Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-19T05:57:20.191Z Has data issue: false hasContentIssue false

Glycogen Synthase Kinase-3 is involved in glycogen metabolism control and embryogenesis of Rhodnius prolixus

Published online by Cambridge University Press:  24 August 2016

FLÁVIA B. MURY
Affiliation:
LIBHM-NUPEM, Universidade Federal do Rio de Janeiro, Macaé, RJ Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular (INCT-EM), Rio de Janeiro, RJ
MAGDA D. LUGON
Affiliation:
LQFPP and UEA-RJ, Universidade Estadual do Norte Fluminense Darci Ribeiro, Campos dos Goytacazes, RJ
RODRIGO NUNES DA FONSECA
Affiliation:
LIBHM-NUPEM, Universidade Federal do Rio de Janeiro, Macaé, RJ Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular (INCT-EM), Rio de Janeiro, RJ
JOSE R. SILVA
Affiliation:
LIBHM-NUPEM, Universidade Federal do Rio de Janeiro, Macaé, RJ Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular (INCT-EM), Rio de Janeiro, RJ
MATEUS BERNI
Affiliation:
Instituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ
HELENA M. ARAUJO
Affiliation:
Instituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ
MARCIO RIBEIRO FONTENELE
Affiliation:
Instituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ
LEONARDO ARAUJO DE ABREU
Affiliation:
LIBHM-NUPEM, Universidade Federal do Rio de Janeiro, Macaé, RJ Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular (INCT-EM), Rio de Janeiro, RJ
MARÍLVIA DANSA
Affiliation:
Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular (INCT-EM), Rio de Janeiro, RJ LQFPP and UEA-RJ, Universidade Estadual do Norte Fluminense Darci Ribeiro, Campos dos Goytacazes, RJ
GLÓRIA BRAZ
Affiliation:
Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular (INCT-EM), Rio de Janeiro, RJ Departamento de Bioquímica, Instituto de Química, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ
HATISABURO MASUDA
Affiliation:
Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular (INCT-EM), Rio de Janeiro, RJ Instituto de Bioquímica Médica, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ
CARLOS LOGULLO*
Affiliation:
Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular (INCT-EM), Rio de Janeiro, RJ LQFPP and UEA-RJ, Universidade Estadual do Norte Fluminense Darci Ribeiro, Campos dos Goytacazes, RJ
*
*Corresponding author: Universidade Estadual do Norte Fluminense Darci Ribeiro, CBB/LQFPP/UEA-RJ, Av. Alberto Lamego, 2000. Zip code: 28013-620. Campos dos Goytacazes, RJ. E-mail: [email protected]

Summary

Rhodnius prolixus is a blood-feeding insect that transmits Trypanosoma cruzi and Trypanosoma rangeli to vertebrate hosts. Rhodnius prolixus is also a classical model in insect physiology, and the recent availability of R. prolixus genome has opened new avenues on triatomine research. Glycogen synthase kinase 3 (GSK-3) is classically described as a key enzyme involved in glycogen metabolism, also acting as a downstream component of the Wnt pathway during embryogenesis. GSK-3 has been shown to be highly conserved among several organisms, mainly in the catalytic domain region. Meanwhile, the role of GSK-3 during R. prolixus embryogenesis or glycogen metabolism has not been investigated. Here we show that chemical inhibition of GSK-3 by alsterpaullone, an ATP-competitive inhibitor of GSK3, does not affect adult survival rate, though it alters oviposition and egg hatching. Specific GSK-3 gene silencing by dsRNA injection in adult females showed a similar phenotype. Furthermore, bright field and 4’−6-diamidino-2-phenylindole (DAPI) staining analysis revealed that ovaries and eggs from dsGSK-3 injected females exhibited specific morphological defects. We also demonstrate that glycogen content was inversely related to activity and transcription levels of GSK-3 during embryogenesis. Lastly, after GSK-3 knockdown, we observed changes in the expression of the Wingless (Wnt) downstream target β-catenin as well as in members of other pathways such as the receptor Notch. Taken together, our results show that GSK-3 regulation is essential for R. prolixus oogenesis and embryogenesis.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abreu, L. A., Calixto, C., Waltero, C. F., Della Noce, B. P., Githaka, N. W., Seixas, A., Parizi, L. F., Konnai, S., Vaz Ida, S., Ohashi, K. and Logullo, C. (2013). The conserved role of the AKT/GSK-3 axis in cell survival and glycogen metabolism in Rhipicephalus (Boophilus) microplus embryo tick cell line BME26. Biochim Biophys Acta. 1830, 25742582.Google Scholar
Acebron, S. P., Karaulanov, E., Berger, B. S., Huang, Y. L. and Niehrs, C. (2014). Mitotic Wnt signaling promotes protein stabilization and regulates cell size. Molecular Cell 54, 663674.Google Scholar
Aljamali, M. N., Sauer, J. R. and Essenberg, R. C. (2002). RNA interference: applicability in tick research. Experimental and Applied Acarology 28, 8996.Google Scholar
Atella, G. C., Gondim, K. C., Machado, E. A., Medeiros, M. N., Silva-Neto, M. A. and Masuda, H. (2005). Oogenesis and egg development in triatomines: a biochemical approach. Anais da Academia Brasileira de Ciencias 77, 405430.Google Scholar
Baron, R., Rawadi, G., Roman-Roman, S. (2006). Wnt signaling: a key regulator of bone mass. Current Topics in Developmental Biology 76, 103127.Google Scholar
Berni, M., Fontenele, M. R., Tobias-Santos, V., Caceres-Rodrigues, A., Mury, F. B., Vionette-do-Amaral, R., Sorgine, M., Nunes da Fonseca, R. and Araujo, H. (2014). Toll signals regulate dorsal-ventral patterning and anterior-posterior placement of the embryo in the hemipteran R. prolixus . EVODEVO 5, 38.Google Scholar
Bernstein, E., Caudy, A. A., Hammond, S. M. and Hannon, G. J. (2001). Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409, 363366.Google Scholar
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248254.CrossRefGoogle ScholarPubMed
Brembeck, F. H., Rosario, M. and Birchmeier, W. (2006). Balancing cell adhesion and Wnt signaling, the key role of beta-catenin. Current Opinion in Genetics & Development 16, 5159.CrossRefGoogle ScholarPubMed
Campos, E., Moraes, J., Facanha, A. R., Moreira, E., Valle, D., Abreu, L., Manso, P. P., Nascimento, A., Pelajo-Machado, M., Lenzi, H., Masuda, A., Vaz Ida, S. Jr. and Logullo, C. (2006). Kinetics of energy source utilization in Boophilus microplus (Canestrini, 1887) (Acari: Ixodidae) embryonic development. Veterinary Parasitology 138, 349357.CrossRefGoogle ScholarPubMed
Canavoso, L. E., Jouni, Z. E., Karnas, K. J., Pennington, J. E. and Wells, M. A. (2001). Fat metabolism in insects. Annual Review of Nutrition 21, 2346.CrossRefGoogle ScholarPubMed
Carthew, R. W. (2001). Gene silencing by double-stranded RNA. Current Opinion in Cell Biology 13, 244248.CrossRefGoogle ScholarPubMed
Cohen, P. and Frame, S. (2001). The renaissance of GSK3. Nature Reviews Molecular Cell Biology 2, 769776.CrossRefGoogle ScholarPubMed
Cole, A. R. (2013). Regulation of Cell Fate in the Brain by GSK3, Trends in Cell Signaling Pathways in Neuronal Fate Decision, Dr Sabine Wislet-Gendebien (Ed.), ISBN: 978-953-51-1059-0, InTech, DOI: 10.5772/55180.Google Scholar
Cross, D. A., Alessi, D. R., Cohen, P., Andjelkovich, M. and Hemmings, B. A. (1995). Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378, 785789.Google Scholar
de la Fuente, J. and Kocan, K. M. (2006 a). Strategies for development of vaccines for control of ixodid tick species. Parasite Immunology 28, 275283.Google Scholar
de la Fuente, J., Almazán, C., Blas-Machado, U., Naranjo, V., Mangold, A. J., Blouin, E. F., Gortazar, C. and Kocan, K. M. (2006 b). The tick protective antigen, 4D8, is a conserved protein involved in modulation of tick blood digestion and reproduction. Vaccine 24, 40824095.Google Scholar
de Lau, W., Barker, N. and Clevers, H. (2007). WNT signaling in the normal intestine and colorectal cancer. Frontiers in Bioscience 12, 471491. http://dx.doi.org/10.2741/2076 Google Scholar
Eldar-Finkelman, H. and Martinez, A. (2011). GSK-3inhibitors: preclinical and clinical focus on CNS. Frontiers in Molecular Neuroscience 4, 32.CrossRefGoogle Scholar
Espinosa, L., Ingles-Esteve, J., Aguilera, C. and Bigas, A. (2003). Phosphorylation by glycogen synthase kinase-3 beta down-regulates Notch activity, a link for Notch and Wnt pathways. Journal of Biological Chemistry 278, 3222732235.Google Scholar
Fabres, A., De Andrade, C. P., Guizzo, M., Sorgine, M. H., Paiva-Silva Gde, O., Masuda, A., Vaz Ida, S. Jr. and Logullo, C. (2010). Effect of GSK-3 activity, enzymatic inhibition and gene silencing by RNAi on tick oviposition and egg hatching. Parasitology 137, 15371546.CrossRefGoogle ScholarPubMed
Ferkey, D. M. and Kimelman, D. (2000). GSK-3: new thoughts on an old enzyme. Developmental Biology 225, 471479.Google Scholar
Fialho, E., Silveira, A. B., Masuda, H. and Silva-Neto, M. A. (2002). Oocyte fertilization triggers acid phosphatase activity during R. prolixus embryogenesis. Insect Biochemistry and Molecular Biology 32, 871880.CrossRefGoogle Scholar
Fraga, A., Ribeiro, L., Lobato, M., Santos, V., Silva, J. R., Gomes, H., da Cunha Moraes, J. L., de Souza Menezes, J., de Oliveira, C. J., Campos, E. and da Fonseca, R. N. (2013). Glycogen and glucose metabolism are essential for early embryonic development of the red flour beetle Tribolium castaneum . PLoS ONE 8, e65125.CrossRefGoogle ScholarPubMed
Fernandes, M. R., Martins, R, Costa, E. P., Pacidônio, E. C., Abreu, L. A., Vaz, I. S., Moreira, L. A., Fonseca, R. N. and Logullo, C. (2014). The modulation of the symbiont/host interaction between Wolbachia pipientis and Aedes fluviatilis embryos by glycogen metabolism. PLoS ONE 9, e98966 doi: 10.1371/journal.pone.0098966 Google Scholar
Foltz, D. R., Santiago, M. C., Berechid, B. E. and Nye, J. S. (2002). Glycogen synthase kinase-3beta modulates Notch signaling and stability. Current Biology 12, 10061011.Google Scholar
Gade, G. and Auerswald, L. (2003). Mode of action of neuropeptides from the adipokinetic hormone family. General and Comparative Endocrinology 132, 1020.CrossRefGoogle ScholarPubMed
Garcia, E. S., Mello, C. B., Azambuja, P. and Ribeiro, J. M. (1994). R. prolixus: salivary antihemostatic components decrease with Trypanosoma rangeli infection. Experimental Parasitology 78, 287293.CrossRefGoogle Scholar
Gondim, K. C., Atella, G. C., Kawooya, J. K. and Masuda, H. (1992). Role of phospholipids in the lipophorin particles of R. prolixus . Archives of Insect Biochemistry and Physiology 20, 303314.CrossRefGoogle Scholar
Grimes, C. A. and Jope, R. S. (2001). The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Progress in Neurobiology 65, 391426.Google Scholar
Heitzler, P. and Simpson, P. (1991). The choice of cell fate in the epidermis of Drosophila. Cell 64, 10831092.Google Scholar
Henschel, A., Buchholz, F. and Habermann, B. (2004). DEQOR: a web-based tool for the design and quality control of sRNAis. Nucleic Acids Research 32, W113W120.Google Scholar
Katagiri, N., Ando, O. and Yamashita, O. (1998). Reduction of glycogen in eggs of the silkworm, Bombyx mori, by use of a trehalase inhibitor, trehazolin, and diapause induction in glycogen-reduced eggs. Journal of Insect Physiology 44, 12051212.Google Scholar
Kocan, K. M., Manzano-Roman, R. and de la Fuente, J. (2007). Transovarial silencing of the subolesin gene in three-host ixodid tick species after injection of replete females with subolesin dsRNA. Parasitology Research 100, 14111415.Google Scholar
Kocan, K., Zivkovic, Z., Blouin, E. F., Naranjo, V., Almazán, C., Mitra, R. and de la Fuente, J. (2009). Silencing of genes involved in Anaplasma marginale-tick interactions affects the pathogen developmental cycle in Dermacentor variabilis . BMC Developmental Biology 9, 42.Google Scholar
Lavore, A., Pagola, L., Esponda-Behrens, N. and Rivera-Pomar, R. (2012). The gap gene giant of R. prolixus is maternally expressed and required for proper head and abdomen formation. Developmental Biology 361, 147155.Google Scholar
Lavore, A., Esponda-Behrens, N., Pagola, L. and Rivera-Pomar, R. (2014). The gap gene Kruppel of R. prolixus is required for segmentation and for repression of the homeotic gene sex comb-reduced. Developmental Biology 387, 121129.Google Scholar
Liu, C., Li, Y., Semenov, M., Han, C., Baeg, G. H., Tan, Y., Zhang, Z., Lin, X. and He, X. (2002). Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108, 837847.Google Scholar
Livak, K. J. and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402408.CrossRefGoogle ScholarPubMed
Majerowicz, D., Alves-Bezerra, M., Logullo, R., Fonseca-de-Souza, A. L., Meyer-Fernandes, J. R., Braz, G. R. and Gondim, K. C. (2011). Looking for reference genes for real-time quantitative PCR experiments in R. prolixus (Hemiptera: Reduviidae). Insect Molecular Biology 20, 713722.Google Scholar
Mariano, A. C., Santos, R., Gonzalez, M. S., Feder, D., Machado, E. A., Pascarelli, B., Gondim, K. C. and Meyer-Fernandes, J. R. (2009). Synthesis and mobilization of glycogen and trehalose in adult male R. prolixus . Archives of Insect Biochemistry and Physiology 72, 115.Google Scholar
Melo, A. C., Valle, D., Machado, E. A., Salerno, A. P., Paiva-Silva, G. O., Cunha, E. S. N. L., de Souza, W. and Masuda, H. (2000). Synthesis of vitellogenin by the follicle cells of R. prolixus . Insect Biochemistry and Molecular Biology 30, 549557.Google Scholar
Moraes, J., Galina, A., Alvarenga, P. H., Rezende, G. L., Masuda, A., da Silva Vaz, I. Jr. and Logullo, C. (2007). Glucose metabolism during embryogenesis of the hard tick Boophilus microplus. Comparative biochemistry and physiology. Part A, Molecular & Integrative Physiology 146, 528533.Google Scholar
Naito, Y., Yamada, T., Matsumiya, T., Ui-Tei, K., Saigo, K. and Morishita, S. (2005). dsCheck: highly sensitive off-target search software for double-stranded RNA-mediated RNA interference. Nucleic Acids Research 33, W589W591.Google Scholar
Nijhof, A. M., Taoufik, A., de la Fuente, J., Kocan, K. M., Vries, E. and Jongejan, F. (2007). Gene silencing of the tick protective antigens, Bm86, Bm91 and subolesin, in the one-host tick Boophilus microplus by RNA interference. International Journal for Parasitology 37, 653662.Google Scholar
Oliveira, P. L., Gondim, K. C., Guedes, D. M. and Masuda, H. (1986). Uptake of yolk proteins in R. prolixus . Journal of Insect Physiology 32, 859866.Google Scholar
Papadopoulou, D., Bianchi, M. W. and Bourouis, M. (2004). Functional studies of shaggy/glycogen synthase kinase 3 phosphorylation sites in Drosophila melanogaster . Molecular and Cellular Biology 24, 49094919.Google Scholar
Papaj, D. R. (2000). Ovarian dynamics and host use. Annual Review of Entomology 45, 423448.Google Scholar
Polakis, P. (2007). The many ways of Wnt in cancer. Current Opinion in Genetics & Development, 17, 4551.CrossRefGoogle ScholarPubMed
Raikhel, A. S. and Dhadialla, T. S. (1992). Accumulation of yolk proteins in insect oocytes. Annual Review of Entomology 37, 217251.Google Scholar
Ramamurty, P. S. (1968). Origin and distribution of glycogen during vitellogenesis of the scorpion fly, Panorpa communis . Journal of Insect Physiology 14, 13251326.Google Scholar
Ruel, L., Bourouis, M., Heitzler, P., Pantesco, V. and Simpson, P.(1993). Drosophila shaggy kinase and rat glycogen synthase kinase-3 have conserved activities and act downstream of Notch. Nature 362, 557560.Google Scholar
Ruiz-Trillo, I., Roger, A. J., Burger, G., Gray, M. W. and Lang, B. F. (2008). A phylogenomic investigation into the origin of metazoa. Molecular Biology and Evolution 25, 664672.Google Scholar
Santos, R., Mariano, A. C., Rosas-Oliveira, R., Pascarelli, B., Machado, E. A., Meyer-Fernandes, J. R. and Gondim, K. C. (2008). Carbohydrate accumulation and utilization by oocytes of R. prolixus . Archives of Insect Biochemistry and Physiology 67, 5562.Google Scholar
Schierwater, B., Eitel, M., Jakob, W., Osigus, H.-J., Hadrys, H., Dellaporta, S. L., Kolokotronis, S.-O. and DeSalle, R. (2009). Concatenated Analysis Sheds Light on Early Metazoan Evolution and Fuels a Modern “Urmetazoon” Hypothesis. PLoS Biology 7, e1000020.CrossRefGoogle Scholar
Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 46734680.CrossRefGoogle ScholarPubMed
Tullai, J. W., Chen, J., Schaffer, M. E., Kamenetsky, E., Kasif, S. and Cooper, G. M. (2007). Glycogen synthase kinase-3 represses cyclic AMP response element-binding protein (CREB)-targeted immediate early genes in quiescent cells. Journal of Biological Chemistry 282, 94829491.CrossRefGoogle ScholarPubMed
Van Noort, M., Meeldijk, J., Van der Zee, R., Destree, O. and Clevers, H. (2002). Wnt signaling controls the phosphorylation status of beta-catenin. Journal of Biological Chemistry 277, 1790117905.Google Scholar
Vital, W., Rezende, G. L., Abreu, L., Moraes, J., Lemos, F. J., Vaz Ida, S. Jr. and Logullo, C. (2010). Germ band retraction as a landmark in glucose metabolism during Aedes aegypti embryogenesis. BMC Developmental Biology 10, 25.Google Scholar
WHO (2008). World Health Organization. Chagas disease (American trypanosomiasis). Available: http://www.who.int/mediacentre/factsheets/fs340/en/. Accessed 27 August 2014.Google Scholar
Wigglesworth, V. B. (1954). The Physiology of Insect Metamorphosis. Cambridge University Press, Cambridge.Google Scholar
Wigglesworth, V. B. (1959). The Control of Growth and Form: A Study of the Epidermal Cell in an Insect. Cornell University Press, Ithaca, NY.Google Scholar
Yamazaki, H. and Nusse, R. (2002). Identification of DCAP, a drosophila homolog of a glucose transport regulatory complex. Mechanisms of Development 119, 115119.Google Scholar
Zdobnov, E. M., Apweiler, R. (2001). InterProScan--an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17, 847848.Google Scholar
Ziegler, R. and Van Antwerpen, R. (2006). Lipid uptake by insect oocytes. Insect Biochemistry and Molecular Biology 36, 264272.CrossRefGoogle ScholarPubMed
Supplementary material: File

Mury supplementary material

Mury supplementary material 1

Download Mury supplementary material(File)
File 985 KB