Folding of the presequence of yeast pAPI into an amphipathic helix determines transport of the protein from the cytosol to the vacuole

Journal of Molecular Biology

Volumn 267, Issue 5, 1997, Pages 1124-1138

  Martinez, Eduardo ^a   Jimenez, M Angeles ^b   Seguí Real, Bartolomé ^a   Vandekerckhove, Joel ^c   Sandoval, Ignacio V ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b INSTITUTO DE ESTRUCTURA DE LA MATERIA   (Spain)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

Author keywords

Amphipathicity; API; Presequence; Sorting; helix

Indexed keywords

ARGININE; ASPARTIC ACID; FUNGAL PROTEIN; GLUTAMIC ACID; GLYCINE; ISOLEUCINE; LYSINE; PROLINE; PROTEIN PRECURSOR;

ALPHA HELIX; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CELL VACUOLE; CYTOSOL; DIPOLE; HYDROPHOBICITY; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN TARGETING; PROTEIN TRANSPORT; PROTON NUCLEAR MAGNETIC RESONANCE; YEAST;

EID: 0031576988     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.0925     Document Type: Article

References (62)

1. Aue W. P. Non-invasive localized NMR spectroscopy in vivo: volume selective excitation. Ann. N. Y. Acad. Sci. 508:1987;360-365.
2. Bankaitis V. A., Johnson L. M., Emr S. D. Isolation of yeast mutants defective in protein targeting to the vacuole. Proc. Natl Acad. Sci. USA. 83:1986;9075-9079.
3. Bax A, Lerner L. Two-dimensional nuclear magnetic resonance spectroscopy. Science. 232:1986;960-967.
4. Blachly Dyson E., Stevens T. H. Yeast carboxypeptidase Y can be translocated and glycosylated without its amino-terminal signal sequence. J. Cell. Biol. 104:1987;1183-1191.
5. Bodanszky A., Ondetti M. A., Mutt V., Bodaszky M. Synthesis of secretin. Secondary structure in a miniature protein. J. Am. Chem. Soc. 91:1969;944-949.
6. Boyd D., Beckwith J. Positively charged amino acid residues can act as topogenic determinants in membrane proteins. Proc. Natl Acad. Sci. USA. 86:1989;9446-9450.
7. Briggs M. S., Gierasch L. M. Exploring the conformational roles of signal sequences: synthesis and conformational analysis of lambda receptor protein wild-type and mutant signal peptides. Biochemistry. 23:1984;3111-3114.
8. Briggs M. S., Gierasch L. M., Zlotnick A., Lear J. D., DeGrado W. F. In vivo function and membrane binding properties are correlated for Escherichia coli lamB signal peptides. Science. 228:1985;1096-1099.
9. Case D. A., Dyson H. J., Wright P. E. Use of chemical shifts and coupling constants in nuclear magnetic resonance structural studies on peptides and proteins. Methods Enzymol. 239:1994;392-416.
10. Chakrabartty A., Schellman J. A., Baldwin R. L. Large differences in the helix propensities of alanine and glycine. Nature. 351:1991;586-588.
11. Dreses Werringloer U., Fischer K., Wachter E., Link T. A., Flugge U. I. cDNA sequence and deduced amino acid sequence of the precursor of the 37-kDa inner envelope membrane polypeptide from spinach chloroplasts. Its transit peptide contains an amphiphilic alpha-helix as the only detectable structural element. Eur. J. Biochem. 195:1991;361-368.
12. Eisenberg D., Weiss R. M., Terwilliger T. C. T. The helical hydrophobic moment: a measure of the amphiphilicity of a helix. Nature. 299:1982;371-374.
13. Eisenberg D., Weiss R. M., Terwilliger T. C. The hydrophobic moment detects periodicity in protein hydrophobicity. Proc. Natl Acad. Sci. USA. 81:1984;140-144.
14. Endo T., Shimada I., Roise D., Inagaki F. N-terminal half of a mitochondrial presequence peptide takes a helical conformation when bound to dodecylphosphocholine micelles: a proton nuclear magnetic resonance study. J. Biochem. Tokyo. 106:1989;396-400.
15. Frey J., Rohm K. H. Subcellular localization and levels of aminopeptidases and dipeptidase in Saccharomyces cerevisiae. Biochim. Biophys. Acta. 527:1978;31-41.
16. Gavel Y., Steppuhn J., Herrmann R., von Heijne G. The 'positive-inside rule' applies to thylakoid membrane proteins. FEBS Letters. 282:1991;41-46.
17. Green R., Kramer R. A., Shields D. Misplacement of the amino-terminal positive charge in the prepro- alpha-factor signal peptide disrupts membrane translocation in vivo. J. Biol. Chem. 264:1989;2963-2968.
18. Greff D., Toma F., Fermandjian S., Low M., Kisfallldy L. Conformational studies of corticotropin1-32 and constitutive peptides by circular dichroism. Biochim. Biophys. Acta. 439:1976;219-231.
19. Guntert P., Braun W., Wüthrich K. Efficient computation of three-dimensional protein structures in solution from nuclear magnetic resonance data using the program DIANA and the supporting programs CALIBA, HABAS and GIOMSA. J. Mol. Biol. 217:1991;517-530.
20. Hendrick J. P., Hartl F. U. The role of molecular chaperones in protein folding. FASEB J. 9:1995;1559-1569.
21. High S., Stirling C. J. Protein translocation across membranes: common themes in divergent organisms. Trends Cell Biol. 3:1993;335-339.
22. Jimenez M. A., Bruix M., Gonzalez C., Blanco F. J., Nieto J. L., Herranz J., Rico M. CD and 1H-NMR studies on the conformational properties of peptide fragments from the C-terminal domain of thermolysin. Eur. J. Biochem. 211:1993;569-581.
23. Jimenez M. A., Munoz V., Rico M., Serrano L. Helix stop and start signals in peptides and proteins. The capping box does not necessarily prevent helix elongation. J. Mol. Biol. 242:1994;487-496.
24. Johnson L. M., Bankaitis V. A., Emr S. D. Distinct sequence determinants direct intracellular sorting and modification of a yeast vacuolar protease. Cell. 48:1987;875-885.
25. Kaiser E. T., Kezdy F. J. Secondary structures of proteins and peptides in amphiphilic environments. Proc. Natl Acad. Sci. USA. 80:1983;1137-1143.
26. Kline A. D., Wüthrich K. Complete sequence-specific 1H nuclear magnetic resonance assignments for the alpha-amylase polypeptide inhibitor tendamistat from Streptomyces tendae. J. Mol. Biol. 192:1986;869-890.
27. Klionsky D. J., Herman P. K., Emr S. D. The fungal vacuole: composition, function, and biogenesis. Microbiol. Rev. 54:1990;266-292.
28. Klionsky D. J., Emr S. D. Membrane protein sorting: biosynthesis, transport and processing of yeast vacuolar alkaline phosphatase. EMBO. J. 8:1989;2241-2250.
29. Klionsky D. J., Cueva R., Yaver D. S. Aminopeptidase I of Saccharomyces cerevisiae is localized to the vacuole independent of the secretory pathway. J. Cell. Biol. 119:1992;287-299.
30. Kumar A., Ernst R. R., Wüthrich K. A two-dimensional nuclear Overhauser enhancement (2D NOE) experiment for the elucidation of complete proton-proton cross-relaxation networks in biological macromolecules. Biochem. Biophys. Res. Commun. 95:1980;1-6.
31. Kunkel T. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl Acad. Sci. USA. 82:1985;488-492.
32. Li S. C., Deber C. M. A measure of helical propensity for amino acids in membrane environments (published erratum appears in Nature Struct. Biol.18, 558l). Nature Struct. Biol. 1:1994;368-373.
33. Lyu P. C., Liff M. I., Marky L. A., Kallenbach N. R. Side chain contributions to the stability of α-helical structure on peptides. Science. 250:1990;669-673.
34. Marcusson E. G., Horazdovsky B. F., Cereghino J. L., Gharakhanian E., Emr S. D. The sorting receptor for yeast vacuolar carboxypeptidase Y is encoded by the VPS10 gene. Cell. 77:1994;579-586.
35. Marion D., Wüthrich K. Application of phase sensitive two-dimensional correlated spectroscopy (COSY) for measurements of 1H-1H spin-spin coupling constants in proteins. Biochem. Biophys. Res. Commun. 113:1983;967-974.
36. Muñoz V., Serrano L. Elucidating the folding problem of helical peptides using empirical parameters. Nature Struct. Biol. 1:1994;399-409.
37. Muñoz V., Serrano L. Elucidating the folding problem of helical peptides using empirical parameters. II. Helix macrodipole effects and rational modification of the helical content of natural peptides. J. Mol. Biol. 245:1995a;275-296.
38. Muñoz V., Serrano L. Elucidating the folding problem of helical peptides using empirical parameters. III. Temperature and pH dependence. J. Mol. Biol. 245:1995b;297-308.
39. Nothwehr S. F., Stevens T. H. Sorting of membrane proteins in the yeast secretory pathway. J. Biol. Chem. 269:1994;10185-10188.
40. Oda M. N., Scott S. V., Hefner-Gravink A., Caffarelli A. D., Klionsky D. J. Identification of a cytoplasm to vacuole targeting determinan in aminopeptidase I. J. Cell Biol. 132:1996;999-1010.
41. Puziss J. W., Strobel S. M., Bassford P. J. J. Export of maltose-binding protein species with altered charge distribution surrounding the signal peptide hydrophobic core in Escherichia coli cells harboring prl suppressor mutations. J. Bacteriol. 174:1992;92-101.
42. Roberts C. J., Nothwehr S. F., Stevens T. H. Membrane protein sorting in the yeast secretory pathway: evidence that the vacuole may be the default compartment. J. Cell. Biol. 119:1992;69-83.
43. Robinson L. J., Michel T. Mutagenesis of palmitoylation sites in endothelial nitric oxide synthase identifies a novel motif for dual acylation and subcellular targeting. Proc. Natl Acad. Sci. USA. 92:1995;11776-11780.
44. Roise D., Horvath S. J., Tomich J. M., Richards J. H., Schatz G. A chemically synthesized pre-sequence of an imported mitochondrial protein can form an amphiphilic helix and perturb natural and artificial phospholipid bilayers. EMBO J. 5:1986;1327-1334.
45. Sahagian G. G., Distler J., Jourdiall G. W. Characterization of a membrane-associated receptor from bovine liver that binds phosphomannosyl residues of bovine testicular beta-galactosidase. Proc. Natl Acad. Sci. USA. 78:1981;4289-4293.
46. Sambrook J., Fritsch E. F., Maniatis T. Molecular Cloning: A Laboratory Manual. 1989;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
47. Schatz G., Dobberstein B. Common principles of protein translocation across membranes. Science. 271:1996;1519-1526.
48. Schiffer M., Edmundson A. B. Use of helical wheels to represent the structures of proteins and to identify segments with helical potential. Biophys. J. 7:1967;121-135.
49. Scott S. V., Klionsky D. J. In vitro reconstitution of cytoplasm to vacuole protein targeting in yeast. J. Cell. Biol. 131:1995;1727-1735.
50. Seguí Real B., Martinez M., Sandoval I. V. Yeast aminopeptidase I is post-translationally sorted from the cytosol to the vacuole by a mechanism mediated by its bipartite N-terminal extension. EMBO J. 14:1995;5476-5484.
51. Segrest J. P., De Loof H., Dohlman J. G., Brouillette C. G., Anantharamaiah G. M. Amphipathic helix motif: classes and properties. Proteins: Struct. Funct. Genet. 8:1990;103-117.
52. Serrano L., Neira J. L., Sancho J., Fersht A. R. Effect of alanine versus glycine in α-helices on protein stability. Nature. 356:1992;453-455.
53. Stevens T. H., Rothman J. H., Payne G. S., Schekman R. Gene dosage-dependent secretion of yeast vacuolar carboxypeptidase Y. J. Cell. Biol. 102:1986;1551-1557.
54. Valls L. A., Hunter C. P., Rothman J. H., Stevens T. H. Protein sorting in yeast: the localization determinant of yeast vacuolar carboxypeptidase Y resides in the propeptide. Cell. 48:1987;887-897.
55. von Heijne G. Signal sequences. The limits of variation. J. Mol. Biol. 184:1985;99-105.
56. von Heijne G. Net N-C charge imbalance may be important for signal sequence function in bacteria. J. Mol. Biol. 192:1986a;287-290.
57. von Heijne G. Mitochondrial targeting sequences may form amphiphilic helices. EMBO J. 5:1986b;1335-1342.
58. von Heijne G. Signals for protein targeting into and across membranes. Subcell. Biochem. 22:1994;1-19.
59. Wishart D. S., Skyes B. D. Chemical shifts as a tool for structure determination. Methods Enzymol. 239:1994;363-392.
60. Wüthrich K. NMR of Proteins and Nucleic Acids. 1986;J. Wiley and Sons, New York.
61. Yang J. T., Bewley T. A., Chen G. C., Li C. H. Conformation of β-endorphin and β-lipoprotein: formation of helical structure in methanol and sodium dodecyl sulfate solutions. Proc. Natl Acad. Sci. USA. 78:1977;3235-3238.
62. Yoshihisa T., Anraku Y. A novel pathway of import of alpha-mannosidase, a marker enzyme of vacuolar membrane, in Saccharomyces cerevisiae. J. Biol. Chem. 265:1990;22418-22425.