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. 1996 Jan 9;93(1):13–20. doi: 10.1073/pnas.93.1.13

Principles of protein-protein interactions.

S Jones 1, J M Thornton 1
PMCID: PMC40170  PMID: 8552589

Abstract

This review examines protein complexes in the Brookhaven Protein Databank to gain a better understanding of the principles governing the interactions involved in protein-protein recognition. The factors that influence the formation of protein-protein complexes are explored in four different types of protein-protein complexes--homodimeric proteins, heterodimeric proteins, enzyme-inhibitor complexes, and antibody-protein complexes. The comparison between the complexes highlights differences that reflect their biological roles.

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Selected References

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  1. Argos P. An investigation of protein subunit and domain interfaces. Protein Eng. 1988 Jul;2(2):101–113. doi: 10.1093/protein/2.2.101. [DOI] [PubMed] [Google Scholar]
  2. Bernstein F. C., Koetzle T. F., Williams G. J., Meyer E. F., Jr, Brice M. D., Rodgers J. R., Kennard O., Shimanouchi T., Tasumi M. The Protein Data Bank: a computer-based archival file for macromolecular structures. J Mol Biol. 1977 May 25;112(3):535–542. doi: 10.1016/s0022-2836(77)80200-3. [DOI] [PubMed] [Google Scholar]
  3. Chothia C. Hydrophobic bonding and accessible surface area in proteins. Nature. 1974 Mar 22;248(446):338–339. doi: 10.1038/248338a0. [DOI] [PubMed] [Google Scholar]
  4. Chothia C., Janin J. Principles of protein-protein recognition. Nature. 1975 Aug 28;256(5520):705–708. doi: 10.1038/256705a0. [DOI] [PubMed] [Google Scholar]
  5. Connolly M. L. Shape complementarity at the hemoglobin alpha 1 beta 1 subunit interface. Biopolymers. 1986 Jul;25(7):1229–1247. doi: 10.1002/bip.360250705. [DOI] [PubMed] [Google Scholar]
  6. Davies D. R., Cohen G. H. Interactions of protein antigens with antibodies. Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):7–12. doi: 10.1073/pnas.93.1.7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Duquerroy S., Cherfils J., Janin J. Protein-protein interaction: an analysis by computer simulation. Ciba Found Symp. 1991;161:237–252. doi: 10.1002/9780470514146.ch15. [DOI] [PubMed] [Google Scholar]
  8. Eigenbrot C., Randal M., Quan C., Burnier J., O'Connell L., Rinderknecht E., Kossiakoff A. A. X-ray structure of human relaxin at 1.5 A. Comparison to insulin and implications for receptor binding determinants. J Mol Biol. 1991 Sep 5;221(1):15–21. [PubMed] [Google Scholar]
  9. Finzel B. C., Weber P. C., Hardman K. D., Salemme F. R. Structure of ferricytochrome c' from Rhodospirillum molischianum at 1.67 A resolution. J Mol Biol. 1985 Dec 5;186(3):627–643. doi: 10.1016/0022-2836(85)90135-4. [DOI] [PubMed] [Google Scholar]
  10. Freymann D., Down J., Carrington M., Roditi I., Turner M., Wiley D. 2.9 A resolution structure of the N-terminal domain of a variant surface glycoprotein from Trypanosoma brucei. J Mol Biol. 1990 Nov 5;216(1):141–160. doi: 10.1016/S0022-2836(05)80066-X. [DOI] [PubMed] [Google Scholar]
  11. Gerstein M., Anderson B. F., Norris G. E., Baker E. N., Lesk A. M., Chothia C. Domain closure in lactoferrin. Two hinges produce a see-saw motion between alternative close-packed interfaces. J Mol Biol. 1993 Nov 20;234(2):357–372. doi: 10.1006/jmbi.1993.1592. [DOI] [PubMed] [Google Scholar]
  12. Gerstein M., Schulz G., Chothia C. Domain closure in adenylate kinase. Joints on either side of two helices close like neighboring fingers. J Mol Biol. 1993 Jan 20;229(2):494–501. doi: 10.1006/jmbi.1993.1048. [DOI] [PubMed] [Google Scholar]
  13. Helmer-Citterich M., Tramontano A. PUZZLE: a new method for automated protein docking based on surface shape complementarity. J Mol Biol. 1994 Jan 21;235(3):1021–1031. doi: 10.1006/jmbi.1994.1054. [DOI] [PubMed] [Google Scholar]
  14. Hubbard S. J., Thornton J. M., Campbell S. F. Substrate recognition by proteinases. Faraday Discuss. 1992;(93):13–23. doi: 10.1039/fd9929300013. [DOI] [PubMed] [Google Scholar]
  15. Hurley J. H., Thorsness P. E., Ramalingam V., Helmers N. H., Koshland D. E., Jr, Stroud R. M. Structure of a bacterial enzyme regulated by phosphorylation, isocitrate dehydrogenase. Proc Natl Acad Sci U S A. 1989 Nov;86(22):8635–8639. doi: 10.1073/pnas.86.22.8635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Janin J., Chothia C. The structure of protein-protein recognition sites. J Biol Chem. 1990 Sep 25;265(27):16027–16030. [PubMed] [Google Scholar]
  17. Janin J., Miller S., Chothia C. Surface, subunit interfaces and interior of oligomeric proteins. J Mol Biol. 1988 Nov 5;204(1):155–164. doi: 10.1016/0022-2836(88)90606-7. [DOI] [PubMed] [Google Scholar]
  18. Johnson J. E. Functional implications of protein-protein interactions in icosahedral viruses. Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):27–33. doi: 10.1073/pnas.93.1.27. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jones S., Thornton J. M. Protein-protein interactions: a review of protein dimer structures. Prog Biophys Mol Biol. 1995;63(1):31–65. doi: 10.1016/0079-6107(94)00008-w. [DOI] [PubMed] [Google Scholar]
  20. Korn A. P., Burnett R. M. Distribution and complementarity of hydropathy in multisubunit proteins. Proteins. 1991;9(1):37–55. doi: 10.1002/prot.340090106. [DOI] [PubMed] [Google Scholar]
  21. Laskowski M., Jr, Kato I. Protein inhibitors of proteinases. Annu Rev Biochem. 1980;49:593–626. doi: 10.1146/annurev.bi.49.070180.003113. [DOI] [PubMed] [Google Scholar]
  22. Lawrence M. C., Colman P. M. Shape complementarity at protein/protein interfaces. J Mol Biol. 1993 Dec 20;234(4):946–950. doi: 10.1006/jmbi.1993.1648. [DOI] [PubMed] [Google Scholar]
  23. Lee B., Richards F. M. The interpretation of protein structures: estimation of static accessibility. J Mol Biol. 1971 Feb 14;55(3):379–400. doi: 10.1016/0022-2836(71)90324-x. [DOI] [PubMed] [Google Scholar]
  24. McDonald I. K., Thornton J. M. Satisfying hydrogen bonding potential in proteins. J Mol Biol. 1994 May 20;238(5):777–793. doi: 10.1006/jmbi.1994.1334. [DOI] [PubMed] [Google Scholar]
  25. Miller S., Lesk A. M., Janin J., Chothia C. The accessible surface area and stability of oligomeric proteins. 1987 Aug 27-Sep 2Nature. 328(6133):834–836. doi: 10.1038/328834a0. [DOI] [PubMed] [Google Scholar]
  26. Miller S. The structure of interfaces between subunits of dimeric and tetrameric proteins. Protein Eng. 1989 Nov;3(2):77–83. doi: 10.1093/protein/3.2.77. [DOI] [PubMed] [Google Scholar]
  27. Mitsui Y., Satow Y., Watanabe Y., Hirono S., Iitaka Y. Crystal structures of Streptomyces subtilisin inhibitor and its complex with subtilisin BPN'. Nature. 1979 Feb 8;277(5696):447–452. doi: 10.1038/277447a0. [DOI] [PubMed] [Google Scholar]
  28. Morgan R. S., Miller S. L., McAdon J. M. The symmetry of self-complementary surfaces. J Mol Biol. 1979 Jan 5;127(1):31–38. doi: 10.1016/0022-2836(79)90456-x. [DOI] [PubMed] [Google Scholar]
  29. Navia M. A., Fitzgerald P. M., McKeever B. M., Leu C. T., Heimbach J. C., Herber W. K., Sigal I. S., Darke P. L., Springer J. P. Three-dimensional structure of aspartyl protease from human immunodeficiency virus HIV-1. Nature. 1989 Feb 16;337(6208):615–620. doi: 10.1038/337615a0. [DOI] [PubMed] [Google Scholar]
  30. Sheriff S., Silverton E. W., Padlan E. A., Cohen G. H., Smith-Gill S. J., Finzel B. C., Davies D. R. Three-dimensional structure of an antibody-antigen complex. Proc Natl Acad Sci U S A. 1987 Nov;84(22):8075–8079. doi: 10.1073/pnas.84.22.8075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Smith D. L., Almo S. C., Toney M. D., Ringe D. 2.8-A-resolution crystal structure of an active-site mutant of aspartate aminotransferase from Escherichia coli. Biochemistry. 1989 Oct 3;28(20):8161–8167. doi: 10.1021/bi00446a030. [DOI] [PubMed] [Google Scholar]
  32. Stanfield R. L., Takimoto-Kamimura M., Rini J. M., Profy A. T., Wilson I. A. Major antigen-induced domain rearrangements in an antibody. Structure. 1993 Oct 15;1(2):83–93. doi: 10.1016/0969-2126(93)90024-b. [DOI] [PubMed] [Google Scholar]
  33. Tainer J. A., Getzoff E. D., Beem K. M., Richardson J. S., Richardson D. C. Determination and analysis of the 2 A-structure of copper, zinc superoxide dismutase. J Mol Biol. 1982 Sep 15;160(2):181–217. doi: 10.1016/0022-2836(82)90174-7. [DOI] [PubMed] [Google Scholar]
  34. Taylor W. R., Orengo C. A. Protein structure alignment. J Mol Biol. 1989 Jul 5;208(1):1–22. doi: 10.1016/0022-2836(89)90084-3. [DOI] [PubMed] [Google Scholar]
  35. Thornton J. M., Edwards M. S., Taylor W. R., Barlow D. J. Location of 'continuous' antigenic determinants in the protruding regions of proteins. EMBO J. 1986 Feb;5(2):409–413. doi: 10.1002/j.1460-2075.1986.tb04226.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Tsunogae Y., Tanaka I., Yamane T., Kikkawa J., Ashida T., Ishikawa C., Watanabe K., Nakamura S., Takahashi K. Structure of the trypsin-binding domain of Bowman-Birk type protease inhibitor and its interaction with trypsin. J Biochem. 1986 Dec;100(6):1637–1646. doi: 10.1093/oxfordjournals.jbchem.a121872. [DOI] [PubMed] [Google Scholar]
  37. Vakser I. A., Aflalo C. Hydrophobic docking: a proposed enhancement to molecular recognition techniques. Proteins. 1994 Dec;20(4):320–329. doi: 10.1002/prot.340200405. [DOI] [PubMed] [Google Scholar]
  38. Walls P. H., Sternberg M. J. New algorithm to model protein-protein recognition based on surface complementarity. Applications to antibody-antigen docking. J Mol Biol. 1992 Nov 5;228(1):277–297. doi: 10.1016/0022-2836(92)90506-f. [DOI] [PubMed] [Google Scholar]
  39. Weis W. I., Kahn R., Fourme R., Drickamer K., Hendrickson W. A. Structure of the calcium-dependent lectin domain from a rat mannose-binding protein determined by MAD phasing. Science. 1991 Dec 13;254(5038):1608–1615. doi: 10.1126/science.1721241. [DOI] [PubMed] [Google Scholar]
  40. Wells J. A. Binding in the growth hormone receptor complex. Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):1–6. doi: 10.1073/pnas.93.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wilson I. A., Stanfield R. L. Antibody-antigen interactions: new structures and new conformational changes. Curr Opin Struct Biol. 1994 Dec;4(6):857–867. doi: 10.1016/0959-440x(94)90267-4. [DOI] [PubMed] [Google Scholar]
  42. Young L., Jernigan R. L., Covell D. G. A role for surface hydrophobicity in protein-protein recognition. Protein Sci. 1994 May;3(5):717–729. doi: 10.1002/pro.5560030501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Zielenkiewicz P., Rabczenko A. Methods of molecular modelling of protein-protein interactions. Biophys Chem. 1988 Apr;29(3):219–224. doi: 10.1016/0301-4622(88)85042-7. [DOI] [PubMed] [Google Scholar]

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