Skip to main content
SpringerLink
Log in

Effects antifreeze peptides on the thermotropic properties of a model membrane

  • Published:
Journal of Bioenergetics and Biomembranes Aims and scope Submit manuscript

Abstract

In this paper, we report on the effect of short segments of type I antifreeze protein (AFP I) on the thermotropic properties of a model membrane. Two different types of dimyristoylphosphatidylcholine model membranes were used, multilamellar vesicles and small unilamellar vesicles. The membrane properties were studied by differential scanning calorimetry (DSC) and fluorescence anisotropy. With the incorporation of AFP I and its short segments, the order of the model membrane increased both in the gel state and in the liquid crystalline state. The interaction of AFPs with the model membrane caused a shift in the phase transition to lower temperatures, which is accompanied by a broadening of the DSC thermogram. This preferential stabilization to a more ordered phase by the AFPs could be due to ordering the hydrophobic membrane core and separation into domains. Overall, this approach of employing short segments of AFP I simplifies the correlation between antifreeze protein characteristics and the effect of these parameters on the interaction mechanism of AFP with cell membranes. The success of this approach can lead to the identification of short peptides with high antifreeze activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adler M, Tritton TR (1988) Fluorescence depolarization measurements on oriented membranes. Biophys J 53:989–1005

    Article  CAS  Google Scholar 

  • Andrich MP, Vanderkooi JM (1976) Temperature-dependence of 1,6-diphenyl-1,3,5-hexatriene fluorescence in phospholipid artificial membranes. Biochemistry 15:1257–1261

    Article  CAS  Google Scholar 

  • Barrett J (2001) Thermal hysteresis proteins. Int J Biochem Cell B 33:105–117

    Article  CAS  Google Scholar 

  • Blandamer MJ, Briggs B, Cullis PM, Engberts JBFN (1995) Gel to liquid-crystal transitions in synthetic amphiphile vesicles. Chem Soc Rev 24:251

    Article  Google Scholar 

  • Borenstain V, Barenholz Y (1993) Characterization of liposomes and other lipid assemblies by multiprobe fluorescence polarization. Chem Phys Lipids 117–127:64

    Google Scholar 

  • Bouvet V, Ben RN (2003) Antifreeze glycoproteins—structure, conformation, and biological applications. Cell Biochem Biophys 39:133–144

    Article  CAS  Google Scholar 

  • Crowe JH, Tablin F, Tsvetkova N, Oliver AE, Walker N, Crowe LM (1999) Are lipid phase transitions responsible for chilling damage in human platelets? Cryobiology 38:180–191

    Article  CAS  Google Scholar 

  • Davies PL, Hew CL (1990) Biochemistry of fish antifreeze proteins. Faseb J 4:2460–2468

    CAS  Google Scholar 

  • Denich TJ, Beaudette LA, Lee H, Trevors JT (2003) Effect of selected environmental and physico-chemical factors on bacterial cytoplasmic membranes. J Microbiol Meth 52:149–182

    Article  CAS  Google Scholar 

  • Devries AL, Wohlschl DE (1969) Freezing resistance in some antarctic fishes. Science 163:1073

    Article  CAS  Google Scholar 

  • Devries AL, Vandenhe J, Feeney RE (1971) Peimary structure of freezing point-depressing glycoproteins. J Biol Chem 246:305

    CAS  Google Scholar 

  • Duman JG, Wu DW, Xu L, Tursman D, Olsen TM (1991) Adaptations of insects to subzero temperatures. Quart Rev Biol 66:387–410

    Article  Google Scholar 

  • Feeney RE, Burcham TS, Yeh Y (1986) Antifreeze glycoproteins from polar fish blood. Annu Rev Biophys Bio 15:59–78

    Article  CAS  Google Scholar 

  • Feller G, Gerday C (1997) Psychrophilic enzymes: molecular basis of cold adaptation. Cell Mol Life Sci 53:830–841

    Article  CAS  Google Scholar 

  • Fletcher GL, Hew CL, Davies PL (2001) Antifreeze proteins of teleost fishes. Annu Rev Physiol 63:359–390

    Article  CAS  Google Scholar 

  • Fuchs P, Parola A, Robbins PW, Blout ER (1975) Fluorescence polarization and viscosities of membrane lipids of 3t3 cells. P Natl Acad Sci U S A 72:3351–3354

    Article  CAS  Google Scholar 

  • Hays LM, Feeney RE, Crowe LM, Crowe JH, Oliver AE (1996) Antifreeze glycoproteins inhibit leakage from liposomes during thermotropic phase transitions. P Natl Acad Sci U S A 93:6835–6840

    Article  CAS  Google Scholar 

  • Hays LM, Crowe JH, Wolkers W, Rudenko S (2001) Factors affecting leakage of trapped solutes from phospholipid vesicles during thermotropic phase transitions. Cryobiology 42:88–102

    Article  CAS  Google Scholar 

  • Hincha DK, Devries AL, Schmitt JM (1993) Cryotoxicity of antifreeze proteins and glycoproteins to spinach thylakoid membranes - comparison with cryotoxic sugar acids. Biochim Biophys Acta 1146:258–264

    Article  CAS  Google Scholar 

  • Kaiser RD, London E (1998) Location of diphenylhexatriene (DPH) and its derivatives within membranes: Comparison of different fluorescence quenching analyses of membrane depth. Biochemistry 37:8180–8190

    Article  CAS  Google Scholar 

  • Komatsu SK, Devries AL, Feeney RE (1970) Studies of structure of freezing point-depressing glycoproteins from an antarctic fish. J Biol Chem 245:2909

    CAS  Google Scholar 

  • Kun H, Mastai Y (2007) Activity of short segments of type I antifreeze protein. Biopolymers 88:807–814

    Article  CAS  Google Scholar 

  • Mabrey S, Mateo PL, Sturtevant JM (1978) High-sensitivity scanning calorimetric study of mixtures of cholesterol with dimyristoylphosphatidylcholines and dipalmitoylphosphatidylcholines. Biochemistry 17:2464–2468

    Article  CAS  Google Scholar 

  • Marsh D (1990) Handbook of lipids bilayers. CRC, Boca Raton, Florida

    Google Scholar 

  • Negulescu PA, Rubinsky B, Fletcher GL, Machen TE (1992) Fish antifreeze proteins block Ca entry into rabbit parietal cells. Am J Physiol Cell Physiol 263:C1310–C1313

    CAS  Google Scholar 

  • Ricker JV, Tsvetkova NM, Wolkers WF, Leidy C, Tablin F, Longo M, Crowe JH (2003) Trehalose maintains phase separation in an air-dried binary lipid mixture. Biophys J 84:3045–3051

    Article  CAS  Google Scholar 

  • Rubinsky B, Arav A, Mattioli M, Fletcher GL (1990) The effect of antifreeze glycopeptides on membrane potential changes at hypothermic temperatures. Biochem Biophys Res Comm 173:1369–1374

    Article  CAS  Google Scholar 

  • Rubinsky B, Mattioli M, Arav A, Barboni B, Fletcher GL (1992) Inhibition of Ca2+ and K+ currents by antifreeze proteins. Am J Physiol 262:R542–R545

    CAS  Google Scholar 

  • Somero GN, Devries AL (1967) Temperature tolerance of some antarctic fishes. Science 156:257

    Article  CAS  Google Scholar 

  • Tablin F, Oliver AE, Walker NJ, Crowe LM, Crowe JH (1996) Membrane phase transition of intact human platelets: Correlation with cold-induced activation. J Cell Physiol 168:305–313

    Article  CAS  Google Scholar 

  • Tomczak MM, Crowe JH (2002) The interaction of antifreeze proteins with model membranes and cells. In Fish Antifreeze Proteins World Scientific Publ., UK

  • Tomczak MM, Hincha DK, Estrada SD, Feeney RE, Crowe JH (2001) Antifreeze proteins differentially affect model membranes during freezing. Bba-Biomembranes 1511:255–263

    Article  CAS  Google Scholar 

  • Tomczak MM, Hincha DK, Estrada SD, Wolkers WF, Crowe LM, Feeney RE, Tablin F, Crowe JH (2002a) A mechanism for stabilization of membranes at low temperatures by an antifreeze protein. Biophys J 874–881:882

    Google Scholar 

  • Tomczak MM, Vigh L, Meyer JD, Manning MC, Hincha DK, Crowe JH (2002b) Lipid unsaturation determines the interaction of AFP type I with model membranes during thermotropic phase transitions. Cryobiology 45:135–142

    Article  CAS  Google Scholar 

  • Tomczak MM, Hincha DK, Crowe JH, Harding MM, Haymet ADJ (2003) The effect of hydrophobic analogues of the type I winter flounder antifreeze protein on lipid bilayers. Febs Lett 551:13–19

    Article  CAS  Google Scholar 

  • Trevors JT (2003) Fluorescent probes for bacterial cytoplasmic membrane research. J Biochem Bioph Meth 57:87–103

    Article  CAS  Google Scholar 

  • Shinitzk M, Inbar M (1974) Difference in microviscosity induced by different cholesterol levels in surface membrane lipid layer of normal lymphocytes and malignant lymphoma-cells. J Mol Biol 85:603–615

    Article  Google Scholar 

  • Shinitzky M, Barenholz Y (1978) Fluidity parameters of lipid regions determined by fluorescence polarization. Biochim Biophys Acta 515:367–394

    CAS  Google Scholar 

  • Sklar LA (1984) Fluorescence polarization studies of membrane fluidity, where do we go from here. Plenum, New York

    Google Scholar 

  • vanderHeide UA, vanGinkel G, Levine YK (1996) DPH is localised in two distinct populations in lipid vesicles. Chem Phys Lett 253:118–122

    Article  CAS  Google Scholar 

  • Wu YL, Fletcher GL (2000) Efficacy of antifreeze protein types in protecting liposome membrane integrity depends on phospholipid class. Bba-Gen Subjects 1524:11–16

    Article  CAS  Google Scholar 

  • Yeh Y, Feeney RE (1978) Anomalous depression of freezing temperature in a biological system. Accounts Chem Res 11:129–135

    Article  CAS  Google Scholar 

  • Yeh Y, Feeney RE (1996) Antifreeze proteins: structures and mechanisms of function. Chem Rev 96:601–617

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Chemistry and the, Institute of Nanotechnology, Bar-Ilan University, Ramat-Gan, 521900, Israel

    Hagit Kun & Yitzhak Mastai

  2. Department of Physics, Bar-Ilan University, Ramat Gan, 521900, Israel

    Refael Minnes

Authors
  1. Hagit Kun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Refael Minnes
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yitzhak Mastai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yitzhak Mastai.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kun, H., Minnes, R. & Mastai, Y. Effects antifreeze peptides on the thermotropic properties of a model membrane. J Bioenerg Biomembr 40, 389–396 (2008). https://doi.org/10.1007/s10863-008-9164-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10863-008-9164-8

Keywords

Search

Navigation