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Structural evidence for adaptive ligand binding of glycolipid transfer protein.

Airenne TT, Kidron H, Nymalm Y, Nylund M, West G, Mattjus P, Salminen TA
J Mol Biol 355 224-36 (2006)
Related entries: 1tfj, 2bv7

Cited: 45 times
EuropePMC logo PMID: 16309699

Abstract

Glycolipids participate in many important cellular processes and they are bound and transferred with high specificity by glycolipid transfer protein (GLTP). We have solved three different X-ray structures of bovine GLTP at 1.4 angstroms, 1.6 angstroms and 1.8 angstroms resolution, all with a bound fatty acid or glycolipid. The 1.4 angstroms structure resembles the recently characterized apo-form of the human GLTP but the other two structures represent an intermediate conformation of the apo-GLTPs and the human lactosylceramide-bound GLTP structure. These novel structures give insight into the mechanism of lipid binding and how GLTP may conformationally adapt to different lipids. Furthermore, based on the structural comparison of the GLTP structures and the three-dimensional models of the related Podospora anserina HET-C2 and Arabidopsis thaliana accelerated cell death protein, ACD11, we give structural explanations for their specific lipid binding properties.

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Reviews citing this publication (7)

  1. Glycolipid transfer proteins. Brown RE, Mattjus P. Biochim Biophys Acta 1771 746-760 (2007)
  2. Glycolipid transfer proteins and membrane interaction. Mattjus P. Biochim Biophys Acta 1788 267-272 (2009)
  3. PLP-dependent enzymes as entry and exit gates of sphingolipid metabolism. Bourquin F, Capitani G, Grütter MG. Protein Sci 20 1492-1508 (2011)
  4. Membranes and mammalian glycolipid transferring proteins. Tuuf J, Mattjus P. Chem Phys Lipids 178 27-37 (2014)
  5. Emerging roles for human glycolipid transfer protein superfamily members in the regulation of autophagy, inflammation, and cell death. Mishra SK, Gao YG, Zou X, Stephenson DJ, Malinina L, Hinchcliffe EH, Chalfant CE, Brown RE. Prog Lipid Res 78 101031 (2020)
  6. How α-Helical Motifs Form Functionally Diverse Lipid-Binding Compartments. Malinina L, Patel DJ, Brown RE. Annu Rev Biochem 86 609-636 (2017)
  7. Sphingolipid-Transporting Proteins as Cancer Therapeutic Targets. Samaha D, Hamdo HH, Wilde M, Prause K, Arenz C. Int J Mol Sci 20 (2019)

Articles citing this publication (29)

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  2. Arabidopsis accelerated cell death 11, ACD11, is a ceramide-1-phosphate transfer protein and intermediary regulator of phytoceramide levels. Simanshu DK, Zhai X, Munch D, Hofius D, Markham JE, Bielawski J, Bielawska A, Malinina L, Molotkovsky JG, Mundy JW, Patel DJ, Brown RE. Cell Rep 6 388-399 (2014)
  3. The liganding of glycolipid transfer protein is controlled by glycolipid acyl structure. Malinina L, Malakhova ML, Kanack AT, Lu M, Abagyan R, Brown RE, Patel DJ. PLoS Biol 4 e362 (2006)
  4. Atomic-resolution conformational analysis of the GM3 ganglioside in a lipid bilayer and its implications for ganglioside-protein recognition at membrane surfaces. DeMarco ML, Woods RJ. Glycobiology 19 344-355 (2009)
  5. Structural and mechanistic analyses of endo-glycoceramidase II, a membrane-associated family 5 glycosidase in the Apo and GM3 ganglioside-bound forms. Caines ME, Vaughan MD, Tarling CA, Hancock SM, Warren RA, Withers SG, Strynadka NC. J Biol Chem 282 14300-14308 (2007)
  6. Identification of a glycosphingolipid transfer protein GLTP1 in Arabidopsis thaliana. West G, Viitanen L, Alm C, Mattjus P, Salminen TA, Edqvist J. FEBS J 275 3421-3437 (2008)
  7. Human GLTP and mutant forms of ACD11 suppress cell death in the Arabidopsis acd11 mutant. Petersen NH, McKinney LV, Pike H, Hofius D, Zakaria A, Brodersen P, Petersen M, Brown RE, Mundy J. FEBS J 275 4378-4388 (2008)
  8. Enhanced selectivity for sulfatide by engineered human glycolipid transfer protein. Samygina VR, Popov AN, Cabo-Bilbao A, Ochoa-Lizarralde B, Goni-de-Cerio F, Zhai X, Molotkovsky JG, Patel DJ, Brown RE, Malinina L. Structure 19 1644-1654 (2011)
  9. Glycolipid acquisition by human glycolipid transfer protein dramatically alters intrinsic tryptophan fluorescence: insights into glycolipid binding affinity. Zhai X, Malakhova ML, Pike HM, Benson LM, Bergen HR, Sugár IP, Malinina L, Patel DJ, Brown RE. J Biol Chem 284 13620-13628 (2009)
  10. 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. Kenoth R, Simanshu DK, Kamlekar RK, Pike HM, Molotkovsky JG, Benson LM, Bergen HR, Prendergast FG, Malinina L, Venyaminov SY, Patel DJ, Brown RE. J Biol Chem 285 13066-13078 (2010)
  11. Human glycolipid transfer protein (GLTP) genes: organization, transcriptional status and evolution. Zou X, Chung T, Lin X, Malakhova ML, Pike HM, Brown RE. BMC Genomics 9 72 (2008)
  12. Sphingolipid transfer proteins defined by the GLTP-fold. Malinina L, Simanshu DK, Zhai X, Samygina VR, Kamlekar R, Kenoth R, Ochoa-Lizarralde B, Malakhova ML, Molotkovsky JG, Patel DJ, Brown RE. Q Rev Biophys 48 281-322 (2015)
  13. Human GLTP: Three distinct functions for the three tryptophans in a novel peripheral amphitropic fold. Kamlekar RK, Gao Y, Kenoth R, Molotkovsky JG, Prendergast FG, Malinina L, Patel DJ, Wessels WS, Venyaminov SY, Brown RE. Biophys J 99 2626-2635 (2010)
  14. The glycolipid transfer protein (GLTP) domain of phosphoinositol 4-phosphate adaptor protein-2 (FAPP2): structure drives preference for simple neutral glycosphingolipids. Kamlekar RK, Simanshu DK, Gao YG, Kenoth R, Pike HM, Prendergast FG, Malinina L, Molotkovsky JG, Venyaminov SY, Patel DJ, Brown RE. Biochim Biophys Acta 1831 417-427 (2013)
  15. Human glycolipid transfer protein gene (GLTP) expression is regulated by Sp1 and Sp3: involvement of the bioactive sphingolipid ceramide. Zou X, Gao Y, Ruvolo VR, Gardner TL, Ruvolo PP, Brown RE. J Biol Chem 286 1301-1311 (2011)
  16. Molecular features of phospholipids that affect glycolipid transfer protein-mediated galactosylceramide transfer between vesicles. Nylund M, Kjellberg MA, Molotkovsky JG, Byun HS, Bittman R, Mattjus P. Biochim Biophys Acta 1758 807-812 (2006)
  17. Conformational folding and stability of the HET-C2 glycolipid transfer protein fold: does a molten globule-like state regulate activity? Kenoth R, Kamlekar RK, Simanshu DK, Gao Y, Malinina L, Prendergast FG, Molotkovsky JG, Patel DJ, Venyaminov SY, Brown RE. Biochemistry 50 5163-5171 (2011)
  18. Human glycolipid transfer protein (GLTP) expression modulates cell shape. Gao Y, Chung T, Zou X, Pike HM, Brown RE. PLoS One 6 e19990 (2011)
  19. Phosphatidylserine Stimulates Ceramide 1-Phosphate (C1P) Intermembrane Transfer by C1P Transfer Proteins. Zhai X, Gao YG, Mishra SK, Simanshu DK, Boldyrev IA, Benson LM, Bergen HR, Malinina L, Mundy J, Molotkovsky JG, Patel DJ, Brown RE. J Biol Chem 292 2531-2541 (2017)
  20. GLTP-fold interaction with planar phosphatidylcholine surfaces is synergistically stimulated by phosphatidic acid and phosphatidylethanolamine. Zhai X, Momsen WE, Malakhov DA, Boldyrev IA, Momsen MM, Molotkovsky JG, Brockman HL, Brown RE. J Lipid Res 54 1103-1113 (2013)
  21. Glucosylceramide acyl chain length is sensed by the glycolipid transfer protein. Backman APE, Halin J, Nurmi H, Möuts A, Kjellberg MA, Mattjus P. PLoS One 13 e0209230 (2018)
  22. Probing the origin of structural stability of single and double stapled p53 peptide analogs bound to MDM2. Guo Z, Streu K, Krilov G, Mohanty U. Chem Biol Drug Des 83 631-642 (2014)
  23. Ceramide-1-phosphate transfer protein (CPTP) regulation by phosphoinositides. Gao YG, Zhai X, Boldyrev IA, Molotkovsky JG, Patel DJ, Malinina L, Brown RE. J Biol Chem 296 100600 (2021)
  24. Ceramide-1-phosphate transfer protein promotes sphingolipid reorientation needed for binding during membrane interaction. Gao YG, McDonald J, Malinina L, Patel DJ, Brown RE. J Lipid Res 63 100151 (2022)
  25. Prediction of a novel RNA binding domain in crocodilepox Zimbabwe Gene 157. Little NS, Quon T, Upton C. Microb Inform Exp 1 12 (2011)
  26. Functional evaluation of tryptophans in glycolipid binding and membrane interaction by HET-C2, a fungal glycolipid transfer protein. Kenoth R, Zou X, Simanshu DK, Pike HM, Malinina L, Patel DJ, Brown RE, Kamlekar RK. Biochim Biophys Acta Biomembr 1860 1069-1076 (2018)
  27. Identification of conserved miRNAs and their targets in Jatropha curcas: an in silico approach. Ahmed F, Bappy MNI, Islam MS. J Genet Eng Biotechnol 21 43 (2023)
  28. Prediction and expression analysis of deleterious nonsynonymous SNPs of Arabidopsis ACD11 gene by combining computational algorithms and molecular docking approach. Rifat MH, Ahmed J, Ahmed M, Ahmed F, Gulshan A, Hasan M. PLoS Comput Biol 18 e1009539 (2022)
  29. Whole-Genome Resequencing Highlights the Unique Characteristics of Kecai Yaks. Kang Y, Guo S, Wang X, Cao M, Pei J, Li R, Bao P, Wang J, Lamao J, Gongbao D, Lamao J, Liang C, Yan P, Guo X. Animals (Basel) 12 2682 (2022)


Related citations provided by authors (1)

  1. Crystallization and X-ray analysis of bovine glycolipid transfer protein.. West G, Nymalm Y, Airenne TT, Kidron H, Mattjus P, Salminen TT Acta Crystallogr D Biol Crystallogr 60 703-5 (2004)

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