Characterization of the first eukaryotic cold-adapted patatin-like phospholipase from the psychrophilic Euplotes focardii: Identification of putative determinants of thermal-adaptation by comparison with the homologous protein from the mesophilic Euplotes crassus

Biochimie

Volumn 95, Issue 9, 2013, Pages 1795-1806

  Yang, Guang ^a   De Santi, Concetta ^b   De Pascale, Donatella ^b   Pucciarelli, Sandra ^a   Pucciarelli, Stefania ^a   Miceli, Cristina ^a  

^a UNIVERSITY OF CAMERINO   (Italy)

^b INSTITUTE OF PROTEIN BIOCHEMISTRY   (Italy)

Author keywords

Molecular cold adaptation; Patatin like phosholipase; Psychrophilic enzymes; Site directed mutagenesis

Indexed keywords

AMINO ACID DERIVATIVE; PHOSPHOLIPASE; PHOSPHOLIPASE A2;

ARTICLE; ENZYME ACTIVITY; EUPLOTES; EUPLOTES CRASSUS; EUPLOTES FOCARDII; LOW TEMPERATURE; NONHUMAN; PH; SITE DIRECTED MUTAGENESIS; TEMPERATURE ACCLIMATIZATION; TEMPERATURE DEPENDENCE; THERMOSTABILITY;

EUKARYOTA; EUPLOTES FOCARDII; MONEUPLOTES CRASSUS; PROTOZOA;

EID: 84881168745     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2013.06.008     Document Type: Article

References (62)

1. A. Casanueva, M. Tuffin, C. Cary, and D.A. Cowan Molecular adaptations to psychrophily: the impact of 'omic' technologies Trends in Microbiology 18 2010 374 381
2. E. Papaleo, M. Pasi, M. Tiberti, and L. De Gioia Molecular dynamics of mesophilic-like mutants of a cold-adapted enzyme: insights into distal effects induced by the mutations PLoS ONE 6 2011 e24214
3. B. Joseph, P.W. Ramteke, and G. Thomas Cold active microbial lipases: some hot issues and recent developments Biotechnology Advances 26 2008 457 470
4. K.S. Siddiqui, and R. Cavicchioli Cold-adapted enzymes Annual Review of Biochemistry 75 2006 403 433
5. P.W.R. Babu Joseph, George Thomas, and Nitisha Shrivastava Standard review cold-active microbial lipases: a versatile tool for industrial applications Biotechnology and Molecular Biology Reviews 2 2 June 2007 039 048
6. A. Macrae, J. Visicchio, and A. Lanot Application of potato lipid acyl hydrolase for the synthesis of monoacylglycerols Journal of the American Oil Chemists' Society 75 1998 1489 1494
7. S. Prat, W.B. Frommer, R. Hofgen, M. Keil, J. Kossmann, M. Koster-Topfer, X.J. Liu, B. Muller, H. Pena-Cortes, and M. Rocha-Sosa Gene expression during tuber development in potato plants FEBS Letters 268 1990 334 338
8. R. Höfgen, and L. Willmitzer Biochemical and genetic analysis of different patatin isoforms expressed in various organs of potato (Solanum tuberosum) Plant Science 66 1990 221 230
9. S. Rosahl, R. Schmidt, J. Schell, and L. Willmitzer Isolation and characterization of a gene from Solanum tuberosum encoding patatin, the major storage protein of potato tubers Molecular and General Genetics 203 1986 214 220
10. D.L. Andrews, B. Beames, M.D. Summers, and W.D. Park Characterization of the lipid acyl hydrolase activity of the major potato (Solanum tuberosum) tuber protein, patatin, by cloning and abundant expression in a baculovirus vector The Biochemical Journal 252 1988 199 206
11. O. Hirayama, H. Matsuda, H. Takeda, K. Maenaka, and H. Takatsuka Purification and properties of a lipid acyl-hydrolase from potato tubers Biochimica et Biophysica acta 384 1975 127 137
12. D.A. Wardale Lipid-degrading enzymes from potato tubers Phytochemistry 19 1980 173 177
13. D. Racusen Esterase specificity of patatin from two potato cultivars Canadian Journal of Botany 64 1986 2104 2106
14. K. Senda, H. Yoshioka, N. Doke, and K. Kawakita A cytosolic phospholipase A2 from potato tissues appears to be patatin Plant & Cell Physiology 37 1996 347 353
15. J.A. Strickland, G.L. Orr, and T.A. Walsh Inhibition of diabrotica larval growth by patatin, the lipid acyl hydrolase from potato tubers Plant Physiology 109 1995 667 674
16. A. Holk, S. Rietz, M. Zahn, H. Quader, and G.F. Scherer Molecular identification of cytosolic, patatin-related phospholipases A from Arabidopsis with potential functions in plant signal transduction Plant Physiology 130 2002 90 101
17. H.J. Hirschberg, J.W. Simons, N. Dekker, and M.R. Egmond Cloning, expression, purification and characterization of patatin, a novel phospholipase A European Journal of Biochemistry/FEBS 268 2001 5037 5044
18. T.J. Rydel, J.M. Williams, E. Krieger, F. Moshiri, W.C. Stallings, S.M. Brown, J.C. Pershing, J.P. Purcell, and M.F. Alibhai The crystal structure, mutagenesis, and activity studies reveal that patatin is a lipid acyl hydrolase with a Ser-Asp catalytic dyad Biochemistry 42 2003 6696 6708
19. J.D. Schrag, and M. Cygler Lipases and alpha/beta hydrolase fold Methods in Enzymology 284 1997 85 107
20. P.C. Kienesberger, M. Oberer, A. Lass, and R. Zechner Mammalian patatin domain containing proteins: a family with diverse lipolytic activities involved in multiple biological functions Journal of Lipid Research 50 Suppl 2009 S63 S68
21. G.F. Scherer, S.B. Ryu, X. Wang, A.R. Matos, and T. Heitz Patatin-related phospholipase A: nomenclature, subfamilies and functions in plants Trends in Plant Science 15 2010 693 700
22. S. Banerji, and A. Flieger Patatin-like proteins: a new family of lipolytic enzymes present in bacteria? Microbiology 150 2004 522 525
23. A. La Terza, G. Papa, C. Miceli, and P. Luporini Divergence between two Antarctic species of the ciliate Euplotes, E. focardii and E. nobilii, in the expression of heat-shock protein 70 genes Molecular Ecology 10 2001 1061 1067
24. A. LA TERZA, C. MICELI, and P. LUPORINI The gene for the heat-shock protein 70 of Euplotes focardii, an Antarctic psychrophilic ciliate Antarctic Science 16 2004 23 28
25. F. Chiappori, S. Pucciarelli, I. Merelli, P. Ballarini, C. Miceli, and L. Milanesi Structural thermal adaptation of beta-tubulins from the Antarctic psychrophilic protozoan Euplotes focardii Proteins 80 2012 1154 1166
26. S. Pucciarelli, A. La Terza, P. Ballarini, S. Barchetta, T. Yu, F. Marziale, V. Passini, B. Methe, H.W. Detrich 3rd, and C. Miceli Molecular cold-adaptation of protein function and gene regulation: the case for comparative genomic analyses in marine ciliated protozoa Marine Genomics 2 2009 57 66
27. S. Pucciarelli, F. Marziale, G. Di Giuseppe, S. Barchetta, and C. Miceli Ribosomal cold-adaptation: characterization of the genes encoding the acidic ribosomal P0 and P2 proteins from the Antarctic ciliate Euplotes focardii Gene 360 2005 103 110
28. A. Valbonesi, and P. Luporini Description of two new species of Euplotes and Euplotes rariseta from Antarctica Polar Biol 11 1990 47 53
29. S. Pucciarelli, and C. Miceli Characterization of the cold-adapted alpha-tubulin from the psychrophilic ciliate Euplotes focardii Extremophiles: Life Under Extreme Conditions 6 2002 385 389
30. T.M. Rose, E.R. Schultz, J.G. Henikoff, S. Pietrokovski, C.M. McCallum, and S. Henikoff Consensus-degenerate hybrid oligonucleotide primers for amplification of distantly related sequences Nucleic Acids Research 26 1998 1628 1635
31. D.C. Hoffman, R.C. Anderson, M.L. DuBois, and D.M. Prescott Macronuclear gene-sized molecules of hypotrichs Nucleic Acids Research 23 1995 1279 1283
32. S.N. Ho, H.D. Hunt, R.M. Horton, J.K. Pullen, and L.R. Pease Site-directed mutagenesis by overlap extension using the polymerase chain reaction Gene 77 1989 51 59
33. N.J. Kruger The Bradford method for protein quantitation Methods in Molecular Biology 32 1994 9 15
34. E.T.S. Teorell Universal buffer over the pH range 2.0 to 12.0 Biochemische Zeitschrift 299 1938 416 419
35. M. Dixon, and E.C. Webb Enzymes 1964 Academic Press New York
36. K. Arnold, L. Bordoli, J. Kopp, and T. Schwede The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling Bioinformatics 22 2006 195 201
37. L. Bordoli, F. Kiefer, K. Arnold, P. Benkert, J. Battey, and T. Schwede Protein structure homology modeling using SWISS-MODEL workspace Nature Protocols 4 2009 1 13
38. F. Jonsson, J. Postberg, and H.J. Lipps The unusual way to make a genetically active nucleus DNA and Cell Biology 28 2009 71 78
39. R. Salacha, F. Kovacic, C. Brochier-Armanet, S. Wilhelm, J. Tommassen, A. Filloux, R. Voulhoux, and S. Bleves The Pseudomonas aeruginosa patatin-like protein PlpD is the archetype of a novel Type V secretion system Environmental Microbiology 12 2010 1498 1512
40. S. D'Amico, T. Collins, J.C. Marx, G. Feller, and C. Gerday Psychrophilic microorganisms: challenges for life EMBO Reports 7 2006 385 389
41. S. Pucciarelli, S.K. Parker, H.W. Detrich 3rd, and R. Melki Characterization of the cytoplasmic chaperonin containing TCP-1 from the Antarctic fish Notothenia coriiceps Extremophiles: Life Under Extreme Conditions 10 2006 537 549
42. P.L. Wintrode, K. Miyazaki, and F.H. Arnold Cold adaptation of a mesophilic subtilisin-like protease by laboratory evolution The Journal of Biological Chemistry 275 2000 31635 31640
43. B. Jaouadi, N. Aghajari, R. Haser, and S. Bejar Enhancement of the thermostability and the catalytic efficiency of Bacillus pumilus CBS protease by site-directed mutagenesis Biochimie 92 2010 360 369
44. Y. Nakagawa, A. Hasegawa, J. Hiratake, and K. Sakata Engineering of Pseudomonas aeruginosa lipase by directed evolution for enhanced amidase activity: mechanistic implication for amide hydrolysis by serine hydrolases Protein Engineering, Design & Selection: PEDS 20 2007 339 346
45. I. Kauffmann, and C. Schmidt-Dannert Conversion of Bacillus thermocatenulatus lipase into an efficient phospholipase with increased activity toward long-chain fatty acyl substrates by directed evolution and rational design Protein Engineering 14 2001 919 928
46. C. De Santi, M.L. Tutino, L. Mandrich, M. Giuliani, E. Parrilli, P. Del Vecchio, and D. de Pascale The hormone-sensitive lipase from Psychrobacter sp. TA144: new insight in the structural/functional characterization Biochimie 92 2010 949 957
47. I.H. Park, S.H. Kim, Y.S. Lee, S.C. Lee, Y. Zhou, C.M. Kim, S.C. Ahn, and Y.L. Choi Gene cloning, purification, and characterization of a cold-adapted lipase produced by Acinetobacter baumannii BD5 Journal of Microbiology and Biotechnology 19 2009 128 135
48. D.M. Lan, N. Yang, W.K. Wang, Y.F. Shen, B. Yang, and Y.H. Wang A novel cold-active lipase from Candida albicans: cloning, expression and characterization of the recombinant enzyme International Journal of Molecular Sciences 12 2011 3950 3965
49. I. Mayordomo, F. Randez-Gil, and J.A. Prieto Isolation, purification, and characterization of a cold-active lipase from Aspergillus nidulans Journal of Agricultural and Food Chemistry 48 2000 105 109
50. D.W. Choo, T. Kurihara, T. Suzuki, K. Soda, and N. Esaki A cold-adapted lipase of an Alaskan psychrotroph, Pseudomonas sp. strain B11-1: gene cloning and enzyme purification and characterization Applied and Environmental Microbiology 64 1998 486 491
51. T. Lonhienne, C. Gerday, and G. Feller Psychrophilic enzymes: revisiting the thermodynamic parameters of activation may explain local flexibility Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology 1543 2000 1 10
52. A.E. Fedoy, N. Yang, A. Martinez, H.K. Leiros, and I.H. Steen Structural and functional properties of isocitrate dehydrogenase from the psychrophilic bacterium Desulfotalea psychrophila reveal a cold-active enzyme with an unusual high thermal stability Journal of Molecular Biology 372 2007 130 149
53. P. Gatti-Lafranconi, A. Natalello, S. Rehm, S.M. Doglia, J. Pleiss, and M. Lotti Evolution of stability in a cold-active enzyme elicits specificity relaxation and highlights substrate-related effects on temperature adaptation Journal of Molecular Biology 395 2010 155 166
54. H.K. Leiros, A.L. Pey, M. Innselset, E. Moe, I. Leiros, I.H. Steen, and A. Martinez Structure of phenylalanine hydroxylase from Colwellia psychrerythraea 34H, a monomeric cold active enzyme with local flexibility around the active site and high overall stability The Journal of Biological Chemistry 282 2007 21973 21986
55. L. Kulakova, A. Galkin, T. Nakayama, T. Nishino, and N. Esaki Cold-active esterase from Psychrobacter sp. Ant300: gene cloning, characterization, and the effects of Gly - >Pro substitution near the active site on its catalytic activity and stability Biochimica et Biophysica acta 1696 2004 59 65
56. S. Dhondt, P. Geoffroy, B.A. Stelmach, M. Legrand, and T. Heitz Soluble phospholipase A2 activity is induced before oxylipin accumulation in tobacco mosaic virus-infected tobacco leaves and is contributed by patatin-like enzymes The Plant Journal: For Cell and Molecular Biology 23 2000 431 440
57. S. La Camera, P. Geoffroy, H. Samaha, A. Ndiaye, G. Rahim, M. Legrand, and T. Heitz A pathogen-inducible patatin-like lipid acyl hydrolase facilitates fungal and bacterial host colonization in Arabidopsis The Plant Journal: For Cell and Molecular Biology 44 2005 810 825
58. D.G. Mordue, C.F. Scott-Weathers, C.M. Tobin, and L.J. Knoll A patatin-like protein protects Toxoplasma gondii from degradation in activated macrophages Molecular Microbiology 63 2007 482 496
59. J. Florin-Christensen, M. Florin-Christensen, J. Knudsen, and L. Rasmussen Phospholipases and phosphonolipids in a ciliate: an attack and defence system? Trends in Biochemical Sciences 11 1986 354 355
60. R.D. Schmid, and R. Verger Lipases: interfacial enzymes with attractive applications Angewandte Chemie 37 1998 1608
61. L. De Maria, J. Vind, K.M. Oxenboll, A. Svendsen, and S. Patkar Phospholipases and their industrial applications Applied Microbiology and Biotechnology 74 2007 290 300
62. J. Mansfeld Plant phospholipases A2: perspectives on biotechnological applications Biotechnology Letters 31 2009 1373 1380