Improved tolerance to salt and water stress in Drosophila melanogaster cells conferred by late embryogenesis abundant protein

Journal of Insect Physiology

Volumn 59, Issue 4, 2013, Pages 377-386

  Marunde, Matthew R ^a   Samarajeewa, Dilini A ^a   Anderson, John ^a   Li, Shumin ^a,b   Hand, Steven C ^a,b   Menze, Michael A ^a  

^a EASTERN ILLINOIS UNIVERSITY   (United States)

^b LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

Bioenergetics; Cellular respirometry; Cryopreservation; Mitochondria; Water stress

Indexed keywords

ARTHROPOD PROTEIN;

BIOENERGETICS; CRYOPRESERVATION; CYTOLOGY; CYTOPLASM; EMBRYO; FLY; MITOCHONDRION; MOISTURE CONTENT; PROTEIN; SALINITY TOLERANCE; WATER STRESS;

AMINO ACID SEQUENCE; ANIMAL; ANIMAL EMBRYO; ARTEMIA; ARTICLE; CELL CULTURE; CELL RESPIRATION; CHEMISTRY; DESICCATION; DROSOPHILA MELANOGASTER; GENETIC TRANSFECTION; GENETICS; METABOLISM; MITOCHONDRION; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRENATAL DEVELOPMENT; SEQUENCE HOMOLOGY; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; ARTEMIA; ARTHROPOD PROTEINS; BLOTTING, WESTERN; CELL RESPIRATION; CELLS, CULTURED; DESICCATION; DROSOPHILA MELANOGASTER; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EMBRYO, NONMAMMALIAN; MITOCHONDRIA; SEQUENCE HOMOLOGY; TRANSFECTION;

EID: 84875070827     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2013.01.004     Document Type: Article

References (71)

1. Attardi G., Schatz G. Biogenesis of mitochondria. Annual Review of Cell Biology 1988, 4:289-333.
2. Babu R., Zhang J., Blum A., Ho T., Wu R., Nguyen H. HVA1, a LEA gene from barley confers dehydration tolerance in transgenic rice (Oryza sativa L.) via cell membrane protection. Plant Science 2004, 166:7.
3. Battaglia M., Olvera-Carrillo Y., Garciarrubio A., Campos F., Covarrubias A.A. The enigmatic LEA proteins and other hydrophilins. Plant Physiology 2008, 148:6-24.
4. Billi D., Potts M. Life and death of dried prokaryotes. Research in Microbiology 2002, 153:7-12.
5. Brand M.D., Nicholls D.G. Assessing mitochondrial dysfunction in cells. Biochemistry Journal 2011, 435:297-312.
6. Bray E.A. Molecular responses to water deficit. Plant Physiology 1993, 103:1035-1040.
7. Chacinska A., Koehler C.M., Milenkovic D., Lithgow T., Pfanner N. Importing mitochondrial proteins: machineries and mechanisms. Cell 2009, 138:628-644.
8. Chakrabortee S., Liu Y., Zhang L., Matthews H.R., Zhang H., Pan N., Cheng C.R., Guan S.H., Guo D.A., Huang Z., Zheng Y., Tunnacliffe A. Macromolecular and small-molecule modulation of intracellular Abeta42 aggregation and associated toxicity. Biochemistry Journal 2012, 442:507-515.
9. Clegg J.S. Do dried Cryptobiotes have a Metabolism? Anhydrobiosis 1973, Dowden, Hutchinson and Ross, Stroudsbourg, PA, p. 5.
10. Clegg J.S. Cryptobiosis - a peculiar state of biological organization. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 2001, 128:613-624.
11. Crowe J.H., Clegg J.S. Anhydrobiosis 1973, Dowden, Stroudsburg, Pa.
12. Crowe J.H., Hoekstra F.A., Crowe L.M. Anhydrobiosis. Annual Review of Physiology 1992, 54:579-599.
13. Crowe J.H., Madin K.A.C. Anhydrobiosis in tardigrades and nematodes. Transactions of the American Microscopical Society 1974, 93:11.
14. Crowe J.H., Madin K.A.C. Anhydrobiosis in nematodes: evaporative water loss and survival. Journal of Experimental Zoology 1975, 193:11.
15. Cuming A. LEA proteins. Seed Proteins 1999, 27. Kluwer Acad, Dordrecht, The Netherlands. P. Shewry, R. Casey (Eds.).
16. Dure L., Galau G.A. Developmental biochemistry of cottonseed embryogenesis and germination. XIII. Regulation of biosynthesis of principle storage proteins. Plant Physiology 1981, 68:187-194.
17. Espelund M., Saeboe-Larssen S., Hughes D.W., Galau G.A., Larsen F., Jakobsen K.S. Late embryogenesis - abundant genes encoding proteins with different numbers of hydrophilic repeats are regulated differentially by abscisic acid and osmotic stress. The Plant Journal 1992, 2:241-252.
18. Furuki T., Shimizu T., Kikawada T., Okuda T., Sakurai M. Salt effects on the structural and thermodynamic properties of a group 3 LEA protein model peptide. Biochemistry 2011, 50:7093-7103.
19. Galau G.A., Hughes D.W., Dure L. Abscisic acid induction of cloned cotton late embryogenesis - abundant (lea) mRNAs. Plant Molecular Biology 1986, 7:15.
20. Goyal K., Walton L.J., Browne J.A., Burnell A.M., Tunnacliffe A. Molecular anhydrobiology: identifying molecules implicated in invertebrate anhydrobiosis. Integrative and Comparative Biology 2005, 45:702-709.
21. Grelet J., Benamar A., Teyssier E., Avelange-Macherel M.H., Grunwald D., Macherel D. Identification in pea seed mitochondria of a late-embryogenesis abundant protein able to protect enzymes from drying. Plant Physiology 2005, 137:157-167.
22. Hand S.C., Jones D., Menze M.A., Witt T.L. Life without water: expression of plant LEA genes by an anhydrobiotic arthropod. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 2007, 307:62-66.
23. Hand S.C., Menze M.A., Toner M., Boswell L., Moore D. LEA proteins during water stress: not just for plants anymore. Annual Review of Physiology 2011, 73:115-134.
24. Hikita H., Asai S., Azuma Y. Solubility and diffusivity of oxygen in aqueous sucrose solutions. The Canadian Journal of Chemical Engineering 1978, 56:3.
25. Hinton H.E. Reversible suspension of metabolism and the origin of life. Proceedings of the Royal Society B, Biological Sciences 1968, 171:43-57.
26. Hoekstra F.A., Golovina E.A., Buitink J. Mechanisms of plant desiccation tolerance. Trends in Plant Science 2001, 6:431-438.
27. Hundertmark M., Hincha D.K. LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 2008, 9:118.
28. Hundertmark M., Popova A.V., Rausch S., Seckler R., Hincha D.K. Influence of drying on the secondary structure of intrinsically disordered and globular proteins. Biochemical and Biophysical Research Communications 2012, 417:122-128.
29. Iturriaga G., Schneider K., Salamini F., Bartels D. Expression of desiccation-related proteins from the resurrection plant Craterostigma plantagineum in transgenic tobacco. Plant Molecular Biology 1992, 20:555-558.
30. Kapardar R.K., Ranjan R., Grover A., Puri M., Sharma R. Identification and characterization of genes conferring salt tolerance to Escherichia coli from pond water metagenome. Bioresource Technology 2010, 101:3917-3924.
31. Keilin D. The problem of anabiosis or latent life: history and current concept. Proceedings of the Royal Society B, Biological Sciences 1959, 150:149-191.
32. Kovacs D., Kalmar E., Torok Z., Tompa P. Chaperone activity of ERD10 and ERD14, two disordered stress-related plant proteins. Plant Physiology 2008, 147:381-390.
33. Lan Y., Cai D., Zheng Y. Expression in Escherichia coli of three different soybean late embryogenesis abundant (LEA) genes to investigate enhanced stress tolerance. Journal of Integrative Plant Biology 2005, 47:8.
34. Lemire B.D., Fankhauser C., Baker A., Schatz G. The mitochondrial targeting function of randomly generated peptide sequences correlates with predicted helical amphiphilicity. Journal of Biological Chemistry 1989, 264:20206-20215.
35. Li D., He X. Desiccation induced structural alterations in a 66-amino acid fragment of an anhydrobiotic nematode late embryogenesis abundant (LEA) protein. Biomacromolecules 2009, 10:1469-1477.
36. Liu Y., Chakrabortee S., Li R., Zheng Y., Tunnacliffe A. Both plant and animal LEA proteins act as kinetic stabilisers of polyglutamine-dependent protein aggregation. FEBS Letters 2011, 585:630-634.
37. Maqbool B., Zhong H., El-Maghraby Y., Ahmad A., Chai B., Wang W., Sabzikar R., Sticklen B. Competence of oat (Avena sativa L.) shoot apical meristems for integrative transformation, inherited expression, and osmotic tolerance of transgenic lines containing hva1. Theoretical and Applied Genetics 2002, 105:201-208.
38. Menze M.A., Boswell L., Toner M., Hand S.C. Occurrence of mitochondria - targeted late embryogenesis abundant (LEA) gene in animals increases organelle resistance to water stress. Journal of Biological Chemistry 2009, 284:10714-10719.
39. Oliver A.E., Leprince O., Wolkers W.F., Hincha D.K., Heyer A.G., Crowe J.H. Non-disaccharide-base mechanisms of protection during drying. Cryobiology 2001, 43:16.
40. Pammenter N.W., Berjak P. A review of recalcitrant seed physiology in relation to desiccation-tolerance mechanisms. Seed Science Research 1999, 9:24.
41. Pichaud N., Chatelain E.H., Ballard J.W., Tanguay R., Morrow G., Blier P.U. Thermal sensitivity of mitochondrial metabolism in two distinct mitotypes of Drosophila simulans: evaluation of mitochondrial plasticity. Journal of Experimental Biology 2010, 213:1665-1675.
42. Pierce V.A., Mueller L.D., Gibbs A.G. Osmoregulation in Drosophila melanogaster selected for urea tolerance. Journal of Experimental Biology 1999, 202:2349-2358.
43. Popova A.V., Hundertmark M., Seckler R., Hincha D.K. Structural transitions in the intrinsically disordered plant dehydration stress protein LEA7 upon drying are modulated by the presence of membranes. Biochimica et Biophysica Acta 2011, 1808:1879-1887.
44. Potts M. Mechanisms of desiccation tolerance in cyanobacteria. European Journal of Phycology 1999, 34:9.
45. Pouchkina-Stantcheva N.N., McGee B.M., Boschetti C., Tolleter D., Chakrabortee S., Popova A.V., Meersman F., Macherel D., Hincha D.K., Tunnacliffe A. Functional divergence of former alleles in an ancient asexual invertebrate. Science 2007, 318:268-271.
46. Reynolds J.A., Hand S.C. Differences in isolated mitochondria are insufficient to account for respiratory depression during diapause in artemia franciscana embryos. Physiological and Biochemical Zoology 2004, 77:366-377.
47. Schmidt O., Pfanner N., Meisinger C. Mitochondrial protein import: from proteomics to functional mechanisms. Nature Reviews Molecular Cell Biology 2010, 11:655-667.
48. Sharon M.A., Kozarova A., Clegg J.S., Vacratsis P.O., Warner A.H. Characterization of a group 1 late embryogenesis abundant protein in encysted embryos of the brine shrimp Artemia franciscana. Biochemistry and Cell Biology 2009, 87:415-430.
49. Shih M.D., Hoekstra F.A., Hsing Y.I.C. Late embryogenesis abundant proteins. Advances in Botanical Research 2008, 48:44.
50. Sivamani E., Bahieldin A., Wraith J.M., Al-Niemi T., Dyer W.E., Ho T.D., Qu R. Improved biomass productivity and water use efficiency under water deficit conditions in transgenic wheat constitutively expressing the barley HVA1 gene. Plant Science 2000, 155:1-9.
51. Solomon A., Salomon R., Paperna I., Glazer I. Desiccation stress of entomopathogenic nematodes induces the accumulation of a novel heat-stable protein. Parasitology 2000, 121(Pt 4):409-416.
52. Stacy R.A., Aalen R.B. Identification of sequence homology between the internal hydrophilic repeated motifs of group 1 late-embryogenesis-abundant proteins in plants and hydrophilic repeats of the general stress protein GsiB of Bacillus subtilis. Planta 1998, 206:476-478.
53. Steinlechner-Maran R., Eberl T., Kunc M., Margreiter R., Gnaiger E. Oxygen dependence of respiration in coupled and uncoupled endothelial cells. American Journal of Physiology 1996, 271:C2053-C2061.
54. Steponkus P.L., Uemura M., Joseph R.A., Gilmour S.J., Thomashow M.F. Mode of action of the COR15a gene on the freezing tolerance of Arabidopsis thaliana. Proceedings of the National Academy of Sciences USA 1998, 95:14570-14575.
55. Stupnikova I., Benamar A., Tolleter D., Grelet J., Borovskii G., Dorne A.J., Macherel D. Pea seed mitochondria are endowed with a remarkable tolerance to extreme physiological temperatures. Plant Physiology 2006, 140:326-335.
56. Tolleter D., Hincha D.K., Macherel D. A mitochondrial late embryogenesis abundant protein stabilizes model membranes in the dry state. Biochimica et Biophysica Acta 2010, 1798:1926-1933.
57. Tolleter D., Jaquinod M., Mangavel C., Passirani C., Saulnier P., Manon S., Teyssier E., Payet N., Avelange-Macherel M.H., Macherel D. Structure and function of a mitochondrial late embryogenesis abundant protein are revealed by desiccation. Plant Cell 2007, 19:1580-1589.
58. Tompa P. Intrinsically unstructured proteins. Trends in Biochemical Sciences 2002, 27:527-533.
59. Tripathi R., Boschetti C., McGee B., Tunnacliffe A. Trafficking of bdelloid rotifer late embryogenesis abundant proteins. Journal of Experimental Biology 2012, 215:2786-2794.
60. Tunnacliffe A., Lapinski J. Resurrecting Van Leeuwenhoek's rotifers: a reappraisal of the role of disaccharides in anhydrobiosis. Philosophical Transactions of the Royal Society B, Biological Sciences 2003, 358:1755-1771.
61. Tunnacliffe A., Wise M.J. The continuing conundrum of the LEA proteins. Naturwissenschaften 2007, 94:791-812.
62. Uversky V.N., Dunker A.K. Understanding protein non-folding. Biochimica et Biophysica Acta 2010, 1804:1231-1264.
63. Warner A.H., Miroshnychenko O., Kozarova A., Vacratsis P.O., MacRae T.H., Kim J., Clegg J.S. Evidence for multiple group 1 late embryogenesis abundant proteins in encysted embryos of Artemia and their organelles. Journal of Biochemistry 2010, 148:581-592.
64. Watanabe M., Kikawada T., Fujita A., Okuda T. Induction of anhydrobiosis in fat body tissue from an insect. Journal of Insect Physiology 2005, 51:727-731.
65. Wise M.J. LEAping to conclusions: a computational reanalysis of late embryogenesis abundant proteins and their possible roles. BMC Bioinformatics 2003, 4:52.
66. Wise M.J., Tunnacliffe A. POPP the question: what do LEA proteins do?. Trends in Plant Science 2004, 9:13-17.
67. Wolkers W.F., McCready S., Brandt W.F., Lindsey G.G., Hoekstra F.A. Isolation and characterization of a D-7 LEA protein from pollen that stabilizes glasses in vitro. Biochimica et Biophysica Acta 2001, 1544:196-206.
68. Wu G., Zhang H., Sun J., Liu F., Ge X., Chen W.H., Yu J., Wang W. Diverse LEA (late embryogenesis abundant) and LEA-like genes and their responses to hypersaline stress in post-diapause embryonic development of Artemia franciscana. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 2011, 160:32-39.
69. Yamaguchi R., Andreyev A., Murphy A.N., Perkins G.A., Ellisman M.H., Newmeyer D.D. Mitochondria frozen with trehalose retain a number of biological functions and preserve outer membrane integrity. Cell Death & Differentiation 2007, 14:616-624.
70. Yancey P.H., Clark M.E., Hand S.C., Bowlus R.D., Somero G.N. Living with water stress: evolution of osmolyte systems. Science 1982, 217:1214-1222.
71. Yu J., Zhang J., Shan L., Chen S. Two new group 3 LEA genes of wheat and their functional analysis in yeast. Journal of Integrative Plant Biology 2005, 47:9.