Human GLTP: Three distinct functions for the three tryptophans in a novel peripheral amphitropic fold

Biophysical Journal

Volumn 99, Issue 8, 2010, Pages 2626-2635

  Kamlekar, Ravi Kanth ^a   Gao, Yongguang ^a   Kenoth, Roopa ^a   Molotkovsky, Julian G ^b   Prendergast, Franklyn G ^c   Malinina, Lucy ^d   Patel, Dinshaw J ^e   Wessels, William S ^c   Venyaminov, Sergei Y ^c   Brown, Rhoderick E ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^c Mayo Clinic   (United States)

^d CIC BIOGUNE   (Spain)

^e MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VERTEBRATA;

EID: 78049351955     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.08.038     Document Type: Article

References (44)

1. Brown, R. E., and P. Mattjus. 2007. Glycolipid transfer proteins. Biochim. Biophys. Acta. 1771:746-760.
2. Lin, X., P. Mattjus, ⋯, R. E. Brown. 2000. Cloning and expression of glycolipid transfer protein from bovine and porcine brain. J. Biol. Chem. 275:5104-5110.
3. Zou, X., T. Chung, ⋯, R. E. Brown. 2008. Human glycolipid transfer protein (GLTP) genes: Organization, transcriptional status and evolution. BMC Genomics. 9:72.
4. Malinina, L., M. L. Malakhova, ⋯, D. J. Patel. 2004. Structural basis for glycosphingolipid transfer specificity. Nature. 430:1048-1053.
5. Malinina, L., M. L. Malakhova, ⋯, D. J. Patel. 2006. The liganding of glycolipid transfer protein is controlled by glycolipid acyl structure. PLoS Biol. 4:e362.
6. Airenne, T. T., H. Kidron, ⋯, T. A. Salminen. 2006. Structural evidence for adaptive ligand binding of glycolipid transfer protein. J. Mol. Biol. 355:224-236.
7. D'Angelo, G., E. Polishchuk, ⋯, M. A. De Matteis. 2007. Glycosphingolipid synthesis requires FAPP2 transfer of glucosylceramide. Nature. 449:62-67.
8. Halter, D., S. Neumann, ⋯, H. Sprong. 2007. Pre- and post-Golgi translocation of glucosylceramide in glycosphingolipid synthesis. J. Cell Biol. 179:101-115.
9. Rao, C. S., T. Chung, ⋯, R. E. Brown. 2005. Glycolipid transfer protein interaction with bilayer vesicles: Modulation by changing lipid composition. Biophys. J. 89:4017-4028.
10. West, G., M. Nylund, ⋯, P. Mattjus. 2006. Membrane interaction and activity of the glycolipid transfer protein. Biochim. Biophys. Acta. 1758:1732-1742.
11. Neumann, S., M. Opacić, ⋯, M. R. Egmond. 2008. Glycolipid transfer protein: Clear structure and activity, but enigmatic function. Adv. Enzyme Regul. 48:137-151.
12. Zhai, X., M. L. Malakhova, ⋯, R. E. Brown. 2009. Glycolipid acquisition by human glycolipid transfer protein dramatically alters intrinsic tryptophan fluorescence: Insights into glycolipid binding affinity. J. Biol. Chem. 284:13620-13628.
13. Mattjus, P. 2009. Glycolipid transfer proteins and membrane interaction. Biochim. Biophys. Acta. 1788:267-272.
14. Cho, W., and R. V. Stahelin. 2005. Membrane-protein interactions in cell signaling and membrane trafficking. Annu. Rev. Biophys. Biomol. Struct. 34:119-151.
15. Hurley, J. H. 2006. Membrane binding domains. Biochim. Biophys. Acta. 1761:805-811.
16. Cho,W. (editor). 2006. Lipid-binding domains. Biochim. Biophys. Acta (Special Issue: Lipid-Binding Domains). 1761:803-968.
17. Lemmon, M. A. 2008. Membrane recognition by phospholipid-binding domains. Nat. Rev. Mol. Cell Biol. 9:99-111.
18. Malakhova, M. L., L. Malinina, ⋯, R. E. Brown. 2005. Point mutational analysis of the liganding site in human glycolipid transfer protein. Functionality of the complex. J. Biol. Chem. 280:26312-26320.
19. Li, X.-M., M. L. Malakhova, ⋯, R. E. Brown. 2004. Human glycolipid transfer protein: Probing conformation using fluorescence spectroscopy. Biochemistry. 43:10285-10294.
20. Rao, C. S., X. Lin, ⋯, R. E. Brown. 2004. Glycolipid transfer protein mediated transfer of glycosphingolipids between membranes: A model for action based on kinetic and thermodynamic analyses. Biochemistry. 43:13805-13815.
21. Venyaminov, S. Y., E. S. Klimtchuk, ⋯, T. A. Craig. 2004. Changes in structure and stability of calbindin-D(28K) upon calcium binding. Anal. Biochem. 334:97-105.
22. Craig, T. A., L. M. Benson, ⋯, R. Kumar. 2006. Metal-binding properties of human centrin-2 determined by micro-electrospray ionization mass spectrometry and UV spectroscopy. J. Am. Soc. Mass Spectrom. 17:1158-1171.
23. Kelly, S. M., T. J. Jess, and N. C. Price. 2005. How to study proteins by circular dichroism. Biochim. Biophys. Acta. 1751:119-139.
24. Bates, P. A., L. A. Kelley, ⋯, M. J. Sternberg. 2001. Enhancement of protein modeling by human intervention in applying the automatic programs 3D-JIGSAWand 3D-PSSM. Proteins. 5 (Suppl 5):39-46.
25. Lakowicz, J. R. 2006. Principles of Fluorescence Spectroscopy, 3rd ed. Springer, New York.
26. Demchenko, A. P. 2002. The red-edge effects: 30 years of exploration. Luminescence. 17:19-42.
27. Raghuraman, H., D. A. Kelkar, and A. Chattopadhyay. 2005. Novel insights into protein structure and dynamics utilizing the red edge excitation shift approach. In Reviews in Fluorescence 2005. C. D. Geddes, and J. R. Lakowicz, editors. Springer, New York. 199-222.
28. Kenoth, R., D. K. Simanshu, ⋯, R. E. Brown. 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. J. Biol. Chem. 285:13066-13078.
29. Johnson, J. E., and R. B. Cornell. 1999. Amphitropic proteins: Regulation by reversible membrane interactions (review). Mol. Membr. Biol. 16:217-235.
30. Tamm, L. K. 2005. Protein-Lipid Interactions: From Membrane Domains to Cellular Networks. Wiley-VCH, Weinheim, Germany.
31. Yau, W.-M., W. C. Wimley, ⋯, S. H. White. 1998. The preference of tryptophan for membrane interfaces. Biochemistry. 37:14713-14718.
32. Sanderson, J. M., and E. J. Whelan. 2004. Characterisation of the interactions of aromatic amino acids with diacetyl phosphatidylcholine. Phys. Chem. Chem. Phys. 6:1012-1017.
33. Esbjörner, E. K., C. E. B. Caesar, ⋯, B. Nordén. 2007. Tryptophan orientation in model lipid membranes. Biochem. Biophys. Res. Commun. 361:645-650.
34. Lomize, A. L., I. D. Pogozheva, ⋯, H. I. Mosberg. 2007. The role of hydrophobic interactions in positioning of peripheral proteins in membranes. BMC Struct. Biol. 7:44.
35. Gallivan, J. P., and D. A. Dougherty. 1999. Cation-p interactions in structural biology. Proc. Natl. Acad. Sci. USA. 96:9459-9464.
36. Yoder, N. C., and K. Kumar. 2006. Selective protein-protein interactions driven by a phenylalanine interface. J. Am. Chem. Soc. 128:188-191.
37. Biedermannova, L., K. E Riley, ⋯, J. Vondrasek. 2008. Another role of proline: Stabilization interactions in proteins and protein complexes concerning proline and tryptophane. Phys. Chem. Chem. Phys. 10:6350-6359.
38. Exarchos, K. P., T. P. Exarchos, ⋯, D. I. Fotiadis. 2009. Detection of discriminative sequence patterns in the neighborhood of proline cis peptide bonds and their functional annotation. BMC Bioinformatics. 10:113.
39. Lorenzen, S., B. Peters, ⋯, C. Frommel. 2005. Conservation of cis prolyl bonds in proteins during evolution. Proteins. 58:589-595.
40. Gaede, H. C., W.-M. Yau, and K. Gawrisch. 2005. Electrostatic contributions to indole-lipid interactions. J. Phys. Chem. B. 109:13014-13023.
41. Sỳkora, J., P. Jurkiewicz, ⋯, M. Hof. 2005. Influence of the curvature on the water structure in the headgroup region of phospholipid bilayer studied by the solvent relaxation technique. Chem. Phys. Lipids. 135:213-221.
42. Joseph, M., and R. Nagaraj. 1995. Conformations of peptides corresponding to fatty acylation sites in proteins. A circular dichroism study. J. Biol. Chem. 270:16749-16755.
43. Christiaens, B., S. Symoens, ⋯, S. Vanderheyden. 2002. Tryptophan fluorescence study of the interaction of penetratin peptides with model membranes. Eur. J. Biochem. 269:2918-2926.
44. Chowdary, T. K., B. Raman, ⋯, ChM. Rao. 2007. Interaction of mammalian Hsp22 with lipid membranes. Biochem. J. 401:437-445.