Behavioral plasticity in honey bees is associated with differences in brain microRNA transcriptome

Genes, Brain and Behavior

Volumn 11, Issue 6, 2012, Pages 660-670

  Greenberg, J K ^a   Xia, J ^b   Zhou, X ^b   Thatcher, S R ^c   Gu, X ^a   Ament, S A ^d,e   Newman, T C ^d   Green, P J ^c   Zhang, W ^b,f   Robinson, G E ^d   Ben Shahar, Y ^a  

^a WASHINGTON UNIVERSITY   (United States)

^b WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

^c UNIVERSITY OF DELAWARE   (United States)

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

^e INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

^f WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Division of labor; Honey bee; MicroRNA; Phylogenetics; Social behavior

Indexed keywords

MICRORNA; TRANSCRIPTOME;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN; BROOD PARASITE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; FORAGER; FORAGING BEHAVIOR; GENE CONTROL; GENE EXPRESSION; GENETIC CONSERVATION; HONEYBEE; LABOR; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; SOCIAL BEHAVIOR; SOCIAL ENVIRONMENT; TRANSCRIPTOMICS;

AGING; ANIMALS; BEES; BEHAVIOR, ANIMAL; BIOLOGICAL EVOLUTION; BRAIN CHEMISTRY; FEMALE; MALE; MICRORNAS; NEURONAL PLASTICITY; PHYLOGENY; TRANSCRIPTOME;

ACULEATA; APIS MELLIFERA; APOIDEA; HYMENOPTERA;

EID: 84864122499     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/j.1601-183X.2012.00782.x     Document Type: Article

References (83)

1. Alvarez-Saavedra, M., Antoun, G., Yanagiya, A., Oliva-Hernandez, R., Cornejo-Palma, D., Perez-Iratxeta, C., Sonenberg, N. & Cheng, H.Y. (2011) miRNA-132 orchestrates chromatin remodeling and translational control of the circadian clock. Hum Mol Genet 20, 731-751.
2. Andersson, M. (1984) The evolution of eusociality. Annu Rev Ecol Syst 15, 165-189.
3. Ashraf, S.I. & Kunes, S. (2006) A trace of silence: memory and microRNA at the synapse. Curr Opin Neurobiol 16, 535-539.
4. Ashraf, S.I., McLoon, A.L., Sclarsic, S.M. & Kunes, S. (2006) Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila. Cell 124, 191-205.
5. Baker, M. (2010) MicroRNA profiling: separating signal from noise. Nat Methods 7, 687-692.
6. Barik, S. (2008) An intronic microRNA silences genes that are functionally antagonistic to its host gene. Nucleic Acids Res 36, 5232-5241.
7. Bartel, D.P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297.
8. Bartel, D.P. (2009) MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233.
9. Behura, S.K. & Whitfield, C.W. (2010) Correlated expression patterns of microRNA genes with age-dependent behavioural changes in honeybee. Insect Mol Biol 19, 431-439.
10. Ben-Shahar, Y. (2005) The foraging gene, behavioral plasticity, and honeybee division of labor. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 191, 987-994.
11. Ben-Shahar, Y. & Robinson, G.E. (2001) Satiation differentially affects performance in a learning assay by nurse and forager honey bees. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 187, 891-899.
12. Ben-Shahar, Y., Robichon, A., Sokolowski, M.B. & Robinson, G.E. (2002) Influence of gene action across different time scales on behavior. Science 296, 741-744.
13. Ben-Shahar, Y., Leung, H.T., Pak, W.L., Sokolowski, M.B. & Robinson, G.E. (2003) cGMP-dependent changes in phototaxis: a possible role for the foraging gene in honey bee division of labor. J Exp Biol, 206, 2507-2515.
14. Ben-Shahar, Y., Dudek, N.L. & Robinson, G.E. (2004) Phenotypic deconstruction reveals involvement of manganese transporter malvolio in honey bee division of labor. J Exp Biol 207, 3281-3288.
15. Ben-Shahar, Y., Thompson, C.K., Hartz, S.M., Smith, B.H. & Robinson, G.E. (2000) Differences in performance on a reversal learning test and division of labor in honey bee colonies. Anim Cogn 3, 119-125.
16. Bonasio, R., Zhang, G., Ye, C., Mutti, N.S., Fang, X., Qin, N., Donahue, G., Yang, P., Li, Q., Li, C., Zhang, P., Huang, Z., Berger, S.L., Reinberg, D., Wang, J. & Liebig, J. (2010) Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 329, 1068-1071.
17. Brennecke, J., Hipfner, D.R., Stark, A., Russell, R.B. & Cohen, S.M. (2003) Bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell 113, 25-36.
18. Brennecke, J., Stark, A., Russell, R.B. & Cohen, S.M. (2005) Principles of microRNA-target recognition. PLoS Biol 3, e85.
19. Brodersen, P. & Voinnet, O. (2009) Revisiting the principles of microRNA target recognition and mode of action. Nat Rev Mol Cell Biol 10, 141-148.
20. Cao, X., Yeo, G., Muotri, A.R., Kuwabara, T. & Gage, F.H. (2006) Noncoding RNAs in the mammalian central nervous system. Annu Rev Neurosci 29, 77-103.
21. Chandrasekar, V. & Dreyer, J.L. (2011) Regulation of MiR-124, Let-7d, and MiR-181a in the accumbens affects the expression, extinction, and reinstatement of cocaine-induced conditioned place preference. Neuropsychopharmacology 36, 1149-1164.
22. Chen, X., Yu, X., Cai, Y., Zheng, H., Yu, D., Liu, G., Zhou, Q., Hu, S. & Hu, F. (2010) Next-generation small RNA sequencing for microRNAs profiling in the honey bee Apis mellifera. Insect Mol Biol 19, 799-805.
23. Cheng, H.Y. & Obrietan, K. (2007) Revealing a role of microRNAs in the regulation of the biological clock. Cell Cycle 6, 3034-3035.
24. Cheng, Y., Ji, R., Yue, J., Yang, J., Liu, X., Chen, H., Dean, D.B. & Zhang, C. (2007) MicroRNAs are aberrantly expressed in hypertrophic heart: do they play a role in cardiac hypertrophy? Am J Pathol 170, 1831-1840.
25. Consortium, H.G.S. (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443, 931-949.
26. Cullen, B.R. (2004) Transcription and processing of human microRNA precursors. Mol Cell 16, 861-865.
27. Djuranovic, S., Nahvi, A. & Green, R. (2011) A parsimonious model for gene regulation by miRNAs. Science 331, 550-553.
28. Edbauer, D., Neilson, J.R., Foster, K.A., Wang, C.F., Seeburg, D.P., Batterton, M.N., Tada, T., Dolan, B.M., Sharp, P.A. & Sheng, M. (2010) Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR-132. Neuron 65, 373-384.
29. Esquela-Kerscher, A. & Slack, F.J. (2006) Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer 6, 259-269.
30. Fabian, M.R., Sonenberg, N. & Filipowicz, W. (2010) Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79, 351-379.
31. Fahrbach, S.E. & Robinson, G.E. (1995) Behavioral development in the honey bee: toward the study of learning under natural conditions. Learn Mem 2, 199-224.
32. Filipowicz, W., Jaskiewicz, L., Kolb, F.A. & Pillai, R.S. (2005) Post-transcriptional gene silencing by siRNAs and miRNAs. Curr Opin Struct Biol 15, 331-341.
33. Fischer, P. & Grozinger, C.M. (2008) Pheromonal regulation of starvation resistance in honey bee workers (Apis mellifera). Naturwissenschaften 95, 723-729.
34. Grozinger, C.M., Sharabash, N.M., Whitfield, C.W. & Robinson, G.E. (2003) Pheromone-mediated gene expression in the honey bee brain. Proc Natl Acad Sci USA 100 (Suppl. 2)), 14519-14525.
35. Heo, I., Joo, C., Cho, J., Ha, M., Han, J. & Kim, V.N. (2008) Lin28 mediates the terminal uridylation of let-7 precursor MicroRNA. Mol Cell 32, 276284.
36. Hofacker, I.L. (2003) Vienna RNA secondary structure server. Nucleic Acids Res 31, 3429-3431.
37. Hori, S., Kaneko, K., Saito, T., Takeuchi, H. & Kubo, T. (2011) Expression of two microRNAs, ame-mir-276 and -1000, in the adult honeybee (Apis mellifera) brain. Apidologie 42, 89-102.
38. Huang, Z.Y. & Robinson, G.E. (1996) Regulation of honey bee division of labor by colony age demography. Behav Ecol Sociobiol 39, 147-158.
39. Huntzinger, E. & Izaurralde, E. (2011) Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 12, 99-110.
40. Kadener, S., Menet, J.S., Sugino, K., Horwich, M.D., Weissbein, U., Nawathean, P., Vagin, V.V., Zamore, P.D., Nelson, S.B. & Rosbash, M. (2009) A role for microRNAs in the Drosophila circadian clock. Genes Dev 23, 2179-2191.
41. Kim, V.N. (2005) MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 6, 376-385.
42. Kozomara, A. & Griffiths-Jones, S. (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 39, D152-D157.
43. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S.L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10, R25.
44. Leoncini, I., Le Conte, Y., Costagliola, G., Plettner, E., Toth, A.L., Wang, M., Huang, Z., Becard, J.M., Crauser, D., Slessor, K.N. & Robinson, G.E. (2004) Regulation of behavioral maturation by a primer pheromone produced by adult worker honey bees. Proc Natl Acad Sci USA 101, 17559-17564.
45. Li, S., Chen, X., Zhang, H., Liang, X., Xiang, Y., Yu, C., Zen, K., Li, Y. & Zhang, C.Y. (2009) Differential expression of microRNAs in mouse liver under aberrant energy metabolic status. J Lipid Res 50, 1756-1765.
46. Liu, N. & Olson, E.N. (2010) MicroRNA regulatory networks in cardiovascular development. Dev Cell 18, 510-525.
47. Lu, C., Meyers, B.C. & Green, P.J. (2007) Construction of small RNA cDNA libraries for deep sequencing. Methods 43, 110-117.
48. Lund, E., Guttinger, S., Calado, A., Dahlberg, J.E. & Kutay, U. (2004) Nuclear export of microRNA precursors. Science 303, 95-98.
49. Lutz, C.C., Rodriguez-Zas, S.L., Fahrbach, S.E. & Robinson, G.E. (2012) Transcriptional response to foraging experience in the honey bee mushroom bodies. Dev Neurobiol 72, 153-166.
50. Makeyev, E.V., Zhang, J., Carrasco, M.A. & Maniatis, T. (2007) The microRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol Cell 27, 435-448.
51. Marsit, C.J., Eddy, K. & Kelsey, K.T. (2006) MicroRNA responses to cellular stress. Cancer Res 66, 10843-10848.
52. Musiyenko, A., Bitko, V. & Barik, S. (2008) Ectopic expression of miR-126*, an intronic product of the vascular endothelial EGF-like 7 gene, regulates prostein translation and invasiveness of prostate cancer LNCaP cells. J Mol Med (Berl) 86, 313-322.
53. Nolo, R., Morrison, C.M., Tao, C., Zhang, X. & Halder, G. (2006) The bantam microRNA is a target of the hippo tumor-suppressor pathway. Curr Biol 16, 1895-1904.
54. Nowak, M.A., Tarnita, C.E. & Wilson, E.O. (2010) The evolution of eusociality. Nature 466, 1057-1062.
55. Olde Loohuis, N.F., Kos, A., Martens, G.J., Van Bokhoven, H., Nadif Kasri, N. & Aschrafi, A. (2012) MicroRNA networks direct neuronal development and plasticity. Cell Mol Life Sci 69, 89-102.
56. Olena, A.F. & Patton, J.G. (2010) Genomic organization of microRNAs. J Cell Physiol 222, 540-545.
57. Pasquinelli, A.E., Reinhart, B.J., Slack, F., Martindale, M.Q., Kuroda, M.I., Maller, B., Hayward, D.C., Ball, E.E., Degnan, B., Muller, P., Spring, J., Srinivasan, A., Fishman, M., Finnerty, J., Corbo, J., Levine, M., Leahy, P., Davidson, E. & Ruvkun, G. (2000) Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408, 86-89.
58. Perkins, D.O., Jeffries, C.D., Jarskog, L.F., Thomson, J.M., Woods, K., Newman, M.A., Parker, J.S., Jin, J. & Hammond, S.M. (2007) microRNA expression in the prefrontal cortex of individuals with schizophrenia and schizoaffective disorder. Genome Biol 8, R27.
59. Peter, M.E. (2009) Let-7 and miR-200 microRNAs: guardians against pluripotency and cancer progression. Cell Cycle 8, 843-852.
60. Qurashi, A., Chang, S. & Peng, J. (2007) Role of microRNA pathway in mental retardation. Sci World J 7, 146-154.
61. Rehmsmeier, M., Steffen, P., Hochsmann, M. & Giegerich, R. (2004) Fast and effective prediction of microRNA/target duplexes. RNA 10, 1507-1517.
62. Reinhart, B.J., Slack, F.J., Basson, M., Pasquinelli, A.E., Bettinger, J.C., Rougvie, A.E., Horvitz, H.R. & Ruvkun, G. (2000) The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403, 901-906.
63. Ruby, J.G., Jan, C.H. & Bartel, D.P. (2007) Intronic microRNA precursors that bypass Drosha processing. Nature 448, 83-86.
64. Schaefer, A., Im, H.I., Veno, M.T., Fowler, C.D., Min, A., Intrator, A., Kjems, J., Kenny, P.J., O'Carroll, D. & Greengard, P. (2010) Argonaute 2 in dopamine 2 receptor-expressing neurons regulates cocaine addiction. J Exp Med 207, 1843-1851.
65. Schratt, G. (2009) microRNAs at the synapse. Nat Rev Neurosci 10, 842-849.
66. Selbach, M., Schwanhausser, B., Thierfelder, N., Fang, Z., Khanin, R. & Rajewsky, N. (2008) Widespread changes in protein synthesis induced by microRNAs. Nature 455, 58-63.
67. Shpigler, H., Patch, H.M., Cohen, M., Fan, Y., Grozinger, C.M. & Bloch, G. (2010) The transcription factor Kruppel homolog 1 is linked to hormone mediated social organization in bees. BMC Evol Biol 10, 120.
68. Stefani, G. & Slack, F.J. (2008) Small non-coding RNAs in animal development. Nat Rev Mol Cell Biol 9, 219-230.
69. Tazawa, H., Tsuchiya, N., Izumiya, M. & Nakagama, H. (2007) Tumor-suppressive miR-34a induces senescence-like growth arrest through modulation of the E2F pathway in human colon cancer cells. Proc Natl Acad Sci USA 104, 15472-15477.
70. Tsuchimoto, M., Aoki, M., Takada, M., Kanou, Y., Sasagawa, H., Kitagawa, Y. & Kadowaki, T. (2004) The changes of gene expression in honeybee (Apis mellifera) brains associated with ages. Zoolog Sci 21, 23-28.
71. Valoczi, A., Hornyik, C., Varga, N., Burgyan, J., Kauppinen, S. & Havelda, Z. (2004) Sensitive and specific detection of microRNAs by northern blot analysis using LNA-modified oligonucleotide probes. Nucleic Acids Res 32, e175.
72. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A. & Speleman, F. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3, RESEARCH0034.
73. Warren, W.C., Clayton, D.F., Ellegren, H., et al. (2010) The genome of a songbird. Nature 464, 757-762.
74. Weaver, D.B., Anzola, J.M., Evans, J.D., Reid, J.G., Reese, J.T., Childs, K.L., Zdobnov, E.M., Samanta, M.P., Miller, J. & Elsik, C.G. (2007) Computational and transcriptional evidence for microRNAs in the honey bee genome. Genome Biol 8, R97.
75. Whitfield, C.W., Cziko, A.M. & Robinson, G.E. (2003) Gene expression profiles in the brain predict behavior in individual honey bees. Science 302, 296-299.
76. Whitfield, C.W., Ben-Shahar, Y., Brillet, C., Leoncini, I., Crauser, D., Leconte, Y., Rodriguez-Zas, S. & Robinson, G.E. (2006) Genomic dissection of behavioral maturation in the honey bee. Proc Natl Acad Sci USA 103, 16068-16075.
77. Wilson, E.O. & Holldobler, B. (2005) Eusociality: origin and consequences. Proc Natl Acad Sci USA 102, 13367-13371.
78. Wing, M.R., Bourdon, D.M. & Harden, T.K. (2003) PLC-epsilon: a shared effector protein in Ras-, Rho-, and G alpha beta gamma-mediated signaling. Mol Interv 3, 273-280.
79. Wolschin, F. & Amdam, G.V. (2007) Plasticity and robustness of protein patterns during reversible development in the honey bee (Apis mellifera). Anal Bioanal Chem 389, 1095-1100.
80. Wulczyn, F.G., Smirnova, L., Rybak, A., Brandt, C., Kwidzinski, E., Ninnemann, O., Strehle, M., Seiler, A., Schumacher, S. & Nitsch, R. (2007) Post-transcriptional regulation of the let-7 microRNA during neural cell specification. FASEB J 21, 415-426.
81. Yang, M., Lee, J.E., Padgett, R.W. & Edery, I. (2008) Circadian regulation of a limited set of conserved microRNAs in Drosophila. BMC Genomics 9, 83.
82. Zeng, Y. & Cullen, B.R. (2004) Structural requirements for pre-microRNA binding and nuclear export by Exportin 5. Nucleic Acids Res 32, 4776-4785.
83. Zhang, W., Gao, S., Zhou, X., Chellappan, P., Chen, Z., Zhang, X., Fromuth, N., Coutino, G., Coffey, M. & Jin, H. (2011) Bacteria-responsive microRNAs regulate plant innate immunity by modulating plant hormone networks. Plant Mol Biol 75, 93-105.