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. 2001 Mar;80(3):1169–1173. doi: 10.1016/S0006-3495(01)76093-6

Modeling Pseudomonas syringae ice-nucleation protein as a beta-helical protein.

S P Graether 1, Z Jia 1
PMCID: PMC1301312  PMID: 11222281

Abstract

Antifreeze proteins (AFPs) inhibit the growth of ice, whereas ice-nucleation proteins (INPs) promote its formation. Although the structures of several AFPs are known, the structure of INP has been modeled thus far because of the difficulty in determining membrane protein structures. Here, we present a novel model of an INP structure from Pseudomonas syringae based on comparison with two newly determined insect AFP structures. The results suggest that both this class of AFPs and INPs may have a similar beta-helical fold and that they could interact with water through the repetitive TXT motif. By theoretical arguments, we show that the distinguishing feature between an ice inhibitor and an ice nucleator lies in the size of the ice-interacting surface. For INPs, the larger surface area acts as a template that is larger than the critical ice embryo surface area required for growth. In contrast, AFPs are small enough so that they bind to ice and inhibit further growth without acting as a nucleator.

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Selected References

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  1. Ala P., Chong P., Ananthanarayanan V. S., Chan N., Yang D. S. Synthesis and characterization of a fragment of an ice nucleation protein. Biochem Cell Biol. 1993 May-Jun;71(5-6):236–240. doi: 10.1139/o93-036. [DOI] [PubMed] [Google Scholar]
  2. Béguin P. Hybrid enzymes. Curr Opin Biotechnol. 1999 Aug;10(4):336–340. doi: 10.1016/S0958-1669(99)80061-5. [DOI] [PubMed] [Google Scholar]
  3. Chao H., Houston M. E., Jr, Hodges R. S., Kay C. M., Sykes B. D., Loewen M. C., Davies P. L., Sönnichsen F. D. A diminished role for hydrogen bonds in antifreeze protein binding to ice. Biochemistry. 1997 Dec 2;36(48):14652–14660. doi: 10.1021/bi970817d. [DOI] [PubMed] [Google Scholar]
  4. Chen G., Jia Z. Ice-binding surface of fish type III antifreeze. Biophys J. 1999 Sep;77(3):1602–1608. doi: 10.1016/S0006-3495(99)77008-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Davies P. L., Sykes B. D. Antifreeze proteins. Curr Opin Struct Biol. 1997 Dec;7(6):828–834. doi: 10.1016/s0959-440x(97)80154-6. [DOI] [PubMed] [Google Scholar]
  6. Govindarajan A. G., Lindow S. E. Size of bacterial ice-nucleation sites measured in situ by radiation inactivation analysis. Proc Natl Acad Sci U S A. 1988 Mar;85(5):1334–1338. doi: 10.1073/pnas.85.5.1334. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Graether S. P., DeLuca C. I., Baardsnes J., Hill G. A., Davies P. L., Jia Z. Quantitative and qualitative analysis of type III antifreeze protein structure and function. J Biol Chem. 1999 Apr 23;274(17):11842–11847. doi: 10.1074/jbc.274.17.11842. [DOI] [PubMed] [Google Scholar]
  8. Graether S. P., Kuiper M. J., Gagné S. M., Walker V. K., Jia Z., Sykes B. D., Davies P. L. Beta-helix structure and ice-binding properties of a hyperactive antifreeze protein from an insect. Nature. 2000 Jul 20;406(6793):325–328. doi: 10.1038/35018610. [DOI] [PubMed] [Google Scholar]
  9. Graham L. A., Liou Y. C., Walker V. K., Davies P. L. Hyperactive antifreeze protein from beetles. Nature. 1997 Aug 21;388(6644):727–728. doi: 10.1038/41908. [DOI] [PubMed] [Google Scholar]
  10. Green R. L., Corotto L. V., Warren G. J. Deletion mutagenesis of the ice nucleation gene from Pseudomonas syringae S203. Mol Gen Genet. 1988 Dec;215(1):165–172. doi: 10.1007/BF00331320. [DOI] [PubMed] [Google Scholar]
  11. Gurian-Sherman D., Lindow S. E. Bacterial ice nucleation: significance and molecular basis. FASEB J. 1993 Nov;7(14):1338–1343. doi: 10.1096/fasebj.7.14.8224607. [DOI] [PubMed] [Google Scholar]
  12. Haymet A. D., Ward L. G., Harding M. M., Knight C. A. Valine substituted winter flounder 'antifreeze': preservation of ice growth hysteresis. FEBS Lett. 1998 Jul 3;430(3):301–306. doi: 10.1016/s0014-5793(98)00652-8. [DOI] [PubMed] [Google Scholar]
  13. Heffron S., Moe G. R., Sieber V., Mengaud J., Cossart P., Vitali J., Jurnak F. Sequence profile of the parallel beta helix in the pectate lyase superfamily. J Struct Biol. 1998;122(1-2):223–235. doi: 10.1006/jsbi.1998.3978. [DOI] [PubMed] [Google Scholar]
  14. Hew C. L., Yang D. S. Protein interaction with ice. Eur J Biochem. 1992 Jan 15;203(1-2):33–42. doi: 10.1111/j.1432-1033.1992.tb19824.x. [DOI] [PubMed] [Google Scholar]
  15. Jia Z., DeLuca C. I., Chao H., Davies P. L. Structural basis for the binding of a globular antifreeze protein to ice. Nature. 1996 Nov 21;384(6606):285–288. doi: 10.1038/384285a0. [DOI] [PubMed] [Google Scholar]
  16. Khurana R., Fink A. L. Do parallel beta-helix proteins have a unique fourier transform infrared spectrum? Biophys J. 2000 Feb;78(2):994–1000. doi: 10.1016/S0006-3495(00)76657-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Liou Y. C., Tocilj A., Davies P. L., Jia Z. Mimicry of ice structure by surface hydroxyls and water of a beta-helix antifreeze protein. Nature. 2000 Jul 20;406(6793):322–324. doi: 10.1038/35018604. [DOI] [PubMed] [Google Scholar]
  18. Lüthy R., Bowie J. U., Eisenberg D. Assessment of protein models with three-dimensional profiles. Nature. 1992 Mar 5;356(6364):83–85. doi: 10.1038/356083a0. [DOI] [PubMed] [Google Scholar]
  19. Margaritis A., Bassi A. S. Principles and biotechnological applications of bacterial ice nucleation. Crit Rev Biotechnol. 1991;11(3):277–295. doi: 10.3109/07388559109069185. [DOI] [PubMed] [Google Scholar]
  20. Meyer K., Keil M., Naldrett M. J. A leucine-rich repeat protein of carrot that exhibits antifreeze activity. FEBS Lett. 1999 Mar 26;447(2-3):171–178. doi: 10.1016/s0014-5793(99)00280-x. [DOI] [PubMed] [Google Scholar]
  21. Mizuno H. Prediction of the conformation of ice-nucleation protein by conformational energy calculation. Proteins. 1989;5(1):47–65. doi: 10.1002/prot.340050107. [DOI] [PubMed] [Google Scholar]
  22. Raetz C. R., Roderick S. L. A left-handed parallel beta helix in the structure of UDP-N-acetylglucosamine acyltransferase. Science. 1995 Nov 10;270(5238):997–1000. doi: 10.1126/science.270.5238.997. [DOI] [PubMed] [Google Scholar]
  23. Schmid D., Pridmore D., Capitani G., Battistutta R., Neeser J. R., Jann A. Molecular organisation of the ice nucleation protein InaV from Pseudomonas syringae. FEBS Lett. 1997 Sep 15;414(3):590–594. doi: 10.1016/s0014-5793(97)01079-x. [DOI] [PubMed] [Google Scholar]
  24. Sidebottom C., Buckley S., Pudney P., Twigg S., Jarman C., Holt C., Telford J., McArthur A., Worrall D., Hubbard R. Heat-stable antifreeze protein from grass. Nature. 2000 Jul 20;406(6793):256–256. doi: 10.1038/35018639. [DOI] [PubMed] [Google Scholar]
  25. Sieber V., Jurnak F., Moe G. R. Circular dichroism of the parallel beta helical proteins pectate lyase C and E. Proteins. 1995 Sep;23(1):32–37. doi: 10.1002/prot.340230105. [DOI] [PubMed] [Google Scholar]
  26. Smallwood M., Worrall D., Byass L., Elias L., Ashford D., Doucet C. J., Holt C., Telford J., Lillford P., Bowles D. J. Isolation and characterization of a novel antifreeze protein from carrot (Daucus carota). Biochem J. 1999 Jun 1;340(Pt 2):385–391. [PMC free article] [PubMed] [Google Scholar]
  27. Southworth M. W., Wolber P. K., Warren G. J. Nonlinear relationship between concentration and activity of a bacterial ice nucleation protein. J Biol Chem. 1988 Oct 15;263(29):15211–15216. [PubMed] [Google Scholar]
  28. Tsuda S., Ito A., Matsushima N. A hairpin-loop conformation in tandem repeat sequence of the ice nucleation protein revealed by NMR spectroscopy. FEBS Lett. 1997 Jun 9;409(2):227–231. doi: 10.1016/s0014-5793(97)00515-2. [DOI] [PubMed] [Google Scholar]
  29. Tyshenko M. G., Doucet D., Davies P. L., Walker V. K. The antifreeze potential of the spruce budworm thermal hysteresis protein. Nat Biotechnol. 1997 Sep;15(9):887–890. doi: 10.1038/nbt0997-887. [DOI] [PubMed] [Google Scholar]
  30. Warren G., Wolber P. Molecular aspects of microbial ice nucleation. Mol Microbiol. 1991 Feb;5(2):239–243. doi: 10.1111/j.1365-2958.1991.tb02104.x. [DOI] [PubMed] [Google Scholar]
  31. Wolber P., Warren G. Bacterial ice-nucleation proteins. Trends Biochem Sci. 1989 May;14(5):179–182. doi: 10.1016/0968-0004(89)90270-3. [DOI] [PubMed] [Google Scholar]
  32. Yang D. S., Hon W. C., Bubanko S., Xue Y., Seetharaman J., Hew C. L., Sicheri F. Identification of the ice-binding surface on a type III antifreeze protein with a "flatness function" algorithm. Biophys J. 1998 May;74(5):2142–2151. doi: 10.1016/S0006-3495(98)77923-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Yoder M. D., Lietzke S. E., Jurnak F. Unusual structural features in the parallel beta-helix in pectate lyases. Structure. 1993 Dec 15;1(4):241–251. doi: 10.1016/0969-2126(93)90013-7. [DOI] [PubMed] [Google Scholar]
  34. Zhang W., Laursen R. A. Structure-function relationships in a type I antifreeze polypeptide. The role of threonine methyl and hydroxyl groups in antifreeze activity. J Biol Chem. 1998 Dec 25;273(52):34806–34812. doi: 10.1074/jbc.273.52.34806. [DOI] [PubMed] [Google Scholar]

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