Mechanisms of suspended animation are revealed by transcript profiling of diapause in the flesh fly

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 33, 2010, Pages 14909-14914

  Ragland, Gregory J ^a   Denlinger, David L ^b   Hahn, Daniel A ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Dormancy; Insulin signaling; Metabolic depression; Sarcophaga crassipalpis; Stress tolerance

Indexed keywords

ANTIOXIDANT; FATTY ACID; GLYOXYLIC ACID; INSULIN; MALATE DEHYDROGENASE; NICOTINAMIDE ADENINE DINUCLEOTIDE; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SUCCINIC ACID;

ANOXIA; ARTICLE; CAENORHABDITIS; COLD TOLERANCE; DIAPAUSE; DNA REPLICATION; DORMANCY; DROSOPHILA MELANOGASTER; ENDOCRINE FUNCTION; FLY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GLUCONEOGENESIS; GLYCOLYSIS; HYPOXIA; INSECT; INVERTEBRATE; METABOLIC INHIBITION; METABOLISM; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SARCOPHAGA CRASSIPALPIS; SEASON; STRESS; SUSPENDED ANIMATION; ANIMAL; DNA MICROARRAY; DNA SEQUENCE; EXPRESSED SEQUENCE TAG; GENE; GENETICS; GROWTH, DEVELOPMENT AND AGING; LARVA; LIFE CYCLE; MOLECULAR GENETICS;

CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; INVERTEBRATA; SARCOPHAGA CRASSIPALPIS; SARCOPHAGIDAE;

ANIMALS; DIPTERA; EXPRESSED SEQUENCE TAGS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, INSECT; LARVA; LIFE CYCLE STAGES; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SEQUENCE ANALYSIS, DNA;

EID: 77957031303     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1007075107     Document Type: Article

References (43)

1. Denlinger DL, Yocum GD, Rinehart JL (2005) Hormonal Control of Diapause: Comprehensive Molecular Insect Science, eds Gilbert LI, Iatrou K, Gill SS (Elsevier Press, Amsterdam), Vol. 3, pp 615-650.
2. Kostál V (2006) Eco-physiological phases of insect diapause. J Insect Physiol 52:113-127.
3. Denlinger DL, Campbell JJ, Bradfield JY (1980) Stimulatory effect of organic solvents on initiating development in diapausing pupae of the flesh fly Sarcophaga crassipalpis and the tobacco hornworm Manduca sexta. Physiol Entomol 5:7-15.
4. Qin W, Neal SJ, Robertson RM, Westwood JT, Walker VK (2005) Cold hardening and transcriptional change in Drosophila melanogaster. Insect Mol Biol 14:607-613. (Pubitemid 44914743)
5. Girardot F, Monnier FV, Tricoire H (2004) Genome wide analysis of common and specific stress responses in adult Drosophila melanogaster. BMC Genomics 5:16.
6. Landis GN, et al. (2004) Similar gene expression patterns characterize aging and oxidative stress in Drosophila melanogaster. Proc Natl Acad Sci USA 101:7663-7668.
7. Liu GW, Roy J, Johnson EA (2006) Identification and function of hypoxia-response genes in Drosophila melanogaster. Physiol Genomics 25:134-141.
8. Beckstead RB, Lam G, Thummel CS (2005) The genomic response to 20-hydroxyecdysone at the onset of Drosophila metamorphosis. Genome Biol 6:R99.
9. Hahn DA, Denlinger DL (2007) Meeting the energetic demands of insect diapause: Nutrient storage and utilization. J Insect Physiol 53:760-773.
10. Kukal O, Denlinger DL, Lee RE, Jr. (1991) Developmental and metabolic changes induced by anoxia in diapausing and non-diapausing flesh fly pupae. J Comp Physiol B 160:683-689.
11. Michaud MR, Denlinger DL (2007) Shifts in the carbohydrate, polyol, and amino acid pools during rapid cold-hardening and diapause-associated cold-hardening in flesh flies (Sarcophaga crassipalpis): A metabolomic comparison. J Comp Physiol B 177:753-763.
12. Denlinger DL, Lee RE (1998) Physiology of Cold Sensitivity. Temperature Sensitivity in Insects and Application in Integrated Pest Management, eds Hallman GJ, Denlinger DL (Westview Press, Oxford), pp 55-95.
13. Guppy M, Withers P (1999) Metabolic depression in animals: Physiological perspectives and biochemical generalizations. Biol Rev Camb Philos Soc 74:1-40. (Pubitemid 29215911)
14. Storey KB, Storey J (2002) Life in the slow lane: Molecular mechanisms of estivation. Comp Biochem Physiol A Mol Integr Physiol 133:733-754.
15. Baker DA, Russell S (2009) Gene expression during Drosophila melanogaster egg development before and after reproductive diapause. BMC Genomics 10:242.
16. Wang J, Kim SK (2003) Global analysis of dauer gene expression in Caenorhabditis elegans. Development 130:1621-1634. (Pubitemid 36527521)
17. Jeong P-Y, Kwon M-S, Joo H-J, Paik Y-K (2009) Molecular time-course and the metabolic basis of entry into dauer in Caenorhabditis elegans. PLoS ONE 4:e4162.
18. Emerson KJ, Bradshaw WE, Holzapfel CM (2010) Microarrays reveal early transcriptional events during the termination of larval diapause in natural populations of the mosquito, Wyeomyia smithii. PLoS ONE 5:e9574.
19. Yocum GD, Kemp WP, Bosch J, Knoblett JN (2005) Temporal variation in overwintering gene expression and respiration in the solitary bee Megachile rotundata. J Insect Physiol 51:621-629. (Pubitemid 40886406)
20. Zhou G, Miesfeld RL (2009) Energy metabolism during diapause in Culex pipiens mosquitoes. J Insect Physiol 55:40-46.
21. Rinehart JP, et al. (2007) Up-regulation of heat shock proteins is essential for cold survival during insect diapause. Proc Natl Acad Sci USA 104:11130-11137.
22. Hahn DA, Ragland GJ, Shoemaker DD, Denlinger DL (2009) Gene discovery using massively parallel pyrosequencing to develop ESTs for the flesh fly Sarcophaga crassipalpis. BMC Genomics 10:234.
23. Jovanovic-Galanovic A, et al. (2007) Antioxidant defense in mitochondria during diapause and post-diapause development of European corn borer. Arch Insect Biochem Physiol 64:111-119.
24. Krishnan N, Kodrík D, Turanli F, Sehnal F (2007) Stage-specific distribution of oxidative radicals and antioxidant enzymes in the midgut of Leptinotarsa decemlineata. J Insect Physiol 53:67-74. (Pubitemid 46039810)
25. Rinehart JP, Robich RM, Denlinger DL (2010) Isolation of diapause-regulated genes from the flesh fly, Sarcophaga crassipalpis by suppressive subtractive hybridization. J Insect Physiol 56:603-609.
26. Goving S (2008) Innate immunity in Drosophila: Pathogens and pathways. Insect Sci 15:29-43.
27. Goto SG (2001) A novel gene that is up-regulated during recovery from cold shock in Drosophila melanogaster. Gene 270:259-264.
28. Apidianakis Y, et al. (2005) Profiling early infection responses: Pseudomonas aeruginosa eludes host defenses by suppressing antimicrobial peptide gene expression. Proc Natl Acad Sci USA 102:2573-2578. (Pubitemid 40279418)
29. Wu Q, Brown MR (2006) Signaling and function of insulin-like peptides in insects. Annu Rev Entomol 51:1-24. (Pubitemid 43107812)
30. Guertin DA, Guntur KVP, Bell GW, Thoreen CC, Sabatini DM (2006) Functional genomics identifies TOR-regulated genes that control growth and division. Curr Biol 16:958-970.
31. Gershman B, et al. (2007) High-resolution dynamics of the transcriptional response to nutrition in Drosophila: A key role for dFOXO. Physiol Genomics 29:24-34. (Pubitemid 46708759)
32. Fielenbach N, Antebi A (2008) C. elegans dauer formation and the molecular basis of plasticity. Genes Dev 22:2149-2165.
33. Arpagaus M (1987) Vertebrate insulin induces diapause termination in Pieris brassicae pupae. Roux's Arch Dev Biol 196:527-530.
34. Tatar M, Yin CM (2001) Slow aging during insect reproductive diapause: Why butterflies, grasshoppers and flies are like worms. Exp Gerontol 36:723-738. (Pubitemid 32273415)
35. Sim C, Denlinger DL (2008) Insulin signaling and FOXO regulate the overwintering diapause of the mosquito Culex pipiens. Proc Natl Acad Sci USA 105:6777-6781.
36. Brown MR, Sieglaff DH, Rees HH (2009) Gonadal ecdysteroidogenesis in arthropoda: Occurrence and regulation. Annu Rev Entomol 54:105-125.
37. Schmidt PS, et al. (2008) An amino acid polymorphism in the couch potato gene forms the basis for climatic adaptation in Drosophila melanogaster. Proc Natl Acad Sci USA 105:16207-16211.
38. Saunders DS, Henrich VC, Gilbert LI (1989) Induction of diapause in Drosophila melanogaster: Photoperiodic regulation and the impact of arrhythmic clock mutations on time measurement. Proc Natl Acad Sci USA 86:3748-3752.
39. Smyth GK, Michaud J, Scott HS (2005) Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics 21:2067-2075.
40. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate - a practical and powerful approach to multiple testing. J R Stat Soc B 57:289-300.
41. Lee M-L, Kuo FC, Whitmore GA, Sklar J (2000) Importance of replication in microarray gene expression studies: Statistical methods and evidence from repetitive cDNA hybridizations. Proc Natl Acad Sci USA 97:9834-9839.
42. Shimodaira H (2002) An approximately unbiased test of phylogenetic tree selection. Syst Biol 51:492-508.
43. Efron B, Tibshirani R (2007) On testing the significance of sets of genes. Ann Appl Stat 1:107-129.