Seasonal accumulation of acetylated triacylglycerols by a freeze-tolerant insect

Journal of Experimental Biology

Volumn 217, Issue 9, 2014, Pages 1580-1587

  Marshall, Katie E ^a,d   Thomas, Raymond H ^a,e   Roxin, Aron ^b,c   Chen, Eric K Y ^a   Brown, Jason C L ^a   Gillies, Elizabeth R ^a   Sinclair, Brent J ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c PRINCESS MARGARET HOSPITAL   (Canada)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^e MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

Author keywords

Acetylated triacylglycerol; Eurosta solidaginis; Freeze tolerance; Lipid; Triglyceride

Indexed keywords

TRIACYLGLYCEROL;

ADAPTATION; ANIMAL; BODY WATER; CHEMISTRY; FREEZING; LARVA; METABOLISM; SEASON; TEPHRITIDAE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BODY WATER; FREEZING; LARVA; SEASONS; TEPHRITIDAE; TRIGLYCERIDES;

EID: 84907205384     PISSN: 00220949     EISSN: 14779145     Source Type: Journal    
DOI: 10.1242/jeb.099838     Document Type: Article

References (42)

1. Baust, J., Grandee, R., Condon, G. and Morrissey, R. (1979). Diversity of overwintering strategies utilized by separate populations of gall insects. Physiol. Zool. 52, 572-580.
2. Bennett, V. A., Pruitt, N. L. and Lee, R. E. (1997). Seasonal changes in fatty acid composition associated with cold-hardening in third instar larvae of Eurosta solidaginis. J. Comp. Physiol. B 167, 249-255.
3. Bicalho, B., David, F., Rumplel, K., Kindt, E. and Sandra, P. (2008). Creating a fatty acid methyl ester database for lipid profiling in a single drop of human blood using high resolution capillary gas chromatography and mass spectrometry. J. Chromatogr. A 1211, 120-128.
4. Boychuk, E. (2012). Cold Tolerance of Each Life Stage of the Sub-Alpine Willow Leaf Beetle, Chrysomela Aeneicollis (Coleoptera: Chrysomelidae). MSc thesis, University of Western Ontario, London, ON, Canada.
5. Butters, T. D. and Hughes, R. C. (1980). Effects of tunicamycin on insect cells. Biochem. Soc. Trans. 8, 170-171.
6. Canavoso, L. E., Jouni, Z. E., Karnas, K. J., Pennington, J. E. and Wells, M. A. (2001). Fat metabolism in insects. Annu. Rev. Nutr. 21, 23-46.
7. Chow, S. C., Sisfontes, L., Björkhem, I. and Jondal, M. (1989). Suppression of growth in a leukemic T cell line by n-3 and n-6 polyunsaturated fatty acids. Lipids 24, 700-704.
8. Churchill, T. H. and Storey, K. B. (1989). Metabolic consequences of rapid cycles of temperature change. J. Insect Physiol. 35, 579-585.
9. Collins, S. D., Allenspach, A. L. and Lee, R. E. (1997). Ultrastructural effects of lethal freezing on brain, muscle and Malpighian tubules from freeze-tolerant larvae of the gall fly, Eurosta solidaginis. J. Insect Physiol. 43, 39-45.
10. Durrett, T. P., McClosky, D. D., Tumaney, A. W., Elzinga, D. A., Ohlrogge, J. and Pollard, M. (2010). A distinct DGAT with sn-3 acetyltransferase activity that synthesizes unusual, reduced-viscosity oils in Euonymus and transgenic seeds. Proc. Natl. Acad. Sci. USA 107, 9464-9469.
11. Graham, J. M. (2002). Preparation of crude subcellular fractions by differential centrifugation. ScientificWorldJournal 2, 1638-1642.
12. Han, E.-N. and Bauce, E. (1995). Glycerol synthesis by diapausing larvae in response to the timing of low temperature exposure, and implications for overwintering survival of the spruce budworm, Choristoneura fumiferana. J. Insect Physiol. 41, 981-985.
13. Han, S. Y., Cho, S. H., Kim, S. Y., Seo, J. T., Moon, S. J. and Jhon, G. J. (1999). Monoacetyldiglycerides as new Ca2+ mobilizing agents in rat pancreatic acinar cells. Bioorg. Med. Chem. Lett. 9, 59-64.
14. Harada, K., Suomalainen, M., Uchida, H., Masui, H., Ohmura, K., Kiviranta, J. and Ikemoto, T. (2000). Insecticidal compounds against mosquito larvae from Oscillatoria agardhii Strain 27. Environ. Toxicol. 15, 114-119.
15. Højsgaard, S., Halekoh, U., Robison-Cox, J., Wright, K. and Leidi, A. A. (2012). Groupwise Summary Statistics, General Linear Contrasts, Population Means (Least-Squares-Means) and Other Utilities. R package version 4.5.0. Available at http://CRAN.R-project.org/package=doBy.
16. Goto, M., Kodali, D. R., Small, D. M., Honda, K. and Kozawa, K. and Uchida, T. (1992). Single crystal structure of a mixed-chain triacylglycerol: 1,2 Dipalmitoyl-3-snglycerol. Proc. Natl. Acad. Sci. USA 89, 8083-8086.
17. Irwin, J. T. and Lee, R. E. (2003). Cold winter microenvironments conserve energy and improve overwintering survival and potential fecundity of the goldenrod gall fly, Eurosta solidaginis. Oikos 100, 71-78.
18. Kim, Y. H., Han, S.-Y., Cho, S.-H., Yoo, J. S. and Jhon, G.-J. (1999). Structural determination of synthetic monoacetyldiglycerides by tandem mass spectrometry of sodium-adducted molecules. Rapid Commun. Mass Spectrom. 13, 481-487.
19. Knothe, G. and Dunn, R. O. (2009). A comprehensive evaluation of the melting points of fatty acids and esters determined by differential scanning calorimetry. J. Am. Oil Chem. Soc. 86, 843-856.
20. Layne, J. R., Edgar, C. L. and Medwith, R. E. (1999). Cold hardiness of the woolly bear caterpillar (Pyrrharctia isabella Lepidoptera: Arctiidae). Am. Midl. Nat. 141, 293-304.
21. Lee, R., McGrath, J., Morason, R. and Taddeo, R. (1993). Survival of intracellular freezing, lipid coalescence and osmotic fragility in fat body cells of the freeze-tolerant gall fly Eurosta solidaginis. J. Insect Physiol. 39, 445-450.
22. Lee, R. E., Dommel, R. A., Joplin, K. H. and Denlinger, D. L. (1995). Cryobiology of the freeze-tolerant gall fly Eurosta solidaginis: Overwintering energetics and heat shock proteins. Clim. Res. 5, 61-67.
23. Limb, J.-K., Kim, Y. H., Han, S.-Y. and Jhon, G.-J. (1999). Isolation and characterization of monoacetyldiglycerides from bovine udder. J. Lipid Res. 40, 2169-2176.
24. MacMillan, H. A. and Sinclair, B. J. (2011). The role of the gut in insect chilling injury: Cold-induced disruption of osmoregulation in the fall field cricket, Gryllus pennsylvanicus. J. Exp. Biol. 214, 726-734.
25. MacMillan, H. A., Guglielmo, C. G. and Sinclair, B. J. (2009). Membrane remodeling and glucose in Drosophila melanogaster: A test of rapid cold-hardening and chilling tolerance hypotheses. J. Insect Physiol. 55, 243-249.
26. McKeel, D. W. and Jarett, L. (1970). Preparation and characterization of a plasma membrane fraction from isolated fat cells. J. Cell Biol. 44, 417-432.
27. McMullen, D. C. and Storey, K. B. (2008). Suppression of Na+K+-ATPase activity by reversible phosphorylation over the winter in a freeze-tolerant insect. J. Insect Physiol. 54, 1023-1027.
28. Mugnano, J., Lee, R. and Taylor, R. (1996). Fat body cells and calcium phosphate spherules induce ice nucleation in the freeze-tolerant larvae of the gall fly Eurosta solidaginis (Diptera, Tephritidae). J. Exp. Biol. 199, 465-471.
29. Norris, D. and Cary, L. (1981). Properties and subcellular distribution of Na+,K+-ATPase and Mg2+-ATPase in the antennae of Periplaneta americana. Insect Biochem. 11, 743-750.
30. Pruitt, N. L. and Lu, C. (2008). Seasonal changes in phospholipid class and classspecific fatty acid composition associated with the onset of freeze tolerance in thirdinstar larvae of Eurosta solidaginis. Physiol. Biochem. Zool. 81, 226-234.
31. Reue, K. (2011). A thematic review series: Lipid droplet storage and metabolism: From yeast to man. J. Lipid Res. 52, 1865-1868.
32. Ribeiro, A. P. B., Basso, R. C., Grimaldi, R., Gioielli, L. A. and Goncalves, L. A. G. (2009). Instrumental methods for the evaluation of interesterified fats. Food Anal. Methods 2, 282-302.
33. Salt, R. W. (1959). Survival of frozen fat body cells in an insect. Nature 184, 1426.
34. Sinclair, B. J. and Renault, D. (2010). Intracellular ice formation in insects: Unresolved after 50 years? Comp. Biochem. Physiol. 155A, 14-18.
35. Storey, J. M. and Storey, K. B. (1985). Freezing and cellular metabolism in the gall fly larva, Eurosta solidaginis. J. Comp. Physiol. B 155, 333-337.
36. Taussky, H. H. and Shorr, E. (1953). A microcolorimetric method for the determination of inorganic phosphorus. J. Biol. Chem. 202, 675-685.
37. Williams, J. B. and Lee, R. E., Jr (2005). Plant senescence cues entry into diapause in the gall fly Eurosta solidaginis: Resulting metabolic depression is critical for water conservation. J. Exp. Biol. 208, 4437-4444.
38. Williams, J. B., Ruehl, N. C. and Lee, R. E., Jr (2004). Partial link between the seasonal acquisition of cold-tolerance and desiccation resistance in the goldenrod gall fly Eurosta solidaginis (Diptera: Tephritidae). J. Exp. Biol. 207, 4407-4414.
39. Williams, C. M., Thomas, R. H., MacMillan, H. A., Marshall, K. E. and Sinclair, B. J. (2011). Triacylglyceride measurement in small quantities of homogenised insect tissue: Comparisons and caveats. J. Insect Physiol. 57, 1602-1613.
40. Yang, H. O., Park, J.-S., Cho, S.-H., Yoon, J.-Y., Kim, M.-G., Jhon, G.-J., Han, S.-Y. and Kim, S. H. (2004). Stimulatory effects of monoacetyldiglycerides on hematopoiesis. Biol. Pharm. Bull. 27, 1121-1125.
41. Yen, C.-L. E., Stone, S. J., Koliwad, S., Harris, C. and Farese, R. V., Jr (2008). Thematic review series: Glycerolipids. DGAT enzymes and triacylglycerol biosynthesis. J. Lipid Res. 49, 2283-2301.
42. Yi, S.-X. and Lee, R. E., Jr (2005). Changes in gut and Malpighian tubule transport during seasonal acclimatization and freezing in the gall fly Eurosta solidaginis. J. Exp. Biol. 208, 1895-1904.