Highly stable mutants of human fibroblast growth factor-1 exhibit prolonged biological action

Journal of Molecular Biology

Volumn 352, Issue 4, 2005, Pages 860-875

  Zakrzewska, Malgorzata ^a   Krowarsch, Daniel ^a   Wiedlocha, Antoni ^b   Olsnes, Sjur ^b   Otlewski, Jacek ^a  

^a UNIVERSITY OF WROC AW   (Poland)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

FGF 1; Half life; Mitogenic activity; Protein engineering; Protein stability

Indexed keywords

FIBROBLAST GROWTH FACTOR 1; HEPARIN; MUTANT PROTEIN;

ARTICLE; CELL CULTURE; CONTROLLED STUDY; DNA DETERMINATION; DNA SYNTHESIS; DRUG HALF LIFE; DRUG POTENCY; FUNCTIONAL PROTEOMICS; HUMAN; HUMAN CELL; MITOGENESIS; MITOGENICITY; MUTAGENESIS; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DENATURATION; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STABILITY; SEQUENCE HOMOLOGY;

EID: 24644439092     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.07.066     Document Type: Article

References (80)

1. P.H. Tan, V. Chu, J.E. Stray, D.K. Hamlin, D. Pettit, and D.S. Wilbur Engineering the isoelectric point of a renal cell carcinoma targeting antibody greatly enhances scFv solubility Immunotechnology 4 1998 107 114
2. J. Temsamani, and P. Vidal The use of cell-penetrating peptides for drug delivery Drug Discov. Today 9 2004 1012 1019
3. B.A. Luxon, M. Grace, D. Brassard, and R. Bordens Pegylated interferons for the treatment of chronic hepatitis C infection Clin. Ther. 24 2002 1363 1383
4. S.W. Pipe, and R.J. Kaufman Characterization of a genetically engineered inactivation-resistant coagulation factor VIIIa Proc. Natl Acad. Sci. USA 94 1997 11851 11856
5. S. Elliott, T. Lorenzini, S. Asher, K. Aoki, D. Brankow, and L. Buck Enhancement of therapeutic protein in vivo activities through glycoengineering Nature Biotechnol. 21 2003 414 421
6. C.A. Sarkar, K. Lowenhaupt, T. Horan, T.C. Boone, B. Tidor, and D.A. Lauffenburger Rational cytokine design for increased lifetime and enhanced potency using pH-activated "histidine switching" Nature Biotechnol. 20 2002 908 913
7. L. Lin Betaseron Dev. Biol. Stand. 96 1998 97 104
8. S.A. Marshall, G.A. Lazar, A.J. Chirino, and J.R. Desjarlais Rational design and engineering of therapeutic proteins Drug Discov. Today 8 2003 212 221
9. G.A. Lazar, S.A. Marshall, J.J. Plecs, S.L. Mayo, and J.R. Desjarlais Designing proteins for therapeutic applications Curr. Opin, Struct. Biol. 13 2003 513 518
10. W. Wang Instability, stabilization, and formulation of liquid protein pharmaceuticals Int. J. Pharm. 185 1999 129 188
11. A.V. Filikov, R.J. Hayes, P. Luo, D.M. Stark, C. Chan, A. Kundu, and B.I. Dahiyat Computational stabilization of human growth hormone Protein Sci. 11 2002 1452 1461
12. P. Luo, R.J. Hayes, C. Chan, D.M. Stark, M.Y. Hwang, and J.M. Jacinto Development of a cytokine analog with enhanced stability using computational ultrahigh throughput screening Protein Sci. 11 2002 1218 1226
13. P.V. Nikolova, J. Henckel, D.P. Lane, and A.R. Fersht Semi-rational design of active tumor suppressor p53 DNA binding domain with enhanced stability Proc. Natl Acad. Sci. USA 95 1998 14675 14680
14. S. Ewert, A. Honegger, and A. Pluckthun Stability improvement of antibodies for extracellular and intracellular applications: CDR grafting to stable frameworks and structure-based framework engineering Methods 34 2004 184 199
15. D.M. Ornitz, and N. Itoh Fibroblast growth factors Genome Biol. 2 2001 3005.1 3005.12
16. N. Itoh, and D.M. Ornitz Evolution of the Fgf and Fgfr gene families Trends Genet. 20 2004 563 569
17. C.A. Orengo, D.T. Jones, and J.M. Thornton Protein superfamilies and domain superfolds Nature 372 1994 631 634
18. X. Zhu, H. Komiya, A. Chirino, S. Faham, G.M. Fox, and T. Arakawa Three-dimensional structures of acidic and basic fibroblast growth factors Science 251 1991 90 93
19. M.J. Bernett, T. Somasundaram, and M. Blaber An atomic resolution structure for human fibroblast growth factor 1 Proteins: Struct. Funct. Genet. 57 2004 626 634
20. J.F. Culajay, S.I. Blaber, A. Khurana, and M. Blaber Thermodynamic characterization of mutants of human fibroblast growth factor 1 with an increased physiological half-life Biochemistry 39 2000 7153 7158
21. R.A. Copeland, H. Ji, A.J. Halfpenny, R.W. Williams, K.C. Thompson, and W.K. Herber The structure of human acidic fibroblast growth factor and its interaction with heparin Arch. Biochem. Biophys. 289 1991 53 61
22. S.I. Blaber, J.F. Culajay, A. Khurana, and M. Blaber Reversible thermal denaturation of human FGF-1 induced by low concentrations of guanidine hydrochloride Biophys. J. 77 1999 470 477
23. W.H. Burgess, and T. Maciag The heparin-binding (fibroblast) growth factor family of proteins Annu. Rev. Biochem. 58 1989 575 606
24. M. Goldfarb Functions of fibroblast growth factors in vertebrate development Cytokine Growth Factor Rev. 7 1996 311 325
25. D. Vasiliauskas, and C.D. Stern Patterning the embryonic axis: FGF signaling and how vertebrate embryos measure time Cell 106 2001 133 136
26. E. Landgren, P. Klint, K. Yokote, and L. Claesson-Welsh Fibroblast growth factor receptor-1 mediates chemotaxis independently of direct SH2-domain protein binding Oncogene 17 1998 283 291
27. G.L. Barnes, P.J. Kostenuik, L.C. Gerstenfeld, and T.A. Einhorn Growth factor regulation of fracture repair J. Bone Miner. Res. 14 1999 1805 1815
28. M.J. Post, R. Laham, F.W. Sellke, and M. Simons Therapeutic angiogenesis in cardiology using protein formulations Cardiovasc. Res. 49 2001 522 531
29. B. Steipe, B. Schiller, A. Pluckthun, and S. Steinbacher Sequence statistics reliably predict stabilizing mutations in a protein domain J. Mol. Biol. 240 1994 188 192
30. S.R. Brych, S.I. Blaber, T.M. Logan, and M. Blaber Structure and stability effects of mutations designed to increase the primary sequence symmetry within the core region of a beta-trefoil Protein Sci. 10 2001 2587 2599
31. M. Zakrzewska, D. Krowarsch, A. Wiedlocha, and J. Otlewski Design of fully active FGF-1 variants with increased stability Protein Eng. Des. Sel. 17 2004 603 611
32. H. Mach, J.A. Ryan, C.J. Burke, D.B. Volkin, and C.R. Middaugh Partially structured self-associating states of acidic fibroblast growth factor Biochemistry 32 1993 7703 7711
33. S.Y. Venyaminov, and J.T. Yang Determination of protein secondary structure G.D. Fasman Circular Dichroism and Conformational Analysis of Biomolecules 1996 Plenum Press New York 69 107
34. C.J. Burke, D.B. Volkin, H. Mach, and C.R. Middaugh Effect of polyanions on the unfolding of acidic fibroblast growth factor Biochemistry 32 1993 6419 6426
35. J.A. Wells Additivity of mutational effects in proteins Biochemistry 29 1990 8509 8517
36. K.A. Dill Additivity principles in biochemistry J. Biol. Chem. 272 1997 701 704
37. S.J. Hubbard The structural aspects of limited proteolysis of native proteins Biochim. Biophys. Acta 1382 1998 191 206
38. O. Buczek, K. Koscielska-Kasprzak, D. Krowarsch, M. Dadlez, and J. Otlewski Analysis of serine proteinase-inhibitor interaction by alanine shaving Protein Sci. 11 2002 806 819
39. B. Reuss, and O. von Bohlen und Halbach Fibroblast growth factors and their receptors in the central nervous system Cell Tissue Res. 313 2003 139 157
40. P. Cuevas, F. Carceller, M. Redondo-Horcajo, R.M. Lozano, and G. Gimenez-Gallego Systemic administration of acidic fibroblast growth factor ameliorates the ischemic injury of the retina in rats Neurosci. Letters 255 1998 1 4
41. P. Cuevas, F. Carceller, D. Reimers, I. Saenz de Tejada, and G. Gimenez-Gallego Acidic fibroblast growth factor rescues gerbil hippocampal neurons from ischemic apoptotic death Neurol. Res. 20 1998 271 274
42. Y.S. Lee, I. Hsiao, and V.W. Lin Peripheral nerve grafts and aFGF restore partial hindlimb function in adult paraplegic rats J. Neurotrauma 19 2002 1203 1216
43. S.S. Kelpke, K.R. Zinn, L.W. Rue, and J.A. Thompson Site-specific delivery of acidic fibroblast growth factor stimulates angiogenic and osteogenic responses in vivo J. Biomed. Mater. Res. A 71 2004 316 325
44. J.A. Ware, and M. Simons Angiogenesis in ischemic heart disease Nature Med. 3 1997 158 164
45. S. Banai, M.T. Jaklitsch, W. Casscells, M. Shou, S. Shrivastav, and R. Correa Effects of acidic fibroblast growth factor on normal and ischemic myocardium Circ. Res. 69 1991 76 85
46. S.B. Freedman, and J.M. Isner Therapeutic angiogenesis for coronary artery disease Ann. Intern. Med. 136 2002 54 71
47. J.J. Lopez, E.R. Edelman, A. Stamler, M.G. Hibberd, P. Prasad, and K.A. Thomas Angiogenic potential of perivascularly delivered aFGF in a porcine model of chronic myocardial ischemia Am. J. Physiol. 274 1998 H930 H936
48. E.G. Hutchinson, and J.M. Thornton PROMOTIF-a program to identify and analyze structural motifs in proteins Protein Sci. 5 1996 212 220
49. E.G. Hutchinson, and J.M. Thornton A revised set of potentials for beta-turn formation in proteins Protein Sci. 3 1994 2207 2216
50. K. Guruprasad, and S. Rajkumar Beta and gamma-turns in proteins revisited: a new set of amino acid turn-type dependent positional preferences and potentials J. Biosci. 25 2000 143 156
51. P.Y. Chou, and G.D. Fasman Prediction of the secondary structure of proteins from their amino acid sequence Advan. Enzymol. Relat. Areas Mol. Biol. 47 1978 45 148
52. Y. Kallberg, M. Gustafsson, B. Persson, J. Thyberg, and J. Johansson Prediction of amyloid fibril-forming proteins J. Biol. Chem. 276 2001 12945 12950
53. A.E. Eriksson, L.S. Cousens, and B.W. Matthews Refinement of the structure of human basic fibroblast growth factor at 1.6 Åresolution and analysis of presumed heparin binding sites by selenate substitution Protein Sci. 2 1993 1274 1284
54. S.K. Olsen, M. Garbi, N. Zampieri, A.V. Eliseenkova, D.M. Ornitz, M. Goldfarb, and M. Mohammadi Fibroblast growth factor (FGF) homologous factors share structural but not functional homology with FGFs J. Biol. Chem. 278 2003 34226 34236
55. J. Kim, S.I. Blaber, and M. Blaber Alternative type I and I' turn conformations in the beta8/beta9 beta-hairpin of human acidic fibroblast growth factor Protein Sci. 11 2002 459 466
56. J.H. Carra, and P.L. Privalov Thermodynamics of denaturation of staphylococcal nuclease mutants: an intermediate state in protein folding FASEB J. 10 1996 67 74
57. T. Spivak-Kroizman, M.A. Lemmon, I. Dikic, J.E. Ladbury, D. Pinchasi, and J. Huang Heparin-induced oligomerization of FGF molecules is responsible for FGF receptor dimerization, activation, and cell proliferation Cell 79 1994 1015 1024
58. D.M. Ornitz FGFs, heparan sulfate and FGFRs: complex interactions essential for development Bioessays 22 2000 108 112
59. D.H. Damon, R.R. Lobb, P.A. D'Amore, and J.A. Wagner Heparin potentiates the action of acidic fibroblast growth factor by prolonging its biological half-life J. Cell. Physiol. 138 1989 221 226
60. J. Schlessinger, I. Lax, and M. Lemmon Regulation of growth factor activation by proteoglycans: what is the role of the low affinity receptors? Cell 83 1995 357 360
61. H. Bussey, and J.L. Francis Heparin overview and issues Pharmacotherapy 24 2004 103S 107S
62. S. Ortega, M.T. Schaeffer, D. Soderman, J. DiSalvo, D.L. Linemeyer, G. Gimenez-Gallego, and K.A. Thomas Conversion of cysteine to serine residues alters the activity, stability, and heparin dependence of acidic fibroblast growth factor J. Biol. Chem. 266 1991 5842 5846
63. D.A. Parsell, and R.T. Sauer The structural stability of a protein is an important determinant of its proteolytic susceptibility in Escherichia coli J. Biol. Chem. 264 1989 7590 7595
64. C. Park, and S. Marqusee Probing the high energy states in proteins by proteolysis J. Mol. Biol. 343 2004 1467 1476
65. X. Zhan, X. Hu, S. Friedman, and T. Maciag Analysis of endogenous and exogenous nuclear translocation of fibroblast growth factor-1 in NIH 3T3 cells Biochem. Biophys. Res. Commun. 188 1992 982 991
66. T. Imamura, S. Oka, T. Tanahashi, and Y. Okita Cell cycle-dependent nuclear localization of exogenously added fibroblast growth factor-1 in BALB/c 3T3 and human vascular endothelial cells Expt. Cell Res. 215 1994 363 372
67. A. Wiedlocha, P.O. Falnes, I.H. Madshus, K. Sandvig, and S. Olsnes Dual mode of signal transduction by externally added acidic fibroblast growth factor Cell 76 1994 1039 1051
68. A. Wiedlocha, P.O. Falnes, A. Rapak, O. Klingenberg, R. Munoz, and S. Olsnes Translocation of cytosol of exogenous, CAAX-tagged acidic fibroblast growth factor J. Biol. Chem. 270 1995 30680 30685
69. A. Wiedlocha, P.O. Falnes, A. Rapak, R. Munoz, O. Klingenberg, and S. Olsnes Stimulation of proliferation of a human osteosarcoma cell line by exogenous acidic fibroblast growth factor requires both activation of receptor tyrosine kinase and growth factor internalization Mol. Cell. Biol. 16 1996 270 280
70. I.A. Prudovsky, N. Savion, T.M. LaVallee, and T. Maciag The nuclear trafficking of extracellular fibroblast growth factor (FGF)-1 correlates with the perinuclear association of the FGF receptor-1alpha isoforms but not the FGF receptor-1beta isoforms J. Biol. Chem. 271 1996 14198 14205
71. T.A. Grieb, and W.H. Burgess The mitogenic activity of fibroblast growth factor-1 correlates with its internalization and limited proteolytic processing J. Cell. Physiol. 184 2000 171 182
72. S. Olsnes, O. Klingenberg, and A. Wiedlocha Transport of exogenous growth factors and cytokines to the cytosol and to the nucleus Physiol. Rev. 83 2003 163 182
73. V.E. Bychkova, R.H. Pain, and O.B. Ptitsyn The "molten globule" state is involved in the translocation of proteins across membranes? FEBS Letters 238 1988 231 234
74. J. Wesche, A. Wiedlocha, P.O. Falnes, S. Choe, and S. Olsnes Externally added aFGF mutants do not require extensive unfolding for transport to the cytosol and the nucleus in NIH/3T3 cells Biochemistry 39 2000 15091 15100
75. N. Guex, and M.C. Peitsch SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling Electrophoresis 18 1997 2714 2723
76. C.A. Kim, and J.M. Berg Thermodynamic beta-sheet propensities measured using a zinc-finger host peptide Nature 362 1993 267 270
77. C.N. Pace, F. Vajdos, L. Fee, G. Grimsley, and T. Gray How to measure and predict the molar absorption coefficient of a protein Protein Sci. 4 1995 2411 2423
78. G. Gimenez-Gallego, G. Conn, V.B. Hatcher, and K.A. Thomas The complete amino acid sequence of human brain-derived acidic fibroblast growth factor Biochem. Biophys. Res. Commun. 138 1986 611 617
79. M.M. Santoro, and D.W. Bolen A test of the linear extrapolation of unfolding free energy changes over an extended denaturant concentration range Biochemistry 31 1992 4901 4907
80. P.J. Fraker, and J.C. Speck Jr Protein and cell membrane iodinations with a sparingly soluble chloroamide, 1,3,4,6-tetrachloro-3a,6a-diphrenylglycoluril Biochem. Biophys. Res. Commun. 80 1978 849 857