The protective role of aquaporins in the freeze-tolerant insect eurosta solidaginis: Functional characterization and tissue abundance of EsAQP1

Journal of Experimental Biology

Volumn 214, Issue 5, 2011, Pages 848-857

  Philip, Benjamin N ^a,b   Kiss, Andor J ^a   Lee Jr , Richard E ^a  

^a MIAMI UNIVERSITY   (United States)

^b RIVIER COLLEGE   (United States)

Author keywords

Acclimation; Cold tolerance; EsAQP1; Osmotic stress; Water balance; Xenopus swelling assay

Indexed keywords

AQUAPORIN 1; INSECT PROTEIN;

ACCLIMATIZATION; ANIMAL; ARTICLE; FREEZING; GROWTH, DEVELOPMENT AND AGING; LARVA; METABOLISM; SEASON; TEPHRITIDAE;

ACCLIMATIZATION; ANIMALS; AQUAPORIN 1; FREEZING; INSECT PROTEINS; LARVA; SEASONS; TEPHRITIDAE;

CHIRONOMIDAE; DIPTERA; EUROSTA SOLIDAGINIS; HEXAPODA; POLYPEDILUM; TEPHRITIDAE; XENOPUS LAEVIS;

EID: 79951791608     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.051276     Document Type: Article

References (61)

1. Azad, A. K., Sawa, Y., Ishikawa, T. and Shibata, H. (2004). Phosphorylation of plasma membrane aquaporin regulates temperature-dependent opening of tulip petals. Plant Cell Physiol. 45, 608-617. (Pubitemid 38791244)
2. Bale, J. S., Hansen, T. N., Nishino, M. and Baust, J. G. (1989). Effect of cooling rate on the survival of larvae, pupariation and adult emergence of the gall fly Eurosta solidaginis. Cryobiology 26, 285-289.
3. Ball, A., Campbell, E. M., Jacob, J., Hoppler, S. and Bowman, A. S. (2009). Identification, functional characterization and expression patterns of a water-specific aquaporin in the brown dog tick, Rhipicephalus sanguineus. Insect Biochem. Mol. Biol. 39, 105-112.
4. Baust, J. G. and Lee, R. E. (1981). Divergent mechanisms of frost-hardiness in two populations of the gall fly, Eurosta solidaginis. J. Insect Physiol. 27, 485-490.
5. Baust, J. G. and Nishino, M. (1991). Freezing tolerance in the goldenrod gall fly (Eurosta solidaginis). In Insects at Low Temperature (ed. R. E. Lee and D. L. Denlinger), pp. 260-275. New York: Chapman and Hall.
6. ε. Bioinformatics 16, 1050-1051. (Pubitemid 32051023)
7. Bennett, V. A. and Lee, R. E. (1997). Modeling seasonal changes in intracellular freeze-tolerance of fat body cells of the gall fly, Eurosta solidaginis (Diptera: Tephritidae). J. Exp. Biol. 200, 185-192. (Pubitemid 27058906)
8. 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. (Pubitemid 27243064)
9. Borgnia, M., Nielsen, S., Engel, A. and Agre, P. (1999). Cellular and molecular biology of the aquaporin water channels. Annu. Rev. Biochem. 68, 425-458. (Pubitemid 29449199)
10. Bossi, E., Fabbrini, M. S. and Ceriotti, A. (2007). Exogenous protein expression in Xenopus oocytes: Basic procedures. In Methods in Molecular Biology, vol. 375, In Vitro Transcription and Translation Protocols, 2nd edn (ed. G. Grandi), pp. 107-131. Totowa, NJ, USA: Humana Press Inc. (Pubitemid 350183384)
11. Campbell, E. M., Ball, A., Hoppler, S. and Bowman, A. (2008). Invertebrate aquaporins: A review. J. Comp. Physiol. B 178, 935-955.
12. Carlson, S. D., Juang, J.-L., Hilgers, S. L. and Garment, M. B. (2000). Blood barriers of insects. Annu. Rev. Entomol. 45, 151-174.
13. Carpenter, J. F. and Crowe, J. H. (1988). The mechanisms of cryoprotection of proteins by solutes. Cryobiology 25, 244-255.
14. Chapman, R. F. (1971). The Insects: Structure and Function. New York: Elsevier North Holland.
15. Collins, S. D., Allenspach, A. 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. (Pubitemid 27324710)
16. Costanzo, J. P., Lee, R. E. and Wright, M. F. (1991). Effect of cooling rate on the survival of frozen wood frogs, Rana sylvatica. J. Comp. Physiol. B 161, 225-229.
17. Davis, D. J. and Lee, R. E. (2001). Intracellular freezing, viability, and composition of fat body cells from freeze-intolerant larvae of Sarcophaga crassipalpis. Arch. Insect Biochem. 48, 199-205. (Pubitemid 33602646)
18. De Castro, E., Sigrist, C. J. A., Gattiker, A., Bulliard, V., Langendijk-Genevaux, P. S., Gasteiger, E., Bairoch, A. and Hulo, N. (2006). ScanProsite: Detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res. 1, 362-365.
19. Echevarria, M., Windhager, E. E. and Frindt, G. (1996). Selectivity of the renal collecting duct water channel aquaporin-3. J. Biol. Chem. 271, 25079-25082. (Pubitemid 26337865)
20. Echevarria, M., Ramirez-Lorca, R., Hernandez, C. S., Gutierriez, A., Mendez- Ferrer, S., Gonzalez, E., Toledo-Aral, J. J., Ilundain, A. A. and Whittembury, G. (2001). Identification of a new water channel (Rp-MIP) in the Malpighian tubules of the insect Rhodnius prolixus. Pflugers Arch. 442, 27-34. (Pubitemid 32336822)
21. Edashige, K., Yamaji, Y., Kleinhans, F. W. and Kasai, M. (2003). Artificial expression of aquaporin-3 improves the survival of mouse oocytes after cryopreservation. Biol. Reprod. 68, 87-94. (Pubitemid 36076322)
22. Elvin, C. M., Bunch, R., Liyou, N. E., Pearson, R. D., Gough, J. and Drinkwater, R. D. (1999). Molecular cloning and expression in Escherichia coli of an aquaporin-like gene from adult buffalo fly (Haematobia irritans exigua). Insect Mol. Biol. 8, 369-380. (Pubitemid 29451839)
23. Hadley, N. F. (1994). Water Relations of Terrestrial Arthropods. New York: Academic Press.
24. Hall, B. G. (2004). Phylogenetic Trees Made Easy: A How-to Manual. Massachusetts: Sinauer Associates.
25. Hall, T. (1999). BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 95-98.
26. Hinton, H. E. (1960). A fly larva that tolerates dehydration and temperatures of -270°to +102°C. Nature 188, 336-337.
27. Holland, L. Z., McFall-Ngai, M. and Somero, G. N. (1997). Evolution of lactate dehydrogenase-A homologs of barracuda fishes (Genus Sphyraena) from different thermal environments: Differences in kinetic properties and thermal stability are due to amino acid substitutions outside the active site. Biochemistry 36, 3207-3215. (Pubitemid 27142393)
28. Humphrey, W., Dalke, A. and Schulten, K. (1996). VMD-Visual Molecular Dynamics. J. Mol. Graph. 14, 33-38.
29. Irwin, J. T., Bennett, V. A. and Lee, R. E. (2001). Diapause development in frozen larvae of the goldenrod gall fly, Eurosta solidaginis Fitch (Diptera: Tephritidae). J. Comp. Physiol. B 171, 181-188.
30. Izumi, Y., Sonoda, S., Yoshida, H., Danks, H. V. and Tsumuki, H. (2006). Role of membrane transport of water and glycerol in the freeze tolerance of the rice stem borer, Chilo suppressalis Walker (Lepidoptera: Pyralidae). J. Insect Physiol. 52, 215-220.
31. Karow, A. M. (1991). Chemical cryoprotection of metazoan cells. Bioscience 41, 155-160.
32. Kataoka, N., Miyake, S. and Azuma, M. (2009). Aquaporin and aquaglyceroporin in silkworms, differently expressed in the hindgut and midgut of Bombyx mori. Insect Mol. Biol. 18, 303-314.
33. Kikawada, T., Saito, A., Kanamori, Y., Fujita, M., Snigorska, K., Watanabe, M. and Okuda, T. (2008). Dehydration-inducible changes in expression of two aquaporins in the sleeping chironomid, Polypedilum vanderplanki. Biochim. Biophys. Acta 1778, 514-520.
34. Kukal, O., Serianni, A. S. and Duman, J. G. (1988). Glycerol metabolism in a freezetolerant arctic insect: An in vivo 13C NMR study. J. Comp. Physiol. B 158, 175-183.
35. Kumar, S., Dudley, J., Nei, M. and Tamura, K. (2008). MEGA: A biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief. Bioinform. 9, 299-306. (Pubitemid 351890826)
36. Kyte, J. and Doolittle, R. F. (1982). A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105-132.
37. Layne, J. R. (1993). Winter microclimate of goldenrod spherical galls and its effects on the gall inhabitant Eurosta solidaginis (Diptera: Tephritidae). J. Therm. Biol. 18, 125-130.
38. Le Caherec, F., Deschamps, S., Delamarche, C., Pellerin, I., Bonnec, G., Guillam, M., Thomas, D., Gouranton, J. and Hubert, J. (1996). Molecular cloning and characterization of an insect aquaporin: Functional comparison with aquaporin 1. Eur. J. Biochem. 241, 707-715. (Pubitemid 26379370)
39. Lee, R. E. (1991). Principles of insect low temperature tolerance. In Insects at Low Temperature (ed. R. E. Lee and D. L. Denlinger), pp. 17-46. New York: Chapman and Hall.
40. Lee, R. E. (2010). A primer on insect cold-tolerance. In Low Temperature Biology of Insects (ed. D. L. Denlinger and R. E. Lee), pp. 3-34. New York: Cambridge University Press.
41. Lee, R. E., McGrath, J. J., Morason, R. T. and Taddeo, R. M. (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.
42. Mazur, P. (1984). Freezing of living cells: Mechanisms and implication. Am. J. Physiol. 247, 125-142.
43. Morrissey, R. E. and Baust, J. G. (1976). The ontogeny of cold tolerance in the gall fly, Eurosta solidaginis. J. Insect Physiol. 22, 431-437.
44. Muldrew, K., Acker, J. P., Elliot, J. A. W. and McGann, L. E. (2004). The water to ice transition: Implications for living cells. In Life in the Frozen State (ed. B. J. Fuller, N. Lane and E. E. Benson), pp. 67-108. New York: CRC Press.
45. Nylander, J. A. A. (2004). MrModeltest v.2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University (http://www.abc.se/ ~nylander/mrmodeltest2/mrmodeltest2.html).
46. Papadopoulos, M. C. and Verkman, A. S. (2007). Aquaporin-4 and brain edema. Pedriatr. Nephrol. 22, 778-784. (Pubitemid 46629610)
47. Papadopoulos, M. C., Manley, G. T., Krishna, S. and Verkman, A. S. (2004). Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema. FASEB J. 18, 1291-1293. (Pubitemid 39561580)
48. Philip, B. N. and Lee, R. E. (2010). Changes in abundance of aquaporin-like proteins occurs concomitantly with seasonal acquisition of freeze tolerance in the goldenrod gall fly, Eurosta solidaginis. J. Insect Physiol. 56, 679-685.
49. Philip, B. N., Yi, S.-X., Elnitsky, M. A. and Lee, R. E. (2008). Aquaporins play a role in desiccation and freeze tolerance in larvae of the goldenrod gall fly, Eurosta solidaginis. J. Exp. Biol. 211, 1114-1119. (Pubitemid 351631911)
50. Preston, G. M., Carroll, T. P., Guggino, W. B. and Agre, P. (1992). Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256, 385-387.
51. Preston, G. M., Jung, J. S., Guggino, W. B. and Agre, P. (1993). The mercurysensitive residue at cysteine 189 in the CHIP28 water channel. J. Biol. Chem. 268, 17-20. (Pubitemid 23021279)
52. Ring, R. A. and Danks, H. V. (1994). Desiccation and cryoprotection: Overlapping adaptations. Cryo Letters 15, 181-190.
53. Rojas, R. R., Lee, R. E. and Baust, J. G. (1986). Relationship of environmental water content to glycerol accumulation in the freezing tolerant larvae of Eurosta solidaginis (Fitch). Cryo Letters 7, 234-245.
54. Sambrook, J. and Russell, D. W. (2001). Molecular Cloning: A Laboratory Manual, 3rd edn. New York: Cold Spring Harbor Laboratory Press.
55. Shakesby, A. J., Wallace, I. S., Isaacs, H. V., Pritchard, J., Roberts, D. M. and Douglas, A. E. (2009). A water-specific aquaporin involved in aphid osmoregulation. Insect Biochem. Mol. Biol. 39, 1-10.
56. Simmons, M. P., Ochoterena, H. and Freudenstein, J. V. (2002). Amino acid vs. nucleotide characters: Challenging preconceived notions. Mol. Phylogenet. Evol. 24, 78-90.
57. Tait, M. J., Saadoun, S., Bell, B. A. and Papadopoulos, M. C. (2008). Water movements in the brain: Role of aquaporins. Trends Neurosci. 31, 37-43.
58. Tanghe, A., Van Dijck, P., Dumortier, F., Teunissen, A., Hohmann, S. and Thevelein, J. M. (2002). Aquaporin expression correlates with freeze tolerance in baker's yeast, and overexpression improves freeze tolerance in industrial strains. Appl. Environ. Microbiol. 68, 5981-5989. (Pubitemid 36342431)
59. Waddell, P. J. and Steel, M. A. (1997). General time-reversible distances with unequal rates across sites: mixing gamma and inverse Gaussian distributions with invariant sites. Mol. Phylogenet. Evol. 8, 398-414. (Pubitemid 127347898)
60. Zhang, R. and Verkman, A. S. (1991). Water and urea permeability properties of Xenopus oocytes: Expression of mRNA from toad urinary bladder. Am. J. Physiol. 260, 26-34.
61. Zimmerman, S. L., Frisbie, J., Goldstein, D. L., West, J., Rivera, K. and Krane, C. M. (2007). Excretion and conservation of glycerol, and expression of aquaporins and glyceroporins, during cold acclimation in Cope's gray tree frog Hyla chrysoscelis. Am. J. Physiol. 292, 544-555.