (PM) is an essential barrier between the cell and the external environment, controlling signal perception and transmission. It consists of an asymmetrical lipid bilayer made up of three different lipid classes: sphingolipids, sterols, and phospholipids. The glycosyl inositol phosphoryl ceramides (GIPCs), representing up to 40% of total sphingolipids, are assumed to be almost exclusively in the outer leaflet of the PM. However, their biological role and properties are poorly defined. In this study, we investigated the role of GIPCs in membrane organization. Because GIPCs are not commercially available, we developed a protocol to extract and isolate GIPC-enriched fractions from eudicots (cauliflower and tobacco) and monocots (leek and rice). Lipidomic analysis confirmed the presence of trihydroxylated long chain bases and 2-hydroxylated very long-chain fatty acids up to 26 carbon atoms. The glycan head groups of the GIPCs from monocots and dicots were analyzed by gas chromatograph–mass spectrometry, revealing different sugar moieties. Multiple biophysics tools, namely Langmuir monolayer, ζ-Potential, light scattering, neutron reflectivity, solid state 2H-NMR, and molecular modeling, were used to investigate the physical properties of the GIPCs, as well as their interaction with free and conjugated phytosterols. We showed that GIPCs increase the thickness and electronegativity of model membranes, interact differentially with the different phytosterols species, and regulate the gel-to-fluid phase transition during temperature variations. These results unveil the multiple roles played by GIPCs in the plant PM. The plant plasma membrane (PM) is an essential barrier between the cell and the external environment, controlling signal perception and transmission. It consists of an asymmetrical lipid bilayer made up of three different lipid classes: sphingolipids, sterols, and phospholipids. The glycosyl inositol phosphoryl ceramides (GIPCs), representing up to 40% of total sphingolipids, are assumed to be almost exclusively in the outer leaflet of the PM. However, their biological role and properties are poorly defined. In this study, we investigated the role of GIPCs in membrane organization. Because GIPCs are not commercially available, we developed a protocol to extract and isolate GIPC-enriched fractions from eudicots (cauliflower and tobacco) and monocots (leek and rice). Lipidomic analysis confirmed the presence of trihydroxylated long chain bases and 2-hydroxylated very long-chain fatty acids up to 26 carbon atoms. The glycan head groups of the GIPCs from monocots and dicots were analyzed by gas chromatograph–mass spectrometry, revealing different sugar moieties. Multiple biophysics tools, namely Langmuir monolayer, ζ-Potential, light scattering, neutron reflectivity, solid state 2H-NMR, and molecular modeling, were used to investigate the physical properties of the GIPCs, as well as their interaction with free and conjugated phytosterols. We showed that GIPCs increase the thickness and electronegativity of model membranes, interact differentially with the different phytosterols species, and regulate the gel-to-fluid phase transition during temperature variations. These results unveil the multiple roles played by GIPCs in the plant PM. The plant plasma membrane (PM) contains three main classes of lipids: phytosterols, sphingolipids, and phospholipids, all with a high level of molecular complexity, see (1Cacas J.L. Buré C. Grosjean K. Gerbeau-Pissot P. Lherminier J. Rombouts Y. Maes E. Bossard C. Gronnier J. Furt F. Fouillen L. Germain V. Bayer E. Cluzet S. 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In animal, sphingolipids are highly studied for their involvement in human health and pathologies (4Hannun Y.A. Obeid L.M. Sphingolipids and their metabolism in physiology and disease.Nat. Rev. Mol. Cell Biol. 2018; 19: 175-191Crossref PubMed Scopus (781) Google Scholar). The most abundant sphingolipid in animal is sphingomyelin (SM) and gangliosides. In plants and fungi, they are absent, whereas other complex lipids comprised of sphingoid bases bound to glycan groups are part of the most abundant sphingolipid. The major sphingolipid subclass of sphingolipids in plants is the glycosyl inositol phosphoryl ceramides (GIPCs). GIPCs were discovered in plants and fungi during the 1950s (5Carter H.E. Gigg R.H. Law J.H. Nakayama T. Weber E. Biochemistry of the sphingolipides. XI. Structure of phytoglycolipide.J. Biol. Chem. 1958; 233: 1309-1314Abstract Full Text PDF PubMed Google Scholar). 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Fast screening of highly glycosylated plant sphingolipids by tandem mass spectrometry.Rapid Commun. Mass Spectrom. 2011; 25: 3131-3145Crossref PubMed Scopus (67) Google Scholar). The GIPC head group linked to the ceramide consists of a phosphate bound to an inositol, forming the inositol phosphoryl ceramide (IPC) backbone, which is then further substituted with further sugar moieties. A broad study of the GIPC polar heads of 23 plant species from algae to monocots showed that polar head structures are largely unknown and vary widely across different biological taxa (8Cacas J.L. Buré C. Furt F. Maalouf J.P. Badoc A. Cluzet S. Schmitter J.M. Antajan E. Mongrand S. Biochemical survey of the polar head of plant glycosylinositolphosphoceramides unravels broad diversity.Phytochemistry. 2013; 96: 191-200Crossref PubMed Scopus (54) Google Scholar). GIPCs are classified into series, based on the degree of glycosylation of their polar head group (7Buré C. Cacas J.L. Wang F. Gaudin K. Domergue F. Mongrand S. Schmitter J.M. Fast screening of highly glycosylated plant sphingolipids by tandem mass spectrometry.Rapid Commun. Mass Spectrom. 2011; 25: 3131-3145Crossref PubMed Scopus (67) Google Scholar). In plants, all GIPCs characterized to date have a glucuronic acid (GlcA) as the first sugar on the IPC, followed by at least one more sugar unit of varying identity. For example, GIPC series A is defined as one monosaccharide addition to the GlcA-IPC form (7Buré C. Cacas J.L. Wang F. Gaudin K. Domergue F. Mongrand S. Schmitter J.M. Fast screening of highly glycosylated plant sphingolipids by tandem mass spectrometry.Rapid Commun. Mass Spectrom. 2011; 25: 3131-3145Crossref PubMed Scopus (67) Google Scholar). In the 1960s, the first characterization of a GIPC structure from Nicotiania tabacum (tobacco) was described (9Hsieh T.C. Lester R.L. Laine R.A. Glycophosphoceramides from plants. 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The GIPC extraction method required hundreds of kilograms of plant material and liters of solvents. From the study, the reported series A GIPC still has the best described structure to date: GlcNAc(α1→4)GlcA(α1→2)inositol-1-O-phosphorylceramide, see Figure 1A. Additional sugar moieties were described, such as glucosamine (GlcN), N-acetyl-glucosamine (GlcNAc), arabinose (Ara), galactose (Gal), and mannose (Man), which may lead to observed glycan patterns of three to seven sugars, the so-called GIPC series B to F. It is noteworthy that Kaul and Lester calculated the ratio between carbohydrate/LCB/inositol in purified polyglycosylated GIPCs and showed that they may contain up to 19 to 20 sugars (12Kaul K. Lester R.L. Characterization of inositol-containing phosphosphingolipids from tobacco leaves.Plant Physiol. 1975; 55: 120-129Crossref PubMed Google Scholar), which opens a very large field of investigation. Polyglycosylated GIPCs found in Zea mays (corn) seeds and Erodium display branched polar heads (13Sperling P. Heinz E. Plant sphingolipids: Structural diversity, biosynthesis, first genes and functions.Biochim. Biophys. Acta. 2003; 1632: 1-15Crossref PubMed Scopus (215) Google Scholar, 14Buré C. Cacas J.L. Badoc A. Mongrand S. Schmitter J.M. Branched glycosylated inositolphosphosphingolipid structures in plants revealed by MS3 analysis.J. Mass Spectrom. 2016; 51: 305-308Crossref PubMed Scopus (4) Google Scholar). GIPC series are species- and tissue-specific. In Arabidopsis, the GIPC series A headgroup Man-GlcA-IPC is predominant in leaves and callus (15Mortimer J.C. Yu X. Albrecht S. Sicilia F. Huichalaf M. Ampuero D. Michaelson L.V. Murphy A.M. Matsunaga T. Kurz S. Stephens E. Baldwin T.C. Ishii T. Napier J.A. Weber A.P. et al.Abnormal glycosphingolipid mannosylation triggers salicylic acid-mediated responses in Arabidopsis.Plant Cell. 2013; 25: 1881-1894Crossref PubMed Scopus (73) Google Scholar, 16Fang L. Ishikawa T. Rennie E.A. Murawska G.M. Lao J. Yan J. Tsai A.Y. Baidoo E.E. Xu J. Keasling J.D. Demura T. Kawai-Yamada M. Scheller H.V. Mortimer J.C. Loss of inositol phosphorylceramide sphingolipid mannosylation induces plant immune responses and reduces cellulose content in arabidopsis.Plant Cell. 2016; 28: 2991-3004Crossref PubMed Scopus (46) Google Scholar), whereas a complex array of N-acetyl glycosylated with up to three pentose units are present in pollen (17Luttgeharm K.D. Kimberlin A.N. Cahoon R.E. Cerny R.L. Napier J.A. Markham J.E. Cahoon E.B. Sphingolipid metabolism is strikingly different between pollen and leaf in Arabidopsis as revealed by compositional and gene expression profiling.Phytochemistry. 2015; 115: 121-129Crossref PubMed Scopus (31) Google Scholar). Amino-acylated and N-acylated GIPCs are found in Arabidopsis seeds and oil (18Tellier F. Maia-Grondard A. Schmitz-Afonso I. Faure J.D. Comparative plant sphingolipidomic reveals specific lipids in seeds and oil.Phytochemistry. 2014; 103: 50-58Crossref PubMed Scopus (24) Google Scholar). GlcN(Ac)-GlcA-IPC is mainly found in rice and tobacco (7Buré C. Cacas J.L. Wang F. Gaudin K. Domergue F. Mongrand S. Schmitter J.M. Fast screening of highly glycosylated plant sphingolipids by tandem mass spectrometry.Rapid Commun. Mass Spectrom. 2011; 25: 3131-3145Crossref PubMed Scopus (67) Google Scholar, 19Nagano M. Ishikawa T. Fujiwara M. Fukao Y. Kawano Y. Kawai-Yamada M. Shimamoto K. Plasma membrane microdomains are essential for Rac1-RbohB/H-mediated immunity in rice.Plant Cell. 2016; 28: 1966-1983Crossref PubMed Scopus (74) Google Scholar). In monocots, the predominant GIPC series is series B (7Buré C. Cacas J.L. Wang F. Gaudin K. Domergue F. Mongrand S. Schmitter J.M. Fast screening of highly glycosylated plant sphingolipids by tandem mass spectrometry.Rapid Commun. Mass Spectrom. 2011; 25: 3131-3145Crossref PubMed Scopus (67) Google Scholar), their core structures are yet to be deciphered. The GIPC's polar head is responsible for the high polarity of the GIPC, accounting for its insolubility in traditional lipid extraction solvents, such as chloroform/methanol. Consequently, they are lost in the aqueous phase or at the interface. GIPCs, although one of the fundamental components of the plant PM model, have been poorly studied, in part because of the absence of commercial preparations. Recent evidence has demonstrated that a loss of the glycosylation is lethal (20Rennie E.A. Ebert B. Miles G.P. Cahoon R.E. Christiansen K.M. Stonebloom S. Khatab H. Twell D. Petzold C.J. Adams P.D. Dupree P. Heazlewood J.L. Cahoon E.B. Scheller H.V. Identification of a sphingolipid α-glucuronosyltransferase that is essential for pollen function in Arabidopsis.Plant Cell. 2014; 26: 3314-3325Crossref PubMed Scopus (63) Google Scholar, 21Ishikawa T. Fang L. Rennie E.A. Sechet J. Yan J. Jing B. Moore W. Cahoon E.B. Scheller H.V. Kawai-Yamada M. Mortimer J.C. GLUCOSAMINE INOSITOLPHOSPHORYLCERAMIDTRANSFERASE1 (GINT1) is a GlcNAc-containing glycosylinositol phosphorylceramide glycosyltransferase.Plant Physiol. 2018; 177: 938-952Crossref PubMed Scopus (25) Google Scholar) and that misglycosylation affects both abiotic and biotic stress responses, as reviewed in (22Mortimer J.C. Scheller H.V. Synthesis and function of complex sphingolipid glycosylation.Trends Plant Sci. 2020; 25: 522-524Abstract Full Text Full Text PDF PubMed Scopus (10) Google Scholar). This highlighted the importance of investigating and understanding the chemical structures of these molecules and their functions in membrane organization. Lipids are not homogeneously distributed within the PM bilayers. The lateral partitioning observed in the PM might be because of differential phase behaviors of different lipid species due to specific interactions between their different lipid species (23Kaiser H.J. Lingwood D. Levental I. Sampaio J.L. Kalvodova L. Rajendran L. Simons K. Order of lipid phases in model and plasma membranes.Proc. Natl. Acad. Sci. U. S. A. 2009; 106: 16645-16650Crossref PubMed Scopus (323) Google Scholar). This was reported in model membranes, using biophysical approaches and super resolution microscopy (24Levental I. Veatch S.L. The continuing mystery of lipid rafts.J. Mol. Biol. 2016; 428: 4749-4764Crossref PubMed Scopus (181) Google Scholar). Lipid domains or liquid-ordered (Lo) phases are formed from saturated phospholipids and sphingolipids in the presence of sterol, whereas liquid-disordered phases are formed mainly from unsaturated phospholipids (25Lingwood D. Simons K. 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Plant sterols in "rafts": A better way to regulate me
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