Impact of the native-state stability of human lysozyme variants on protein secretion by Pichia pastoris

FEBS Journal

Volumn 273, Issue 4, 2006, Pages 711-720

  Kumita, Janet R ^a   Johnson, Russell J K ^a   Alcocer, Marcos J C ^b   Dumoulin, Mireille ^a   Holmqvist, Fredrik ^b   McCammon, Margaret G ^a   Robinson, Carol V ^a   Archer, David B ^b   Dobson, Christopher M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Amyloidosis; Lysozyme; Protein degradation; Protein folding; Protein secretion

Indexed keywords

ENZYME VARIANT; LYSOZYME; MESSENGER RNA;

ARTICLE; CORRELATION ANALYSIS; ENZYME ANALYSIS; ENZYME STABILITY; GENE MUTATION; GENETIC TRANSCRIPTION; NONHUMAN; PICHIA PASTORIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN SECRETION; PROTEIN STABILITY; QUALITY CONTROL; THERMOSTABILITY; YEAST;

AMYLOIDOSIS; ENZYME STABILITY; HUMANS; ISOENZYMES; MODELS, MOLECULAR; MURAMIDASE; PICHIA; PROTEIN DENATURATION; PROTEIN STRUCTURE, TERTIARY; RNA, MESSENGER;

PICHIA PASTORIS;

EID: 33644939444     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2005.05099.x     Document Type: Article

References (48)

1. Fleming A 1922 On a remarkable bacteriolytic element found in tissues and secretions Proc R Soc Lond B 93 306 317
2. Artymiuk PJ Blake CCF 1981 Refinement of human lysozyme at 1.5 Å resolution analysis of non-bonded and hydrogen-bond interactions J Mol Biol 152 737 762
3. Taniyama Y Yamamoto Y Kuroki R Kikuchi M 1990 Evidence for difference in the roles of two cysteine residues involved in disulfide bond formation in the folding of human lysozyme J Biol Chem 265 7570 7575
4. Hooke SD Radford SE Dobson CM 1994 The refolding of human lysozyme: a comparison with the structurally homologous hen lysozyme Biochemistry 33 5867 5876
5. Hooke SD Eyles SJ Miranker A Radford SE Robinson CV Dobson CM 1995 Cooperative elements in protein folding monitored by electrospray ionization mass spectrometry J Am Chem Soc 117 7548 7549
6. Haezebrouck P Joniau M Van Dael H Hooke SD Woodruff ND Dobson CM 1995 An equilibrium partially folded state of human lysozyme at low pH J Mol Biol 246 382 387
7. Muraki M Harata K 1996 Origin of carbohydrate recognition specificity of human lysozyme revealed by affinity labeling Biochemistry 35 13562 13567
8. Funahashi J Takano K Ogasahara K Yamagata Y Yutani K 1996 The structure, stability, and folding process of amyloidogenic mutant human lysozyme J Biochem (Tokyo) 120 1216 1223
9. Canet D Sunde M Last AM Miranker A Spencer A Robinson CV Dobson CM 1999 Mechanistic studies of the folding of human lysozyme and the origin of amyloidogenic behavior in its disease-related variants Biochemistry 38 6419 6427
10. Funahashi J Takano K Yamagata Y Yutani K 2000 Role of surface hydrophobic residues in the conformational stability of human lysozyme at three different positions Biochemistry 39 14448 14456
11. Takano K Funahashi J Yutani K 2001 The stability and folding process of amyloidogenic mutant human lysozymes Eur J Biochem 268 155 159
12. Dumoulin M Last AM Desmyter A Decanniere K Canet D Larsson G Spencer A Archer DB Sasse J Muyldermans S et al. 2003 A camelid antibody fragment inhibits the formation of amyloid fibrils by human lysozyme Nature 424 783 788
13. Dumoulin M Canet D Last AM Pardon E Archer DB Muyldermans S Wyns L Matagne A Robinson CV Redfield C et al. 2005 Reduced global cooperativity is a common feature underlying the amyloidogenicity of pathogenic lysozyme mutations J Mol Biol 346 773 788
14. Dumoulin M Bellotti V Dobson CM 2005 Hereditary systemic amyloidosis associated with mutational variants of human lysozyme Amyloid Proteins: The Beta Pleated Sheet Conformation and Disease Sipe J, ed.), pp. 635 656 Wiley-VCH-Verlag Weinheim
15. Pepys MB Hawkins PN Booth DR Vigushin DM Tennent GA Soutar AK Totty N Nguyen O Blake CCF Terry CJ et al. 1993 Human lysozyme gene mutations cause hereditary systemic amyloidosis Nature 362 553 557
16. Gillmore JD Booth DR Madhoo S Pepys MB Hawkins PN 1999 Hereditary renal amyloidosis associated with variant lysozyme in a large English family Nephrol Dial Transplant 14 2639 2644
17. Booth DR Sunde M Bellotti V Robinson CV Hutchinson WL Fraser PE Hawkins PN Dobson CM Radford SE Blake CCF et al. 1997 Instability, unfolding and aggregation of human lysozyme variants underlying amyloid fibrillogenesis Nature 385 787 793
18. Booth DR Pepys MB Hawkins PN 2000 A novel variant of human lysozyme (T70N) is common in the normal population Hum Mutat 16 180
19. Yazaki M Farrell SA Benson MD 2003 A novel lysozyme mutation Phe57Ile associated with hereditary renal amyloidosis Kidney Int 63 1652 1657
20. Esposito G Garcia J Mangione P Giorgetti S Corazza A Viglino P Chiti F Andreola A Dumy P Booth D et al. 2003 Structural and folding dynamics properties of T70N variant of human lysozyme J Biol Chem 278 25910 25918
21. Johnson RJK Christodoulou J Dumoulin M Caddy G Alcocer MJ Murtagh GJ Kumita JR Larsson G Robinson CV Archer DB et al. 2005 Rationalising lysozyme amyloidosis: insight from the structure and solution dynamics of T70N lysozyme J Mol Biol 352 823 836
22. Harata K Abe Y Muraki M 1998 Full-matrix least-squares refinement of lysozymes and analysis of anisotropic thermal motion Prot Struct Funct Genet 30 232 243
23. Canet D Last AM Tito P Sunde M Spencer A Archer DB Redfield C Robinson CV Dobson CM 2002 Local cooperativity in the unfolding of an amyloidogenic variant of human lysozyme Nat Struct Biol 9 308 315
24. Valleix S Drunat S Philit JB Adoue D Piette JC Droz D MacGregor B Canet D Delpech M Grateau G 2002 Hereditary renal amyloidosis caused by a new variant lysozyme W64R in a French family Kidney Int 61 907 912
25. Takano K Ogasahara K Kaneda D Yamagata Y Fujii S Kanaya E Kikuchi M Oobatake M Yutani K 1995 Contribution of hydrophobic residues to the stability of human lysozyme: caliometric studies and X-ray structural analysis of the five isoleucine to valine mutants J Mol Biol 254 62 76
26. Takano K Yamagata Y Fujii S Yutani K 1997 Contribution of the hydrophobic effect to the stability of human lysozyme: calorimetric studies and X-ray structural analyses of the nine valine to alanine mutants Biochemistry 36 688 698
27. Takano K Yamagata Y Kubota M Funahashi J Fujii S Yutani K 1999 Contribution of hydrogen bonds to the conformational stability of human lysozyme: calorimetry and X-ray analysis of six Ser to Ala mutants Biochemistry 38 6623 6629
28. Funahashi J Takano K Yamagata Y Yutani K 1999 Contribution of amino acid substitutions at two different interior positions to the conformational stability of human lysozyme Protein Eng 12 841 850
29. Takano K Yamagata Y Funahashi J Hioki Y Kuramitsu S Yutani K 1999 Contribution of intra- and intermolecular hydrogen bonds to the conformational stability of human lysozyme Biochemistry 38 12698 12708
30. Horikoshi T Sakakibara M 2000 Quantification of relative mRNA expression in the rat brain using simple RT-PCR and ethidium bromide staining J Neurosci Methods 99 45 51
31. Engelhard M Evans PA 1995 Kinetics of interaction of partially folded proteins with a hydrophobic dye: evidence that molten globule character is maximal in early folding intermediates Protein Sci 4 1553 1562
32. Cereghino GP Cereghino JL Ilgen C Cregg JM 2002 Production of recombinant proteins in fermenter cultures of the yeast Pichia pastoris Curr Opin Biotechnol 13 329 332
33. Outeiro TF Lindquist S 2003 Yeast cells provide insight into alpha-synuclein biology and pathobiology Science 302 1772 1775
34. Kowalski JM Parekh RN Wittrup KD 1998 Secretion efficiency in Saccharomyces cerevisiae of bovine pancreatic trypsin inhibitor mutants lacking disulfide bonds is correlated with thermodynamic stability Biochemistry 37 1264 1273
35. Kjeldsen T Pettersson AF 2003 Relationship between self association of insulin and its secretion efficiency in yeast Protein Expr Purif 27 331 337
36. Song Y Sakai J Usui M Azakami H Kato A 2002 Relationship between the stability of lysozymes mutated at the inside hydrophobic core and secretion in Saccharomyces cerevisisae Nahrung 46 209 213
37. Shusta EV Kieke MC Parke E Kranz DM Wittrup KD 1999 Yeast polypeptide fusion surface display levels predict thermal stability and soluble secretion efficiency J Mol Biol 292 949 956
38. Goda S Takano K Yamagata Y Katakura Y Yutani K 2000 Effect of extra N-terminal residues on the stability and folding of human lysozyme expressed in Pichia pastoris Protein Eng 13 299 307
39. Taniyama Y Ogasahara K Yutani K Kikuchi M 1992 Folding mechanism of mutant human lysozyme C77/95A with increased secretion efficiency in yeast J Biol Chem 267 4619 4624
40. Calloni G Zoffoli S Stefani M Dobson CM Chiti F 2005 Investigating the effects of mutations on protein aggregation in the cell J Biol Chem 280 10607 10613
41. Chrunyk BA Evans J Lillquist J Young P Wetzel R 1993 Inclusion body formation and protein stability in sequence variants of interleukin-1β J Biol Chem 268 18053 18061
42. Sekijima Y Wiseman RL Matteson J Hammarström P Miller SR Sawkar AR Balch WE Kelly JW 2005 The biological and chemical basis for tissue selective amyloid disease Cell 121 73 85
43. Brake AJ Merryweather JP Coit DG Heberlein UA Masiarz FR Mullenbach GT Urdea MS Valenzuela P Barr PJ 1984 α-Factor-directed synthesis and secretion of mature foreign proteins in Saccharomyces cerevisiae Proc Natl Acad Sci USA 81 4642 4646
44. Oka C Tanaka M Muraki M Harata K Suzuki K Jigami Y 1999 Human lysozyme secretion increased by alpha-factor pro-sequence in Pichia pastoris Biosci Biotechnol Biochem 63 1977 1983
45. Lee YC Yang D 2002 Determination of lysozyme activities in a microplate format Anal Biochem 310 223 224
46. Gill SC von Hippel PH 1989 Calculation of protein extinction coefficients from amino acid sequence data Anal Biochem 182 319 326
47. Mombelli E Afshar M Fusi P Mariani M Tortora P Connelly JP Lange R 1997 The role of phenylalanine 31 in maintaining the conformational stability of ribonuclease P2 from Sulfolobus solfataricus under extreme conditions of temperature and pressure Biochemistry 36 8733 8742
48. Koradi R Billeter M Wuthrich K 1996 MOLMOL: a program for display and analysis of macromolecular structures J Mol Graph 14 51-5 29 32