Enhanced tolerance against freezing stress in Escherichia coli cells expressing an algal cyclophilin gene

Biotechnology and Bioprocess Engineering

Volumn 12, Issue 5, 2007, Pages 502-507

  Cho, Eun Kyung ^a  

^a Silla University   (South Korea)

Author keywords

Cyclophilin; Escherichia coli; Freezing tolerance; Griffithsia japonica; In vivo and in vitro function

Indexed keywords

ARABINOSE; COMPLEMENTARY DNA; CYCLOPHILIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CELL; BACTERIAL GENETICS; CELL INCLUSION; CELL VIABILITY; COLD STRESS; CONTROLLED STUDY; ESCHERICHIA COLI; FREEZE THAWING; FREEZING TOLERANCE; GENE EXPRESSION; GENE FUNCTION; GENE ISOLATION; GENE OVEREXPRESSION; IN VITRO STUDY; NONHUMAN; PROTEIN INDUCTION; PROTEIN STABILITY; RED ALGA; TEMPERATURE DEPENDENCE; THERMOSTABILITY;

ALGAE; ESCHERICHIA COLI; GRIFFITHSIA JAPONICA; RHODOPHYTA;

EID: 36049050959     PISSN: 12268372     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF02931347     Document Type: Article

References (46)

1. Antikainen, M. and M. Griffith (1997) Antifreeze protein accumulation in freezing-tolerant cereals. Physiol. Plant. 99: 423-432.
2. Boothe, J. G., F. D. Sonnichsen, M. D. de Beus, and A. M. Johnson-Flanagan (1997) Purification, characterization, and structural analysis of a plant low-temperature-induced protein. Plant Physiol. 113: 367-376.
3. Ndong, C., F. Ouellet, M. Houde, and F. Sarhan (1997) Gene expression during cold acclimation in strawberry. Plant Cell Physiol. 38: 863-870.
4. Tiku, P. E., A. Y. Gracey, A. I. Macartney, R. J. Beynon, and A. R. Cossins (1996) Cold-induced expression of delta 9-desaturase in carp by transcriptional and post-transcriptional mechanisms. Science 271: 815-818.
5. Yamashita, M., N. Ojima, and T. Sakamoto (1996) Molecular cloning and cold-inducible gene expression of ferritin H subunit isoforms in rainbow trout cells. J. Biol. Chem. 271: 26908-26913.
6. Pearce, R. S. (1999) Molecular analysis of acclimation to cold. Plant Growth Regul. 29: 47-76.
7. Arora, R., L. J. Rowland, and G. R. Panta (1997) Chill-responsive dehydrins in blueberry: Are they associated with cold hardiness or dormancy transitions? Physiol. Plant. 101: 8-16.
8. Ferullo, J. M., L. P. Vezina, J. Rail, S. Laberge, P. Nadeau, and Y. Castonguay (1997) Differential accumulation of two glycine-rich proteins during cold-acclimation alfalfa. Plant Mol. Biol. 33: 625-633.
9. Sokolova, I. M. and H. O. Pötner (2003) Metabolic plasticity and critical temperatures for aerobic scope in a eurythermal marine invertebrate (Littorina saxatilis, Gastropoda: Littorinidae) from different latitudes. J. Exp. Biol. 206: 195-207.
10. Zhu, B., T. H. H. Chen, and P. H. Li (1993) Expression of an ABA-responsive osmotin-like gene during the induction of freezing tolerance in Solanum commersonii. Plant Mol. Biol. 21: 729-735.
11. Lewis, J. G., R. P. Learmonth, and K. Watson (1995) Induction of heat, freezing and salt tolerance by heat and salt shock in Saccharomyces cerevisiae. Microbiology 141: 687-694.
12. Queitsch, C., S. W. Hong, E. Vierling, and S. Lindquist (2000) Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. Plant Cell 12: 479-492.
13. Boston, R. S., P. V. Viitanen, and E. Vierling (1996) Molecular chaperones and protein folding in plants. Plant Mol. Biol. 32: 191-222.
14. Cho, E. K., Y. K. Lee, and C. B. Hong (2005) A cyclophilin from Griffithsia japonica has thermoprotective activity and is affected by CsA. Mol. Cells 20: 142-150.
15. Luan, S., W. S. Lane, and S. L. Schreiber (1994) pCyP B: a chloroplast-localized, heat shock-responsive cyclophilin from fava bean. Plant Cell 6: 885-892.
16. Marivet, J., M. Margis-Pinheiro, P. Frendo, and G. Burkard (1994) Bean cyclophilin gene expression during plant development and stress conditions. Plant Mol. Biol. 26: 1181-1189.
17. Marivet, J., M. Margispinheiro, P. Frendo, and G. Burkard (1995) DNA sequence analysis of a cyclophilin gene from maize: developmental expression and regulation by salicylic acid. Mol. Gen. Genet. 247: 222-228.
18. Mark, P. J., B. K. Ward, P. Kumar, H. Lahooti, R. F. Minchin, and T. Ratajczak (2001) Human cyclophilin 40 is a heat shock protein that exhibits altered intracellular localization following heat shock. Cell Stress Chaperones 6: 59-70.
19. Clubb, R. T., S. B. Ferguson, C. T. Walsh, and G. Wagner (1994) Three-dimensional solution structure of Escherichia coli periplasmic cyclophilin. Biochemistry 33: 2761-2772.
20. Fejzo, J., F. A. Etzkorn, R. T. Clubb, Y. Shi, C. T. Walsh, and G. Wagner (1994) The mutant Escherichia coli F112W cyclophilin binds cyclosporin A in nearly identical conformation as human cyclophilin. Biochemistry 33: 5711-5720.
21. Lee, Y. K., C. B. Hong, Y. Suh, and I. K. Lee (2002) A cDNA clone for cyclophilin from Griffithsia japonica and phylogenetic analysis of cyclophilins. Mol. Cells 13: 12-20.
22. English, T. E. and K. B. Storey (2003) Freezing and anoxia stresses induce expression of metallothionein in the foot muscle and hepatopancreas of the marine gastropod Littorina littorea. J. Exp. Biol. 206: 2517-2524.
23. Larade, K., A. Nimigan, and K. B. Storey (2001) Transcription pattern of ribosomal protein L26 during anoxia exposure in Littorina littorea. J. Exp. Zool. 290: 759-768.
24. Mcnally, J. D., S. B. Wu, C. M. Sturgeon, and K. B. Storey (2002) Identification and characterization of a novel freezing inducible gene, li16, in the wood frog Rana sylvatica. FASEB J. 16: 902-904.
25. Kim, K. P., M. K. Joe, and C. B. Hong (2004) Tobacco small heat-shock protein, NtHSP18.2, has broad substrate range as a molecular chaperone. Plant Sci. 167: 1017-1025.
26. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 72: 248-254.
27. Sambrook, J., E. F. Fritsch, and T. Maniatis (1989) Molecular Cloning: A Laboratory Manual. 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA.
28. Duina, A. A., J. A. Marsh, R. B. Kurtz, H. J. Chang, S. Lindquist, and R. F. Gaber (1998) The peptidyl-prolyl isomerase domain of the CyP-40 cyclophilin homolog Cpr7 is not required to support growth or glucocorticoid receptor activity in Saccharomyces cerevisiae. J. Biol. Chem. 273: 10819-10822.
29. Liu, X. D., K. A. Morano, and D. J. Thiele (1999) The yeast Hsp100 family member, Sse1, is an Hsp90 cochaperone. J. Biol. Chem. 274: 26654-26660.
30. Weisman, R., J. Creanor, and P. Fantes (1996) A multicopy suppressor of a cell cycle defect in Schizosaccharomyces pombe encodes a heat shock-inducible 40 kDa cyclophilin-llke protein. EMBO J. 15: 447-456.
31. Küllertz, G., A. Liebau, P. Rücknagel, A. Schierhom, B. Diettrich, G. Fischer, and M. Luckner (1999) Stress-induced expression of cyclophilins in proembryonic masses of Digitalis lanata does not protect against freezing/thawing stress. Planta 208: 599-605.
32. Guy, C. L., D. Haskell, and Q. B. Li (1998) Association of proteins with the stress 70 molecular chaperones at low temperature: evidence for the existence of cold labile proteins in spinach. Cryobiology 36: 301-314.
33. Sung, D. Y., E. Vierling, and C. L. Guy (2001) Comprehensive expression profile analysis of the Arabidopsis Hsp70 gene family. Plant Physiol. 126: 789-800.
34. Lopez-Matas, M. A., P. Nuñez, A. Soto, I. Allona, R. Casado, C. Collada, M. A. Guevara, C. Aragoncillo, and L. Gomez (2004) Protein cryoprotective activity of a cytosolic small heat shock protein that accumulates constitutively in chestnut stems and is up-regulated by low and high temperatures. Plant Physiol. 134: 1708-1717.
35. Place, S. P. and G. E. Hofmann (2005) Temperature differentially affects adenosine triphosphatase activity in Hsc70 orthologs from Antarctic and New Zealand notothenioid fishes. Cell Stress Chaperones 10:104-113.
36. Walker, D. C., H. S. Girgis, and T. R. Klaenhammer (1999) The groESL chaperone operon of Lactobacillus johnsonii. Appl. Environ. Microbiol. 65: 3033-3041.
37. Chow, K. C. and W. L. Tung (1998) Overexpression of dnaK/dnaJ and groEL confers freeze tolerance to Escherichia coli. Biochem. Biophys. Res. Commun. 253: 502-505.
38. Tesic, M., J. A. Marsh, S. B. Cullinan, and R. F. Gaber (2003) Functional interactions between Hsp90 and the co-chaperones Cns1 and Cpr7 in Saccharomyces cerevisiae. J. Biol. Chem. 278: 32692-32701.
39. Edvardsson, A., S. Eshaghi, A. V. Vener, and B. Andersson (2003) The major peptidyl-prolyl isomerase activity in thylakoid lumen of plant chloroplasts belongs to a novel cyclophilin TLP20. FEBS Lett. 542: 137-141.
40. Kern, G., D. Kern, F. X. Schmid, and G. Fischer (1994) Reassessment of the putative chaperone function of prolylcis/trans-isomerase. FEBS Lett. 348: 145-148.
41. Rutherford, S. L. and C. S. Zuker (1994) Protein folding and the regulation of signaling pathways. Cell 79: 1129-1132.
42. Kinoshita, T. and K. I. Shimazaki (1999) Characterization of cytosolic cyclophilin from guard cells of Vicia faba L. Plant Cell Physiol. 40: 53-59.
43. Schneider, H., N. Charara, R. Schmitz, S. Wehrli, V. Mikol, M. G. Zurini, V. F. Quesniaux, and N. R. Movva (1994) Human cyclophilin C: primary structure, tissue distribution, and determination of binding specificity for cyclosporins. Biochemistry 33: 8218-8224.
44. Kim, J. E., E. J. Kim, W. J. Rhee, and T. H. Park (2005) Enhanced production of recombinant protein in Escherichia coli using silkworm hemolymph. Biotechnol. Bioprocess Eng. 10: 353-356.
45. Shin, E. J., S. L. Park, S. J. Jeon, J. W. Lee, Y. T. Kim, Y. H. Kim, and S. W. Nam (2006) Effect of molecular chaperones on the soluble expression of alginate lyase in E. coli. Biotechnol. Bioprocess Eng. 11: 414-419.
46. Kim, H. and I. H. Kim (2005) Refolding of fusion ferritin by gel filtration chromatography (GFC). Biotechnol. Bioprocess Eng. 10: 500-504.