FK506-binding protein 22 from a psychrophilic bacterium, a cold shock-inducible peptidyl prolyl isomerase with the ability to assist in protein folding

International Journal of Molecular Sciences

Volumn 12, Issue 8, 2011, Pages 5261-5284

  Budiman, Cahyo ^a,c   Koga, Yuichi ^a   Takano, Kazufumi ^a,b   Kanaya, Shigenori ^a  

^a OSAKA UNIVERSITY   (Japan)

^b KYOTO PREFECTURAL UNIVERSITY   (Japan)

^c BOGOR AGRICULTURAL UNIVERSITY   (Indonesia)

Author keywords

Cold adaptation; FKBP22; Folding; Peptidyl prolyl cis trans isomerases (PPIases); Shewanella sp. SIB1

Indexed keywords

CHAPERONE; COLD SHOCK PROTEIN; FK 506 BINDING PROTEIN; FK 506 BINDING PROTEIN 22; PEPTIDYLPROLYL ISOMERASE; PROLINE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; PROTEIN BINDING;

CATALYSIS; COLD ACCLIMATIZATION; COLD SHOCK RESPONSE; COLD STRESS; DIMERIZATION; ENZYME ACTIVITY; ISOMERIZATION; NONHUMAN; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; PSYCHROPHILIC BACTERIUM; REVIEW; TEMPERATURE SENSITIVITY; ADAPTATION; CHEMISTRY; COLD; ENZYME ACTIVATION; ENZYME STABILITY; ISOMERISM; METABOLISM; SHEWANELLA; ULTRASTRUCTURE;

BACTERIA (MICROORGANISMS); SHEWANELLA SP.;

ADAPTATION, BIOLOGICAL; BACTERIAL PROTEINS; COLD TEMPERATURE; ENZYME ACTIVATION; ENZYME STABILITY; ISOMERISM; PROTEIN BINDING; PROTEIN FOLDING; SHEWANELLA; TACROLIMUS BINDING PROTEINS;

EID: 80052146969     PISSN: None     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms12085261     Document Type: Review

References (68)

1. Ray, M.K. Cold-stress response of low temperature adapted bacteria. Res. Signpost 2006, 37, 1-23.
2. Hendrik, J.P.; Hartl, F.U. Molecular chaperone functions of heat-shock proteins. Annu. Rev. Biochem. 1993, 62, 349-384.
3. Stetter, K.O. Hyperthermophilic prokaryotes. FEMS Microbiol. Rev. 1996, 1, 149-158.
4. Cavicchioli, R.; Charlton, T.; Ertan, H.; Omar, S.M.; Sidiqui, K.S.; Williams, T.J. Biotechnological uses of enzymes from psychrophiles. Microb. Biotechnol. 2011, 4, 449-460.
5. Kasana, R.C.; Gulati, A. Cellullase from psychrophilic microorganism: A review. J. Basic Microbiol. 2001, 5, 1-8.
6. Kasana, R.C. Protease from psychrotrophs: An overview. Crit. Rev. Microbiol. 2010, 2, 134-145.
7. Joseph, B.; Ramteke, P.W.; Thomas, G. Cold active microbial lipases: some hot issues and recent developments. Biotechnol. Adv. 2008, 5, 457-470.
8. Suzuki, Y.; Mizutani, Y.; Tsuji, T.; Ohtani, N.; Takano, K.; Haruki, M.; Morikawa, M.; Kanaya, S. Gene cloning, overproduction, and characterization of thermolabile alkaline phosphatase from a psychrotrophic bacterium. Biosci. Biotechnol. Biochem. 2005, 69, 364-373.
9. Feller, G.; Gerday, C. Psychrophylic enzymes: Hot topics in cold adaptation. Nat. Rev. Microbiol. 2003, 1, 200-208.
10. Piette, F.; D'Amico, S.; Struvay, C.; Mazzucchelli, G.; Renaut, J.; Tutino, M.L.; Danchin, A.; Leprince, P.; Feller, G. Proteomic of life at low temperatures: trigger factor is the primary chaperone in the Antartic bacterium Pseudoalteromonas haloplanktis TAC125. Mol. Microb. 2010, 76, 120-132.
11. Jacob, R.P.; Schmid, F.X. Energetic coupling between native-state prolyl isomerization and conformational protein folding. J. Mol. Biol. 2008, 377, 1560-1575.
12. Kay, J.E. Structure-function relationships in the FK5-506-binding protein (FKBP) family of peptidylprolyl cis-trans isomerases. Biochem. J. 1996, 314, 361-385.
13. Wang, C.C.; Tsou, C.L. Enzymes as chaperones and chaperones as enzymes. FEBS Lett. 1998, 425, 382-384.
14. Theuerkorn, M.; Fischer, G.; Schiene-Fischer, C. Prolyl cis/trans isomerase signaling pathway in cancer. Curr. Opin. Pharmacol. 2011, 11, 1-7.
15. Fanganel, J.; Fischer, G. Insights into the catalytic mechanism of peptidyl prolyl cis/trans isomerases. Front. Biosci. 2004, 9, 3453-3478.
16. Edlich, F.; Fischer, G. Pharmacological targeting of catalyzed protein folding: The example of peptide bond cis/trans isomerases. Handb. Exp. Pharmacol. 2006, 172, 359-404.
17. Scholz, C.; Eckert, B.; Hagn, F.; Schaarschmidt, P.; Balbach, J.; Schmid, F.X. SlyD proteins from different species exhibit high prolyl isomerase and chaperone activities. Biochemistry 1996, 45, 20-33.
18. Weininger, U.; Haupt, C.; Schweimer, K.; Graubner, W.; Kovermann, M.; Bruser, T.; Szholz, C.; Scaarshmidt, P.; Zoldak, G.; Schmid, F.X.; et al. NMR solution structure of SlyD from Escherichia coli: Spatial separation of prolyl isomerase and chaperone function. J. Mol. Biol. 2009, 387, 295-305.
19. Saul, F.A.; Arie, J.P.; Vulliez-le Normand, B.; Kahn, R.; Betto, N.J.M.; Bentley, G.A. Structure and functional studies of FkpA from Escherichia coli, a cis/trans peptidyl-prolyl isomerase with chaperone activity. J. Mol. Biol. 2004, 335, 595-608.
20. Suzuki, R.; Nagata, K.; Yumoto, F.; Kawakami, M.; Nemoto, N.; Furutani, M.; Adachi, K.; Maruyama, T.; Tanokura, M. Three-dimensional solution structure of an archaeal FKBP with a dual function of peptidyl prolyl cis-trans isomerase and chaperone-like activities. J. Mol. Biol. 2003, 328, 1149-1160.
21. Li, Z.Y.; Liu, C.P.; Zhu, L.Q.; Jing, G.Z.; Zhou, J.M. The chaperone activity of trigger factor is distinct from its isomerase activity during co-expression with adenylate kinase in Escherichia coli. FEBS Lett. 2001, 506, 108-112.
22. Pirkl, F.; Buchner, J. Functional analysis of the Hsp90-associated human peptidyl prolyl cis/trans isomerases FKBP51, FKBP52 and Cyp40. J. Mol. Biol. 2001, 308, 795-806.
23. Martinez-Heckert, E.; Hendrickson, W.A. Structural analysis of protein folding by the long-chain archeal chaperone FKBP26. J. Mol. Biol. 2011, 3, 450-464.
24. Budde, I.; Steil, L.; Scharf, C.; Volker, U.; Bremer, E. Adaptation of Bacillus subtilis to growth at low temperature: A combined transcriptomic and proteomic appraisal. Microbiology 2006, 3, 831-853.
25. Jaremko, L.; Jaremko, M.; Elfaki, I.; Mueller, J.W.; Ejchart, A.; Bayer, P.; Zhukov, I. Structure and dynamics of the first archaeal parvulin reveal a new functionally important loop in parvulin-type. J. Biol. Chem. 2011, 8, 6554-6565.
26. Suzuki, Y.; Haruki, M.; Takano, K.; Morikawa, M.; Kanaya, S. Possible involvement of an FKBP family member protein from a psychrotrophic bacterium Shewanella sp. SIB1 in cold-adaptation. Eur. J. Biochem. 2004, 271, 1372-1381.
27. Kato, T.; Haruki, M.; Imanaka, T.; Morikawa, M.; Kanaya, S. Isolation and characterization of psychotrophic bacteria from oil-reservoir water and oil sands. Appl. Microbiol. Biotechnol. 2001, 55, 794-800.
28. Kulakova, L.; Galkin, A.; Kurihara, T.; Yoshimura, T.; Esaki, N. Cold-active serine alkaline protease from the psychrotrophic bacterium Shewanella strain Ac10: Gene cloning and enzyme purification and characterization. Appl. Environ. Microbiol. 1999, 65, 611-617.
29. Ohtani, N.; Haruki, M.; Morikawa, M.; Kanaya, S. Heat labile ribonuclease HI from a psychrotrophic bacterium: gene cloning, characterization, and site-directed mutagenesis. Protein Eng. 2001, 14, 975-982.
30. Chon, H.; Tadokoro, T.; Ohtani, N.; Koga, Y.; Takano, K.; Kanaya, S. Identification of RNase HII from psychrotrophic bacterium, Shewanella sp. SIB1 as a high-activity type RNase H. FEBS J. 2006, 273, 2264-2275.
31. Sato, A.; Yokotani, S.; Tadokoro, T.; Tanaka, S.; Angkawidjaja, C.; Koga, Y.; Takano, K.; Kanaya, S. Crystal structure of stable protein CutA1 from psychrotrophic bacterium Shewanella sp. SIB1. J. Synchrotron Radiat. 2011, 18, 6-10.
32. Soni, K. A; Nannapaneni, R.; Tasara, T. The contribution of transcriptomic and proteomic analysis in elucidating stress adaptation responses of Listeria monocytogenes. Foodborne Pathog. Dis. 2011, 8, 843-852.
33. Tasara, T.; Stephan, R. Cold stress tolerance of Listeria monocytogenes: A review of molecular adaptive mechanisms and food safety implications. J. Food. Prot. 2006, 6, 1473-1484.
34. Garnier, M.; Matamoros, S.; Chevret, D.; Pilet, M.F.; Leori, F.; Tresse, O. Adaptation to cold and proteomic responses of the psychrotrophic biopreservative Lactococcus piscium strain CNCM I-4031. Appl. Environ. Microbiol. 2010, 24, 8011-8018.
35. Ting, L.; Williams, T.J.; Cowley, M.J.; Lauro, F.M.; Guilhaus, M.; Raftery, M.J.; Cavicchioli, R. Cold adaptation in the marine bacterium, Sphingopyxis alaskensis, assesed using quantitative proteomic. Environ. Microbiol. 2010, 10, 2658-2676.
36. Rahfeld, J.U.; Rucknagel, K. P; Stoller, G.; Horne S.M.; Schierhorn, A.; Young, K.D.; Fischer, G. Isolation and amino acid sequence of a new 22-kDa FKBP-like peptidyl-prolyl cis/transisomerase of Escherichia coli Similarity to Mip-like proteins of pathogenic bacteria. J. Biol. Chem. 1996, 271, 22130-22138.
37. Horne, S.M.; Young, K.D. Escherichia coli and other species of the Enterobacteriaceae encode a protein similar to the family of Mip-like FK506-binding proteins. Arch. Microbiol. 1995, 165, 357-365.
38. Engleberg, N.C.; Carter, C.; Weber, D.R.; Cianciotto, N.P.; Eisenstein, B.I. DNA sequence of mip, a Legionella pneumophila gene associated with macrophage infectivity. Infect. Immun. 1989, 57, 1263-1270.
39. Suzuki, Y.; Takano, K.; Kanaya, S. Stabilities and activities of the N-and C-domains of FKBP22 from a psychrotrophic bacterium overproduced in E. coli. FEBS J. 2005, 272, 632-642.
40. Budiman, C.; Bando, K.; Angkawidjaja, C.; Koga, Y.; Takano, K.; Kanaya, S. Engineering of monomeric FK506-binding protein 22 with peptidyl prolyl cis-trans isomerase: Importance of V-shaped dimeric structure for binding to protein substrate. FEBS J. 2009, 276, 4091-4101.
41. Tradler, T.; Stoller, G.; Rucknagel, K.P.; Schierhorn, A.; Rahfeld, J.U.; Fischer, G. Comparative mutational analysis of peptidyl prolyl cis/trans isomerases: active sites of Escherichia coli trigger factor and human FKBP12. FEBS Lett. 1997, 40, 184-190.
42. D'Amico, S.; Marx, J.C.; Gerday, C.; Feller, G. Activity-stability relationships in extremophilic enzymes. J. Biol. Chem. 2003, 278, 7891-7896.
43. Collins, T.; Meuwis, M.A.; Gerday, C.; Feller, G. Activity, stability and flexibility in glycosidases adapted to extreme thermal environments. J. Mol. Biol. 2003, 328, 419-428.
44. Fields, P.A.; Somero, G.N. Hot spots in cold adaptation: localized increases in conformational flexibility in lactate dehydrogenase A4 orthologs of Antarctic notothenioid fishes. Proc. Natl. Acad. Sci. USA 1998, 95, 11476-11481.
45. 1. 1. Existence of multiple unfolded states created by proline isomerization. Biochemistry 1990, 29, 3051-3061.
46. 1. 2. Kinetic models for the folding and unfolding reactions. Biochemistry 1990, 29, 3061-3070.
47. 1. Eur. J. Biochem. 1996, 241, 516-524.
48. Knappe, T.A.; Eckert, B.; Schaarschmidt, P.; Scholz, C.; Schmid, F.X. Insertion of a chaperone domain converts FKBP12 into a powerful catalyst of protein folding. J. Mol. Biol. 2007, 368, 1458-1468.
49. Hayer-Hartl, M.K.; Ewbank, J.J.; Creighton, T.E.; Hartl, F.U. Conformational specificity of the chaperonin GroEL for the compact folding intermediates of-lactalbumin. EMBO J. 1994, 13, 3192-3202.
50. Okazaki, A.; Ikura, T.; Nikaido, K.; Kuwajima, K. The chaperonin GroEL does not recognize apo-α-lactalbumin in the molten globule state. Nat. Struct. Biol. 1994, 1, 439-446.
51. Scholz, C.; Stoller, G.; Zarnt, T.; Fischer, G.; Schmid F.X. Cooperation of enzymatic and chaperone functions of trigger factor in the catalysis of protein folding. EMBO J. 1997, 16, 54-58.
52. Ramm, K.; Pluckthun, A. High enzymatic activity and chaperone function are mechanistically related features to the dimeric E. coli peptidyl-prolyl-isomerase FkpA. J. Mol. Biol. 2001, 310, 485-498.
53. Acharya, K.R.; Stuart, D.I.; Walker, N.P.; Lewis, M.; Philips, D.C. Refined structure of baboon-lactalbumin at 1.7 Å resolution. Comparison with C-type lysozyme. J. Mol. Biol. 1989, 1, 99-127.
54. Acharya, K. R; Ren, J.S.; Sturart, D.I.; Philips, D.; Fenna, R.E. Crystal structure of human-lactalbumin at 1.7 Å resolution. J. Mol. Biol. 1991, 2, 571-581.
55. Kuwajima, K. The molten globule state as a clue for understanding the folding and cooperativity of globular-protein structure. Proteins 1989, 6, 87-103.
56. Suzuki, Y.; Win, O.Y.; Koga, Y.; Takano, K.; Kanaya, S. Binding analysis of a psychrotrophic FKBP22 to a folding intermediate of protein using surface plasmon resonance. FEBS Lett. 2005, 579, 5781-5784.
57. Arie J.P.; Sassoon, N.; Betton, J.M. Chaperone function of FkpA, a heat shock prolyl isomerase, in the periplasm of Escherichia coli. Mol. Microbiol. 2001, 39, 199-210.
58. Hu, K.; Galius, V.; Pervushin, K. Structural plasticity of peptidyl-prolyl isomerase sFkpA is a key to its chaperone function as revealed by solution NMR. Biochemistry 2006, 45, 11983-11991.
59. Strocchi, M.; Ferrer, M.; Timmis, K.N.; Golyshin, P.N. Low temperature-induced system failure in Escherichia coli: insight from rescue by cold-adapted chaperones. Proteomics 2006, 6, 193-206.
60. Lu, K.P.; Finn, G.; Lee, T.H.; Nicholson, L.L. Prolyl cis-trans isomerization as molecular timer. Nat. Chem. Biol. 2007, 3, 619-629.
61. Ideno, A.; Yoshida, T.; Iida, T.; Furutani, M.; Maruyama, T. FK506-binding protein of hyperthermophilic archeum, Thermococcus sp. KS-1, a cold-shock-inducible peptidyl-prolyl cis-trans isomerase with activities to trap and refold denatured proteins. Biochem. J. 2001, 357, 465-471.
62. Kandror, O.; Goldberg, A.L. Trigger factor is induced upon cold shock and enhances viability of Escherichia coli at low temperatures. Proc. Natl. Acad. Sci. USA 1997, 94, 4978-4981.
63. Pissavin, C.; Hugouvieux-Cotte-Pattat, N. Characterization of a periplasmic peptidyl-prolyl cis-trans isomerase in Erwinia chrysanthemi. FEMS Microbiol. Lett. 1997, 157, 59-65.
64. Missiakas, D.; Raina, S. Protein folding in the bacterial periplasm. J. Bacteriol. 1997, 179, 2465-2471.
65. Rouviere, P.E.; Gross, C.A. SurA, a periplasmic protein with peptidyl-prolyl isomerase activity, participates in the assembly of outer membrane porins. Genes Dev. 1996, 10, 3170-3182.
66. Basak, C.; Pathak, S.K.; Bhattacharyya, A.; Pathak, S.; Basu, J.; Kundu, M. The secreted peptidyl prolyl cis, trans-isomerase HP0175 of Helicobacter pylori induces apoptosis of gastric epithelial cells in a TLR4-and apoptosis signal-regulating kinase 1-dependent manner. J. Immunol. 2005, 174, 5672-5680.
67. DebRoy, S.; Aragon, V.; Kurtz, S.; Cianciotto, N.P. Legionella pneumophila Mip, a surface-exposed peptidylproline cis-trans-isomerase, promotes the presence of phospholipase Clike activity in culture supernatants. Infect. Immun. 2006, 74, 5152-5160.
68. Soderberg, M.A.; Rossier, O.; Cianciotto, N.P. The type II protein secretion system of Legionella pneumophila promotes growth at low temperatures. J. Bacteriol. 2004, 186, 3712-3720.