Resurrection of a functional phosphatidylinositol transfer protein from a pseudo-Sec14 scaffold by directed evolution

Molecular Biology of the Cell

Volumn 22, Issue 6, 2011, Pages 892-905

  Schaaf, Gabriel ^a,b   Dynowski, Marek ^b,c   Mousley, Carl J ^a   Shah, Sweety D ^a   Yuan, Peihua ^a   Winklbauer, Eva M ^b   De Campos, Marília K F ^b   Trettin, Kyle ^a   Quinones, Mary Chely ^d   Smirnova, Tatyana I ^d   Yanagisawa, Lora L ^e   Ortlund, Eric A ^f   Bankaitis, Vytas A ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

^d NORTH CAROLINA STATE UNIVERSITY   (United States)

^e UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

^f EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; LIPID TRANSFER PROTEIN; PHOSPHATIDYLINOSITOL; PROTEIN SEC14; PROTEIN SFH1; UNCLASSIFIED DRUG;

ALLELE; AMINO ACID SUBSTITUTION; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; ENDOSOME; HYDROPHILICITY; HYDROPHOBICITY; LIGAND BINDING; MICROENVIRONMENT; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; MUTAGENESIS; MUTATIONAL ANALYSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; STRUCTURE ANALYSIS; TRANS GOLGI NETWORK;

AMINO ACID SEQUENCE; CELL CYCLE PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; DIRECTED MOLECULAR EVOLUTION; ENDOSOMES; GOLGI APPARATUS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PHENOTYPE; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLINOSITOLS; PHOSPHOLIPID TRANSFER PROTEINS; PROTEIN CONFORMATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TRANS-GOLGI NETWORK;

EID: 79952855542     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-11-0903     Document Type: Article

References (40)

1. Alaouie AM, Smirnov AI (2006). Ultra-stable temperature control in EPR experiments: thermodynamics of gel-to-liquid phase transition in spin-labeled PL bilayers and bilayer perturbations by spin labels. J Mag Res 182, 229-238. (Pubitemid 44466449)
2. Balla T (2005). Inositol-lipid binding motifs: signal integrators through protein-lipid and protein-protein interactions. J Cell Sci 118, 2093-2104.
3. Bankaitis VA, Aitken JR, Cleves AE, Dowhan W (1990). An essential role for a phospholipid transfer protein in yeast Golgi function. Nature 347, 561-562
4. Bankaitis VA, Mousley CJ, Schaaf G (2010). The Sec14-superfamily and mechanisms for crosstalk between lipid metabolism and lipid signaling. Trends Biochem Sci 35, 150-160.
5. Benomar M et al. (2002). Clinical comparison between AVED patients with 744 del A mutation and Friedreich ataxia with GAA expansion in 15 Moroccan families. J Neurol Sci 198, 25-29.
6. Bomar JM et al. (2003). Mutations in a novel gene encoding a CRAL-TRIO domain cause human Cayman ataxia and ataxia/dystonia in the jittery mouse. Nature Genetics 35, 264-269. (Pubitemid 37363181)
7. Cleves AE, McGee TP, Whitters EA, Champion KM, Aitken JR, Dowhan W, Goebl M, Bankaitis VA (1991). Mutations in the CDP-choline pathway for phospholipid biosynthesis bypass the requirement for an essential phospholipid transfer protein. Cell 64, 789-800. (Pubitemid 121001166)
8. Cleves AE, Novick PJ, Bankaitis VA (1989). Mutations in the SAC1 gene suppress defects in yeast Golgi and yeast actin function. J Cell Biol 109, 2939-2950.
9. D'Angelo I, Welti S, Bonneau F, Scheffzek K (2006). A novel bipartite phospholipid-binding module in the neurofibromatosis type 1 protein. EMBO Rep 7, 174-179.
10. Emsley P, Cowtan K (2004). Coot, model-building tools for molecular graphics. Acta Crystallographica D60, 2126-2132. (Pubitemid 41742764)
11. Fang M, Kearns BG, Gedvilaite A, Kagiwada S, Kearns M, Fung MKY, Bankaitis VA (1996). Kes1 shares homology with human oxysterol binding protein and participates in a novel regulatory pathway for yeast Golgi-derived transport vesicle biogenesis. EMBO J 15, 6447-6459. (Pubitemid 26413778)
12. Foti M, Audhya A, Emr SD (2001). Sac1 lipid phosphatase and Stt4 phosphatidylinositol-4-kinase regulate a pool of phosphatidylinositol 4-phosphate that functions in control of the actin cytoskeleton and vacuole morphology. Mol Biol Cell 12, 2396-2411. (Pubitemid 33051964)
13. Fruman DA, Meyers RE, Cantley LC (1998). Phosphoinositide kinases. Annu Rev Biochem 67, 481-507. (Pubitemid 28411136)
14. Guo S, Stolz LE, Lemrow SM, York JD (1999). SAC1-like domains of yeast SAC1, INP52, and INP53 and of human synaptojanin encode polyphosphoinositide phosphatases. J Biol Chem 274, 12990-12995.
15. Ile KE et al. (2010). The zebrafish class 1 phosphatidylinositol transfer protein family, PITPβ isoforms and double cone cell outer segment integrity in retina. Traffic 11, 1151-1167.
16. Ile KE, Schaaf G, Bankaitis VA (2006). Phosphatidylinositol transfer proteins and cellular nanoreactors for lipid signaling. Nature Chem Biol 2, 576-583. (Pubitemid 44610341)
17. Kearns MA et al. (1998). Novel developmentally regulated phosphoinositide binding proteins from soybean whose expression bypasses the requirement for an essential phosphatidylinositol transfer protein in yeast. EMBO J 17, 4004-4017. (Pubitemid 28333985)
18. Lemmon MA (2008). Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol 9, 99-111.
19. Li X, Routt S, Xie Z, Cui X, Fang M, Kearns MA, Bard M, Kirsch D, Bankaitis VA (2000). Identification of a novel family of nonclassical yeast PITPs whose function modulates activation of phospholipase D and Sec14p-independent cell growth. Mol Biol Cell 11, 1989-2005. (Pubitemid 30408059)
20. Lücke C, Huang S, Rademacher M, Rüterjans H (2002). New insights into intracellular lipid binding proteins: the role of buried water. Protein Sci 11, 2382-2392.
21. Majerus PW (1997). Inositol phosphatases and kinases in cell signaling. FASEB J 11, A1297.
22. McLaughlin S, Murray D (2005). Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438, 605-611. (Pubitemid 41740564)
23. Meier R, Tomizaki T, Schulze-Briese C, Baumann U, Stocker A (2003). The molecular basis of vitamin E retention: structure of human tocopherol transfer protein. J Mol Biol 331, 725-734. (Pubitemid 36937156)
24. Modig K, Rademacher M, Lücke C, Halle B (2003). Water dynamics in the large cavity of three lipid-binding proteins monitored by 17O magnetic relaxation dispersion. J Mol Biol 332, 965-977. (Pubitemid 37101381)
25. Nemoto Y, Kearns BG, Wenk MR, Chen H, Mori K, Alb JG Jr, De Camilli P, Bankaitis VA (2000). Functional characterization of a mammalian Sac1 and mutants exhibiting substrate specific defects in PIP phosphatase activity. J Biol Chem 275, 14446-14456.
26. Otwinowski Z (1993). Data collection and processing. In Proceedings of the CCP4 Study Weekend, Sawyer L, Isaacs N, and Bailey S, eds., Daresbury, UK: SERC Danesbury Laboratory, 56-62.
27. Ouachi K, Arita M, Kayden H, Faycal H, Hamida MB, Sokol R, Arai H, Inoue K, Mandel J-L, Koenig M (1995). Ataxia with vitamin E deficiency is caused by mutations in the α-tocopherol transfer protein. Nature Genetics 9, 141-145.
28. Phillips SE et al. (1999). Yeast Sec14p deficient in phosphatidylinositol transfer activity is functional in vivo. Mol Cell 4, 187-197. (Pubitemid 29456887)
29. Rivas MP, Kearns BG, Xie Z, Guo S, Sekar MC, Hosaka K, Kagiwada S, York JD, Bankaitis VA (1999). pleiotropic alterations in lipid metabolism in yeast sac1 mutants: relationship to "bypass Sec14p" and inositol auxotrophy. Mol Biol Cell 10, 2235-2250. (Pubitemid 29343132)
30. Routt SM, Ryan MM, Tyeryar K, Rizzieri K, Roumanie O, Brennwald PJ, Bankaitis VA (2005). Nonclassical PITPs activate phospholipase D via an Stt4p-dependent pathway and modulate function of late stages of the secretory pathway in vegetative yeast cells. Traffic 6, 1157-1172. (Pubitemid 41632267)
31. Ryan MM, Temple BRS, Phillips SE, Bankaitis VA (2007). Conformational dynamics of the major yeast phosphatidylinositol transfer protein Sec14: insights into the mechanisms of PL exchange and diseases of Sec14-like protein deficiencies. Mol Biol Cell 18, 1928-1942. (Pubitemid 46717572)
32. Schaaf G, Betts L, Garrett TA, Raetz CRH, Bankaitis VA (2006). Crystallization and preliminary X-ray diffraction analysis of phospholipid-bound Sfh1p: a member of the Saccharomyces cerevisiae Sec14p-like phosphatidylinositol transfer protein family. Acta Crystallographica F 62, 1156-1160.
33. Schaaf G, Ortlund E, Tyeryar K, Mousley C, Ile K, Woolls M, Garrett T, Raetz CRH, Redinbo M, Bankaitis VA (2008). The functional anatomy of phospholipid binding and regulation of phosphoinositide homeostasis by proteins of the Sec14-superfamily. Molecular Cell 29, 191-206. (Pubitemid 351172821)
34. Schorn K, Marsh D (1997). Extracting order parameters from powder EPR lineshapes for spin-labelled lipids in membranes. Spectrochimica Acta A 53, 2235-2240. (Pubitemid 127368760)
35. Sha B, Phillips SE, Bankaitis VA, Luo M (1998). Crystal structure of the Saccharomyces cerevisiae phosphatidylinositol transfer protein Sec14p. Nature 391, 506-510.
36. Smirnova T, Chadwick TG, MacArthur R, Poluekov O, Song L, Ryan M, Schaaf G, Bankaitis VA (2006). The chemistry of PL binding by the Saccharomyces cerevisiae phosphatidylinositol transfer protein Sec14 as determined by electron paramagnetic resonance spectroscopy. J Biol Chem 281, 34897-34908.
37. Smirnova T, Chadwick TG, van Tol J, Ozarowski A, Poluektov O, Schaaf G, Ryan MM, Bankaitis VA (2007). Local polarity and hydrogen bonding inside the Sec14 PL-binding cavity: high-field multifrequency studies. Biophys J 92, 3686-3695. (Pubitemid 46698657)
38. Strahl T, Thorner J (2007). Synthesis and function of membrane phosphoinositides in budding yeast, Saccharomyces cerevisiae. Biochim Biophys Acta 1771, 353-404. (Pubitemid 46428617)
39. Xie Z, Fang M, Rivas MP, Faulkner A, Sternweis PC, Engebrecht J, Bankaitis VA (1998). Phospholipase D activity is required for suppression of yeast phosphatidylinositol transfer protein defects. Proc Natl Acad Sci USA 95, 12346-12351. (Pubitemid 28483768)
40. Yanagisawa L, Marchena J, Xie Z, Li X, Poon PP, Singer R, Johnston G, Randazzo PA, Bankaitis VA (2002). Activity of specific lipid-regulated ARFGAPs is required for Sec14p-dependent Golgi secretory function in yeast. Mol Biol Cell 13, 2193-2206. (Pubitemid 34831326)