Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-19T23:38:33.292Z Has data issue: false hasContentIssue false
  • English
  • Français

Sphingolipid transfer proteins defined by the GLTP-fold

Published online by Cambridge University Press:  23 March 2015

Lucy Malinina ,
Dhirendra K. Simanshu ,
Xiuhong Zhai ,
Valeria R. Samygina ,
RaviKanth Kamlekar ,
Roopa Kenoth ,
Borja Ochoa-Lizarralde ,
Margarita L. Malakhova ,
Julian G. Molotkovsky  and
Dinshaw J. Patel
...Show all authors
Lucy Malinina*
Affiliation:
The Hormel Institute, University of Minnesota, Austin, MN 55912, USA Structural Biology Unit, CICbioGUNE, Technology Park of Bizkaia, 48160 Derio-Bilbao, Spain
Dhirendra K. Simanshu
Affiliation:
Structural Biology Program, Memorial Sloan-Kettering Cancer Center, New York, NY 10065, USA
Xiuhong Zhai
Affiliation:
The Hormel Institute, University of Minnesota, Austin, MN 55912, USA
Valeria R. Samygina
Affiliation:
Structural Biology Unit, CICbioGUNE, Technology Park of Bizkaia, 48160 Derio-Bilbao, Spain
RaviKanth Kamlekar
Affiliation:
The Hormel Institute, University of Minnesota, Austin, MN 55912, USA
Roopa Kenoth
Affiliation:
The Hormel Institute, University of Minnesota, Austin, MN 55912, USA
Borja Ochoa-Lizarralde
Affiliation:
Structural Biology Unit, CICbioGUNE, Technology Park of Bizkaia, 48160 Derio-Bilbao, Spain
Margarita L. Malakhova
Affiliation:
The Hormel Institute, University of Minnesota, Austin, MN 55912, USA
Julian G. Molotkovsky
Affiliation:
Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, Moscow, Russia
Dinshaw J. Patel*
Affiliation:
Structural Biology Program, Memorial Sloan-Kettering Cancer Center, New York, NY 10065, USA
Rhoderick E. Brown*
Affiliation:
The Hormel Institute, University of Minnesota, Austin, MN 55912, USA
*
*Authors for correspondence: Lucy Malinina, Dinshaw J. Patel, Rhoderick E. Brown. E-mails: [email protected], [email protected], [email protected]
*Authors for correspondence: Lucy Malinina, Dinshaw J. Patel, Rhoderick E. Brown. E-mails: [email protected], [email protected], [email protected]
*Authors for correspondence: Lucy Malinina, Dinshaw J. Patel, Rhoderick E. Brown. E-mails: [email protected], [email protected], [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Glycolipid transfer proteins (GLTPs) originally were identified as small (~24 kDa), soluble, amphitropic proteins that specifically accelerate the intermembrane transfer of glycolipids. GLTPs and related homologs now are known to adopt a unique, helically dominated, two-layer ‘sandwich’ architecture defined as the GLTP-fold that provides the structural underpinning for the eukaryotic GLTP superfamily. Recent advances now provide exquisite insights into structural features responsible for lipid headgroup selectivity as well as the adaptability of the hydrophobic compartment for accommodating hydrocarbon chains of differing length and unsaturation. A new understanding of the structural versatility and evolutionary premium placed on the GLTP motif has emerged. Human GLTP-motifs have evolved to function not only as glucosylceramide binding/transferring domains for phosphoinositol 4-phosphate adaptor protein-2 during glycosphingolipid biosynthesis but also as selective binding/transfer proteins for ceramide-1-phosphate. The latter, known as ceramide-1-phosphate transfer protein, recently has been shown to form GLTP-fold while critically regulating Group-IV cytoplasmic phospholipase A2 activity and pro-inflammatory eicosanoid production.

Type
Review Article
Information
Quarterly Reviews of Biophysics , Volume 48 , Issue 3 , August 2015 , pp. 281 - 322
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

†

Present address: Frederick National Laboratory of National Cancer Institute, Frederick, MD, USA.

‡

Present address: Institute of Crystallography RAS, Leninsky pr.59, 119333 Moscow, Russia.

§

Present address: Environmental & Analytical Chemistry Division, School of Advanced Sciences, VIT University, Vellore-632014, TN, India.

References

12 References

Abe, A. & Sasaki, T. (1985). Purification and some properties of the glycolipid transfer protein from pig brain. The Journal of Biological Chemistry 260, 11231–11239.Google Scholar
Abe, A. & Sasaki, T. (1989a). Formation of an intramolecular disulfide bond of glycolipid transfer protein. Biochimica et Biophysica Acta 985, 45–50.Google Scholar
Abe, A. & Sasaki, T. (1989b). Sulfhydryl groups in glycolipid transfer protein: formation of an intramolecular disulfide bond and oligomers by Cu2+-catalyzed oxidation. Biochimica et Biophysica Acta 985, 38–44.Google Scholar
Abe, A., Yamada, K. & Sasaki, T. (1982). A protein purified from pig brain accelerates the intermembranous translocation of mono- and dihexosylceramides, but not the translocation of phospholipids. Biochemical and Biophysical Research Communications 104, 1386–1393.Google Scholar
Airenne, T. T., Kidron, H., Nymalm, Y., Nylund, M., West, G. P., Mattjus, P. & Salminen, T. A. (2006). Structural evidence for adaptive ligand binding of glycolipid transfer protein. Journal of Molecular Biology 355, 224–236.Google Scholar
Alpy, F. & Tomasetto, C. (2005). Give lipids a START: the StAR-related lipid transfer (START) domain in mammals. Journal of Cell Science 118, 2791–2801.Google Scholar
Aubert-Jousset, E., Garmy, N., Sbarra, V., Fantini, J., Sadoulet, M.-O. & Lombardo, D. (2004). The combinatorial extension method reveals a sphingolipid binding domain on pancreatic bile salt-dependent lipase: role in secretion. Structure 12, 1437–1447.Google Scholar
Bastiaans, E., Debets, A. J. M., Aanen, D. K., van Diepeningen, A. D., Saupe, S. J. & Paoletti, M. (2014). Natural variation of heterokaryon incompatibility gene het-c2 in Podospora anserina reveals diversifying selection. Molecular Biology and Evolution 31, 962–974.Google Scholar
Bazzi, M. D., Youakim, M. A. & Nelsestuen, G. L. (1992). Importance of phosphatidylethanolamine for association of protein kinase C and other cytoplasmic proteins with membranes? Biochemistry 31, 1125–1134.Google Scholar
Berna, A., Bernier, F., Chabriere, E., Perera, T. & Scott, K. (2008). DING proteins; novel members of a prokaryotic phosphate-binding protein superfamily which extends into the eukaryotic kingdom. The International Journal of Biochemistry & Cell Biology 40, 170–175.Google Scholar
Berna, A., Bernier, F., Chabriere, E., Elias, M., Scott, K. & Suh, A. (2009). For whom the bell tolls? DING proteins in health and disease. Cellular and Molecular Life Sciences 66, 2205–2218.Google Scholar
Blind, R. D., Sabling, E. P., Kuchenbecker, K. M., Chiu, H.-J., Deacon, A. M., Das, D., Fletterick, R. J. & Ingraham, H. A. (2014). The signaling phospholipid PIP3 creates a new interaction surface on the nuclear receptor SF-1. Proceedings of the National Academy of Sciences of the United States of America 111, 15054–15059.Google Scholar
Bornancin, F. (2011). Ceramide kinase: the first decade. Cellular Signaling 23, 999–1008.Google Scholar
Bourquin, F., Riezman, H., Capitani, G. & Grutter, M. G. (2010). Structure and function of sphingosine-1-phosphate lyase, a key enzyme of sphingolipid metabolism. Structure 18, 1054–1065.Google Scholar
Breslow, D. K. & Weissman, J. S. (2010). Membranes in balance: mechanisms of sphingolipid homeostasis. Molecular Cell 40, 267–279.Google Scholar
Brodersen, P., Malinovsky, F. G., Hématy, K., Newman, M. A. & Mundy, J. (2005). The role of salicylic acid in the induction of cell death in Arabidopsis acd11. Plant Physiology 138, 1037–1045.Google Scholar
Brodersen, P., Petersen, M., Pike, H. M., Olszak, B., Skov, S., Odum, N., Jorgensen, L. B., Brown, R. E. & Mundy, J. (2002). Knockout of Arabidopsis accelerated-cell-death 11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense. Genes & Development 16, 490–502.Google Scholar
Brown, M. F. (2012). Curvature forces in membrane lipid–protein interactions. Biochemistry 51, 9782–9795.Google Scholar
Brown, R. E. & Brockman, H. L. (2007). Using monomolecular films to characterize lipid lateral interactions. Methods in Molecular Biology 398, 41–58.Google Scholar
Brown, R. E. & Mattjus, P. (2007). Glycolipid transfer proteins. Biochimica et Biophysica Acta 1771, 746–760.Google Scholar
Brown, R. E., Jarvis, K. L. & Hyland, K. J. (1990). Purification and characterization of glycolipid transfer protein from bovine brain. Biochimica et Biophysica Acta 1044, 77–83.Google Scholar
Brown, R. E., Stephenson, F. A., Markello, T., Barenholz, Y. & Thompson, T. E. (1985). Properties of a specific glycolipid transfer protein from bovine brain. Chemistry and Physics of Lipids 38, 79–93.Google Scholar
Bruhn, H. (2005). A short guided tour through functional and structural features of saposin-like proteins. Biochemical Journal 389, 249–257.Google Scholar
Chakravarty, B., Gu, Z., Chirala, S. S., Wakil, S. J. & Quiocho, F. A. (2004). Human fatty acid synthase: structure and substrate selectivity of the thioesterase domain. Proceedings of the National Academy of Sciences of the United States of America 101, 15567–15572.Google Scholar
Cho, W. & Stahelin, R. V. (2005). Membrane-protein interactions in cell signaling and membrane trafficking. Annual Reviews of Biophysics and Biomolecular Structure 34, 119–151.Google Scholar
Chong, S. S. Y., Taneva, S. G., Lee, J. M. C. & Cornell, R. B. (2014). The curvature sensitivity of a membrane-binding amphipathic helix can be modulated by the charge on a flanking region. Biochemistry 53, 450–461.Google Scholar
D'Angelo, G., Polishchuk, E., Di Tullio, G., Santoro, M., Di Campli, A., Godi, A., West, G., Bielawski, J., Chuang, C.-C., van der Spoel, A. C., Platt, F. M., Hannun, Y. A., Polishchuk, R., Mattjus, P. & De Matteis, M. A. (2007). Glycosphingolipid synthesis requires FAPP2 transfer of glucosylceramide. Nature 449, 62–67.Google Scholar
D'Angelo, G., Uemura, T., Chuang, C.-C., Polishchuk, E., Santoro, M., Ohvo-Rekilä, H., Sato, T., Di Tullio, G., Varriale, A., D'Auria, S., Daniele, T., Capuani, F., Johannes, L., Mattjus, P., Monti, M., Pucci, P., Williams, R. L., Burke, J. E., Platt, F. M., Harada, A. & De Matteis, M. A. (2013). Vesicular and non-vesicular transport feed distinct glycosylation pathways in the Golgi. Nature 501, 116–121.Google Scholar
De Libero, G. & Mori, L. (2012). Novel insights into lipid antigen presentation. Trends in Immunology 33, 103–111.Google Scholar
Drin, G. (2014). Topological regulation of lipid balance in cells. Annual Review of Biochemistry 83, 51–77.Google Scholar
Diehl, C., Engström, O., Delaine, T., Håkansson, M., Genheden, S., Modig, K., Leffler, H., Ryde, U., Nilsson, U. J. & Akke, M. (2010). Protein flexibility and conformational entropy in ligand design targeting the carbohydrate recognition domain of Galectin-3. Journal of the American Chemical Society 132, 14577–14589.Google Scholar
Dougherty, D. A. (2013). The cation-π interaction. Accounts of Chemical Research 46, 885–893.Google Scholar
Dowhan, W. & Bogdanov, M. (2009). Lipid-dependent membrane protein topogenesis. Annual Review of Biochemistry 78, 515–540.Google Scholar
Egli, M. (2010). On stacking. In Structure and Function (ed. Comba, P.), Heidelberg, Germany: Springer, 177–196.Google Scholar
Fedorova, N. D., Badger, J. H., Robson, G. D., Wortman, J. R. & Nierman, W. C. (2005). Comparative analysis of programmed cell death pathways in filamentous fungi. BMC Genomics 6, e177.Google Scholar
Frolov, V. A., Shnyrova, A. V. & Zimmerberg, J. (2011). Lipid polymorphisms and membrane shape. Cold Spring Harbor Perspectives in Biology 3, a004747.Google Scholar
Furuita, K., Jee, J., Fukada, H., Mishima, M. & Kojima, C. (2010). Electrostatic interaction between oxysterol-binding protein and VAMP-associated protein A revealed by NMR and mutagenesis studies. The Journal of Biological Chemistry 285, 12961–12970.Google Scholar
Gallivan, J. P. & Dougherty, D. A. (1999). Cation-π interactions in structural biology. Proceedings of the National Academy of Sciences of the United States of America 96, 9459–9464.Google Scholar
Gammon, C. M., Vaswani, K. K. & Ledeen, R. E. (1987). Isolation of two glycolipid transfer proteins from bovine brain: reactivity towards gangliosides and neutral glycosphingolipids. Biochemistry 26, 6239–6243.Google Scholar
Gao, Y., Chung, T., Zou, X., Pike, H. M. & Brown, R. E. (2010). Human glycolipid transfer protein (GLTP) expression modulates cell shape. Public Library of Science ONE 6, e19990.Google Scholar
Garzón, D., Anselmi, C., Bond, P. J. & Faraldo-Gómez, J. D. (2013). Dynamics of the antigen-binding grooves in CD1 protein: reversible hydrophobic collapse in the lipid-free state. The Journal of Biological Chemistry 288, 19528–19536.Google Scholar
Glass, N. L. & Kaneko, I. (2003). Fatal attraction: nonself recognition and heterokaryon incompatibility in filamentous fungi. Eukaryotic Cell 2, 1–8.Google Scholar
Grzyb, J., Latowski, D. & Strzaika, K. (2006). Lipocalins – a family portrait. Journal of Plant Physiology 163, 895–915.Google Scholar
Halter, D., Neumann, S., van Dijk, S. M., Wolthoorn, J., de Maziere, A. M., Vieira, O. V., Mattjus, P., Klumperman, J., van Meer, G. & Sprong, H. (2007). Pre- and post-Golgi translocation of glucosylceramide in glycosphingolipid synthesis. The Journal of Cell Biology 179, 101–115.Google Scholar
Hamilton, J. A. (2004). Fatty acid interactions with proteins: what X-ray crystal and NMR solution structures tell us. Progress in Lipid Research 43, 177–199.Google Scholar
Hanada, K. (2006). Discovery of the molecular machinery CERT for endoplasmic reticulum-to-Golgi trafficking of ceramide. Molecular and Cellular Biochemistry 286, 22–31.Google Scholar
Hashikawa, D., Shindou, H., Harayama, T., Ogasawara, R., Suwabe, A. & Shimizu, T. (2013). Identification of Sec14-like 3 as a novel lipid-packing sensor in the lung. The Journal of the Federation of American Societies for Experimental Biology 27, 5131–5140.Google Scholar
Heller, W. T., He, K., Ludtke, S. J., Harroun, T. A. & Huang, H. W. (1997). Effect of changing the size of lipid headgroup on peptide insertion into membranes. Biophysical Journal 73, 239–244.Google Scholar
Hirsch, A. K., Fischer, F. R. & Diederich, F. (2007). Phosphate recognition in structural biology. Angewandte Chemie International Edition 46, 338–352.Google Scholar
Hoang, K. C., Malakhov, D., Momsen, W. E. & Brockman, H. L. (2006). Open, microfluidic flow cell for studies of interfacial processes at gas-liquid interfaces. Analytical Chemistry 78, 1657–1664.Google Scholar
Holthuis, J. C. M. & Menon, A. K. (2014). Lipid landscapes and pipelines in membrane homeostasis. Nature 510, 48–57.Google Scholar
Huang, K. C. & Ramamurthi, K. S. (2010). Macromolecules that prefer their membranes curvy. Molecular Microbiology 76, 822–832.Google Scholar
Kaiser, S. E., Brickner, J. H., Reilein, A. R., Fenn, T. D., Walter, P. & Brunger, A. T. (2005). Structural basis of FFAT motif-mediated ER targeting. Structure 13, 1035–1045.Google Scholar
Kamlekar, R.-K., Gao, Y. -G., Kenoth, R., Molotkovsky, J. G., Prendergast, F. G., Malinina, L., Patel, D. J., Wessels, W. S., Venyaminov, S. Y. & Brown, R. E. (2010). Human GLTP: three distinct functions for the three tryptophans in a novel peripheral amphitropic fold. Biophysical Journal 99, 2626–2635.Google Scholar
Kamlekar, R.-K., Simanshu, D. K., Gao, Y. -G., Kenoth, R., Pike, H. M., Prendergast, F. G., Malinina, L., Molotkovsky, J. G., Venyaminov, S. Y., Patel, D. J. & Brown, R. E. (2013). The glycolipid transfer protein (GLTP) domain of phosphoinositol 4-phosphate adaptor protein-2 (FAPP2): structure drives preference for simple neutral glycosphingolipids. Biochimica et Biophysica Acta 1831, 417–427.Google Scholar
Kawano, M., Kumagai, K., Nishijima, M. & Hanada, K. (2006). Efficient trafficking of ceramide from the endoplasmic reticulum to the Golgi apparatus requires a VAMP-associated protein-interacting FFAT motif of CERT. The Journal of Biological Chemistry 281, 30279–30288.Google Scholar
Kenoth, R., Kamlekar, R.-K., Simanshu, D. K., Gao, Y., Malinina, L., Prendergast, F. G., Molotkovsky, J. G., Patel, D. J., Venyaminov, S. Y. & Brown, R. E. (2011). Conformational folding and stability of the HET-C2 glycolipid transfer protein fold: Does a molten globule-like state regulate activity? Biochemistry 50, 5163–5171.Google Scholar
Kenoth, R., Simanshu, D. K., Kamlekar, R.-K., Pike, H. M., Molotkovsky, J. G., Benson, L. M., Bergen, H. R. III, Prendergast, F. G., Malinina, L., Venyaminov, S. Y., Patel, D. J. & Brown, R. E. (2010). Structural determination and tryptophan fluorescence of heterokaryon incompatibility C2 protein (HET-C2), a fungal glycolipid transfer protein (GLTP), provide novel insights into glycolipid specificity and membrane interaction by the GLTP fold. The Journal of Biological Chemistry 285, 13066–13078.Google Scholar
Khan, I., Katikaneni, D. S., Han, Q., Sanchez-Felipe, L., Hanada, K., Ambrose, R. L., Mackenzie, J. M. & Konan, K. V. (2014). Modulation of hepatitis C virus genome replication by glycosphingolipids and four-phosphate adaptor protein 2. Journal of Virology 88, 12276–12295.Google Scholar
Killian, J. A. & von Heijne, G. (2000). How proteins adapt to a membrane-water interface. Trends in Biochemical Sciences 25, 429–434.Google Scholar
Kjellberg, M. A., Backman, A. P. E., Ohvo-Rekilä, H. & Mattjus, P. (2014). Alternation in the glycolipid transfer protein expression causes changes in the cellular lipidome. Public Library of Science ONE 9, e97263.Google Scholar
Kjellberg, M. A. & Mattjus, P. (2013). Glycolipid transfer protein expression is affected by glycosphingolipid synthesis. Public Library of Science ONE 8, e70283.Google Scholar
Kolter, T. (2012). Ganglioside biochemistry. International Scholarly Research Notices Biochemistry 2012, e506160 Google Scholar
Kolter, T., Winau, F., Schaible, U. E., Leippe, M. & Sandhoff, K. (2005). Lipid-binding proteins in membrane digestion, antigen presentation, and antimicrobial defense. The Journal of Biological Chemistry 280, 41125–41128.Google Scholar
Kono, N., Ohto, U., Hiramatsu, T., Urabe, M., Uchida, Y., Satow, Y. & Arai, H. (2013). Impaired α-TTP-PIPs interaction underlies familial vitamin E deficiency. Science 340, 1106–1110.Google Scholar
Kudo, N., Kumagai, K., Tomishige, N., Yamaji, T., Wakatsuki, S., Nishijima, M., Hanada, K. & Kato, R. (2008). Structural basis for specific lipid recognition by CERT responsible for nonvesicular trafficking of ceramide. Proceedings of the National Academy of Sciences of the United States of America 105, 488–493.Google Scholar
Kutateladze, T. G. (2010). Translation of the phosphoinositide code by PI effectors. Nature Chemical Biology 6, 507–513.Google Scholar
Laughrey, Z. R., Kiehna, S. E., Riemen, A. J. & Waters, M. L. (2008). Carbohydrate-π interactions: what are they worth? Journal of American Chemical Society 130, 14625–14633.Google Scholar
Lauria, I., van Ǚüm, J., Mjumjunov-Crncevic, E., Walrafen, D., Spitta, L., Thiele, C. & Lang, T. (2013). GLTP-mediated non-vesicular GM1 transport between native membranes. Public Library of Science ONE 8, e59871.Google Scholar
Lemmon, M. A. (2008). Membrane recognition by phospholipid-binding domains. Nature Reviews Molecular Cell Biology 9, 99–111.Google Scholar
Li, S. J. & Yamazaki, M. (2004). Low concentration of dioleoylphosphatidic acid induces an inverted hexagonal (HII) phase transition in dipalmitoleoylphosphatidylethanolamine membranes. Biophysical Chemistry 109, 149–155.Google Scholar
Li, X. -M., Malakhova, M. L., Lin, X., Pike, H. M., Chung, T., Molotkovsky, J. G. & Brown, R. E. (2004). Human glycolipid transfer protein: probing conformation using fluorescence spectroscopy. Biochemistry 43, 10285–10294.Google Scholar
Lin, X., Mattjus, P., Pike, H. M., Windebank, A. J. & Brown, R. E. (2000). Cloning and expression of glycolipid transfer protein from bovine and porcine brain. Journal of Biological Chemistry 275, 5104–5110.Google Scholar
Loewen, C. J., Roy, A. & Levine, T. P. (2003). A conserved ER targeting motif in three families of lipid binding proteins and in Opi1p binds VAP. European Molecular Biology Organization Journal 22, 2025–2035.Google Scholar
Lomize, A. L., Pogozheva, I. D. & Mosberg, H. I. (2011). Anisotropic solvent model of the lipid bilayer. 2. Energetics of insertion of small molecules, peptides, and proteins in membranes. Journal of Chemical Information and Modeling 51, 930–946.Google Scholar
Luecke, H. & Quiocho, F. A. (1990). High specificity of a phosphate transport protein determined by hydrogen bonds. Nature 347, 402–406.Google Scholar
Luoma, A. M., Castro, C. D. & Adams, E. J. (2014). γδ T cell surveillance via CD1 molecules. Trends in Immunology 35, 613–621.Google Scholar
Maceyka, M. & Spiegel, S. (2014). Sphingolipid metabolites in inflammatory disease. Nature 510, 58–67.Google Scholar
Maeda, K., Anand, K., Chiapparino, A., Kumar, A., Poletto, M., Kaksonen, M.& Gavin, A.-C. (2013). Interactome map uncovers phosphatidylserine transport by oxysterol-binding proteins. Nature 501, 257–261.Google Scholar
Mahfoud, R., Garmy, N., Maresca, M., Yahi, N., Puigserver, A. & Fantini, J. (2002). Identification of a common sphingolipid-binding domain in Alzheimer, prion, and HIV-1 proteins. The Journal of Biological Chemistry 277, 11292–11296.Google Scholar
Malakhova, M. L., Malinina, L., Pike, H. M., Kanack, A. T., Patel, D. J. & Brown, R. E. (2005). Point mutational analysis of the liganding site in human glycolipid transfer protein: functionality of the complex. The Journal of Biological Chemistry 280, 26312–26320.Google Scholar
Malinina, L., Malakhova, M. L., Kanak, A. T., Lu, M., Abagyan, R., Brown, R. E. & Patel, D. J. (2006). The liganding mode of glycolipid transfer protein is controlled by glycosphingolipid structure. Public Library of Science Biology 4, e362.Google Scholar
Malinina, L., Malakhova, M. L., Teplov, A., Brown, R. E. & Patel, D. J. (2004). Structural basis for glycosphingolipid transfer specificity. Nature 430, 1048–1053.Google Scholar
Mattjus, P. (2009). Glycolipid transfer proteins and membrane interaction. Biochimica et Biophysica Acta 1788, 267–272.Google Scholar
Mattjus, P., Molotkovsky, J. G., Smaby, J. M. & Brown, R. E. (1999). A fluorescence resonance energy transfer approach for monitoring protein-mediated glycolipid transfer between vesicle membranes. Analytical Biochemistry 268, 297–304.Google Scholar
Mattjus, P., Pike, H. M., Molotkovsky, J. G. & Brown, R. E. (2000). Charged membrane surfaces impede the protein-mediated transfer of glycosphingolipids between phospholipid bilayers. Biochemistry 39, 1067–1075.Google Scholar
Mattjus, P., Turcq, B., Pike, H. M., Molotkovsky, J. G. & Brown, R. E. (2003). Glycolipid intermembrane transfer is accelerated by HET-C2, a filamentous fungus gene product involved in the cell–cell incompatibility response. Biochemistry 42, 535–542.Google Scholar
McLaughlin, S., Wang, J., Gambhir, A. & Murray, D. (2002). PIP2 and proteins: interactions, organization and information flow. Annual Review of Biophysics and Biomolecular Structure 31, 151–175.Google Scholar
Mesmin, B., Bigay, J., von Filseck, J. M., Lacas-Gervais, S., Drin, G. & Antonny, B. (2013). A four-step cycle driven by PI(4)P hydrolysis directs sterol/PI(4)P exchange by the ER–Golgi tether OSBP. Cell 155, 830–843.Google Scholar
Metz, R. J. & Radin, N. S. (1980). Glucosylceramide uptake from spleen cytosol. The Journal of Biological Chemistry 255, 4463–4467.Google Scholar
Metz, R. J. & Radin, N. S. (1982). Purification and properties of a cerebroside transfer protein. The Journal of Biological Chemistry 257, 12901–12907.Google Scholar
Mikitova, V. & Levine, T. P. (2012). Analysis of the key elements of FFAT-like motifs identifies new proteins that potentially bind VAP on the ER, including two AKAPs and FAPP2. Public Library of Science ONE 7, e30455.Google Scholar
Momsen, W. E., Mizuno, N. K., Lowe, M. E. & Brockman, H. L. (2005). Real-time measurement of solute partitioning to lipid monolayers. Analytical Biochemistry 346, 139–149.Google Scholar
Moody, D. B., Zajonc, D. M. & Wilson, I. A. (2005). Anatomy of CD1-lipid antigen complexes. Nature Reviews Immunology 5, 387–399.Google Scholar
Murray, D., Ben-Tal, N., Honig, B. & McLaughlin, S. (1997). Electrostatic interaction of myristoylated proteins with membranes: simple physics, complicated biology. Structure 5, 985–989.Google Scholar
Neumann, S., Opacic, M., Wechselberger, R. W., Sprong, H. & Egmond, M. R. (2008). Glycolipid transfer protein: clear structure and activity, but enigmatic function. Advances in Enzyme Regulation 48, 137–151.Google Scholar
Ng, T. B., Cheung, R. C. F., Wong, J. H. & Ye, X. (2012). Lipid transfer proteins. Biopolymers (Peptide Science) 98, 268–279.Google Scholar
Nylund, M., Fortelius, C., Palonen, E. K., Molotkovsky, J. G. & Mattjus, P. (2007). Membrane curvature effects on glycolipid transfer protein activity. Langmuir 23, 11726–11733.Google Scholar
Ohvo-Rekilä, H. & Mattjus, P. (2011). Monitoring glycolipid transfer protein activity and membrane interaction with the surface plasmon resonance technique. Biochimica et Biophysica Acta 1808, 47–54.Google Scholar
Olkkonen, V. M. & Li, S. (2013). Oxysterol-binding proteins: sterol and phosphoinositide sensors coordinating transport, signaling and metabolism. Progress in Lipid Research 52, 529–538.Google Scholar
Olmeda, B., Garcıá-Alvarez, B. & Pérez-Gil, J. (2013). Structure–function correlations of pulmonary surfactant protein SP-B and the saposin-like family of proteins. European Biophysics Journal 42, 209–222.Google Scholar
Olsen, J. V., Vermeulen, M., Santamaria, A., Kumar, C., Miller, M. L., Jensen, L. J., Gnad, F., Cox, J., Jensen, T. S., Nigg, E. A., Brunak, S. & Mann, M. (2010). Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Science Signaling 3, ra3.Google Scholar
Paoletti, M., Saupe, S. J. & Clave, C. (2007). Genesis of a fungal non-self recognition repertoire. Public Library of Science One 2, ee283.Google Scholar
Petersen, N. H., McKinney, L. V., Pike, H., Hofius, D., Zakaria, A., Brodersen, P., Petersen, M., Brown, R. E. & Mundy, J. (2008). Human GLTP and mutant forms of ACD11 suppress cell death in the Arabidopsis acd11 mutant. Federation of European Biochemical Societies Journal 275, 4378–4388.Google Scholar
Powl, A. M., East, J. M. & Lee, A. G. (2005). Heterogeneity in the binding of lipid molecules to the surface of a membrane protein: hot spots for anionic lipids on the mechanosensitive channel of large conductance MscL and effects on conformation. Biochemistry 44, 5873–5883.Google Scholar
Quinn, P. J. (2011). The structure of complexes between phosphatidylethanolamine and glucosylceramide: a matrix for membrane rafts. Biochimica et Biophysica Acta 1808, 2894–2904.Google Scholar
Quinn, P. J. (2012). Lipid–lipid interactions in bilayer membranes: married couples and casual liaisons. Progress in Lipid Research 51, 179–198.Google Scholar
Rao, C. S., Chung, T., Pike, H. M. & Brown, R. E. (2005). Glycolipid transfer protein interaction with bilayer vesicles: modulation by changing lipid composition. Biophysical Journal 89, 4017–4028.Google Scholar
Rao, C. S., Lin, X., Pike, H. M., Molotkovsky, J. G. & Brown, R. E. (2004). Glycolipid transfer protein mediated transfer of glycosphingolipids between membranes: a model for action based on kinetic and thermodynamic analyses. Biochemistry 43, 13805–13815.Google Scholar
Ren, J., Lin, C. P. -C., Pathak, M. C., Temple, B. R. S., Nile, A. H., Mousley, C. J., Duncan, M. C., Eckert, D. M., Leiker, T. J., Ivanova, P. T., Myers, D. S., Murphy, R. C., Brown, H. A., Verdaasdonk, J., Bloom, K. S., Ortlund, E. A., Neiman, A. M. & Bankaitis, V. A. (2014). A phosphatidylinositol transfer protein integrates phosphoinositide signaling with lipid droplet metabolism to regulate a developmental program of nutrient stress-induced membrane biogenesis. Molecular Biology of the Cell 25, 712–727.Google Scholar
Rosen, H., Gonzalez-Cabrera, P. J., Sanna, M. G. & Brown, S. (2009). Sphingosine 1-phosphate receptor signaling. Annual Review of Biochemistry 78, 743–768.Google Scholar
Rossmann, M. G., Moras, D. & Olsen, K. W. (1974). Chemical and biological evolution of nucleotide-binding protein. Nature 250, 194–199.Google Scholar
Roulin, P. S., Lötzerich, M., Torta, F., Tanner, L. B., van Kuppeveld, F. J. M., Wenk, M. R. & Greber, U. F. (2014). Rhinovirus uses a phosphatidylinositol 4-phosphate/cholesterol counter-current for the formation of replication compartments at the ER–Golgi interface. Cell Host & Microbe 16, 677–690.Google Scholar
Samygina, V. R., Ochoa-Lizarralde, B., Popov, A. N., Cabo-Bilbao, A., Goni-de-Cerio, F., Molotkovsky, J. G., Patel, D. J., Brown, R. E. & Malinina, L. (2013). Structural insights into lipid-dependent reversible dimerization of human GLTP. Acta Crystallographica, Section D D69, 603–616.Google Scholar
Samygina, V. R., Popov, A. N., Cabo-Bilbao, A., Ochoa-Lizarralde, B., Goni-de-Cerio, F., Zhai, X., Molotkovsky, J. G., Patel, D. J., Brown, R. E. & Malinina, L. (2011). Enhanced selectivity for sulfatide by engineered human glycolipid transfer protein. Structure 19, 1644–1654.Google Scholar
Sandhoff, K. & Harzer, K. (2013). Gangliosides and gangliosidoses: principles of molecular and metabolic pathogenesis. The Journal of Neuroscience 33, 10195–10208.Google Scholar
Saraboji, K., Håkansson, M., Genheden, S., Diehl, C., Qvist, J., Weininger, U., Nilsson, U. J., Leffler, H., Ryde, U., Akke, M. & Logan, D. T. (2012). The carbohydrate-binding site in Galectin-3 Is preorganized to recognize a sugarlike framework of oxygens: ultra-high-resolution structures and water dynamics. Biochemistry 51, 296–306.Google Scholar
Saupe, S. J. (2000). Molecular genetics of heterokaryon incompatibility in filamentous Ascomycetes. Microbiology Molecular Biology Reviews 64, 489–502.Google Scholar
Saupe, S., Descamps, C., Turcq, B. & Begueret, J. (1994). Inactivation of the Podospora anserina vegetative incompatibility locus het-c2, whose product resembles a glycolipid transfer protein, drastically impairs ascospore production. Proceedings of the National Academy of Sciences of the United States of America 91, 5927–5931.Google Scholar
Schulze, H. & Sandhoff, K. (2014). Sphingolipids and lysosomal pathologies. Biochimica et Biophysica Acta 1841, 799–810.Google Scholar
Silk, J. D., Salio, M., Brown, J., Jones, E. Y. & Cerundolo, V. (2008). Structural and functional aspects of lipid binding by CD1 molecules. Annual Review of Cell and Developmental Biology 24, 369–395.Google Scholar
Simanshu, D. K., Kamlekar, R. -K., Wijesinghe, D. S., Zou, X., Zhai, X., Mishra, S. K., Molotkovsky, J. G., Malinina, L., Hinchcliffe, E. H., Chalfant, C. E., Brown, R. E. & Patel, D. J. (2013). Non-vesicular trafficking by a ceramide-1-phosphate transfer protein regulates eicosanoids. Nature 500, 463–468.Google Scholar
Simanshu, D. K., Zhai, X., Munch, D., Hofius, D., Markham, J. E., Bielawski, J., Bielawska, A., Malinina, L., Molotkovsky, J. G., Mundy, J. W., Patel, D. J. & Brown, R. E. (2014). Arabidopsis accelerated cell death 11, ACD11, is a ceramide-1-phosphate transfer protein and intermediary regulator of phytoceramide levels. Cell Reports 6, 388–399.Google Scholar
Stahelin, R. V. (2009). Lipid binding domains: more than simple lipid effectors. The Journal of Lipid Research 50, S299–S304.Google Scholar
Stahelin, R. V. (2014). Identification of ceramide-1-phosphate transport proteins. American Society of Biochemistry and Molecular Biology TODAY 2014, 10–12.Google Scholar
Stahelin, R. V., Scott, J. L. & Frick, C. T. (2014). Cellular and molecular interactions of phosphoinositides and peripheral proteins. Chemistry and Physics of Lipids 182, 3–18.Google Scholar
Stahelin, R. V., Subramanian, P., Vora, M., Cho, W. & Chalfant, C. E. (2007). Ceramide-1-phosphate binds group IVA cytosolic phospholipase A2 via a novel site in the C2 domain. The Journal of Biological Chemistry 282, 20467–20474.Google Scholar
Storch, J. & McDermott, L. (2009). Structural and functional analysis of fatty acid-binding proteins. The Journal of Lipid Research 50, S126–S131.Google Scholar
Sujatha, M. S. & Balaji, P. V. (2004). Identification of common structural features of binding sites in galactose-specific proteins. Proteins: Structure, Function, and Bioinformatics 55, 44–65.Google Scholar
Sujatha, M. S., Sasidhar, Y. U. & Balaji, P. V. (2004). Energetics of galactose- and glucose-aromatic amino acid interactions: implications for binding in galactose-specific proteins. Protein Science 13, 2502–2514.Google Scholar
Thorsell, A.-G., Lee, W. H., Persson, C., Siponen, M. I., Nilsson, M., Busam, R. D., Kotenyova, T., Schüler, H. & Lehtiö, L. (2011). Comparative structural analysis of lipid binding START domains. Public Library of Science ONE 6, e19521.Google Scholar
Tuuf, J. & Mattjus, P. (2007). Human glycolipid transfer protein—intracellular localization and effects on the sphingolipid synthesis. Biochimica et Biophysica Acta 1771, 1353–1363.Google Scholar
Tuuf, J. & Mattjus, P. (2014). Membranes and mammalian glycolipid transferring proteins. Chemistry and Physics of Lipids 178, 27–27.Google Scholar
Tuuf, J., Wistbacka, L. & Mattjus, P. (2009). The glycolipid transfer protein interacts with the vesicle-associated membrane protein associated protein VAP-A. Biochemical and Biophysical Research Communications 388, 395–399.Google Scholar
van den Berg, B., Black, P. N., Clemons, W. M. Jr. & Rapoport, T. A. (2004). Crystal structure of the long-chain fatty acid transporter FadL. Science 304, 1506–1509.Google Scholar
van den Brink-van der Laan, E., Killian, J. A. & de Kruijff, B. (2004). Nonbilayer lipids affect peripheral and integral membrane proteins via changes in the lateral pressure profile. Biochimica et Biophysica Acta 1666, 275–288.Google Scholar
Vyas, N. K., Vyas, M. N. & Quiocho, F. A. (1988). Sugar and signal-transducer binding sites of the Escherichia coli galactose chemoreceptor protein. Science 242, 1290–1295.Google Scholar
Wagner, S. A., Beli, P., Weinert, B. T., Nielsen, M. L., Cox, J., Mann, M. & Choudhary, C. (2011). A proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles. Molecular & Cellular Proteomics 10, M111.Google Scholar
Walker, J. E., Saraste, M., Runswick, M. J. & Gay, N. J. (1982). Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. European Molecular Biology Organization Journal 1, 945–951.Google Scholar
Warnock, D. E., Lutz, M. S., Blackburn, W. A., Young, W. W. Jr. & Baenziger, J. U. (1994). Transport of newly synthesized glucosylceramide to the plasma membrane by a non-Golgi pathway. Proceedings of the National Academy of Sciences of the United States of America 91, 2708–2712.Google Scholar
Weis, W. I. & Drickamer, K. (1996). Structural basis of lectin–carbohydrate interactions. Annual Review of Biochemistry 65, 441–473.Google Scholar
West, G., Nylund, M., Slotte, J. P. & Mattjus, P. (2006). Membrane interaction and activity of the glycolipid transfer protein. Biochimica et Biophysica Acta 1758, 1732–1742.Google Scholar
West, G., Viitanen, L., Alm, C., Mattjus, P., Salminen, T. A. & Edqvist, J. (2008). Identification of a glycosphingolipid transfer protein GLTP1 in Arabidopsis thaliana . Federation of European Biochemical Societies Journal 275, 3421–3437.Google Scholar
White, S. H. & Wimley, W. C. (1998). Hydrophobic interactions of peptides with membrane interfaces. Biochimica et Biophysica Acta 1376, 339–352.Google Scholar
Wojciak, J. M., Zhu, N., Schuerenberg, K. T., Moreno, K., Shestowsky, W. S., Hiraiwa, M., Sabbadini, R. & Huxford, T. (2009). The crystal structure of sphingosine-1-phosphate in complex with a Fab fragment reveals metal bridging of an antibody and its antigen. Proceedings of the National Academy of Sciences of the United States of America 106, 17717–17722.Google Scholar
Wong, M., Brown, R. E., Barenholz, Y. & Thompson, T. E. (1984). Glycolipid transfer protein from bovine brain. Biochemistry 23, 6498–6505.Google Scholar
Wright, C. S., Zhao, Q. & Rastinejad, F. (2003). Structural analysis of lipid complexes of GM2-activator protein. Journal of Molecular Biology 331, 951–964.Google Scholar
Wyles, J. P., McMaster, C. R. & Ridgway, N. D. (2002). Vesicle-associated membrane protein-associated protein-A (VAP-A) interacts with the oxysterol-binding protein to modify export from the endoplasmic reticulum. The Journal of Biological Chemistry 277, 29908–29918.Google Scholar
Yeats, T. H. & Rose, J. K. C. (2008). The biochemistry and biology of extracellular plant lipid transfer proteins (LTPs). Protein Science 17, 191–198.Google Scholar
Yoder, M. D., Thomas, L. M., Tremblay, J. M., Oliver, R. L., Yarbrough, L. R., Helmkamp, G. M. Jr. (2001). Structure of a multifunctional protein. Mammalian phosphatidylinositol transfer protein complexed with phosphatidylcholine. The Journal of Biological Chemistry 276, 9246–9252.Google Scholar
Zhai, X., Malakhova, M., Pike, H. M., Benson, L. M., Bergen, H. R. III, Sugar, I. P., Malinina, L., Patel, D. J. & Brown, R. E. (2009). Glycolipid acquisition by human glycolipid transfer protein dramatically alters intrinsic tryptophan fluorescence: insights into glycolipid binding affinity. The Journal of Biological Chemistry 284, 13620–13628.Google Scholar
Zhai, X., Momsen, W. E., Malakhov, D. A., Boldyrev, I. A., Momsen, M. M., Molotkovsky, J. G., Brockman, H. L.& Brown, R. E. (2013). GLTP-fold interaction with planar phosphatidylcholine surfaces is synergistically stimulated by phosphatidic acid and phosphatidylethanolamine. The Journal of Lipid Research 54, 1103–1113.Google Scholar
Zou, X., Chung, T., Lin, X., Malakhova, M. L., Pike, H. M. & Brown, R. E. (2008). Human glycolipid transfer protein (GLTP) genes: organization, transcriptional status, and evolution. BMC Genomics 9, e72.Google Scholar
Zou, X., Gao, Y., Ruvolo, V. R., Gardner, T. L., Ruvolo, P. P.& Brown, R. E. (2011). Human glycolipid transfer protein gene (GLTP) expression is regulated by Sp1 and Sp3: involvement of the bioactive sphingolipid ceramide. The Journal of Biological Chemistry 286, 1301–1311.Google Scholar