Antifreeze Protein from Freeze-Tolerant Grass Has a Beta-Roll Fold with an Irregularly Structured Ice-Binding Site

Middleton, Adam J.; Marshall, Christopher B.; Faucher, Frédérick; Bar-Dolev, Maya; Braslavsky, Ido; Campbell, Robert L.; Walker, Virginia K.; Davies, Peter L.

doi:10.1016/j.jmb.2012.01.032

Cited by 117 publications

(124 citation statements)

References 73 publications

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“…The plant AFP, Lolium perenne AFP (LpAFP), was modeled as a β-solenoid with internal asparagine ladders and a small hydrophobic core of apposed valines (37). All these crucial structural features were validated by the crystal structure done more than 10 y later, albeit the modeled solenoid was of the opposite handedness (38). The bacterial ice adhesion domain of MpAFP was correctly modeled as a β-solenoid based on the RTX repeats of an alkaline protease, which predicted that one of the two rows of internal Ca 2+ ions was absent and replaced by hydrophobic packing (8,30).…”

Section: Discussionmentioning

confidence: 99%

Flies expand the repertoire of protein structures that bind ice

Basu

Graham

Campbell

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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An antifreeze protein (AFP) with no known homologs has been identified in Lake Ontario midges (Chironomidae). The midge AFP is expressed as a family of isoforms at low levels in adults, which emerge from fresh water in spring before the threat of freezing temperatures has passed. The 9.1-kDa major isoform derived from a preproprotein precursor is glycosylated and has a 10-residue tandem repeating sequence xxCxGxYCxG, with regularly spaced cysteines, glycines, and tyrosines comprising one-half its 79 residues. Modeling and molecular dynamics predict a tightly wound left-handed solenoid fold in which the cysteines form a disulfide core to brace each of the eight 10-residue coils. The solenoid is reinforced by intrachain hydrogen bonds, side-chain salt bridges, and a row of seven stacked tyrosines on the hydrophobic side that forms the putative ice-binding site. A disulfide core is also a feature of the similar-sized beetle AFP that is a β-helix with seven 12-residue coils and a comparable circular dichroism spectrum. The midge and beetle AFPs are not homologous and their ice-binding sites are radically different, with the latter comprising two parallel arrays of outward-pointing threonines. However, their structural similarities is an amazing example of convergent evolution in different orders of insects to cope with change to a colder climate and provide confirmation about the physical features needed for a protein to bind ice.

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Section: Discussionmentioning

confidence: 99%

Flies expand the repertoire of protein structures that bind ice

Basu

Graham

Campbell

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…Despite this lack regularity in the IBS these proteins are able to bind both basal and prism planes. [59][60][61]65 Crystal structures of various AFPs reveal ordered waters associated with the protein IBS, 48,56,58,65 which are thought to play an important role in ice-binding (see Sec. VI E for more details).…”

Section: -58mentioning

confidence: 99%

Interaction of ice binding proteins with ice, water and ions

et al. 2016

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Articles you may be interested inExplicit-water theory for the salt-specific effects and Hofmeister series in protein solutions J. Chem. Phys. 144, 215101 (2016) Ice binding proteins (IBPs) are produced by various cold-adapted organisms to protect their body tissues against freeze damage. First discovered in Antarctic fish living in shallow waters, IBPs were later found in insects, microorganisms, and plants. Despite great structural diversity, all IBPs adhere to growing ice crystals, which is essential for their extensive repertoire of biological functions. Some IBPs maintain liquid inclusions within ice or inhibit recrystallization of ice, while other types suppress freezing by blocking further ice growth. In contrast, ice nucleating proteins stimulate ice nucleation just below 0 C. Despite huge commercial interest and major scientific breakthroughs, the precise working mechanism of IBPs has not yet been unraveled. In this review, the authors outline the state-of-the-art in experimental and theoretical IBP research and discuss future scientific challenges. The interaction of IBPs with ice, water and ions is examined, focusing in particular on ice growth inhibition mechanisms.

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“…These proteins are a subset of an expanding group of identified proteins, whose salient feature is ice binding (3,4). AFPs are characterized by their ability to cause a temperature difference (hysteresis) in the melting and freezing of ice and are classified as hyperactive or moderately active according to the magnitude of their freezing hysteresis (FH) activity (5).…”

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Microfluidic experiments reveal that antifreeze proteins bound to ice crystals suffice to prevent their growth

Celik

Drori

Pertaya-Braun

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Antifreeze proteins (AFPs) are a subset of ice-binding proteins that control ice crystal growth. They have potential for the cryopreservation of cells, tissues, and organs, as well as for production and storage of food and protection of crops from frost. However, the detailed mechanism of action of AFPs is still unclear. Specifically, there is controversy regarding reversibility of binding of AFPs to crystal surfaces. The experimentally observed dependence of activity of AFPs on their concentration in solution appears to indicate that the binding is reversible. Here, by a series of experiments in temperature-controlled microfluidic devices, where the medium surrounding ice crystals can be exchanged, we show that the binding of hyperactive Tenebrio molitor AFP to ice crystals is practically irreversible and that surface-bound AFPs are sufficient to inhibit ice crystal growth even in solutions depleted of AFPs. These findings rule out theories of AFP activity relying on the presence of unbound protein molecules.thermal hysteresis | ice structuring proteins A ntifreeze proteins (AFPs) are found in a variety of coldadapted organisms, where they serve as inhibitors of ice crystal growth and recrystallization (1, 2). These proteins are a subset of an expanding group of identified proteins, whose salient feature is ice binding (3, 4). AFPs are characterized by their ability to cause a temperature difference (hysteresis) in the melting and freezing of ice and are classified as hyperactive or moderately active according to the magnitude of their freezing hysteresis (FH) activity (5). The FH activity is defined as the difference between the melting temperature of ice crystals and the nonequilibrium freezing temperature at which rapid crystal growth commences. Although the FH activity has been investigated for more than four decades, the actual mechanism of action of AFPs is still not clear. This is partly because the interactions between molecules of AFPs, water, and ice at the ice-water interface are difficult to study experimentally due to the delicate, transitory nature of the ice-water interface.FH activity is thought to be due to an adsorption-inhibition mechanism that states that AFPs bind to ice surfaces and allow ice crystal growth only in surface regions between the bound AFP molecules (6, 7). This patchy growth pattern causes increased local microcurvature of the ice front that leads to larger surface energy, making the transformation of water into ice less energetically favorable and thus reducing the freezing temperature (GibbsThompson effect). It has been argued that the binding of AFPs to ice surfaces must be irreversible, because AFP desorption would result in rapid crystal growth in the areas where the AFP molecules have been desorbed from the ice surface (6,8). This theory has been criticized for assuming that the ice-water interface is sharp, contrary to the experimental evidence that the transitions from an ordered solid phase to a liquid phase at the ice-water interfaces are gradual and occur over seve...

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Antifreeze Protein from Freeze-Tolerant Grass Has a Beta-Roll Fold with an Irregularly Structured Ice-Binding Site

Cited by 117 publications

References 73 publications

Flies expand the repertoire of protein structures that bind ice

Flies expand the repertoire of protein structures that bind ice

Interaction of ice binding proteins with ice, water and ions

Microfluidic experiments reveal that antifreeze proteins bound to ice crystals suffice to prevent their growth

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