The intramolecular chaperone-mediated protein folding

Current Opinion in Structural Biology

Volumn 18, Issue 6, 2008, Pages 765-770

  Chen, Yu Jen ^a   Inouye, Masayori ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CONFORMATION; HUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW;

ANIMALS; CRYSTALLOGRAPHY; HUMANS; MOLECULAR CHAPERONES; PROTEIN CONFORMATION; PROTEIN FOLDING; SUBTILISINS;

EID: 57049117303     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2008.10.005     Document Type: Review

References (51)

1. Crick F.H. On protein synthesis. Symp Soc Exp Biol 12 (1958) 138-163
2. Anfinsen C.B. Principles that govern the folding of protein chains. Science 181 (1973) 223-230
3. Ikemura H., Takagi H., and Inouye M. Requirement of pro-sequence for the production of active subtilisin E in Escherichia coli. J Biol Chem 262 (1987) 7859-7864. The propeptide-mediated protein folding was described for the first time with the use of prosubtilisin.
4. Silen J.L., Frank D., Fujishige A., Bone R., and Agard D.A. Analysis of prepro-alpha-lytic protease expression in Escherichia coli reveals that the pro region is required for activity. J Bacteriol 171 (1989) 1320-1325
5. Winther J.R., and Sorensen P. Propeptide of carboxypeptidase Y provides a chaperone-like function as well as inhibition of the enzymatic activity. Proc Natl Acad Sci U S A 88 (1991) 9330-9334
6. Inouye M. Intramolecular chaperone: the role of the pro-peptide in protein folding. Enzyme 45 (1991) 314-321. The studies of propeptide-mediated protein folding were reviewed and the term, intramolecular chaperon, was mentioned for the first time and defined.
7. Shinde U., and Inouye M. Intramolecular chaperones: polypeptide extensions that modulate protein folding. Semin Cell Dev Biol 11 (2000) 35-44
8. Eder J., and Fersht A.R. Pro-sequence-assisted protein folding. Mol Microbiol 16 (1995) 609-614
9. Kobayashi T., and Inouye M. Functional analysis of the intramolecular chaperone. Mutational hot spots in the subtilisin pro-peptide and a second-site suppressor mutation within the subtilisin molecule. J Mol Biol 226 (1992) 931-933
10. Shinde U., Fu X., and Inouye M. A pathway for conformational diversity in proteins mediated by intramolecular chaperones. J Biol Chem 274 (1999) 15615-15621
11. Shinde U.P., Liu J.J., and Inouye M. Protein memory through altered folding mediated by intramolecular chaperones. Nature 389 (1997) 520-522. The 'protein-memory' phenomenon was discovered for the first time.
12. Almog O., Gallagher T., Tordova M., Hoskins J., Bryan P., and Gilliland G.L. Crystal structure of calcium-independent subtilisin BPN' with restored thermal stability folded without the prodomain. Proteins 31 (1998) 21-32. By introducing stabilizing mutations and removal of the calcium-binding site, the authors demonstrated successful refolding of subtilisin without the intramolecular chaperone despite the slow folding rate. The structure of the refolded subtilisin variant is shown in this article.
13. Ruan B., Hoskins J., and Bryan P.N. Rapid folding of calcium-free subtilisin by a stabilized pro-domain mutant. Biochemistry 38 (1999) 8562-8571
14. Takagi H., Koga M., Katsurada S., Yabuta Y., Shinde U., Inouye M., and Nakamori S. Functional analysis of the propeptides of subtilisin E and aqualysin I as intramolecular chaperones. FEBS Lett 508 (2001) 210-214
15. Kojima S., Iwahara A., and Yanai H. Inhibitor-assisted refolding of protease: a protease inhibitor as an intramolecular chaperone. FEBS Lett 579 (2005) 4430-4436
16. Buevich A.V., Shinde U.P., Inouye M., and Baum J. Backbone dynamics of the natively unfolded pro-peptide of subtilisin by heteronuclear NMR relaxation studies. J Biomol NMR 20 (2001) 233-249
17. Falzon L., Patel S., Chen Y.J., and Inouye M. Autotomic behavior of the propeptide in propeptide-mediated folding of prosubtilisin E. J Mol Biol 366 (2007) 494-503
18. Tanaka S., Saito K., Chon H., Matsumura H., Koga Y., Takano K., and Kanaya S. Crystal structure of unautoprocessed precursor of subtilisin from a hyperthermophilic archaeon: evidence for Ca2+-induced folding. J Biol Chem 282 (2007) 8246-8255
19. Jain S.C., Shinde U., Li Y., Inouye M., and Berman H.M. The crystal structure of an autoprocessed Ser221Cys-subtilisin E-propeptide complex at 2.0 Å resolution. J Mol Biol 284 (1998) 137-144
20. Takeuchi Y., Noguchi S., Satow Y., Kojima S., Kumagai I., Miura K., Nakamura K.T., and Mitsui Y. Molecular recognition at the active site of subtilisin BPN': crystallographic studies using genetically engineered proteinaceous inhibitor SSI (Streptomyces subtilisin inhibitor). Protein Eng 4 (1991) 501-508
21. Anderson D.E., Peters R.J., Wilk B., and Agard D.A. alpha-lytic protease precursor: characterization of a structured folding intermediate. Biochemistry 38 (1999) 4728-4735. A model was proposed to depict the molecular mechanism of the intramolecular chaperone-mediated protein folding on the basis of the structural studies on α-lytic protease.
22. Cunningham E.L., Jaswal S.S., Sohl J.L., and Agard D.A. Kinetic stability as a mechanism for protease longevity. Proc Natl Acad Sci U S A 96 (1999) 11008-11014
23. Cunningham E.L., Mau T., Truhlar S.M., and Agard D.A. The pro region N-terminal domain provides specific interactions required for catalysis of alpha-lytic protease folding. Biochemistry 41 (2002) 8860-8867
24. Cunningham E.L., and Agard D.A. Interdependent folding of the N- and C-terminal domains defines the cooperative folding of alpha-lytic protease. Biochemistry 42 (2003) 13212-13219
25. Truhlar S.M., and Agard D.A. The folding landscape of an alpha-lytic protease variant reveals the role of a conserved beta-hairpin in the development of kinetic stability. Proteins 61 (2005) 105-114
26. Sauter N.K., Mau T., Rader S.D., and Agard D.A. Structure of alpha-lytic protease complexed with its pro region. Nat Struct Biol 5 (1998) 945-950
27. Ibanez C.F. Jekyll-Hyde neurotrophins: the story of proNGF. Trends Neurosci 25 (2002) 284-286
28. Kliemannel M., Rattenholl A., Golbik R., Balbach J., Lilie H., Rudolph R., and Schwarz E. The mature part of proNGF induces the structure of its pro-peptide. FEBS Lett 566 (2004) 207-212
29. Nykjaer A., Lee R., Teng K.K., Jansen P., Madsen P., Nielsen M.S., Jacobsen C., Kliemannel M., Schwarz E., Willnow T.E., et al. Sortilin is essential for proNGF-induced neuronal cell death. Nature 427 (2004) 843-848
30. Rattenholl A., Ruoppolo M., Flagiello A., Monti M., Vinci F., Marino G., Lilie H., Schwarz E., and Rudolph R. Pro-sequence assisted folding and disulfide bond formation of human nerve growth factor. J Mol Biol 305 (2001) 523-533
31. McDonald N.Q., Lapatto R., Murray-Rust J., Gunning J., Wlodawer A., and Blundell T.L. New protein fold revealed by a 2.3-Å resolution crystal structure of nerve growth factor. Nature 354 (1991) 411-414
32. Brems D.N., Brown P.L., Heckenlaible L.A., and Frank B.H. Equilibrium denaturation of insulin and proinsulin. Biochemistry 29 (1990) 9289-9293
33. Min C.Y., Qiao Z.S., and Feng Y.M. Unfolding of human proinsulin. Intermediates and possible role of its C-peptide in folding/unfolding. Eur J Biochem 271 (2004) 1737-1747
34. Munte C.E., Vilela L., Kalbitzer H.R., and Garratt R.C. Solution structure of human proinsulin C-peptide. FEBS J 272 (2005) 4284-4293
35. Ohtomo Y., Bergman T., Johansson B.L., Jornvall H., and Wahren J. Differential effects of proinsulin C-peptide fragments on Na+, K+-ATPase activity of renal tubule segments. Diabetologia 41 (1998) 287-291
36. Stummeyer K., Dickmanns A., Muhlenhoff M., Gerardy-Schahn R., and Ficner R. Crystal structure of the polysialic acid-degrading endosialidase of bacteriophage K1F. Nat Struct Mol Biol 12 (2005) 90-96
37. Muhlenhoff M., Stummeyer K., Grove M., Sauerborn M., and Gerardy-Schahn R. Proteolytic processing and oligomerization of bacteriophage-derived endosialidases. J Biol Chem 278 (2003) 12634-12644
38. Schwarzer D., Stummeyer K., Gerardy-Schahn R., and Muhlenhoff M. Characterization of a novel intramolecular chaperone domain conserved in endosialidases and other bacteriophage tail spike and fiber proteins. J Biol Chem 282 (2007) 2821-2831
39. Kadler K.E., Holmes D.F., Trotter J.A., and Chapman J.A. Collagen fibril formation. Biochem J 316 Pt 1 (1996) 1-11
40. Hulmes D.J. Building collagen molecules, fibrils, and suprafibrillar structures. J Struct Biol 137 (2002) 2-10
41. Khoshnoodi J., Cartailler J.P., Alvares K., Veis A., and Hudson B.G. Molecular recognition in the assembly of collagens: terminal noncollagenous domains are key recognition modules in the formation of triple helical protomers. J Biol Chem 281 (2006) 38117-38121
42. Sundaramoorthy M., Meiyappan M., Todd P., and Hudson B.G. Crystal structure of NC1 domains. Structural basis for type IV collagen assembly in basement membranes. J Biol Chem 277 (2002) 31142-31153
43. Rosenberg J.B., Haberichter S.L., Jozwiak M.A., Vokac E.A., Kroner P.A., Fahs S.A., Kawai Y., and Montgomery R.R. The role of the D1 domain of the von Willebrand factor propeptide in multimerization of VWF. Blood 100 (2002) 1699-1706
44. Voorberg J., Fontijn R., Calafat J., Janssen H., van Mourik J.A., and Pannekoek H. Assembly and routing of von Willebrand factor variants: the requirements for disulfide-linked dimerization reside within the carboxy-terminal 151 amino acids. J Cell Biol 113 (1991) 195-205
45. Haberichter S.L., Fahs S.A., and Montgomery R.R. von Willebrand factor storage and multimerization: 2 independent intracellular processes. Blood 96 (2000) 1808-1815
46. Rozenfeld R., Muller L., El Messari S., and Llorens-Cortes C. The C-terminal domain of aminopeptidase A is an intramolecular chaperone required for the correct folding, cell surface expression, and activity of this monozinc aminopeptidase. J Biol Chem 279 (2004) 43285-43295
47. Bath K.G., and Lee F.S. Variant BDNF (Val66Met) impact on brain structure and function. Cogn Affect Behav Neurosci 6 (2006) 79-85. This review article describes the effects of a single mutation in the propeptide domain of brain-derived neurotrophic factor (BDNF) on human brain. Although further structure studies were needed, this may be the first example of protein-memory diseases.
48. Suzuki M., Zhang J., Liu M., Woychik N.A., and Inouye M. Single protein production in living cells facilitated by an mRNA interferase. Mol Cell 18 (2005) 253-261
49. Serber Z., Keatinge-Clay A.T., Ledwidge R., Kelly A.E., Miller S.M., and Dotsch V. High-resolution macromolecular NMR spectroscopy inside living cells. J Am Chem Soc 123 (2001) 2446-2447
50. Burz D.S., and Shekhtman A. In-cell biochemistry using NMR spectroscopy. PLoS ONE 3 (2008) e2571
51. Hsu S.T., Fucini P., Cabrita L.D., Launay H., Dobson C.M., and Christodoulou J. Structure and dynamics of a ribosome-bound nascent chain by NMR spectroscopy. Proc Natl Acad Sci U S A 104 (2007) 16516-16521. This paper describes the first structural and dynamics study of a newly synthesized polypeptide chain in a cell-free system, which is bound to a ribosome.