Structural and morphological characterization of ultralente insulin crystals by atomic force microscopy: Evidence of hydrophobically driven assembly

Biophysical Journal

Volumn 75, Issue 3, 1998, Pages 1172-1179

  Yip, Christopher M ^a,c   DeFelippis, Michael R ^a   Frank, Bruce H ^a   Brader, Mark L ^a   Ward, Michael D ^b  

^a ELI LILLY AND COMPANY   (United States)

^b University of Minnesota   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BOVINE INSULIN; INSULIN ZINC SUSPENSION; PIG INSULIN; RECOMBINANT HUMAN INSULIN;

AMINO ACID SEQUENCE; ARTICLE; ATOMIC FORCE MICROSCOPY; CHEMICAL STRUCTURE; CRYSTAL; CRYSTAL STRUCTURE; DISSOLUTION; HORMONE STRUCTURE; HYDROPHOBICITY; INSULIN SYNTHESIS; MOLECULAR INTERACTION; SPECIES DIFFERENCE; STRUCTURE ACTIVITY RELATION;

BOVINAE; SUIDAE; SUS SCROFA;

EID: 0031713768     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(98)74036-6     Document Type: Article

References (41)

1. Abola, E. E., F. C. Bernstein, S. H. Bryant, T. F. Koetzle, and J. Weng. 1987. Protein Data Bank. In Crystallographic Databases - Information Content, Software Systems, Scientific Applications. F. H. Allen, G. Bergerhoff, and R. Sievers, editors. Data Commission of the International Union of Crystallography, Bonn, Cambridge, Chester. 107-132.
2. Baker, E. N., T. L. Blundell, J. F. Cutfield, S. M. Cutrfield, E. J. Dodson, G. G. Dodson, D. M. Crowfoot Hodgkin, R. E. Hubbard, N. W. Isaacs, C. D. Reynolds, K. Sakabe, N. Sakabe, and N. Vijayan. 1988. The structure of 2Zn pig insulin crystals at 1.5 Å resolution. Philos. Trans. R. Soc. Lond. B. 319:369-456.
3. Bernstein, F. C., T. F. Koetzle, G. J. B. Williams, Meyer, E. F., Jr., M. D. Brice, J. R. Rodgers, O. Kennard, T. Shimanouchi, and M. Tasumi. 1977. The Protein Data Bank: a computer-based archival file for macromolecular structures. J. Mol. Biol. 112:535-542.
4. Berson, S. A., and R. S. Yalow. 1966. Insulin in blood and insulin antibodies. Am. J. Med. 40:676-690.
5. Carter, P. W., A. C. Hillier, and M. D. Ward. 1994. Nanoscale surface topography and growth of molecular crystals: the role of anisotropic intermolecular bonding. J. Am. Chem. Soc. 116:944-953.
6. Carugo, O., and P. Argos. 1997. Protein-protein crystal-packing contacts. Protein Sci. 6:2261-2263.
7. B29-human insulin. Structure. 3:615-622.
8. Derewenda, U., Z. Derewenda, E. J. Dodson, G. G. Dodson, C. D. Reynolds, G. D. Smith, C. Sparks, and D. Swenson. 1989. Phenol stabilizes more helix in a new symmetrical zinc insulin hexamer. Nature. 338: 594-596.
9. Durbin, S. D., and W. E. Carlson. 1992. Lysozyme crystal growth studied by atomic force microscopy. J. Cryst. Growth. 122:71-79.
10. Durbin, S. D., W. E. Carlson, and M. T. Saros. 1993. In situ studies of protein crystal growth by atomic force microscopy. J. Phys. D Appl. Phys. 26:B128-B132.
11. Durbin, S. D., and G. Feher. 1996., Protein crystallization. Annu. Rev. Phys. Chem. 47:171-204.
12. Galloway, J. A., and R. E. Chance. 1994. Improving insulin therapy: achievements and challenges. Horm. Metab. Res. 26:591-598.
13. Gammeltoft, S. 1988. Insulin Receptors, Part A: Methods for the Study of Structure and Function. Allan R. Liss, New York.
14. Graham, D. T., and A. R. Pomeroy. 1984. An in-vitro test for the duration of action of insulin suspensions. Pharm. Pharmacol. 36:427-430.
15. Hallas-Møller, K. Petersen, and J. Schlichtkrull. 1952. Crystalline and amorphous insulin-zinc compounds with prolonged action. Science. 116: 394-398
16. Haycock, P. 1983. History of insulin therapy. In Intensive Insulin Therapy. D. S. Schade, J. V. Santiago, J. S. Skyler, and R. A. Rizza, editors. Excerpta Medica, Amsterdam. 1-19.
17. 3 on graphite. Chem. Mater. 6:2222-2226.
18. Hillier, A. C., and M. D. Ward. 1994. Atomic force microscopy of the electrochemical nucleation and growth of molecular crystals. Science. 263:1261-1264.
19. Hollenberg, M. D. 1990. Receptor triggering and receptor regulation: structure-activity relationships from the receptor's point of view. J. Med. Chem. 33:1275-1281.
20. Kaarsholm, N. C., H.-C. Ko, and M. F. Dunn. 1989. Comparison of the solution structure flexibility and zinc binding domains for insulin, proinsulin and miniproinsulin. Biochemistry. 28:4427-4435.
21. Konnert, J. H., P. D'Antonio, and K. B. Ward. 1994. Observations of growth steps, spiral dislocations and molecular packing on the surface of lysozyme crystals with the atomic force microscope. Acta. Crystallogr. D50:603-613.
22. Kuznetsov, Y. G., A. J. Malkin, T. A. Land, J. J. DeYorco, A. P. Barba, J. Konnert, and A. McPherson. 1997. Molecular resolution imaging of macromolecular crystals by atomic force microscopy. Biophys. J. 72: 2357-2364.
23. Land, T. J., A. J. Malkin, Y. G. Kuznetsov, A. McPherson, and J. J. DeYoreo. 1995. Mechanisms of protein crystal growth: an atomic force microscopy study of canavalin crystallization. Phys. Rev. Lett. 75: 2774-2777.
24. Land, T. J., A. J. Malkin, Y. G. Kutznesov, A. McPherson, and J. J. DeYoreo. 1996. Mechanisms of protein and virus crystal growth: an atomic force microscopy study of canavalin and STMV crystallization. J. Cryst. Growth. 166:893-899.
25. Last, J. A., and M. D. Ward. 1996. Electrochemical annealing and friction anisotropy of domains in epitaxial molecular films. Adv. Mater. 8:730-733.
26. Lijnzaad, P., and P. Argos. 1997. Hydrophobic patches on protein subunit interfaces: characteristics and prediction. Proteins Struct. Funct. Genet. 28:333-343.
27. Lyon, M. K., K. M. Marr, and P. S. Furcinitti. 1993. Formation and characterization of two-dimensional crystals of photosystem II. J. Struct. Biol. 110:133-140.
28. Malkin, A. J., Y. G. Kuznetsov, and A. McPherson. 1996. Defect structure in macromolecular crystals. J. Struct. Biol. 117:124-137.
29. Malkin, A. J., T. J. Land, Y. G. Kuznetsov, A. McPherson, and J. J. DeYoreo. 1995. Investigation of virus crystal growth mechanisms by in-situ atomic force microscopy. Phys. Rev. Lett. 75:2778-2781.
30. Mao, G., L. Lobo, R. Scaringe, and M. D. Ward. 1997. Nanoscale visualization of crystal habit modification by atomic force microscopy. Chem. Mater. 9:773-783.
31. McPherson, A., A. J. Malkin, Y. G. Kuznetsov, S. Koszelak. 1996. Incorporation of impurities into macromolecular crystals. J. Cryst. Growth. 168:74-92.
32. Melander, W., and C. Horvath. 1977. Salt effect on hydrophobic interactions in precipitation and chromatography of proteins: an interpretation of the lyotropic series. Arch. Biochem. Biophys. 183:200-215.
33. Muller, D. J., A. Engel, J. L. Carrascosa, and M. Velez. 1997. The bacteriophage phi29 head-tail connector imaged at high resolution with the atomic force microscope in buffer solution. EMBO J. 16:2547-2553.
34. Nicholls, A., K. Sharp, and B. Honig. 1991. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins Struct. Funct. Genet. 11:281.
35. Schabert, F. A., C. Henn, and A. Engel. 1995. Native Escherichia coli OmpF porin surfaces probed by atomic force microscopy. Science. 268:92-94.
36. Schlichtkrull, J. 1956. Insulin crystal II. Shape of rhombohedral zinc-insulin crystals in relation to species and crystallization media. Acta Chem. Scand. 10:1459-1464.
37. Smith, G. D., D. C. E. J. Swenson, G. G. Dodson, and C. D. Reynolds. 1984. Structural stability in the 4-zinc human insulin hexamer. Proc. Natl. Acad. Sci. USA. 81:7093-7097.
38. Tiller, W. A. 1991. The Science of Crystallization: Microscopic Interfacial Phenomena. Cambridge University Press, Cambridge.
39. Walz, T., P. Tittmann, K. H. Fuchs, D. J. Müller, B. L. Smith, P. Agre, H. Gross, and A. Engel. 1996. Surface topographies at subnanometer-resolution reveal asymmetry and sidedness of aquaporin-1. J. Mol. Biol. 264:907-918.
40. Yip, C. M., M. L. Brader, M. D. Ward, and M. R. DeFelippis. 1998. Atomic force microscopy of crystalline insulins: the influence of sequence variation on crystallization and interfacial structure. Biophys. J. 74:2199-2209.
41. Yip, C. M., and M. D. Ward. 1996. Atomic force microscopy of insulin single crystals: direct visualization of molecules and crystal growth. Biophys. J. 71:1071-1078.