Structural thermal adaptation of β-tubulins from the Antarctic psychrophilic protozoan Euplotes focardii

Proteins: Structure, Function and Bioinformatics

Volumn 80, Issue 4, 2012, Pages 1154-1166

  Chiappori, Federica ^a   Pucciarelli, Sandra ^b   Merelli, Ivan ^a   Ballarini, Patrizia ^b   Miceli, Cristina ^b   Milanesi, Luciano ^a  

^a CNR   (Italy)

^b UNIVERSITY OF CAMERINO   (Italy)

Author keywords

Cellular function; Cilia; Isotypes; Ligand effect; Microtubule; Molecular dynamics; Structural flexibility

Indexed keywords

AMINO ACID; BETA TUBULIN; POLYPEPTIDE; PROTEIN EFBT2; PROTEIN EFBT3; PROTEIN EFBT4; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANTARCTICA; ARTICLE; COLD; CONTROLLED STUDY; ENVIRONMENTAL TEMPERATURE; EUKARYOTIC FLAGELLUM; EUPLOTES FOCARDII; HYDROPHOBICITY; MICROTUBULE ASSEMBLY; MOLECULAR DYNAMICS; MORPHOLOGICAL ADAPTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; PROTEIN TERTIARY STRUCTURE; PROTOZOON; PSYCHROPHILE; TEMPERATURE ACCLIMATIZATION; TEMPERATURE DEPENDENCE;

ACCLIMATIZATION; AMINO ACID SUBSTITUTION; ANTARCTIC REGIONS; BLOTTING, NORTHERN; CHROMOSOMES; CILIA; COLD TEMPERATURE; COMPUTER SIMULATION; EUPLOTES; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MOLECULAR DYNAMICS SIMULATION; NEPHELOMETRY AND TURBIDIMETRY; POLYMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTOZOAN PROTEINS; RNA, PROTOZOAN; TRANSCRIPTION, GENETIC; TUBULIN;

EUKARYOTA; EUPLOTES; EUPLOTES FOCARDII; PROTOZOA;

EID: 84857794404     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24016     Document Type: Article

References (38)

1. Nogales E, Downing KH, Amos LA, Löwe J. Tubulin and FtsZ form a distinct family of GTPases. Nat Struct Biol 1998; 5: 451-458.
2. Tran PT, Joshi P, Salmon ED. How tubulin subunits are lost from the shortening ends of microtubules. J Struct Biol 1997; 118: 107-118.
3. Desai A, Mitchison TJ. Microtubule polymerization dynamics. Annu Rev Cell Dev Biol 1997; 13: 83-117.
4. Buey RM, Díaz JF, Andreu JM. The nucleotide switch of tubulin and microtubule assembly: a polymerization-driven structural change. Biochemistry 2006; 45: 5933-5938.
5. Löwe J, Li H, Downing KH, Nogales E. Refined structure of αβ-tubulin at 3.5 Å resolution. J Mol Biol 2001; 313: 1045-1057.
6. Joe PA, Banerjee A, Ludueña RF. The roles of cys124 and ser239 in the functional properties of human betaIII tubulin. Cell Motil Cytoskeleton 2008; 65: 476-486.
7. Wallin M, Strömberg E. Cold-stable and cold-adapted microtubules. Int Rev Cytol 1995; 157: 1-31.
8. Detrich HW, III, Parker SK, Williams RC, Jr, Nogales E, Downing KH. Cold adaptation of microtubule assembly and dynamics. Structural interpretation of primary sequence changes present in the alpha- and beta-tubulins of Antarctic fishes. J Biol Chem 2000; 275: 37038-37047.
9. Valbonesi A, Luporini P. Biology of Euplotes focardii an Antarctic ciliate. Polar Biol 1990; 13: 489-493.
10. Pucciarelli S, Miceli C. Characterization of the cold-adapted alpha-tubulin from the psychrophilic ciliate Euplotes focardii. Extremophiles 2002; 5: 385-389.
11. Miceli C, Ballarini P, Di Giuseppe G, Valbonesi A, Luporini P. Identification of the tubulin gene family and sequence determination of one β-tubulin gene in a cold-poikilotherm protozoan, the Antarctic ciliate Euplotes focardii. J Eukaryot Microbiol 1994; 41: 420-427.
12. Pucciarelli S, La TA, Ballarini P, Barchetta S, Yu T, Marziale F, Passini V, Methé B, Detrich HW, III, Miceli C. Molecular cold-adaptation of protein function and gene regulation: the case for comparative genomic analyses in marine ciliated protozoa. Mar Genomics 2009; 2: 57-66.
13. Huzil JT, Ludueña RF, Tuszynski J. Comparative modeling of human β tubulin isotypes and implications for drug binding. Nanotechnology 2006; 17: S90-S100.
14. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227: 680-685.
15. Bradford MM. Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem 1976; 72: 248-254.
16. Detrich HW, III, Jordan MA, Wilson L, Williams RC, Jr. Mechanism of microtubule assembly. Changes in polymer structure and organization during assembly of sea urchin egg tubulin. J Biol Chem 1985; 260: 9479-9490.
17. Marziale F, Pucciarelli S, Ballarini P, Melki R, Uzun A, Ilyin VL, Detrich HW, III, Miceli C. Different roles of two γ-tubulin isotypes in the cytoskeleton of the Antarctic ciliate Euplotes focardii. FEBS J 2008; 275: 5367-5382.
18. Hoffman DC, Anderson RC, DuBois ML, Prescott DM. Macronuclear gene-sized molecules of hypotrichs. Nucleic Acids Res 1995; 23: 1279-83.
19. Sambrook J, Russel DW. Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York, NY; 2001.
20. Eswar N, Webb B, Marti-Renom MA, Madhusudhan MS, Eramian D, Shen MY, Pieper U, Sali A. Comparative protein structure modeling with MODELLER. Curr Protoc Bioinformatics 2006, Unit 5.6.
21. Shen M, Sali A. Statistical potential for assessment and prediction of protein structures. Protein Sci 2006; 15: 2507-2524.
22. Benkert P, Tosatto SCE, Schomburg D. QMEAN: a comprehensive scoring function for model quality assessment. Proteins 2008; 71: 261-277.
23. Arnold K, Bordoli L, Kopp J, Schwede T. The SWISS-MODEL Workspace: a web-based environment for protein structure homology modelling. Bioinformatics 2006; 22: 195-201.
24. Hess B, Kutzner C, van der Spoel D, Lindahl E. GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J Chem Theory Coumput 2008; 4: 435-447.
25. Hess B, Bekker H, Berendsen HJC, Fraaije JGEM: LINCS. A linear constraint solver for molecular simulations. J Comp Chem 1997; 18: 1463-1472.
26. Essman U, Perera L, Berkowitz ML, Darden T, Lee H, Pedersen LG. A smooth particle mesh ewald potential. J Chem Phys 1995; 103: 8577-8592.
27. Humphrey W, Dalke A, Schulten K. VMD-visual molecular dynamics. J Mol Graph 1996; 14: 33-38.
28. Cheung CH, Wu SY, Lee TR, Chang CY, Wu JS, Hsieh HP, Chang JY. Cancer cells acquire mitotic drug resistance properties through beta I-tubulin mutations and alterations in the expression of beta-tubulin isotypes. PLoS One 2010; 5: e12564.
29. Yin S, Bhattacharya R, Cabral F. Human mutations that confer paclitaxel resistance. Mol Cancer Ther 2010; 9: 327-335.
30. Feller G, Gerday C. Psychrophilic enzymes: molecular basis of cold adaptation. Cell Mol Life Sci 1997; 53: 830-841.
31. Metpally RPR, Reddy BVB. Comparative proteome analysis of psychrophilic versus mesophilic bacterial species: insights into the molecular basis of cold adaptation of proteins. BMC Genomics 2009; 10: 11.
32. Nogales E, Wolf SG, Downing KH. Structure of the alpha beta tubulin dimer by electron crystallography. Nature 1998; 391: 199-203.
33. Keskin O, Durell SR, Bahar I, Jernigan RL, Covell DG. Relating molecular flexibility to function: a case study of tubulin. Biophys J 2002; 83: 663-680.
34. Panda D, Miller HP, Banerjee A, Ludueña RF, Wilson L. Microtubule dynamics in vitro are regulated by the tubulin isotype composition. Proc Natl Acad Sci USA 1994; 91: 11358-11362.
35. Richards KL, Anders KR, Nogales E, Schwartz K, Downing KH, Botstein D. Structure-function relationships in yeast tubulins. Mol Biol Cell 2000; 11: 1887-1903.
36. Willem S, Srahna M, Devos N, Gerday C, Loppes R, Matagne RF. Protein adaptation to low temperatures: a comparative study of alpha-tubulin sequences in mesophilic and psychrophilic algae. Extremophiles 1999; 3: 221-226.
37. Shang Y, Tsao CC, Gorovsky MA. Mutational analyses reveal a novel function of the nucleotide-binding domain of gamma-tubulin in the regulation of basal body biogenesis. J Cell Biol 2005; 171: 1035-1044.
38. Hesketh JE, Ciesielski-Treska J, Aunis D. Cold-stable microtubules and microtubule-organing centres in astrocytes in primary culture. Neurosci Lett 1984; 51: 155-160.