期刊论文详细信息
BMC Systems Biology
Invariance and plasticity in the Drosophila melanogaster metabolomic network in response to temperature
Daniel E L Promislow1  Dean P Jones5  Quinlyn A Soltow2  Ariel S Thomas3  Jessica M Hoffman6  Ramkumar Hariharan4 
[1] Department of Biology, University of Washington, Seattle 98195, WA, USA;ClinMet Inc, 3210 Merryfield Row, San Diego 92121, CA, USA;Washington University School of Medicine, 660 S. Euclid Avenue, St. Louis 63108, MO, USA;Laboratory for Integrated Bioinformatics, RIKEN Center for Integrative Medical Sciences, Yokohama 230-0045, Kanagawa, Japan;Department of Medicine, Clinical Biomarkers Laboratory, Emory University, Atlanta 30322, GA, USA;Department of Genetics, University of Georgia, Athens 30602, GA, USA
关键词: Differential coexpression;    Networks;    Metabolomics;    Temperature;    Drosophila melanogaster;   
Others  :  1091120
DOI  :  10.1186/s12918-014-0139-6
 received in 2014-08-19, accepted in 2014-12-11,  发布年份 2014
PDF
【 摘 要 】

Background

Metabolomic responses to extreme thermal stress have recently been investigated in Drosophila melanogaster. However, a network level understanding of metabolomic responses to longer and less drastic temperature changes, which more closely reflect variation in natural ambient temperatures experienced during development and adulthood, is currently lacking. Here we use high-resolution, non-targeted metabolomics to dissect metabolomic changes in D. melanogaster elicited by moderately cool (18°C) or warm (27°C) developmental and adult temperature exposures.

Results

We find that temperature at which larvae are reared has a dramatic effect on metabolomic network structure measured in adults. Using network analysis, we are able to identify modules that are highly differentially expressed in response to changing developmental temperature, as well as modules whose correlation structure is strongly preserved across temperature.

Conclusions

Our results suggest that the effect of temperature on the metabolome provides an easily studied and powerful model for understanding the forces that influence invariance and plasticity in biological networks.

【 授权许可】

   
2015 Hariharan et al.; licensee BioMed Central.

【 预 览 】
附件列表
Files Size Format View
20150128165715463.pdf 3570KB PDF download
Figure 4. 135KB Image download
Figure 3. 197KB Image download
Figure 2. 43KB Image download
Figure 1. 37KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】
  • [1]Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL: Effects of size and temperature on metabolic rate. Science 2001, 293(5538):2248-2251.
  • [2]Pichaud N, Chatelain EH, Ballard JW, Tanguay R, Morrow G, Blier PU: Thermal sensitivity of mitochondrial metabolism in two distinct mitotypes of Drosophila simulans: evaluation of mitochondrial plasticity. J Exp Biol 2010, 213(10):1665-1675.
  • [3]Koštál V, Šimek P, Zahradníčková H, Cimlová J, Štětina T: Conversion of the chill susceptible fruit fly larva (Drosophila melanogaster) to a freeze tolerant organism. Proc Natl Acad Sci U S A 2012, 109(9):3270-3274.
  • [4]Malmendal A, Overgaard J, Bundy JG, Sørensen JG, Nielsen NC, Loeschcke V, Holmstrup M: Metabolomic profiling of heat stress: hardening and recovery of homeostasis in Drosophila. Am J Physiol Regul Integr Comp Physiol 2006, 291(1):R205-R212.
  • [5]Sejerkilde M, Sorensen JG, Loeschcke V: Effects of cold- and heat hardening on thermal resistance in Drosophila melanogaster. J Insect Physiol 2003, 49(8):719-726.
  • [6]Maynard Smith J: Acclimatization to high temperatures in inbred and outbred Drosophila subobscura. J. Genet. 1956, 54, 497–505. J Genet 1956, 84(1):37-45.
  • [7]Feder ME, Hofmann GE: Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 1999, 61:243-282.
  • [8]Arya R, Mallik M, Lakhotia SC: Heat shock genes - integrating cell survival and death. J Biosci 2007, 32(3):595-610.
  • [9]Koštál V, Korbelová J, Rozsypal J, Zahradníčková H, Cimlová J, Tomčala A, Šimek P: Long-term cold acclimation extends survival time at 0 degrees C and modifies the metabolomic profiles of the larvae of the fruit fly Drosophila melanogaster. PLoS One 2011, 6(9):e25025.
  • [10]Vesala L, Salminen TS, Koštál V, Zahradníčková H, Hoikkala A: Myo-inositol as a main metabolite in overwintering flies: seasonal metabolomic profiles and cold stress tolerance in a northern drosophilid fly. J Exp Biol 2012, 215(16):2891-2897.
  • [11]Zhang J, Marshall KE, Westwood JT, Clark MS, Sinclair BJ: Divergent transcriptomic responses to repeated and single cold exposures in Drosophila melanogaster. J Exp Biol 2011, 214(Pt 23):4021-4029.
  • [12]Sinclair BJ, Gibbs AG, Roberts SP: Gene transcription during exposure to, and recovery from, cold and desiccation stress in Drosophila melanogaster. Insect Mol Biol 2007, 16(4):435-443.
  • [13]Qin W, Neal SJ, Robertson RM, Westwood JT, Walker VK: Cold hardening and transcriptional change in Drosophila melanogaster. Insect Mol Biol 2005, 14(6):607-613.
  • [14]Colinet H, Overgaard J, Com E, Sørensen JG: Proteomic profiling of thermal acclimation in Drosophila melanogaster. Insect Biochem Mol Biol 2013, 43(4):352-365.
  • [15]Vermeulen CJ, Pedersen KS, Beck HC, Petersen J, Gagalova KK, Loeschcke V: Proteomic Characterization of Inbreeding-Related Cold Sensitivity in Drosophila melanogaster.Plos One 2013, 8(5):e62680.
  • [16]Colinet H, Hoffmann AA: Comparing phenotypic effects and molecular correlates of developmental, gradual and rapid cold acclimation responses in Drosophila melanogaster. Funct Ecol 2012, 26(1):84-93.
  • [17]Pedersen KS, Kristensen TN, Loeschcke V, Petersen BO, Duus JØ, Nielsen NC, Malmendal A: Metabolomic signatures of inbreeding at benign and stressful temperatures in Drosophila melanogaster. Genetics 2008, 180(2):1233-1243.
  • [18]Sanders MM, Kon C: Glutamine is a powerful effector of heat-shock protein expression in Drosophila Kc cells. J Cell Physiol 1991, 146(1):180-190.
  • [19]Wishart DS: Computational approaches to metabolomics. Methods Mol Biol 2010, 593:283-313.
  • [20]Jones DP, Park Y, Ziegler TR: Nutritional metabolomics: progress in addressing complexity in diet and health. Annu Rev Nutr 2012, 32:183-202.
  • [21]Park YH, Lee K, Soltow QA, Strobel FH, Brigham KL, Parker RE, Wilson ME, Sutliff RL, Mansfield KG, Wachtman LM, Ziegler TR, Jones DP: High-performance metabolic profiling of plasma from seven mammalian species for simultaneous environmental chemical surveillance and bioeffect monitoring. Toxicology 2012, 295(1–3):47-55.
  • [22]Tesson BM, Breitling R, Jansen RC: DiffCoEx: a simple and sensitive method to find differentially coexpressed gene modules.BMC Bioinformatics 2010, 11:497.
  • [23]Langfelder P, Horvath S: WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 2008, 9:559. BioMed Central Full Text
  • [24]Amar D, Safer H, Shamir R: Dissection of regulatory networks that are altered in disease via differential co-expression. PLoS Comput Biol 2013, 9(3):e1002955.
  • [25]Fukushima A, Kusano M, Redestig H, Arita M, Saito K: Metabolomic correlation-network modules in Arabidopsis based on a graph-clustering approach. BMC Syst Biol 2011, 5:1. BioMed Central Full Text
  • [26]Kotze HL, Armitage EG, Sharkey KJ, Allwood JW, Dunn WB, Williams KJ, Goodacre R: A novel untargeted metabolomics correlation-based network analysis incorporating human metabolic reconstructions. BMC Syst Biol 2013, 7:107. BioMed Central Full Text
  • [27]Muller-Linow M, Weckwerth W, Hutt MT: Consistency analysis of metabolic correlation networks. BMC Syst Biol 2007, 1:44. BioMed Central Full Text
  • [28]Oms-Oliu G, Hertog MLATM, Van de Poel B, Ampofo-Asiama J, Geeraerd AH, Nicolai BM: Metabolic characterization of tomato fruit during preharvest development, ripening, and postharvest shelf-life. Postharvest Biology and Technology 2011, 62(1):7-16.
  • [29]Barkai N, Leibler S: Robustness in simple biochemical networks. Nature 1997, 387(6636):913-917.
  • [30]Gibson G: Robustness and evolvability in living systems. Science 2005, 310(5746):237-237.
  • [31]Mackay TF, Richards S, Stone EA, Barbadilla A, Ayroles JF, Zhu D, Casillas S, Han Y, Magwire MM, Cridland JM, Richardson MF, Anholt RR, Barrón M, Bess C, Blankenburg KP, Carbone MA, Castellano D, Chaboub L, Duncan L, Harris Z, Javaid M, Jayaseelan JC, Jhangiani SN, Jordan KW, Lara F, Lawrence F, Lee SL, Librado P, Linheiro RS, Lyman RF, et al.: The Drosophila melanogaster genetic reference panel. Nature 2012, 482(7384):173-178.
  • [32]Li S, Park Y, Duraisingham S, Strobel FH, Khan N, Soltow QA, Jones DP, Pulendran B: Predicting network activity from high throughput metabolomics. PLoS Comput Biol 2013, 9(7):e1003123.
  • [33]Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T: Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003, 13(11):2498-2504.
  • [34]Hoffmann AA: Physiological climatic limits in Drosophila: patterns and implications. J Exp Biol 2010, 213(6):870-880.
  • [35]Clark MS, Worland MR: How insects survive the cold: molecular mechanisms-a review. J Comp Physiol B 2008, 178(8):917-933.
  • [36]Feder ME, Blair N, Figueras H: Natural thermal stress and heat-shock protein expression in Drosophila larvae and pupae. Funct Ecol 1997, 11(1):90-100.
  • [37]Dillon ME, Wang G, Garrity PA, Huey RB: Thermal preference in Drosophila. J Therm Biol 2009, 34(3):109-119.
  • [38]Czarnoleski M, Cooper BS, Kierat J, Angilletta MJ Jr: Flies developed small bodies and small cells in warm and in thermally fluctuating environments. J Exp Biol 2013, 216(Pt 15):2896-2901.
  • [39]Ueno T, Tomita J, Kume S, Kume K: Dopamine Modulates Metabolic Rate and Temperature Sensitivity in Drosophila melanogaster.Plos One 2012, 7(2):e31513.
  • [40]Hirsh J, Riemensperger T, Coulom H, Iché M, Coupar J, Birman S: Roles of dopamine in circadian rhythmicity and extreme light sensitivity of circadian entrainment. Curr Biol 2010, 20(3):209-214.
  • [41]Alexander GJ, Schwenk E: Studies on biosynthesis of cholesterol. IX. Zymosterol as a precursor of cholesterol. Arch Biochem Biophys 1957, 66(2):381-387.
  • [42]Gault CR, Obeid LM, Hannun YA: An overview of sphingolipid metabolism: from synthesis to breakdown. Adv Exp Med Biol 2010, 688:1-23.
  • [43]Carvalho M, Sampaio JL, Palm W, Brankatschk M, Eaton S, Shevchenko A: Effects of diet and development on the Drosophila lipidome. Mol Syst Biol 2012, 8:600.
  • [44]Piper MD, Blanc E, Leitão-Gonçalves R, Yang M, He X, Linford NJ, Hoddinott MP, Hopfen C, Soultoukis GA, Niemeyer C, Kerr F, Pletcher SD, Ribeiro C, Partridge L: A holidic medium for Drosophila melanogaster. Nat Methods 2014, 11(1):100-105.
  • [45]Sigrist SJ, Carmona-Gutierrez D, Gupta VK, Bhukel A, Mertel S, Eisenberg T, Madeo F: Spermidine-triggered autophagy ameliorates memory during aging. Autophagy 2014, 10(1):178-179.
  • [46]Tautenhahn R, Cho K, Uritboonthai W, Zhu Z, Patti GJ, Siuzdak G: An accelerated workflow for untargeted metabolomics using the METLIN database. Nat Biotechnol 2012, 30(9):826-828.
  • [47]Castro C, Krumsiek J, Lehrbach NJ, Murfitt SA, Miska EA, Griffin JL: A study of Caenorhabditis elegans DAF-2 mutants by metabolomics and differential correlation networks. Mol Biosyst 2013, 9(7):1632-1642.
  • [48]Ghalambor CK, McKay JK, Carroll SP, Reznick DN: Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 2007, 21(3):394-407.
  • [49]Bockmayr M, Klauschen F, Györffy B, Denkert C, Budczies J: New network topology approaches reveal differential correlation patterns in breast cancer.Systems Biology 2013, 7:78.
  • [50]Bhattacharyya M, Bandyopadhyay S: Studying the differential co-expression of microRNAs reveals significant role of white matter in early Alzheimer’s progression. Mol Biosyst 2013, 9(3):457-466.
  • [51]Rotival M, Petretto E: Leveraging gene co-expression networks to pinpoint the regulation of complex traits and disease, with a focus on cardiovascular traits. Brief Funct Genomics 2014, 13(1):66-78.
  • [52]Dumas ME: Metabolome 2.0: quantitative genetics and network biology of metabolic phenotypes. Mol Biosyst 2012, 8(10):2494-2502.
  • [53]Hoffman JM, Soltow QA, Li S, Sidik A, Jones DP, Promislow DE: Effects of age, sex, and genotype on high-sensitivity metabolomic profiles in the fruit fly, Drosophila melanogaster.Aging Cell 2014, 13(4):596–604.
  • [54]Bo TH, Dysvik B, Jonassen I: LSimpute: accurate estimation of missing values in microarray data with least squares methods. Nucleic Acids Res 2004, 32(3):e34.
  • [55]Benjamini Y, Hochberg Y: Controlling the false discovery rate - a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B-Methodological 1995, 57(1):289-300.
  文献评价指标  
  下载次数:71次 浏览次数:28次