Apidologie

, Volume 49, Issue 1, pp 71–83 | Cite as

Circadian clock genes are differentially modulated during the daily cycles and chronological age in the social honeybee (Apis mellifera)

  • Fabiano C. P. Abreu
  • Flávia C. P. Freitas
  • Zilá L. P. Simões
Original article
  • 114 Downloads

Abstract

The circadian clock is an advantageous adaptive system that enables organisms to predict and anticipate the daily environmental changes. The circadian rhythms are generated molecularly through the expression of clock genes, based on autoregulatory feedback loops. Honeybees are an excellent model to investigate how the circadian rhythms are modulated accordingly to the social context, behavioral plasticity, and task-related activities. Here, we show how the clock genes behave during the daily cycles in adult worker heads of Apis mellifera. Our results point to the clock genes period and cryptochrome as essential regulators of the circadian rhythms associated to the behavioral maturation in this social insect. We also identified putative miRNA-target and protein-protein interactions involving honeybee clock genes, indicating regulatory networks behind the adjustment of the molecular clock.

Keywords

circadian clock clock genes circadian rhythms honeybees miRNAs 

Notes

Funding

FAPESP, Process Nº 2014/14194-4.

Authors’ contribution

All authors have contributed equally to the work: Fabiano C.P. Abreu and Zilá L.P. Simões elaborated the idea of this work, experimental procedures were performed by Fabiano C. P. Abreu, and Flavia C.P. Freitas performed the computational analyses.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

13592_2017_558_MOESM1_ESM.docx (14 kb)
ESM 1. (DOCX 14 kb)
13592_2017_558_Fig5_ESM.gif (91 kb)
ESM 2.

(GIF 90 kb)

13592_2017_558_MOESM2_ESM.tif (236 kb)
High Resolution (TIFF 235 kb)

References

  1. Asgari, S. (2013) MicroRNA functions in insects. Insect. Biochem. Mol. Biol. 43 (4): 388–97CrossRefPubMedGoogle Scholar
  2. Ashby, R., Forêt, S., Searle, I., Maleszka, R. (2016) MicroRNAs in honey bee caste determination. Sci. Rep.. 7; 6: 18794CrossRefGoogle Scholar
  3. 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.PubMedGoogle Scholar
  4. Bell-Pedersen, D., Cassone, V. M., Earnest, D. J., Golden, S. S., Hardin, P. E., Thomas T. L., Zoran, M. J. (2005) Circadian rhythms from multiple oscillators: lessons from diverse organisms. Nat. Rev. Genet. 6, 544–56.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Benna, C., Bonaccorsi, S., Wülbeck, C., Helfrich-Förster, C., Gatti, M., Kyriacou, C. P. & Sandrelli, F. (2010) Drosophila timeless2 is required for chromosome stability and circadian photoreception. Curr. Biol. 20 (4), 346–352CrossRefPubMedGoogle Scholar
  6. Bloch, G. (2010) The social clock of the honeybee. J. Biol. Rhythms. 25, 307–17.CrossRefPubMedGoogle Scholar
  7. Bloch, G., Toma, D. P., Robinson, G. E. (2001) Behavioral Rhythmicity, Age, Division of Labor and period Expression in the Honey Bee Brain. J. Biol. Rhythms. 16 (5), 444–456.CrossRefPubMedGoogle Scholar
  8. Bloch, G., Solomon, S. M., Robinson, G. E., Fahrbach, S. E. (2003) Patterns of PERIOD and pigment-dispersing hormone immunoreactivity in the brain of the European honeybee (Apis mellifera): age- and time-related plasticity. J. Comp. Neurol. 464 (3): 269–284.CrossRefPubMedGoogle Scholar
  9. Chatr-aryamontri, A., Oughtred, R., Boucher, L., Rust, J., Chang, C., et al. (2017) The BioGRID interaction database: 2017 update. Nucleic Acids Res. 45(D1):D369-D379.CrossRefPubMedGoogle Scholar
  10. Chaudhari, A., Gupta, R., Makwana, K., Kondratov, R. (2017) Circadian clocks, diet and aging. Nutr. Healthy Aging. 4, 101–112.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chawla, G., Deosthale, P., Childress, S., Wu, Y.C., Sokol, N.S. (2016) A let-7-to-miR-125 MicroRNA Switch Regulates Neuronal Integrity and Lifespan in Drosophila. PLoS. Genet. 12 (8): e1006247CrossRefPubMedPubMedCentralGoogle Scholar
  12. Chen, X., Rosbash, M. (2016) MicroRNA-92a is a circadian modulator of neuronal excitability in Drosophila. Nature Commun. 8: 14707.CrossRefGoogle Scholar
  13. 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.CrossRefPubMedGoogle Scholar
  14. Chen, W., Liu, Z., Li, T., Zhang, R., Xue, Y., Zhong, Y., Bai, W., Zhou, D., Zhao, Z. (2014) Regulation of Drosophila circadian rhythms by miRNA let-7 is mediated by a regulatory cycle. Nat. Commun. 5: 5549.CrossRefPubMedGoogle Scholar
  15. Cheng, H. Y., Papp, J. W., Varlamova, O., Dziema, H., Russell, B., Curfman, J. P., Nakazawa, T., Shimizu, K., Okamura, H., Impey, S., et al. (2007). microRNA modulation of circadian-clock period and entrainment. Neuron. 54, 813–829.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Chiu, J. C., Vanselow, J. T., Kramer, A., & Edery, I. (2008). The phospho-occupancy of an atypical SLIMB-binding site on PERIOD that is phosphorylated by DOUBLETIME controls the pace of the clock. Genes Dev. 22 (13), 1758–1772.CrossRefPubMedPubMedCentralGoogle Scholar
  17. Crane, B. R., Young, M. W. (2014). Interactive features of proteins composing eukaryotic circadian clocks. Annu. Rev. Biochem. 83, 191–219.CrossRefPubMedGoogle Scholar
  18. Cristino, A. S., Barchuk, A. R., Freitas, F. C., Narayanan, R. K., Biergans, S. D., Zhao, Z., Simoes, Z. L., Reinhard, J., Claudianos, C. (2014) Neuroligin-associated microRNA-932 targets actin and regulates memory in the honeybee. Nat. Commun. 20; 5: 5529.CrossRefGoogle Scholar
  19. Cyran, S. A., Buchsbaum, A. M., Reddy, K. L., Lin, M. V., Glossop, N. R., Hardin, P. E., Young, M. W., Storti, R. V., Blau, J. (2003) vrille, Pdp1, and dClock form a second feedback loop in the Drosophila circadian clock. Cell 112: 329–341.CrossRefPubMedGoogle Scholar
  20. Cyran, S. A., Yiannoulos, G., Buchsbaum, A. M., Saez, L., Young, M. W., & Blau, J. (2005). The double-time protein kinase regulates the subcellular localization of the Drosophila clock protein period. J. Neurosci. 25 (22), 5430–5437.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Dunlap, J., Loros, J., DeCoursey, P. (2004) Chronobiology: biological timekeeping. Sunderland: Sinauer AssociatesGoogle Scholar
  22. Eban-Rothschild, A., Shemesh, Y., Bloch, G. (2012) The colony environment, but not direct contact with conspecifics, influences the development of circadian rhythms in honey bees. J. Biol. Rhythms. 27 (3): 217:225.CrossRefPubMedGoogle Scholar
  23. Elsik, C. G., Worley, K. C., Bennett, A. K., Beye, M., Camara, F., Childers, C. P., & Elhaik, E. (2014). Finding the missing honey bee genes: lessons learned from a genome upgrade. BMC genomics, 15(1), 86Google Scholar
  24. Freitas, F. C. P., Pires, C. V., Claudianos, C., Cristino, A. S., Simões, Z. L. P. (2017) MicroRNA-34 directly targets pair-rule genes and cytoskeleton component in the honey bee. Sci. Rep. 7: 40884.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Frisch, B., Koeniger, N. (1994) Social synchronization of the activity rhythms of honeybees within a colony. Behav. Ecol. Sociobiol. 35, 91–98CrossRefGoogle Scholar
  26. Fuchikawa, T., Eban-Rothschild, A., Nagari, M., Shemesh, Y., Bloch, G. (2016) Potent social synchronization can override photic entrainment of circadian rhythms. Nat. Commun. 7: 11662.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Fuchikawa, T., Beer, K., Linke-Winnebeck, C., Ben-David, R., Kotowoy, A., Tsang, V. W. K., Warman, G. R., Winnebeck, E. C., Helfrich-Foster, C., Bloch, G. (2017) Neuronal circadian clock protein oscillations are similar in behaviourally rhythmic forager honeybees and in arrhythmic nurses. Open Biol. 7: 170047Google Scholar
  28. George, H., Terracol, R. (1997) The vrille gene of Drosophila is a maternal enhancer of decapentaplegic and encodes a new member of the bZIP family of transcription factors. Genetics 146, 1345–1363.PubMedPubMedCentralGoogle Scholar
  29. Gotter A. L., Manganaro T., Weaver D. R., Kolakowski L. F., Possidente B., Sriram S., MacLaughlin D. T., Reppert S. M. (2000) A time-less function for mouse Timeless. Nat. Neurosci. 3: 755–756.CrossRefPubMedGoogle Scholar
  30. Gu, H., Xiao, J., Niu, L., Wang, B., Ma, G., Dunn, D. W., Huang, D. (2014) Adaptive evolution of the circadian gene timeout in insects. Sci. Rep. 4: 4212Google Scholar
  31. Ingram, K. K., Kutowoi, A., Wurm, Y., Shoemaker, D., Meier, R., Bloch, G. (2012) The Molecular Clockwork of the Fire Ant Solenopsis invicta. PLoS One 7(11): e45715.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Jung, J. H., Seo, Y. H., Seo, P. J., Reyes, J. L., Yun, J., Chua, N. H. and Park, C. M. (2007). The GIGANTEA-regulated microRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis. Plant. Cell. 19, 2736–2748.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Kadener, S., Stoleru, D., McDonald, M., Nawathean, P., Rosbash, M. (2007). Clockwork Orange is a transcriptional repressor and a new Drosophila circadian pacemaker component. Genes. Dev. 21: 1675–1686.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Kadener, S., Menet, J. S., Sugino, K., Horwich, M. D., Weissbein, U., Nawathean, P., Vagin, V. V., Zamore, P. D., Nelson, S. B. and Rosbash, M. (2009). A role for microRNAs in the Drosophila circadian clock. Genes Dev. 23, 2179–2191.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Kloss, B., Price, J. L., Saez, L., Blau, J., Rothenfluh, A., Wesley, C. S., Young, M. W. (1998). The Drosophila clock gene double-time encodes a protein closely related to human casein kinase Iε. Cell. 94 (1), 97–107.CrossRefPubMedGoogle Scholar
  36. Knapek, K., Sigrist, S., Tanimoto, H. (2011) Bruchpilot, a synaptic active zone protein for anesthesia-resistant memory. J. Neurosci. 31(9): 3453–3458CrossRefPubMedGoogle Scholar
  37. Ko, H. W., Jiang, J., & Edery, I. (2002). Role for Slimb in the degradation of Drosophila Period protein phosphorylated by Doubletime. Nature, 420 (6916), 673–678CrossRefPubMedGoogle Scholar
  38. Kojima, S., Shingle, D. L., & Green, C. B. (2011). Post-transcriptional control of circadian rhythms. J Cell Sci, 124(3), 311–320.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Kruger, J., Rehmsmeier, M. (2006) RNAhybrid: microRNA target prediction easy, fast and flexible. Nucleic Acids Res. 34: W451-W454.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Lim, C., Chung, B. Y., Pitman, J. L., McGill, J. J., Pradhan, S., Lee, J., Keegan, K. P., Choe, J., Allada, R. (2007) Clockwork orange encodes a transcriptional repressor important for circadian-clock amplitude in Drosophila. Curr Biol 17:1082–1089CrossRefPubMedPubMedCentralGoogle Scholar
  41. Liu, F., Peng, W., Li, Z., Li, W., Li, L., Pan, J., Zhang, S., Miao, Y., Chen, S., Su, S. (2012a) Next-generation small RNA sequencing for microRNAs profiling in Apis mellifera: comparison between nurses and foragers. Insect Mol. Biol. 21: 297–303.CrossRefPubMedGoogle Scholar
  42. Liu, N., Landreh, M., Cao, K., Abe, M., Hendriks, G. J., Kennerdell, J. R., Zhu, Y., Wang, L. S., Bonini, N. M. (2012b) The microRNA miR-34 modulates ageing and neurodegeneration in Drosophila. Nature. 482 (7386): 519–523.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Livak, K. J., Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods. 25,402–408.CrossRefPubMedGoogle Scholar
  44. Lourenço, A. P., Mackert, A., Cristino, A. S., Simoes, Z. L. P. (2008) Validation of reference genes for gene expression studies in the honey bee, Apis mellifera, by quantitative real-time RT-PCR. Apidologie. 39, 372–385CrossRefGoogle Scholar
  45. Luhur, A., Chawla, G., Sokol, N. S. (2013) MicroRNAs as components of systemic signaling pathways in Drosophila melanogaster. Curr. Top. Dev. Biol. 105: 97–123.CrossRefPubMedGoogle Scholar
  46. Macedo, L. M., Nunes, F. M., Freitas, F. C., Pires, C. V., Tanaka, E. D., Martins, J. R., Piulachs, M. D., Cristino, A. S., Pinheiro, D. G., Simões, Z. L. (2016) MicroRNA signatures characterizing caste-independent ovarian activity in queen and worker honeybees (Apis mellifera L.). Insect Mol Biol. 25: 216–226.CrossRefPubMedGoogle Scholar
  47. Matsumoto, A., Ukai-Tadenuma, M., Yamada, R. G., Houl, J., Umo, K.D., et al. (2007) A functional genomics strategy reveals clockwork orange as a transcriptional regulator in the Drosophila circadian clock. Genes Dev. 21:1687–1700CrossRefPubMedPubMedCentralGoogle Scholar
  48. Meshi, A., Bloch, G. (2007) Monitoring circadian rhythms of individual honey bees in a social environment reveals social influences on postembryonic ontogeny of activity rhythms. J. Biol. Rhythms. 22 (4): 343–355.CrossRefPubMedGoogle Scholar
  49. Nagari, M., Bloch, G. (2012) The involvement of the antennae in mediating the brood influence on circadian rhythms in “nurse” honey bee (Apis mellifera) workers. J. Insect. Physiol. 58 (8): 1096–1103.CrossRefPubMedGoogle Scholar
  50. Nandi, A., Vaz, C., Bhattacharya, A., Ramaswamy, R. (2009). miRNA-regulated dynamics in circadian oscillator models. BMC Syst Biol. 3, 45–47.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Panda, S., Hogenesch, J. B., Kay, S. A. (2002) Circadian rhythms from flies to human. Nature 417 (6886): 329–335.CrossRefPubMedGoogle Scholar
  52. Pires, C. V., Freitas, F. C., Cristino, A. S., Dearden, P. K., Simões, Z. L. (2016) Transcriptome Analysis of Honeybee (Apis Mellifera) Haploid and Diploid Embryos Reveals Early Zygotic Transcription during Cleavage. PLoS One 11(1): e0146447.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Price, J. L., Blau, J., Rothenfluh, A., Abodeely, M., Kloss, B., & Young, M. W. (1998). double-time is a novel Drosophila clock gene that regulates PERIOD protein accumulation. Cell. 94 (1), 83–95.CrossRefPubMedGoogle Scholar
  54. Qin, Q. H., Wang, Z. L., Tian, L. Q., Gan, H. Y., Zhang, S. W., Zeng, Z. J. (2014). The integrative analysis of microRNA and mRNA expression in Apis mellifera following maze-based visual pattern learning. Insect Sci. 21: 619–36.CrossRefPubMedGoogle Scholar
  55. Reddy, K. L., Wohlwill, A., Katzen, A., Dzitoeva, S., Lin, M., Holbrook, S., Storti, R.V. (2000) The Drosophila PAR Domain Protein 1 (Pdp1) gene encodes multiple differentially expressed mRNAs and proteins through the use of multiple enhancers and promoters. Dev. Biol. 224, 401–414.Google Scholar
  56. Reddy, K. L., Rovani, M. K., Wohlwill, A., Katzen, A., Storti, R. V. (2006) The Drosophila Par domain protein I gene, Pdp1, is a regulator of larval growth, mitosis and endoreplication. Dev. Biol. 289: 100–114CrossRefPubMedGoogle Scholar
  57. Reischl, S., Kramer, A. (2011). Kinases and phosphatases in the mammalian circadian clock. FEBS Lett. 585 (10), 1393–1399.CrossRefPubMedGoogle Scholar
  58. Reppert, S. M., Weaver, D. R. (2000) Comparing clockworks: mouse versus fly. J. Biol. Rhythms. 15, 357–64.CrossRefPubMedGoogle Scholar
  59. Rodriguez-Zas, S. L., Southey, B. R., Shemesh, Y., Rubin, E. B., Cohen, M., Robinson, G. E., Bloch, G. (2012) Microarray Analysis of Natural Socially-Regulated Plasticity in Circadian Rhythms of Honey Bees. J. Biol. Rhythms 27(1): 12–24CrossRefPubMedPubMedCentralGoogle Scholar
  60. Rubin, E. B., Shemesh, Y., Cohen, M., Elgavish, S., Robertson, H. M., Bloch, G. (2006) 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. Gen. Res. 16:1352–1365CrossRefGoogle Scholar
  61. Sadd, B. M., Barribeau, S. M., Bloch, G., de Graaf, G. C., Dearden, P. (2015) The genomes of two key bumblebee species with primitive eusocial organization. Genome Biol. 16(1): 76.CrossRefPubMedPubMedCentralGoogle Scholar
  62. Sandrelli, F., Costa, R., Kyriacou, C. P., & Rosato, E. (2008). Comparative analysis of circadian clock genes in insects. Insect. Mol. Biol. 17 (5), 447–46CrossRefPubMedGoogle Scholar
  63. Sangoram, A. M., Saez, L., Antoch, M. P., Gekakis, N., Staknis, D., et al. (1998) Mammalian circadian autoregulatory loop: a timeless ortholog and mPer1 interact and negatively regulate CLOCK-BMAL1-induced transcription. Neuron. 21, 1101–1113CrossRefPubMedGoogle Scholar
  64. Saunders, D. S. (2002). Insect clocks. Amsterdam: Elsevier.Google Scholar
  65. Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., Ideker, T. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13(11): 2498–2504.CrossRefPubMedPubMedCentralGoogle Scholar
  66. Shemesh, Y., Cohen, M., Bloch, G. (2007) Natural plasticity in circadian rhythms is mediated by reorganization in the molecular clockwork in honeybees. FASEB J. 21, 2304–2311.CrossRefPubMedGoogle Scholar
  67. Shemesh, Y., Eban-Rothschild, A., Cohen, M., Bloch, G. (2010) Molecular dynamics and social regulation of context-dependent plasticity in the circadian clockwork of the honey bee. J. Neurosci. 30, 12517–25.CrossRefPubMedGoogle Scholar
  68. Sire, C., Moreno, A. B., Garcia-Chapa, M., Lopez-Moya, J. J., San Segundo, B. (2009). Diurnal oscillation in the accumulation of Arabidopsis microRNAs, miR167, miR168, miR171 and miR398. FEBS Lett. 583, 1039–1044.CrossRefPubMedGoogle Scholar
  69. Szuplewski, S., Kottler, B., & Terracol, R. (2003). The Drosophila bZIP transcription factor Vrille is involved in hair and cell growth. Development. 130 (16), 3651–3662.CrossRefPubMedGoogle Scholar
  70. Szuplewski, S., Fraisse-Véron, I., George, H., Terracol, R. (2010) vrille is required to ensure tracheal integrity in Drosophila embryo. Dev. Growth Differ. 52 (5): 409–418.CrossRefPubMedGoogle Scholar
  71. Takumi, T., Nagamine, Y., Miyake, S., Matsubara, C., Taguchi, K., et al. (1999) A mammalian ortholog of Drosophila timeless, highly expressed in SCN and retina, forms a complex with mPER1. Genes Cells. 4, 67–75.CrossRefPubMedGoogle Scholar
  72. Toma, D. P., Bloch, G., Moore, D., Robinson, G. E. (2000) Changes in period mRNA levels in the brain and division of labor in honey bee colonies. Proc. Nat. Acad. Sci. U S A. 97:6914–6919.CrossRefGoogle Scholar
  73. Tomioka, K., Matsumoto, A. (2010) A comparative view of insect circadian clock systems. Cell. Mol. Life Sci. 67:1397–1406.CrossRefPubMedGoogle Scholar
  74. Vansteensel, M. J., Michel, S., Meijer, J. H. (2008) Organization of cell and tissue circadian pacemakers: A comparison among species. Brain Res. Rev. 58 (1): 18–47CrossRefPubMedGoogle Scholar
  75. Wagh, D. A., Rasse, T. M., Asan, E., Hofbauer, A., Schwenkert, I., et al. (2006) Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron. 49(6): 833–844.CrossRefPubMedGoogle Scholar
  76. 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 (6): R97.CrossRefPubMedPubMedCentralGoogle Scholar
  77. Weber, F., Zorn, D., Rademacher, C., & Hung, H. C. (2011). Post-translational timing mechanisms of the Drosophila circadian clock. FEBS Lett. 585 (10), 1443–1449CrossRefPubMedGoogle Scholar
  78. Weinstock, G. M., Robinson, G. E., Gibbs, R. A., Worley, K. C., Evans, J. D. et al. (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature, 443 (7114), 931–949.CrossRefGoogle Scholar
  79. Woźnicka, O., Görlich, A., Sigrist, S., Pyza, E. (2015) BRP-170 and BRP190 isoforms of Bruchpilot protein differentially contribute to the frequency of synapses and synaptic circadian plasticity in the visual system of Drosophila. Front. Cell. Neurosc. 9: 238Google Scholar
  80. Xing, W., Busino, L., Hinds, T. R., Marionni, S. T., Saifee, N. H., Bush, M. F., … & Zheng, N. (2013). SCFFBXL3 ubiquitin ligase targets cryptochromes at their cofactor pocket. Nature, 496 (7443), 64–68Google Scholar
  81. Xu, S., Witmer, P. D., Lumayag, S., Kovacs, B., Valle, D. (2007). MicroRNA (miRNA) transcriptome of mouse retina and identification of a sensory organ-specific miRNA cluster. J. Biol. Chem. 282, 25053–25066.CrossRefPubMedGoogle Scholar
  82. Yang, M., Lee, Jung-Eun., Padgett, R. W., Edery, I. (2008) Circadian regulation of a limited set of conserved microRNAs in Drosophila. BMC Genomics, 9:83.CrossRefPubMedPubMedCentralGoogle Scholar
  83. Yoo, S. H., Mohawk, J. A., Siepka, S. M., Shan, Y., Huh, S. K., Hong, H. K., … & Nussbaum, J. (2013). Competing E3 ubiquitin ligases govern circadian periodicity by degradation of CRY in nucleus and cytoplasm. Cell, 152 (5), 1091–1105.Google Scholar
  84. Young, M. W., Kay, S. A. (2001) Time zones: A comparative genetics of circadian clocks. Nat. Rev. Genet. 2 (9): 702–715CrossRefPubMedGoogle Scholar

Copyright information

© INRA, DIB and Springer-Verlag France SAS, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Departamento de Genética, Faculdade de Medicina de Ribeirão PretoUniversidade de São PauloRibeirão PretoBrazil
  2. 2.Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão PretoUniversidade de São PauloRibeirão PretoBrazil

Personalised recommendations