Ligand binding modulates the mechanical stability of dihydrofolate reductase

Biophysical Journal

Volumn 89, Issue 5, 2005, Pages 3337-3344

  Ainavarapu, Sri Rama Koti ^a   Li, Lewyn ^a   Badilla, Carmen L ^a   Fernandez, Julio M ^a  

^a Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DIHYDROFOLATE REDUCTASE; DIHYDROFOLIC ACID; METHOTREXATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME DEGRADATION; ENZYME STABILITY; FORCE; LIGAND BINDING; NONHUMAN; PROTEIN FOLDING; PROTEIN UNFOLDING; SPECTROSCOPY;

EID: 27744581873     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.062034     Document Type: Article

References (51)

1. Schnell, J. R., H. J. Dyson, and P. E. Wright. 2004. Structure, dynamics, and catalytic function of dihydrofolate reductase. Annu. Rev. Biophys. Biomol. Struct. 33:119-140.
2. Benkovic, S. J., and S, Hammes-Schiffer. 2003. A perspective on enzyme catalysis. Science. 301:1196-1202.
3. Pineda, P., A. Kanter, R. S. McIvor, S. J. Benkovic, A. Rosowsky, and C. R. Wagner. 2003. Dihydrofolate reductase mutant with exceptional resistance to methotrexate but not to trimetrexate. J. Med. Chem. 46: 2816-2818.
4. Davies, J. F., T. J. Delcamp, N. J. Prendergast, V. A. Ashford, J. H. Freisheim, and J. Kraut. 1990. Crystal structures of recombinant human dihydrofolate reductase complexed with folate and 5-deazafolate. Biochemistry. 29:9467-9479.
5. Focia, P. J., I. V. Shepotinovskaya, J. A. Seidler, and D. M. Freymann. 2004. Heterodimeric GTPase core of the SRP targeting complex. Science. 303:373-377.
6. Bouzat, C., F. Gumilar, G. Spitzmaul, H.-L. Wang, D. Rayes, S. B. Hansen, P. Taylor, and S. M. Sine. 2004. Coupling of agonist binding to channel gating in an ACh-binding protein linked to an ion channel. Nature. 430:896-900.
7. Yamniuk, A. P., L. T. Nguyen, T. T. Hoang, and H. J. Vogel. 2004. Metal ion binding properties and conformational states of calcium- and integrin-binding protein. Biochemistry. 43:2558-2568.
8. Brzeska, H., S. V. Venyaminov, Z. Gravarek, and W. Drabikowski. 1983. Comparative studies on thermostability of calmodulin, skeletal muscle troponin C and their triptic fragments. FEBS Lett. 153:169-173.
9. Wallace, L. A., and C. R. Matthews. 2002. Highly divergent dihydrofolate reductases conserve complex folding mechanisms. J. Mol. Biol. 315:193-211.
10. Eilers, M., and G. Schatz. 1986. Binding of a specific ligand inhibits import of a purified precursor protein into mitochondria. Nature. 322:228-232.
11. Matouschek, A., N. Pfanner, and W. Voos. 2000. Protein unfolding by mitochondria. The Hsp70 import motor. EMBO J. 1:404-410.
12. Lee, C., M, P. Schwartz, S. Prakash, M. Iwakura, and A. Matouschek, 2001. ATP-dependent proteases degrade their substrates by processively unraveling them from the degradation signal. Mol. Cell. 7: 627-637.
13. Prakash, S., L. Tian, K. S. Ratliff, R. E. Lehotzky, and A. Matouschek, 2004. An unstructured initiation site is required for efficient proteasome-mediated degradation. Nat. Struct. Mol. Biol. 11:830-837.
14. Hill, K., K. Model, M. T. Ryan, K. Dietmeier, F. Martin, R. Wagner, and N. Pfanner. 1998. Tom40 forms the hydrophilic channel of the mitochondrial import pore for preproteins. Nature. 395:516-521 [see comment].
15. Kunekle, K. P., S. Heins, M. Dembowski, F. E. Nargang, R. Benz, M. Thieffry, J. Walz, R. Lill, S. Nussberger, and W. Neupert. 1998. The preprotein translocation channel of the outer membrane of mitochondria. Cell. 93:1009-1019.
16. Okamoto, K., A. Brinker, S. A. Paschen, I. Moarefi, M. Hayer-Hartl, W. Neupert, and M. Brunner. 2002. The protein import motor of mitochondria: a targeted molecular ratchet driving unfolding and translocation. EMBO J. 21:3659-3671.
17. Prakash, S., and A. Matouschek. 2004. Protein unfolding in the cell. Trends Biochem. Sci. 29:593-600.
18. + proteases and disassembly machines. Cell. 119:9-18.
19. Matouschek, A. 2003. Protein unfolding-an important process in vivo? Curr. Opin. Struct. Biol. 13:98-109.
20. Kenniston, J. A., T. A. Baker, and R. T. Sauer. 2005. Partitioning between unfolding and release of native domains during ClpXP degradation determines substrate selectivity and partial processing. Proc. Natl. Acad. Sci. USA. 102:1390-1395.
21. Huang, S., K. S. Ratliff, M. P. Schwartz, J. M. Spenner, and A. Matouschek. 1999. Mitochondria unfold precursor proteins by unraveling them from their N-termini. Nat. Struct. Biol. 6:1132-1138.
22. Matouschek, A., A. Azem, K. Ratliff, B. S. Glick, K. Schmid, and G. Schatz. 1997. Active unfolding of precursor proteins during mitochondrial protein import. EMBO J. 16:6727-6736.
23. Thrower, J. S., L. Hoffman, M. Rechsteiner, and C. M. Pickart. 2000. Recognition of the polyubiquitin proteolytic signal. EMBO J. 19:94-102.
24. Fisher, T. E., A. F. Oberhauser, M. Carrion-Vazquez, P. E. Marszalek, and J. M. Fernandez. 1999. The study of protein mechanics with the atomic force microscope. Trends Biochem. Sci. 24:379-384.
25. Carrion-Vazquez, M., A. F. Oberhauser, T. E. Fisher, P. E. Marszalek, H. Li, and J. M. Fernandez. 2000. Mechanical design of proteins studied by single-molecule force spectroscopy and protein engineering. Prog. Biophys. Mol. Biol. 74:63-91.
26. Rief, M., M. Gautel, F. Oesterhelt, J. M. Fernandez, and H. E. Gaub. 1997. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science. 276:1109-1112.
27. Marszalek, P. E., H. Lu, H. Li, M. Carrion-Vazquez, A. F. Oberhauser, K. Schulten, and J. M. Fernandez. 1999. Mechanical unfolding intermediates in titin modules. Nature. 402:100-103.
28. Carrion-Vazquez, M., A. F. Oberhauser, S. B. Fowler, P. E. Marszalek, S. E. Broedel, J. Clarke, and J. M. Fernandez. 1999. Mechanical and chemical unfolding of a single protein: a comparison. Proc. Natl. Acad. Sci. USA. 96:3694-3699.
29. Li, H., A. F. Oberhauser, S. B. Fowler, J. Clarke, and J. M. Fernandez. 2000. Atomic force microscopy reveals the mechanical design of a modular protein. Proc. Natl. Acad. Sci. USA. 97:6527-6531.
30. + degradation machine. Cell. 114:511-520.
31. Carrion-Vazquez, M., H. Li, H. Lu, P. E. Marszalek, A. F. Oberhauser, and J. M. Fernandez. 2003. The mechanical stability of ubiquitin is linkage-dependent. Nat. Struct. Biol. 10:738-743.
32. Brockwell, D. J., E. Paci, R. C. Zinober, G. S. Beddard, P. D. Olmsted, D. A. Smith, R. N. Perham, and S. E. Radford. 2003. Pulling geometry defines the mechanical resistance of a β-sheet protein. Nat. Struct. Biol. 10:731-737.
33. Oberhauser, A. F., P. E. Marszalek, H. P. Erickson, and J. M. Fernandez. 1998. The molecular elasticity of the extracellular matrix protein tenascin. Nature. 393:181-185.
34. Florin, E. L., M. Rief, H. Lehmann, M. Ludwig, K. Dornmair, V. T. Moy, and H. E. Gaub. 1995. Sensing specific molecular interactions with the atomic force microscope. Biosens. Bioelectron. 10:895-901.
35. Carrion-Vazquez, M., P. E. Marszalek, A. F. Oberhauser, and J. M. Fernandez. 1999. Atomic force microscopy captures length phenotypes in single proteins. Proc. Natl. Acad. Sci. USA. 96:11288-11292.
36. Fisher, T. E., P. E. Marszalek, and J. M. Fernandez. 2000. Stretching single molecules into novel conformations using the atomic force microscope. Nat. Struct. Biol. 7:719-724.
37. Li, H., A. F. Oberhauser, S. D. Redick, M. Carrion-Vazquez, H. P. Erickson, and J. M. Fernandez. 2001. Multiple conformations of PEVK proteins detected by single-molecule techniques. Proc. Natl. Acad. Sci. USA. 98:10682-10686.
38. Best, R. B., B. Li, A. Steward, V. Daggett, and J. Clarke. 2001. Can non-mechanical proteins withstand force? Stretching barnase by atomic force microscopy and molecular dynamics simulation. Biophys. J. 81: 2344-2356.
39. Endo, T., and G. Schatz. 1988. Latent membrane perturbation activity of a mitochondrial precursor protein is exposed by unfolding. EMBO J. 7:1153-1158.
40. Atreya, C. E., and K. S. Anderson. 2004. Kinetic characterization of bifunctional thymidylate synthase-dihydrofolate reductase (TS-DHFR) from Cryptosporidium hominis: a paradigm shift for TS activity and channeling behavior. J. Biol. Chem. 279:18314-18322.
41. Tsay, J.-T., J. R. Appleman, W. A. Beard, N. J. Prendergast, T. J. Delcamp, J. H. Freisheim, and R. L. Blakley. 1990. Kinetic investigation of the functional role of phenylalanine-31 of recombinant human dihydrofolate reductase. Biochemistry. 29:6428-6436.
42. Appleman, J. R., N. Prendergast, T. J. Delcamp, J. H. Freisheim, and R. L. Blakley. 1988. Kinetics of the formation and isomerization of methotrexate complexes of recombinant human dihydrofolate reductase. J. Biol. Chem. 263:10304-10313.
43. Bystroff, C., and J. Kraut. 1991. Crystal structure of unliganded Escherichia coli dihydrofolate reductase. Ligand-induced conformational changes and cooperativity in binding. Biochemistry. 30:2227-2239.
44. Sawaya, M. R., and J. Kraut. 1997. Loop and subdomain movements in the mechanism of Escherichia coli dihydrofolate reductase: crystallographic evidence. Biochemistry. 36:586-603.
45. Yamamoto, T., S. Izumi, and K. Gekko. 2004. Mass spectrometry on hydrogen/deuterium exchange of dihydrofolate reductase: effects of ligand binding. J. Biochem. (Tokyo). 135:663-671.
46. Larsen, C. N., and D. Finley. 1997. Protein translocation channels in the proteasome and other proteases. Cell. 91:431-434.
47. Horwich, A. L., E. U. Weber-Ban, and D. Finley. 1999. Chaperone rings in protein folding and degradation. Proc. Natl. Acad. Sci. USA. 96:11033-11040.
48. Hochstrasser, M., and J. Wang. 2001. Unraveling the means to the end in ATP-dependent proteases. Nat. Struct. Biol. 8:294-296.
49. Rief, M., J. M. Fernandez, and H. E. Gaub. 1998. Elastically coupled two-level systems as a model for biopolymer extensibility. Phys. Rev. Lett. 81:4764-4767.
50. Vale, R. D. 2000. AAA proteins. Lords of the ring. J. Cell Biol. 150:F13-F19.
51. Smith, D. E., S. J. Tans, S. B. Smith, S. Grimes, D. L. Anderson, and C. Bustamante. 2001. The bacteriophage straight φp29 portal motor can package DNA against a large internal force. Nature. 413:748-752.