Abstract
Antifreeze glycoproteins (AFGPs) are a novel class of biologically significant compounds that possess the ability to inhibit the growth of ice both in vitro and in vivo. Any organic compound that possesses the ability to inhibit the growth of ice has many potential medical, industrial, and commercial applications. In an effort to elucidate the molecular mechanism of action, various spectroscopic and physical techniques have been used to investigate the solution conformations of these glycoproteins. This review examines the characterization of AFGPs and potential biological applications relating to stabilization of lipid membranes and vitrification adjuvants.
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Sun, X., Griffith, M., Pasternak, J. J., and Glick, B. R. (1995) Low temperature growth, freezing survival and production of antifreeze protein by the plant growth promoting Rhizobacterium Pseudomonas putida GR12-2. Can. J. Microbiol. 41, 776–784.
Yeh, Y. and Feeney, R. E. (1996) Antifreeze proteins: structures and mechanisms of action. Chem. Rev. 96, 601–617.
Davies, P. L. and Sykes, B. D. (1997) Antifreeze proteins. Curr. Opin. Struc. Biol. 7, 828–834.
Feeney, R. E. and Yeh, Y. (1993) Antifreeze proteins: properties, mechanism of action and possible applications. Food Technol. 47, 82–88.
Cheng, C. C. and DeVries, A. L. (1991) The role of antifreeze glycopeptides and peptides in the freezing avoidance of cold water fish in freezing avoidance of cold water fish. In Life Under Extreme Conditions (di Prisco, G., ed.), Springer-Verlag, Berlin, pp. 1–14.
Fletcher, G. L., Hew, C. L., and Davies, P. L. (2001) Antifreeze proteins of teleost fishes. Annu. Rev. Physiol. 63, 359–390.
Morris, H. R., Thompson, M. R., Osuga, D. T., Ahmed, A. I., Chan, S. M., Vandenheede, J. R., and Feeney, R. E. (1978) Antifreeze glycoproteins from the blood of an Antarctic fish-the structure of the proline-containing glycopeptides. J. Biol. Chem. 253, 5155–5162.
Brown, R. A. and Feeney, R. E. (1985) Direct evidence for antifreeze glycoprotein adsorption onto an ice surface. Biopolymers 24, 1265–1270.
Ananthanaryanan, V. S. (1989) Antifreeze proteins: structural diversity and mechanism of action. Life Chem. Rep. 7, 1–32.
Wilson, P. (1993) Explaining thermal hysteresis by the Kelvin effect. Cryo-Letters 14, 31–36.
Knight, C. A., Cheng, C. C., and Devries, A. L. (1991) Adsorption of alpha helical antifreeze peptides on specific ice crystal surface planes. Biophys. J. 59, 409–408.
Wilson, P. W., Beaglehole, D., and DeVries, A. L. (1993) Antifreeze glycopeptide adsorption on single crystal ice surfaces using ellipsometry. Biophys. J. 64, 1878.
Hall, D. G. and Lips, A. (1999) Phenomenology and mechanism of antifreeze peptide activity. Langmuir 15, 1905–1912.
Knight, C. A., Driggers, E., and Devries, A. L., (1993) Adsorption to ice of fish antifreeze glycopeptide-7 and glycopeptide-8. Biophys. J. 64, 252–259.
Wierzbicki, A., Taylor, M. S., Knight, C. A., Madura, J. D., Harrington, J. P., and Sikes, C. S. (1996) Analysis of shorthorn sculpin antifreeze protein stereospecific binding to (2–10) faces of ice. Biophys. J. 71, 8–18.
Chao, H. M., Houston, M. E. Jr., Hodges, R. S., Kay, C. M., Sykes, B. D., Loewen, M. C., et al. (1997) A diminished role for hydrogen bonds in antifreeze protein binding to ice. Biochemistry 36, 14652–14660.
DeLuca, C. I., Comley, R., and Davies, P. L. (1998) Antifreeze proteins bind independently to ice. Biophys. J. 74, 1502–1508.
Gronwald, W., Chao, H., Reddy, D. V., Davies, P. L., Sykes, B. D., and Sonnichsen, F. D. (1996) NMR characterization of side-chain flexibility and backbone structure in the type I antifreeze protein near freezing temperatures. Biochemistry 35, 16698–16704.
Karim, O. A. and Haymet, A. D. J. (1988) The ice-water interface: a molecular dynamics simulation study. J. Chem. Phys. 89, 6889–6896.
Martin, Y. C. (1978) Quantitative Drug Design: A Critical Introduction, Marcel Decker, New York.
Franks, F. and Morris, E. R. (1978) Blood glyco-protein from Antarctic fish. Possible conformational origins of antifreeze activity. Biochem. Biophys. Acta. 540, 346–356.
Bush, C. A., Feeney, R. E., Osuga, D. S. T., Talapati, S., and Yeh, Y. (1981) Antifreeze glycoprotein conformation model based upon vacuum ultraviolet circular dichroism data. J. Peptide Protein Res. 17, 125–129.
Bush, C. A. and Feeney, R. E. (1986) Conformation of the glycotropeptide repeating unit of antifreeze glycoprotein of polar fish as determined from the fully assigned NMR spectrum. Int. J. Peptide Protein Res. 28, 386–397.
Rao, B. N. and Bush, C. A. (1987) Comparison by proton NMR spectroscopy of the conformation of the 2600 dalton antifreeze glycopeptide of polar cod with that of the high molecular weight antifreeze glycoprotein. Biopolymers 26, 1227–1244.
Lane, A. N., Hays, L. M., Feeney, R. E., Crowe, L. M., and Crowe, J. H. (1998) Conformational and dynamic properties of a 14 residue antifreeze glycopeptide from Antarctic cod. Protein Sci. 7, 1555–1563.
Tsvetkova, N. M., Phillips, B. L., Krishnan, V. V., Feeney, R. E., Fink, W. H., Crowe, J. H., Risbud, S. H., Talbin, F., and Yeh, Y. (2002) Dynamics of antifreeze glycoproteins in the presence of ice. Biophys. J. 82, 464–473.
Lavalle, P., DeVries, A. L., Cheng, C. C. C., Scheuring, S., and Ramsden, J. J. (2000) Direct observation of postadsorption aggregation of antifreeze glycoproteins on silicates. Langmuir 16, 5785–5789.
Hansen, T. N., Devries, A. L., and Baust, J. G. (1991) Calorimetric analysis of antifreeze glycoproteins of the polar fish, Dissostichus-Mawsoni. Biochim. et Biophys. Acta 1079, 169–173.
Block, W. (1994) Differencial scanning calorimetry in ecophysiological research. Acta Ecol. 15, 13–22.
Baust, J. M. (2002) Molecular mechanisms of cellular demise associated with cryopreservation failure. Cell Preservation Technol. 1, 17–31.
Glander, A. J. and Schaller J. (1999) Binding of annexin V to plasma membranes of human spermatozoa: A rapid assay for detection of membrane changes after cryostorage. Mol. Hum. Reprod. 5, 109–115.
Baust, J. M., Van Buskirk, R. G., and Baust, J. G. (2000) Cell viability improves following inhibition of cryopreservation-induced apoptosis. In Vitro Cell. Dev. Biol. Animal 36, 262–270.
Fowke, K. R., Behnke, J., Hanson, C., Shea, K., and Cosentino, M. (2000) Apoptosis: A method for evaluating the cryopreservation of whole blood mononuclear cells. J. Immunol. Mech. 244, 139–144.
Hilbert, S. L., Luna, R. E., Zhang, J., Wang, Y., Hopkins, R. A., Yu, Z. X., and Ferran, V. T. (1999) Allograft heart valves: the role of apoptosis-mediated cell loss. J. Thorac. Cardiovasc. Surg. 117, 454–462.
Villalba, R., Pena, J., Luque, E., and Gomez-Villagran, J. L. (2001) Characterization of ultrastructural damage of valves cryopreserved under standard conditions. Crybiology 43, 81–84.
Mazur, P. (1963) Kinetic of water loss from cells at subzero temperatures and the likelihood of intracellular freezing. J. Gen. Physiol. 47, 347–369.
Rubinsky, B., Arav, A., and Devries, A. L. (1992) The cryoprotective effect of antifreeze glycopeptides from Antarctic fishes. Cryobiology 29, 69–79.
Storey, K. B., Bischof, J., and Rubinsky, B. (1992) Cryomicroscopic analysis of freezing in liver of the freeze tolerant wood frog. Am. J. Physiol. 263, R185-R194.
Hincha, D. K., Devries, A. L., and Schmitt, J. M. (1993) Cryotoxicity of antifreeze proteins and glycoproteins to spinach thylakoid membranes —comparison with cryotoxic sugar acids. Biochim. Biophys. Acta 1146, 258–264.
Cheng, C. and Devries, A. L. (1992) Do antifreeze proteins have a role in maintenance of ion gradients across cell membranes in polar fishes and invertebrates? Cryobiology 29, 783.
Payne, S. R., Oliver, J. E., and Upreti, G. C. (1994) Effect of antifreeze proteins on the motility of ram spermatozoa. Cryobiology 31, 180–184.
Hays, L., Feeney, R. E., Crowe, L. M., Crowe, J. H., and Oliver, A. E. (1996) Antifreeze glycoproteins inhibit leakage from liposomes during thermotropic phase transitions. Proc. Natl. Acad. Sci. USA 93, 6835–6840.
Quinn, P. J. (1995) A liquid-phase separation model of low temperature damage to biological membranes. Crybiology 22, 128–146.
Clerc, S. G. and Thompson, T. G. (1995) Permeability of dimyristoyl phosphatidylcholine/dipalmitoyl phosphatidylcholine bilayer-membranes with coexisting gel and liquid-crystalline phases. Biophys. J. 68, 2333–2341.
Wu, Y. and Fletcher, G. L. (2000) Efficacy of antifreeze protein types in protecting liposome membrane integrity depends on phospholipid class. Biochim. Biophys. Acta 1524, 11–16.
Arav, A., Yavin, S., Zeron, Y., Natan, D., Dekel, I., and Gacitua, H. (2002) New trends in gamete's cryopreservation. Mol. Cell. Endocrinol. 187, 77–81.
Marsland, T. P., Evans, S., and Pegg, D. E. (1981) Dielectric measurements for design of an electromagnetic rewarming system. Cryobiology 24, 311–323.
Robinson, M. P. and Pegg, D. E. (1999) Rapid electromagnetic warming of cells and tissues. IEEE Trans. Biomed. Eng. 46, 1413–1425.
Pegg, D. E. (2002) The history and principles of cryopreservation. Semin. Reprod. Med. 20, 5–13.
Rubinsky, B., Arav, A., and Devries, A. L. (1991) Cryopreservation of oocytes using directional cooling and antifreeze glycoproteins. Cryo-Letters 12, 93–106.
Eto, T. K. and Rubinsky, B. (1993) Antifreeze glycoproteins increase solution viscosity. Biochem. Biophys. Res. Commun. 197, 927–931.
Wu, Y., Banoub, J., Goddard, S. V., Kao, M. H., and Fletcher G. L. (2001) Antifreeze glycoproteins: relationship between molecular weight, thermal hysteresis and the inhibition of leakage from liposomes during thermotropic phase transition. Comp. Biochem. Physiol. Part B 128, 265–273.
Pickering, S. J., Braude, P. R., Johnson, M. H., Can, A., and Currie, J. (1990) Transient cooling to room temperature can cause irreversible disruption of the meiotic spindle in the human oocyte. Fertil. Steril. 54, 102–108.
Pickering, S. J. and Johnson, M. H. (1987) The influence of cooling on the organization of the meiotic spindle of the mouse oocyte. Hum. Reprod. 2, 207–216.
O'Neil, L., Paynter, S. J., Fuller, B. J., Shaw, R. W., and DeVries, A. L. (1998) Vitrification of mature mouse oocytes in a 6M Me2SO solution supplemented with antifreeze glycoproteins: The effect of temperature. Cryobiology 37, 59–66.
Vincent, C. and Johnson, M. H. (1992) Cooling, cryoprotectants, and the cytoskeleton of the mammalian oocyte. Oxford Rev. Reprod. Biol. 14, 73–100.
Filira, F., Biondi, L., Scolaro, B., Foffani, M. T., Mammi, S., Peggion, E., and Rocchi, R. (1990) Solid phase synthesis and conformation of sequential glycosylated polypeptide sequences related to antifreeze glycoproteins. Int. J. Biol. Macromol. 12, 41–49.
Tsuda, T. and Nishimura, S. I. (1996) Synthesis of an antifreeze glycoprotein analogue: Efficient preparation of sequential glycopolymers. Chem. Commun. 24, 2779–2780.
Meldal, M. and Jensen, K. J. (1990) Pentafluorophenyl esters for the temporary protection of the α-carboxy group in solid phase synthesis. J. Chem. Soc. Chem. Commun. 483–485.
Anisuzzaman, A. K. M., Anderson, L., and Navia, J. L. (1988) Synthesis of a close analogue of the repeating unit of the antifreeze glycoproteins of polar fish. Carbohydr. Res. 174, 265–278.
Tseng, P. H., Jiiang, W. T., Chang, M. Y., and Chen, S. T. (2001) Facile solid phase synthesis of an antifreeze glycoprotein. Chem. Eur. J. 7, 585–590.
Enaide, A. and Ben, R. N., (2001) Fully convergent solid phase synthesis of antifreeze glycoprotein analogues. Biomacromolecules 2, 557–561.
Ben, R. N., Enaide, A., and Hauer, L. (1999) Synthesis of a C-linked antifreeze glycoprotein (AFGP) mimic: Probes for investigating the mechanism of action. Org. Lett. 1, 1759–1762.
Eniade, A., Murphy, A. V., Landreau, G., and Ben, R. N. (2001) A general synthesis of structurally diverse building blocks for preparing analogues of C-linked antifreeze glycoproteins. Bioconjugate Chem. 12, 817–823.
Arnott, J. On the Treatment of Cancer by Regulated Application of an Anesthetic Temperature, Churchill, London, 1851.
Koushafar, H. and Rubinsky, B. (1997) Effect of antifreeze proteins on frozen primary prostatic adenocarcinoma cells. Urology 49, 421–425.
Pham, L., Dahiya, R., and Rubinsky, B. (1999) An in vivo study of antifreeze protein adjuvant cryosurgery. Cryosurgery 38, 169–175.
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Bouvet, V., Ben, R.N. Antifreeze glycoproteins. Cell Biochem Biophys 39, 133–144 (2003). https://doi.org/10.1385/CBB:39:2:133
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DOI: https://doi.org/10.1385/CBB:39:2:133