A thermal hysteresis-producing xylomannan glycolipid antifreeze associated with cold tolerance is found in diverse taxa

Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

Volumn 181, Issue 5, 2011, Pages 631-640

  Walters Jr , Kent R ^a,d   Serianni, Anthony S ^a   Voituron, Yann ^b   Sformo, Todd ^c,e   Barnes, Brian M ^c   Duman, John G ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b UNIVERSITÉ LYON 1   (France)

^c UNIVERSITY OF ALASKA FAIRBANKS   (United States)

^d UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^e DEPARTMENT OF WILDLIFE MANAGEMENT   (United States)

Author keywords

Antifreeze glycolipid; Antifreeze proteins; Cold adaptation; Cryoprotection; Freeze tolerance

Indexed keywords

ANTIFREEZE PROTEIN; CRYOPROTECTIVE AGENT; GLYCOLIPID; MANNAN;

ACCLIMATIZATION; ANIMAL; ARTICLE; BEETLE; CHEMISTRY; FROG; INSECT; ISOLATION AND PURIFICATION; METABOLISM; NUCLEAR MAGNETIC RESONANCE; PHYSIOLOGY; SOLANUM;

ACCLIMATIZATION; ANIMALS; ANTIFREEZE PROTEINS; BEETLES; CRYOPROTECTIVE AGENTS; GLYCOLIPIDS; INSECTS; MANNANS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; RANIDAE; SOLANUM;

ANURA; ARTHROPODA; COLEOPTERA; FUNGI; HEXAPODA;

EID: 79959261060     PISSN: 01741578     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00360-011-0552-8     Document Type: Article

References (44)

1. Alberts B, Bray D, Hopkin K, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2004) Essential cell biology: an introduction to the molecular biology of the cell. Taylor & Francis, New York.
2. Bennett VA, Sformo T, Walters K, Toien O, Jeannet K, Hochstrasser R, Pan Q, Serianni AS, Barnes BM, Duman JG (2005) Comparative overwintering physiology of Alaska and Indiana populations of the beetle Cucujus clavipes (Fabricius): roles of antifreeze proteins, polyols, dehydration and diapause. J Exp Biol 208: 4467-4477.
3. Block W (1990) Cold tolerance of insects and other arthropods. Phil Trans R Soc Lond B 326: 613-633.
4. Brown CL, Bale JS, Walters KFA (2004) Freezing induces a loss of freeze tolerance in an overwintering insect. Proc R Soc Lond B 271: 1507-1511.
5. Curatolo W (1987) Glycolipid function. Biochim Biophys Acta 906: 137-160.
6. Denlinger DL, Lee RE (2010) Low temperature biology of insects. Cambridge University Press, New York.
7. DeVries AL (1971) Glycoproteins as biological antifreeze agents in antarctic fishes. Science 172: 1152-1155.
8. DeVries AL (1988) The role of antifreeze glycopeptides and peptides in the freezing avoidance of Antarctic fishes. Comp Biochem and Physiol B 90: 611-621.
9. DeVries AL (2004) Ice, antifreeze proteins, and antifreeze genes in polar fishes. In: Barnes BM, Carey HV (eds) Life in the cold: evolution, mechanisms, adaptation and application. University of Alaska Press, Fairbanks, pp 307-328.
10. DeVries AL, Cheng CHC (2005) Antifreeze proteins and organismal freezing avoidance in polar fishes. Fish Physiol 22: 155-201.
11. Duman JG (1984) Change in overwintering mechanism of the Cucujid beetle, Cucujus clavipes. J Insect Physiol 30: 235-239.
12. Duman JG (2001) Antifreeze and ice nucleator proteins in terrestrial arthropods. Annu Rev Physiol 63: 327-357.
13. Duman JG, Olsen TM (1993) Thermal hysteresis protein activity in bacteria, fungi, and phylogenetically diverse plants. Cryobiology 30: 322-328.
14. Duman JG, Bennett V, Sformo T, Hochstrasser R, Barnes BM (2004) Antifreeze proteins in Alaskan insects and spiders. J Insect Physiol 50: 259-266.
15. Duman JG, Walters KR, Sformo T, Carrasco MA, Nickell PK, Lin X, Barnes BM (2010) Antifreeze and ice-nucleator proteins. In: Denlinger DL, Lee RE (eds) Low temperature biology of insects. Cambridge University Press, New York, pp 59-90.
16. Graether SP, Sykes BD (2004) Cold survival of freeze intolerant insects: the structure and function of beta-helical antifreeze proteins. Eur J Biochem 271: 3285-3296.
17. Graether SP, Kuiper MJ, Gagne SM, Walker VK, Jia Z, Sykes BD, Davies PL (2000) Beta-helix structure of a hyperactive antifreeze protein from an insect. Nature 406: 325-328.
18. Griffith M, Yaish MW (2004) Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci 9: 399-405.
19. Hays LM, Feeney RE, Crowe LM, Crowe JH, Oliver AE (1996) Antifreeze glycoproteins inhibit leakage from liposomes during thermotropic phase transitions. Proc Natl Acad Sci USA 93: 6835-6840.
20. Horwath KL, Duman JG (1984) Yearly variations in the overwintering mechanisms of the cold-hardy beetle Dendroides canadensis. Physiol Zool 57: 40-45.
21. Knight CA, Duman JG (1986) Inhibition of recrystallization of ice by insect thermal hysteresis proteins: a possible cryoprotective role. Cryobiology 23: 256-262.
22. Knight CA, Wen D, Laursen RA (1995) Nonequilibrium antifreeze peptides and the recrystallization of ice. Cryobiology 32: 23-34.
23. Kuiper MJ, Lankin C, Gauthier SY, Walker VK, Davies PL (2003) Purification of antifreeze proteins by adsorption to ice. Biochem Biophys Res Commun 300: 645-648.
24. Neven LG, Duman JG, Beals JM, Castellino FJ (1986) Overwintering adaptations of the stag beetle, Ceruchus piceus: removal of ice nucleators in winter to promote supercooling. J Comp Physiol B 156: 707-716.
25. Olsen TM, Duman JG (1996) Maintenance of the supercooled state in overwintering pyrochroid beetle larvae, Dendroides canadensis: role of hemolymph ice nucleators and antifreeze proteins. J Comp Physiol B 167: 105-113.
26. Olsen T, Sass S, Li N, Duman J (1998) Factors contributing to seasonal increases in inoculative freezing resistance in overwintering fire-colored beetle larvae Dendroides canadensis. J Exp Biol 20: 1585-1594.
27. Robinson CH (2001) Cold adaptation in Arctic and Antarctic fungi. New Phytol 151: 341-353.
28. Rubinsky B, Arav A, Mattioli M, DeVries AL (1990) The effect of antifreeze glycopeptides on membrane potential changes at hypothermic temperatures. Biochem Biophys Res Commun 173: 1369-1374.
29. Sformo T, Kohl F, McIntyre J, Kerr P, Duman JG, Barnes BM (2009) Simultaneous freeze tolerance and avoidance in individual fungus gnats, Exechia nugatoria. J Comp Physiol B 179: 897-902.
30. Sformo T, Walters KR, Jeannet K, Wowk B, Fahy G, Barnes BM, Duman JG (2010) Deep supercooling, vitrification, and limited survival to -100°C in the Alaskan beetle larvae Cucujus clavipespuniceus (Coleoptera: Cucujuidae). J Exp Biol 213: 502-509.
31. Steponkus PL, Lynch DV, Uemura M (1990) Influence of cold acclimation on the lipid composition and cryobehaviour of the plasma membrane of isolated rye protoplasts. Phil Trans R Soc Lond B 326: 571-583.
32. Storey KB (1990) Life in a frozen state: adaptive strategies for natural freeze tolerance in amphibians and reptiles. Am J Physiol Regul Integr Comp Physiol 258: R559-R568.
33. Storey KB, Storey JM (1996) Natural freezing survival in animals. Annu Rev Ecol Syst 27: 365-386.
34. Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50: 571-599.
35. Tomčala A, Tollarová M, Overgaard J, Šimek P, Koštál V (2006) Seasonal acquisition of chill-tolerance and restructuring of membrane glycerophospholipids in an overwintering insect: triggering by low temperature, desiccation and diapauses progression. J Exp Biol 209: 4102-4114.
36. Tomczak MM, Crowe JH (2002) The interaction of antifreeze proteins with model membranes and cells. In: Ewart K, Hew C (eds) Fish antifreeze proteins. World Scientific, New Jersey, pp 187-212.
37. Tursman D, Duman JG (1995) Cryoprotective effects of thermal hysteresis protein on survivorship of frozen gut cells from the freeze-tolerant centipede Lithobius forficatus. J Exp Zool 272: 249-257.
38. Tursman D, Duman JG, Knight CA (1994) Freeze tolerance adaptations in the centipede, Lithobius forficatus. J Exp Zool 268: 347-353.
39. Voituron Y, Joly P, Eugène M, Barré H (2005) Freezing tolerance of the European water frogs: the good, the bad, and the ugly. Am J Physiol Regul Integr Comp Physiol 288: R1563-R1570.
40. Walters KR, Sformo T, Barnes BM, Duman JG (2009a) Freeze tolerance in the Arctic Alaska stonefly, Nemoura arctica. J Exp Biol 212: 305-312.
41. Walters KR, Serianni AS, Sformo T, Barnes BM, Duman JG (2009b) A non-protein thermal hysteresis-producing xylomannan antifreeze in the freeze-tolerant Alaskan beetle, Upis ceramboides. Proc Natl Acad Sci USA 106: 210-215.
42. Wilson SL, Kelley DL, Walker VK (2006) Ice-active characteristics of soil bacteria selected by ice-affinity. Environ Microbiol 8: 1816-1824.
43. Zacchariassen KE, Kristiansen E (2000) Ice nucleation and antinucleation in nature. Cryobiology 41: 257-259.
44. Zachariassen KE, Hammel HT (1976) Nucleating agents in the haemolymph of insects tolerant to freezing. Nature 262: 285-287.