Microarray analysis of natural socially regulated plasticity in circadian rhythms of honey bees

Journal of Biological Rhythms

Volumn 27, Issue 1, 2012, Pages 12-24

  Rodriguez Zas, Sandra L ^a   Southey, Bruce R ^a   Shemesh, Yair ^b   Rubin, Elad B ^b   Cohen, Mira ^b   Robinson, Gene E ^a   Bloch, Guy ^b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

clock genes; gene expression; honey bee; P450; social behavior; transcriptome

Indexed keywords

CYTOCHROME P450; MESSENGER RNA; NERVE PROTEIN; SCOTOPSIN;

ANIMAL; ARTICLE; BEE; BRAIN; CIRCADIAN RHYTHM; DNA MICROARRAY; GENETIC ASSOCIATION; GENETICS; METABOLISM; MOTOR ACTIVITY; PERIODICITY; PHYSIOLOGY; SOCIAL BEHAVIOR;

ANIMALS; BEES; BRAIN; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; CYTOCHROME P-450 ENZYME SYSTEM; GENOME-WIDE ASSOCIATION STUDY; MOTOR ACTIVITY; NERVE TISSUE PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PERIODICITY; RNA, MESSENGER; ROD OPSINS; SOCIAL BEHAVIOR;

APIS MELLIFERA; APOIDEA;

EID: 84856717663     PISSN: 07487304     EISSN: 15524531     Source Type: Journal    
DOI: 10.1177/0748730411431404     Document Type: Article

References (75)

1. Adams HA, Southey BR, Everts RE, Marjani SL, Tian CX, Lewin HA, Rodriguez-Zas SL. Transferase activity function and system development process are critical in cattle embryo development. Funct Integr Genomics. 2011 ; 11: 139-150
2. Akhtar RA, Reddy AB, Maywood ES, Clayton JD, King VM, Smith AG, Gant TW, Hastings MH, Kyriacou CP. Circadian cycling of the mouse liver transcriptome, as revealed by cDNA microarray, is driven by the suprachiasmatic nucleus. Curr Biol. 2002 ; 12: 540-550 (Pubitemid 34271367)
3. Alaux C, Sinha S, Hasadsri L, Hunt GJ, Guzman-Novoa E, DeGrandi-Hoffman G, Uribe-Rubio JL, Southey BR, Rodriguez-Zas S, Robinson GE. Honey bee aggression supports a link between gene regulation and behavioral evolution. Proc Natl Acad Sci U S A. 2009 ; 106: 15400-15405
4. Al-Shahrour F, Carbonell J, Minguez P, Goetz S, Conesa A, Tarraga J, Medina I, Alloza E, Montaner D, Dopazo J. Babelomics: advanced functional profiling of transcriptomics, proteomics and genomics experiments. Nucleic Acids Res. 2008 ; 36: W341 - W346
5. Bass J, Takahashi JS. Circadian integration of metabolism and energetics. Science. 2010 ; 330: 1349-1354
6. Bell-Pedersen D, Cassone VM, Earnest DJ, Golden SS, Hardin PE, Thomas TL, Zoran MJ. Circadian rhythms from multiple oscillators: lessons from diverse organisms. Nat Rev Genet. 2005 ; 6: 544-556 (Pubitemid 40910431)
7. Ben Shahar Y, Robichon A, Sokolowski MB, Robinson GE. Influence of gene action across different time scales on behavior. Science. 2002 ; 296: 741-744 (Pubitemid 34442003)
8. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Statist Soc Ser B. 1995 ; 59: 289-300
9. Blasing OE, Gibon Y, Gunther M, Hohne M, Morcuende R, Osuna D, Thimm O, Usadel B, Scheible WR, Stitt M. Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell. 2005 ; 17: 3257-3281
10. Bloch G Organization of Insect Societies: From Genome to Sociocomplexity. Gadau J Fewell J Wilson EO, ed. Cambridge, MA: Harvard University Press ; 2009: 402-431.
11. Bloch G. The social clock of the honeybee. J Biol Rhythms. 2010 ; 25: 307-317
12. Bloch G, Rubinstein CD, Robinson GE. Period expression in the honey bee brain is developmentally regulated and not affected by light, flight experience, or colony type. Insect Biochem Mol Biol. 2004 ; 34: 879-891 (Pubitemid 40047466)
13. Bloch G, Toma DP, Robinson GE. Behavioral rhythmicity, age, division of labor and period expression in the honey bee brain. J Biol Rhythms. 2001 ; 16: 444-456 (Pubitemid 32997028)
14. Ceriani MF, Hogenesch JB, Yanovsky M, Panda S, Straume M, Kay SA. Genome-wide expression analysis in Drosophila reveals genes controlling circadian behavior. J Neurosci. 2002 ; 22: 9305-9319 (Pubitemid 35356174)
15. Cirelli C, LaVaute TM, Tononi G. Sleep and wakefulness modulate gene expression in Drosophila. J Neurochem. 2005 ; 94: 1411-1419 (Pubitemid 41232596)
16. Claridge-Chang A, Wijnen H, Naef F, Boothroyd C, Rajewsky N, Young MW. Circadian regulation of gene expression systems in the Drosophila head. Neuron. 2001 ; 32: 657-671 (Pubitemid 33145199)
17. Claudianos C, Ranson H, Johnson RM, Biswas S, Schuler MA, Berenbaum MR, Feyereisen R, Oakeshott JG. A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee. Insect Mol Biol. 2006 ; 15: 615-636 (Pubitemid 44652091)
18. Doherty CJ, Kay SA. Circadian control of global gene expression patterns. Annu Rev Genet. 2010 ; 44: 419-444
19. Duffield GE. DNA microarray analyses of circadian timing: the genomic basis of biological time. J Neuroendocrinol. 2003 ; 15: 991-1002 (Pubitemid 37193017)
20. Dunlap JC, Loros JJ, DeCoursey PJ Chronobiology: Biological Timekeeping. Sunderland, MA: Sinauer Associates ; 2004:
21. Eban-Rothschild AD, Bloch G. Differences in the sleep architecture of forager and young honeybees (Apis mellifera). J Exp Biol. 2008 ; 211: 2408-2416
22. Eisenstein EM, Eisenstein D. A behavioral homeostasis theory of habituation and sensitization, II: further developments and predictions. Rev Neurosci. 2006 ; 17: 533-557 (Pubitemid 44836223)
23. Feyereisen R. Insect P450 enzymes. Annu Rev Entomol. 1999 ; 44: 507-533 (Pubitemid 29096982)
24. Green CB, Takahashi JS, Bass J. The meter of metabolism. Cell. 2008 ; 134: 728-742
25. Harbison ST, Sehgal A. Energy stores are not altered by long-term partial sleep deprivation in Drosophila melanogaster. PLoS One. 2009 ; 4: e6211
26. Insights into social insects from the genome of the honeybee Apis mellifera. Nature. 2006 ; 443: 931-949
27. Kadener S, Stoleru D, McDonald M, Nawathean P, Rosbash M. Clockwork Orange is a transcriptional repressor and a new Drosophila circadian pacemaker component. Genes Dev. 2007 ; 21: 1675-1686 (Pubitemid 47026370)
28. Kaiser W, Steiner-Kaiser J. Neuronal correlates of sleep, wakefulness and arousal in a diurnal insect. Nature. 1983 ; 301: 707-709 (Pubitemid 13164064)
29. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M. The KEGG resource for deciphering the genome. Nucleic Acids Res. 2004 ; 32: D277 - D280 (Pubitemid 38081656)
30. Katti C, Kempler K, Porter ML, Legg A, Gonzalez R, Garcia-Rivera E, Dugger D, Battelle BA. Opsin co-expression in Limulus photoreceptors: differential regulation by light and a circadian clock. J Exp Biol. 2010 ; 213: 2589-2601
31. Keegan KP, Pradhan S, Wang JP, Allada R. Meta-analysis of Drosophila circadian microarray studies identifies a novel set of rhythmically expressed genes. PLoS Comput Biol. 2007 ; 3: e208
32. Ko Y, Zhai C, Rodriguez-Zas SL. Discovery of gene network variability across samples representing multiple classes. Int J Bioinform Res Appl. 2010 ; 6: 402-417
33. Ko Y, Zhai C, Rodriguez-Zas SL. Inference of gene pathways using mixture Bayesian networks. BMC Syst Biol. 2009 ; 3: 54
34. Li P, Chaurasia SS, Gao Y, Carr AL, Iuvone PM, Li L. CLOCK is required for maintaining the circadian rhythms of opsin mRNA expression in photoreceptor cells. J Biol Chem. 2008 ; 283: 31673-31678
35. Lim C, Chung BY, Pitman JL, McGill JJ, Pradhan S, Lee J, Keegan KP, Choe J, Allada R. Clockwork Orange encodes a transcriptional repressor important for circadian-clock amplitude in Drosophila. Curr Biol. 2007 ; 17: 1082-1089 (Pubitemid 46899538)
36. Lin Y, Han M, Shimada B, Wang L, Gibler TM, Amarakone A, Awad TA, Stormo GD, Van Gelder RN, Taghert PH. Influence of the period-dependent circadian clock on diurnal, circadian, and aperiodic gene expression in Drosophila melanogaster. Proc Natl Acad Sci U S A. 2002 ; 99: 9562-9567 (Pubitemid 34764652)
37. Loor JJ, Dann HM, Everts RE, Oliveira R, Green CA, Guretzky NA, Rodriguez-Zas SL, Lewin HA, Drackley JK. Temporal gene expression profiling of liver from periparturient dairy cows reveals complex adaptive mechanisms in hepatic function. Physiol Genomics. 2005 ; 23: 217-226 (Pubitemid 44437980)
38. Loor JJ, Dann HM, Guretzky NA, Everts RE, Oliveira R, Green CA, Litherland NB, Rodriguez-Zas SL, Lewin HA, Drackley JK. Plane of nutrition prepartum alters hepatic gene expression and function in dairy cows as assessed by longitudinal transcript and metabolic profiling. Physiol Genomics. 2006 ; 27: 29-41 (Pubitemid 44511823)
39. Marler MR, Gehrman P, Martin JL, Ancoli-Israel S. The sigmoidally transformed cosine curve: a mathematical model for circadian rhythms with symmetric non-sinusoidal shapes. Stat Med. 2006 ; 25: 3893-3904 (Pubitemid 44718178)
40. Matsumoto A, Ukai-Tadenuma M, Yamada RG, Houl J, Uno KD, Kasukawa T, Dauwalder B, Itoh TQ, Takahashi K, Ueda R, et al. A functional genomics strategy reveals. Clockwork Orange. 2007 ; 21: 1687-1700
41. McDonald MJ, Rosbash M. Microarray analysis and organization of circadian gene expression in Drosophila. Cell. 2001 ; 107: 567-578 (Pubitemid 34014859)
42. McQuibban GA, Lee JR, Zheng L, Juusola M, Freeman M. Normal mitochondrial dynamics requires rhomboid-7 and affects Drosophila lifespan and neuronal function. Curr Biol. 2006 ; 16: 982-989 (Pubitemid 43728227)
43. Merino B, Somoza B, Ruiz-Gayo M, Cano V. Circadian rhythm drives the responsiveness of leptin-mediated hypothalamic pathway of cholecystokinin-8. Neurosci Lett. 2008 ; 442: 165-168
44. Mikulich SK, Zerbe GO, Jones RH, Crowley TJ. Comparing linear and nonlinear mixed model approaches to cosinor analysis. Stat Med. 2003 ; 22: 3195-3211 (Pubitemid 37220627)
45. Naeger NL, Van Nest BN, Johnson JN, Boyd SD, Southey BR, Rodriguez-Zas SL, Moore D, Robinson GE. Neurogenomic signatures of spatiotemporal memories in time-trained forager honey bees. J Exp Biol. 2011 ; 214: 979-987
46. Nagoshi E, Sugino K, Kula E, Okazaki E, Tachibana T, Nelson S, Rosbash M. Dissecting differential gene expression within the circadian neuronal circuit of Drosophila. Nat Neurosci. 2010 ; 13: 60-68
47. Pan Y, Michael TP, Hudson ME, Kay SA, Chory J, Schuler MA. Cytochrome P450 monooxygenases as reporters for circadian-regulated pathways. Plant Physiol. 2009 ; 150: 858-878
48. Panda S, Antoch MP, Miller BH, Su AI, Schook AB, Straume M, Schultz PG, Kay SA, Takahashi JS, Hogenesch JB. Coordinated transcription of key pathways in the mouse by the circadian clock. Cell. 2002 ; 109: 307-320 (Pubitemid 34606874)
49. Peitsch D, Fietz A, Hertel H, de Souza J, Ventura DF, Menzel R. The spectral input systems of hymenopteran insects and their receptor-based colour vision. J Comp Physiol A. 1992 ; 170: 23-40
50. Rewitz KF, O'Connor MB, Gilbert LI. Molecular evolution of the insect Halloween family of cytochrome P450s: phylogeny, gene organization and functional conservation. Insect Biochem Mol Biol. 2007 ; 37: 741-753 (Pubitemid 47030923)
51. Rodriguez-Zas SL, Gianola D, Shook GE. Bayesian analysis via Gibbs sampling of susceptibility to intramammary infection in Holstein cattle. J Dairy Sci. 1998 ; 81: 2710-2722 (Pubitemid 128444940)
52. Rodriguez-Zas SL, Gianola D, Shook GE. Factors affecting susceptibility to intramammary infection and mastitis: an approximate Bayesian analysis. J Dairy Sci. 1997 ; 80: 75-85 (Pubitemid 127447117)
53. Rodriguez-Zas SL, Ko Y Applied Statistics for Network Biology: Methods in Systems Biology. Dehmer M Emmert-Streib F Graber A Salvador A, ed. Weinheim, Germany: Wiley-VCH Verlag GmbH & Co. KGaA ; 2011: 91-103.
54. Rodriguez-Zas SL, Southey BR, Heyen DW, Lewin HA. Detection of quantitative trait loci influencing dairy traits using a model for longitudinal data. J Dairy Sci. 2002a ; 85: 2681-2691 (Pubitemid 38571468)
55. Rodriguez-Zas SL, Southey BR, Heyen DW, Lewin HA. Interval and composite interval mapping of somatic cell score, yield, and components of milk in dairy cattle. J Dairy Sci. 2002b ; 85: 3081-3091 (Pubitemid 38571432)
56. Rodriguez-Zas SL, Southey BR, Whitfield CW, Robinson GE. Semiparametric approach to characterize unique gene expression trajectories across time. BMC Genomics. 2006 ; 7: 233
57. Rubin EB, Shemesh Y, Cohen M, Elgavish S, Robertson HM, Bloch G. Molecular and phylogenetic analyses reveal mammalian-like clockwork in the honey bee (Apis mellifera) and shed new light on the molecular evolution of the circadian clock. Genome Res. 2006 ; 16: 1352-1365 (Pubitemid 44664678)
58. Sasagawa H, Narita R, Kitagawa Y, Kadowaki T. The expression of genes encoding visual components is regulated by a circadian clock, light environment and age in the honeybee (Apis mellifera). Eur J Neurosci. 2003 ; 17: 963-970 (Pubitemid 36411593)
59. Sato TK, Panda S, Kay SA, Hogenesch JB. DNA arrays: applications and implications for circadian biology. J Biol Rhythms. 2003 ; 18: 96-105 (Pubitemid 37187295)
60. Sehgal A, Mignot E. Genetics of sleep and sleep disorders. Cell. 2011 ; 146: 194-207
61. Shang Y, Griffith LC, Rosbash M. Light-arousal and circadian photoreception circuits intersect at the large PDF cells of the Drosophila brain. Proc Natl Acad Sci U S A. 2008 ; 105: 19587-19594
62. Shemesh Y, Cohen M, Bloch G. Natural plasticity in circadian rhythms is mediated by reorganization in the molecular clockwork in honeybees. FASEB J. 2007 ; 21: 2304-2311 (Pubitemid 47230660)
63. Shemesh Y, Eban-Rothschild A, Cohen M, Bloch G. Molecular dynamics and social regulation of context-dependent plasticity in the circadian clockwork of the honey bee. J Neurosci. 2010 ; 30: 12517-12525
64. Sieglaff DH, Duncan KA, Brown MR. Expression of genes encoding proteins involved in ecdysteroidogenesis in the female mosquito, Aedes aegypti. Insect Biochem Mol Biol. 2005 ; 35: 471-490 (Pubitemid 40440939)
65. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005 ; 102: 15545-15550 (Pubitemid 41528093)
66. Taghert PH. How does the circadian clock send timing information to the brain?. Semin Cell Dev Biol. 2001 ; 12: 329-341
67. Tauber E, Kyriacou CP. Molecular evolution and population genetics of circadian clock genes. Methods Enzymol. 2005 ; 393: 797-817 (Pubitemid 40486559)
68. Toma DP, Bloch G, Moore D, Robinson GE. Changes in period mRNA levels in the brain and division of labor in honey bee colonies. Proc Natl Acad Sci U S A. 2000 ; 97: 6914-6919 (Pubitemid 30412814)
69. Ueda HR, Matsumoto A, Kawamura M, Iino M, Tanimura T, Hashimoto S. Genome-wide transcriptional orchestration of circadian rhythms in Drosophila. J Biol Chem. 2002 ; 277: 14048-14052 (Pubitemid 34968014)
70. Velarde RA, Sauer CD, Walden KK, Fahrbach SE, Robertson HM. Pteropsin: a vertebrate-like non-visual opsin expressed in the honey bee brain. Insect Biochem Mol Biol. 2005 ; 35: 1367-1377 (Pubitemid 41606708)
71. von Frisch K The Dance Language and Orientation of Bees. Cambridge, MA: Belknap Press of Harvard University Press ; 1967:
72. Ware JH, Bowden RE. Circadian rhythm analysis when output is collected at intervals. Biometrics. 1977 ; 33: 566-571 (Pubitemid 8194093)
73. Wijnen H, Naef F, Boothroyd C, Claridge-Chang A, Young MW. Control of daily transcript oscillations in Drosophila by light and the circadian clock. PLoS Genet. 2006 ; 2: e39
74. Yanagawa S, Matsuda Y, Lee JS, Matsubayashi H, Sese S, Kadowaki T, Ishimoto A. Casein kinase I phosphorylates the Armadillo protein and induces its degradation in Drosophila. EMBO J. 2002 ; 21: 1733-1742 (Pubitemid 34614629)
75. Yerushalmi S, Green RM. Evidence for the adaptive significance of circadian rhythms. Ecol Lett. 2009 ; 12: 970-981