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hormone nuclear receptor (EcR) exhibits circadian cycling in certain tissues, but not others, during development in Rhodnius prolixus (Hemiptera)

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Abstract

The insect moulting hormones, viz. the ecdysteroids, regulate gene expression during development by binding to an intracellular protein, the ecdysteroid receptor (EcR). In the insect Rhodnius prolixus, circulating levels of ecdysteroids exhibit a robust circadian rhythm. This paper demonstrates associated circadian rhythms in the abundance and distribution of EcR in several major target tissues of ecdysteroids, but not in others. Quantitative analysis of immunofluorescence images obtained by confocal laser-scanning microscopy following the use of anti-EcR has revealed a marked daily rhythm in the nuclear abundance of EcR in cells of the abdominal epidermis, brain, fat body, oenocytes and rectal epithelium of Rhodnius. This EcR rhythm is synchronous with the rhythm of circulating hormone levels. It free-runs in continuous darkness for several cycles, showing that EcR nuclear abundance is under circadian control. Circadian control of a nuclear receptor has not been shown previously in any animal. We infer that the above cell types detect and respond to the temporal signals in the rhythmic ecdysteroid titre. In several cell types, the rhythm in cytoplasmic EcR peaks several hours prior to the EcR peak in the nucleus each day, thereby implying a daily migration of EcR from the cytoplasm to the nucleus. This finding shows that EcR is not a constitutive nuclear receptor, as has previously been assumed. In the brain, rhythmic nuclear EcR has been found in peptidergic neurosecretory cells, indicating a potential pathway for feedback regulation of the neuroendocrine system by ecdysteroids, and also in regions containing circadian clock neurons, suggesting that the circadian timing system in the brain is also sensitive to rhythmic ecdysteroid signals.

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References

  • Ampleford EJ, Steel CGH (1985) Circadian control of a daily rhythm in haemolymph ecdysteroid titre in the insect Rhodnius prolixus (Hemiptera). Gen Comp Endocrinol 59:453–459

    Article  PubMed  CAS  Google Scholar 

  • Arbeitman MN, Hogness DS (2000) Molecular chaperones activate the Drosophila ecdysone receptor, an RXR heterodimer. Cell 101:67–77

    Article  PubMed  CAS  Google Scholar 

  • Bao AM, Liu RY, van Someren EJW, Hofman MA, Cao YX, Zhou JN (2003) Diurnal rhythm of free estradiol during the menstrual cycle. Eur J Endocrinol 148:227–232

    Article  PubMed  CAS  Google Scholar 

  • Baumann CT, Maruvada P, Hager GL, Yen PM (2001) Nuclear cytoplasmic shuttling by thyroid hormone receptors: multiple protein interactions are required for nuclear retention. J Biol Chem 276:11237–11245

    Article  PubMed  CAS  Google Scholar 

  • Beaulaton J, Porcheron P, Gras R, Cassier P (1984) Cytophysiological correlations between prothoracic gland activity and hemolymph ecdysteroid concentration in Rhodnius prolixus during the fifth larval instar: further studies in normal and decapitated larvae. Gen Comp Endocrinol 53:1–16

    Article  PubMed  CAS  Google Scholar 

  • Chapman RF (1998) The insects: structure and function. Harvard University Press, Cambridge, Mass.

    Google Scholar 

  • Cherbas IL, Cherbas L (1996) Molecular aspects of ecdysteroid hormone action. In: Gilbert LI, Tata JR, Atkinson BG (eds) Metamorphosis: post-embryonic reprogramming of gene expression in amphibian and insect cells. Academic Press, San Diego, pp 175–221

    Google Scholar 

  • Cymborowski B, Muszynska-Pytel M, Porcheron P, Cassier P (1991) Hemolymph ecdysteroid titers controlled by a circadian clock mechanism in larvae of the wax moth, Galleria mellonella. J Insect Physiol 37:35–40

    Article  CAS  Google Scholar 

  • Dai J-D, Costello MJ, Gilbert LI (1994) The prothoracic glands of Manduca sexta: a microscopic analysis of gap junctions and intercellular bridges. Invertebr Reprod Dev 25:93–110

    Google Scholar 

  • Doulabi BZ, Schiphorst MP, van Beeren HC, Laruyere WT, Lamers WH, Fliers E, Bakker O, Wiersinga WM (2002) TR beta1 protein is preferentially expressed in the pericentral zone of rat liver and exhibits marked diurnal variation. Endocrinology 143:979–984

    Article  PubMed  CAS  Google Scholar 

  • Eagon PK, Dileo A, Polimeno L, Francavilla A, van Thiel DH, Guglielmi F, Starzl TE (1986) Circadian rhythm of hepatic cytosolic and nuclear estrogen receptors. Chronobiol Int 3:207–212

    Article  PubMed  CAS  Google Scholar 

  • Francavilla A, Eagon PK, Dileo A, van Thiel DH, Panella C, Polimeno L, Amoruso C, Ingrosso M, Aquilino AM, Starzl TE (1986) Circadian rhythm of hepatic cytosolic and nuclear estrogen and androgen receptors. Gastroenterology 91:182–188

    PubMed  CAS  Google Scholar 

  • Gupta D, Haldar C, Coeleveld M, Roth J (1993) Ontogeny, circadian rhythm pattern and hormonal modulation of 5-alpha-dihydrosterone receptors in the rat pineal. Neuroendocrinology 57:45–53

    PubMed  CAS  Google Scholar 

  • Hall JC (2003) Genetics and molecular biology of rhythms in Drosophila and other insects. Adv Genet 48:1–286

    Article  PubMed  CAS  Google Scholar 

  • Hau M, Romero ML, Brawn JD, Van't Hof TJ (2001) Effect of polar day on plasma profiles of melatonin, testosterone, and estradiol in high-arctic lapland longspurs. Gen Comp Endocrinol 126:101–112

    Article  CAS  Google Scholar 

  • Helfrich-Förster C (2003) The neuroarchitecture of the circadian clock in the brain of Drosophila melanogaster. Microsc Res Tech 62:94–102

    Article  PubMed  Google Scholar 

  • Helfrich-Förster C, Stengl M, Homberg U (1998) Organization of the circadian system in insects. Chronobiol Int 15:567–594

    PubMed  Google Scholar 

  • Henrich V, Lepesant J-A (2005) The ecdysteroid receptor (EcR). In: Gilbert LI, Iatrou K, Gill S (eds) Comprehensive molecular insect science, vol. 3. Elsevier Science, Oxford, pp 243–285

    Google Scholar 

  • Herman JP, Watson SJ, Chao HM, Coirini H, McEwen BS (1993) Diurnal regulation of glucocorticoid receptor and mineralocorticoid receptor mRNAs in rat hippocampus. Mol Cell Neurosci 4:181–190

    Article  CAS  Google Scholar 

  • Hirai M, Shinoda T, Kamimura M, Tomita S, Shiotsuki T (2002) Bombyx mori orphan receptor, BmHR78: cDNA cloning, testis abundant expression and putative dimerization partner from Bombyx ultraspiracle. Mol Cell Endocrinol 189:201–211

    Article  PubMed  CAS  Google Scholar 

  • Hiruma K, Bőcking D, Lafont R, Riddiford LM (1997) Action of different ecdysteroids on the regulation of mRNAs for the ecdysone receptor, MHR3, dopa decarboxylase, and a larval cuticle protein in the larval epidermis of the tobacco hornworm, Manduca sexta. Gen Comp Endocrinol 107:84–97

    Article  PubMed  CAS  Google Scholar 

  • Holmes MC, French KL, Secki JR (1995) Modulation of serotonin and corticorticoid receptor gene expression in the rat hippocampus with circadian rhythm and stress. Mol Brain Res 28:186–192

    Article  PubMed  CAS  Google Scholar 

  • Htun H, Holth LT, Walker D, Davie JR, Hager GL (1999) Direct visualization of the human estrogen receptor α reveals a role for ligand in the nuclear distribution of the receptor. Mol Biol Cell 10:471–486

    PubMed  CAS  Google Scholar 

  • Imhof MO, Rusconi S, Lezzi M (1993) Cloning of a Chironomus tentans cDNA encoding a protein (cEcRH) homologous to the Drosophila melanogaster ecdysteroid receptor (dEcR). Insect Biochem Mol Biol 23:115–124

    Article  PubMed  CAS  Google Scholar 

  • Jindra M, Malone F, Hiruma K, Riddiford LM (1996) Developmental profiles and ecdysteroid regulation of the mRNA for two ecdysone receptor isoforms in the epidermis and wings of the tobacco hornworm, Manduca sexta. Dev Biol 180:258–272

    Article  PubMed  CAS  Google Scholar 

  • Kaneko M, Hall JC (2000) Neuroanatomy of cells expressing clock genes in Drosophila: transgenic manipulation of the period and timeless genes to mark the perikarya of circadian pacemaker neurons and their projections. J Comp Neurol 422:66–94

    Article  PubMed  CAS  Google Scholar 

  • Karim FD, Thummel CS (1992) Temporal coordination of regulatory gene expression by the steroid hormone ecdysone. EMBO J 11:4083–4093

    PubMed  CAS  Google Scholar 

  • Kato S (2000) Molecular mechanism of transcriptional control of nuclear vitamin receptors. Br J Nutr 84(Suppl 2):S229–S233

    Article  PubMed  CAS  Google Scholar 

  • Kerdelhue B, Brown S, Lenoir V, Queenan JT, Jones GS, Scholler R, Jones HW (2002) Timing of initiation of the preovulatory luteinizing hormone surge and its relationship with the circadian cortisol rhythm in the human. Neuroendocrinology 75:158–163

    Article  PubMed  CAS  Google Scholar 

  • Kitchener P, Di Blasi F, Borelli E, Piazza PV (2004) Differences between brain structures in nuclear translocation and DNA binding of the glucocorticoid receptor during stress and the circadian cycle. Eur J Neurosci 19:1837–1846

    Article  PubMed  Google Scholar 

  • Kozlova T, Thummel CS (2002) Spatial patterns of ecdysteroid receptor activation during the onset of Drosophila metamorphosis. Development 129:1739–1750

    PubMed  CAS  Google Scholar 

  • Leiner KA, MacKenzie DS (2001) The effects of photoperiod on growth rate and circulating thyroid hormone levels in the red drum, Sciaenops ocellatus: evidence for a free-running circadian rhythm of T4 secretion. Comp Biochem Physiol [A] 130:141–149

    CAS  Google Scholar 

  • Mangeldorf DJ, Thummel C, Beato M, Herrlich P, Schuetz G, Umesono K, Blumnberg B, Kastner P, Mark M, Chambon P, Evans RM (1995) The nuclear receptor superfamily: the second decade. Cell 83:835–839

    Article  PubMed  Google Scholar 

  • Maruvada P, Baumann CT, Hager GL, Yen PM (2003) Dynamic shuttling and intranuclear hormone receptors. J Biol Chem 278:12425–12432

    Article  PubMed  CAS  Google Scholar 

  • Mizoguchi A, Ohashi Y, Hosoda K, Ishibashi J, Kataoka H (2001) Developmental profile of the changes in the prothoracicotropic hormone titer in hemolymph of the silkworm Bombyx mori: correlation with ecdysteroid secretion. Insect Biochem Mol Biol 31:349–358

    Article  PubMed  CAS  Google Scholar 

  • Mizoguchi A, Dedos SG, Fugo H, Kataoka H (2002) Basic pattern of fluctuation in hemolymph PTTH titers during larval-pupal and pupal-adult development of the silkworm, Bombyx mori. Gen Comp Endocrinol 127:181–189

    Article  PubMed  CAS  Google Scholar 

  • Moeller H, Goecke B, Herter F (1988) Seasonal and diurnal changes of prostatic androgen receptor and circulating testosterone in young mature rats. Res Exp Med 188:451–462

    Article  CAS  Google Scholar 

  • Pelc D, Steel CGH (1997) Rhythmic steroidogenesis by the prothoracic glands of the insect Rhodnius prolixus in the absence of rhythmic neuropeptide input: implications for the role of prothoracicotropic hormone. Gen Comp Endocrinol 108:358–365

    Article  PubMed  CAS  Google Scholar 

  • Peng Y, Stoleru D, Levine JD, Hall JC, Rosbash M (2003) Drosophila free-running rhythms require intercellular communication. PLoS Biol 1:1–9

    Article  Google Scholar 

  • Potla L, Horohov DW, Keadle TL, Littlefieldchabaud MA, Kamerling SG, Melrose PA (1993) Diurnal changes in specific binding of cortisol to cytosolic and nuclear fractions from equine peripheral-blood mononuclear-cells. J Equine Vet Sci 13:578–581

    Article  Google Scholar 

  • Riddiford LM (1985) Hormone action at the cellular level. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology, vol. 7. Pergamon, Oxford, pp 37–84

    Google Scholar 

  • Riddiford LM, Hiruma K, Lan Q, Zhou B (1999) Regulation and role of nuclear receptors during larval molting and metamorphosis of Lepidoptera. Am Zool 39:736–746

    CAS  Google Scholar 

  • Riddiford LM, Hiruma K, Zhou XF, Nelson CA (2003) Insights into the molecular basis of the hormonal control of molting and metamorphosis from Manduca sexta and Drosophila melanogaster. Insect Biochem Mol Biol 33:1327–1338

    Article  PubMed  CAS  Google Scholar 

  • Sakurai S (2005) Feedback regulation of prothoracic gland activity. In: Gilbert LI, Iatrou K, Gill S (eds) Comprehensive molecular insect science, vol. 3. Elsevier Science, Oxford, pp 409–431

    Google Scholar 

  • Sakurai S, Kaya M, Satake S (1998) Hemolymph ecdysteroid titer and ecdysteroid-dependent developmental events in the larval-pupal stadium of the silkworm, Bombyx mori: role of low ecdysteroid titer in larval-pupal metamorphosis and a reappraisal of the head critical period. J Insect Physiol 44:867–881

    Article  PubMed  CAS  Google Scholar 

  • Schmidt T, Meyer AS (1994) Autoregulation of corticosteroids receptors: how, when, where and why? Receptor 4:229–257

    PubMed  CAS  Google Scholar 

  • Schulz P, Chardon F, Degli Agosti R, Schaad N, Rivest RW (1995) Parallel nocturnal secretion of melatonin and testosterone in the plasma of normal men. J Pineal Res 19:16–22

    Article  PubMed  CAS  Google Scholar 

  • Spencer RL, Miller AH, Moday H, Stein M, McEwen BS (1993) Diurnal differences in basal and acute stress levels of type-I and type-II adrenal-steroid receptor activation in neural and immune tissues. Endocrinology 113:1941–1950

    Article  Google Scholar 

  • Stanewsky R (2002) Clock mechanisms in Drosophila. Cell Tissue Res 309:11–26

    Article  PubMed  CAS  Google Scholar 

  • Steel CGH (1973) Humoral regulation of the cerebral neurosecretory system of Rhodnius prolixus (Stal) during growth and moulting. J Exp Biol 58:177–187

    Google Scholar 

  • Steel CGH (1975) A neuroendocrine feedback mechanism in the insect moulting cycle. Nature 253:267–269

    Article  PubMed  CAS  Google Scholar 

  • Steel CG, Harmsen R (1971). Dynamics of the neurosecretory system in the brain of an insect, Rhodnius prolixus, during growth and molting. Gen. Comp. Endocr 17, 125-141

    Article  PubMed  CAS  Google Scholar 

  • Steel CGH, Vafopoulou X (2002) Physiology of circadian systems. In: Saunders DS (with Steel CGH, Vafopoulou X, Lewis RD) Insect clocks, 3rd edn. Elsevier Science, Amsterdam, pp 115–188

    Google Scholar 

  • Talbot WS, Swyryd EA, Hogness DS (1993) Drosophila tissues with different metamorphic responses to ecdysone express different ecdysone receptor isoforms. Cell 73:1323–1337

    Article  PubMed  CAS  Google Scholar 

  • Tata JR (2000) Autoinduction of nuclear hormone receptors during metamorphosis and its significance. Insect Biochem Mol Biol 30:645–651

    Article  PubMed  CAS  Google Scholar 

  • Terry KJ, Steel CGH (2002) Neuropeptide and steroid hormone rhythms are regulated by distinct cellular oscillators during the development of the insect Rhodnius prolixus. In: Goos HJT, Rastogi RK, Vaudry H, Pierantoni R (eds) Perspective in comparative endocrinology: unity and diversity. Monduzzi Editore, Italy, pp 309–314

    Google Scholar 

  • Truman JW, Talbot WS, Fahrbach SE, Hogness DS (1994) Ecdysone receptor expression in the CNS correlates with stage-specific responses to ecdysteroids during Drosophila and Manduca development. Development 120:219–234

    PubMed  CAS  Google Scholar 

  • Tsang PW, Orchard I (1991) Distribution of FMRF-amide-related peptides in the blood feeding bug Rhodnius prolixus. J Comp Neurol 311:17–32

    Article  PubMed  CAS  Google Scholar 

  • Vafopoulou X, Steel CGH (1991) Circadian regulation of synthesis of ecdysteroids by prothoracic glands of the insect Rhodnius prolixus: evidence of a dual oscillator system. Gen Comp Endocrinol 83:27–34

    Article  PubMed  CAS  Google Scholar 

  • Vafopoulou X, Steel CGH (1996) The insect neuropeptide prothoracicotropic hormone is released with a daily rhythm: re-evaluation of its role in development. Proc Natl Acad Sci U S A 93:3368–3372

    Article  PubMed  CAS  Google Scholar 

  • Vafopoulou X, Steel CGH (1998) A photosensitive circadian oscillator in an insect endocrine gland: photic induction of rhythmic steroidogenesis in vitro. J Comp Physiol [A] 182:343–349

    Article  Google Scholar 

  • Vafopoulou X, Steel CGH (2001) Induction of rhythmicity in prothoracicotropic hormone and ecdysteroids in Rhodnius prolixus: roles of photic and neuroendocrine Zeitgebers. J Insect Physiol 47:935–941

    Article  CAS  Google Scholar 

  • Vafopoulou X, Steel CGH (2005) Circadian organization of the endocrine system. In: Gilbert LI, Iatrou K, Gill S (eds) Comprehensive molecular insect science, vol. 3. Elsevier Science, Oxford, pp 551–614

    Google Scholar 

  • Vafopoulou X, Steel CGH, Terry K (2005) Ecdysteroid receptor (EcR) shows marked differences in temporal patterns between tissues during larval-adult development in Rhodnius prolixus: correlations with haemolymph ecdysteroid titres. J Insect Physiol 51:27–38

    Article  PubMed  CAS  Google Scholar 

  • Wang SF, LI C, Sun G, Zhu J, Raikhel S (2002) Differential expression and regulation by 20-hydroxyecdysone of mosquito ecdysteroid receptor isoforms A and B. Mol Cell Endocrinol 196:29–42

    Article  PubMed  CAS  Google Scholar 

  • White KP, Hurban P, Watanabe T, Hogness DS (1997) Coordination of Drosophila melanogaster metamorphosis by two ecdysone-induced nuclear receptors. Science 276:114–117

    Article  PubMed  CAS  Google Scholar 

  • Wilson ME, Rosewell KL, Kashon ML, Shughrue PJ, Merchenthaler I, Wise PM (2002) Age differentially influences estrogen receptor-α (Erα) and estrogen receptor-β (Erβ) gene expression in specific regions of the rat brain. Mech Ageing Dev 123:593–601

    Article  PubMed  CAS  Google Scholar 

  • Wright ML, Guertin CJ, Duffy JL, Szatkowski MC, Visconti RF, Alves CD (2003) Developmental and diel profiles of plasma corticosteroids in the bullfrog, Rana catesbeiana. Comp Biochem Physiol 135A:585–595

    CAS  Google Scholar 

  • Zádovská R, Šauman I, Sehnal F (2003) Distribution of PER protein, pigment-dispersing hormone, prothoracicotropic hormone and eclosion hormone in the cephalic nervous system of insects. J Biol Rhythms 18:106–122

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We are grateful to Dr. Markus Lezzi for critical advice, helpful discussions and encouragement during this work, Dr. Arthur Forer for critical advice regarding the analysis of confocal immunofluorescence images and Dr. Peter Moens for continuous support and advice throughout these studies.

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  1. Department of Biology, York University, 4700 Keele St, Toronto, Ontario, M3J 1P3, Canada

    Xanthe Vafopoulou & Colin G. H. Steel

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  1. Xanthe Vafopoulou
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  2. Colin G. H. Steel
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Correspondence to Xanthe Vafopoulou.

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This work was supported by a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada.

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Vafopoulou, X., Steel, C.G.H. hormone nuclear receptor (EcR) exhibits circadian cycling in certain tissues, but not others, during development in Rhodnius prolixus (Hemiptera). Cell Tissue Res 323, 443–455 (2006). https://doi.org/10.1007/s00441-005-0076-1

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