Glucose metabolomic profile during embryogenesis in the tick Rhipicephalus microplus.
Embryogenesis
Gluconeogenesis
Glucose metabolism
Metabolomic
Tick
Journal
Metabolomics : Official journal of the Metabolomic Society
ISSN: 1573-3890
Titre abrégé: Metabolomics
Pays: United States
ID NLM: 101274889
Informations de publication
Date de publication:
31 08 2021
31 08 2021
Historique:
received:
08
10
2020
accepted:
17
08
2021
entrez:
31
8
2021
pubmed:
1
9
2021
medline:
15
1
2022
Statut:
epublish
Résumé
Metabolomic approaches can assess the actual state of an organism's energy metabolism during a specific morphological event, providing a more accurate insight into the correlations between physiology and metabolic regulation. The study of the metabolomic profile aim to identify the largest possible number of biomolecules in a certain organism or specific structures. For this purpose, mass spectrometry (MS) and chromatography have been used in the present study. In this context, the aim of the present work is to evaluate the glucose metabolomic profile during embryogenesis in Rhipicephalus microplus tick, investigating the dynamics of nutrient utilization during tick embryo formation, as well as the control of glucose metabolism. We show that glycogen reserves are preferentially mobilized to sustain the energy-intensive process of embryogenesis. Subsequently, the increase in concentration of specific amino acids indicates that protein degradation would provide carbons to fuel gluconeogenesis, supplying the embryo with sufficient glucose and glycogen during development. Altogether, these results demonstrated the presence of a very refined catabolic and anabolic control during embryogenesis in R. microplus tick, suggesting the pronounced gluconeogenesis as a strategy to secure embryo development. Moreover, this research contributes to the understanding of the mechanisms that control glucose metabolism during tick embryogenesis and may aid the identification of putative targets for novel chemical or immunological control methods, which are essential to improve the prevention of tick infestations.
Identifiants
pubmed: 34463832
doi: 10.1007/s11306-021-01830-2
pii: 10.1007/s11306-021-01830-2
doi:
Substances chimiques
Glycogen
9005-79-2
Glucose
IY9XDZ35W2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
79Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Alseekh, S., & Fernie, A. R. (2018). Metabolomics 20 years on: What have we learned and what hurdles remain? Plant Journal, 94, 933–942. https://doi.org/10.1111/tpj.13950
doi: 10.1111/tpj.13950
An, P. N. T., & Fukusaki, E. (2018). Metabolomics: State-of-the-art technologies and applications on Drosophila melanogaster. Advances in experimental medicine and biology (pp. 257–276). Springer.
An, P. N. T., Yamaguchi, M., Bamba, T., Fukusaki, E., & Penny, S. (2014). Metabolome analysis of Drosophila melanogaster during embryogenesis. PLoS ONE, 9, e99519. https://doi.org/10.1371/journal.pone.0099519
doi: 10.1371/journal.pone.0099519
pubmed: 25121768
pmcid: 4133167
Aretz, I., & Meierhofer, D. (2016). Advantages and pitfalls of mass spectrometry based metabolome profiling in systems biology. International Journal of Molecular Sciences. https://doi.org/10.3390/ijms17050632
doi: 10.3390/ijms17050632
pubmed: 27128910
pmcid: 4881458
Atallah, J., & Lott, S. E. (2018). Evolution of maternal and zygotic mRNA complements in the early Drosophila embryo. PLOS Genetics, 14, e1007838. https://doi.org/10.1371/journal.pgen.1007838
doi: 10.1371/journal.pgen.1007838
pubmed: 30557299
pmcid: 6312346
Avilés-Pagán, E. E., & Orr-Weaver, T. L. (2018). Activating embryonic development in Drosophila. Seminars in Cell & Developmental Biology, 84, 100–110. https://doi.org/10.1016/j.semcdb.2018.02.019
doi: 10.1016/j.semcdb.2018.02.019
Babicki, S., Arndt, D., Marcu, A., Liang, Y., Grant, J. R., Maciejewski, A., & Wishart, D. S. (2016). Heatmapper: Web-enabled heat mapping for all. Nucleic Acids Research, 44, W147–W153. https://doi.org/10.1093/nar/gkw419
doi: 10.1093/nar/gkw419
pubmed: 27190236
pmcid: 4987948
Bligh, E. G., & Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology, 37, 911–917. https://doi.org/10.1139/o59-099
doi: 10.1139/o59-099
pubmed: 13671378
Boja, E. S., Kinsinger, C. R., Rodriguez, H., & Srinivas, P. (2014). Integration of omics sciences to advance biology and medicine. In: Clinical proteomics. BioMed Central Ltd., p. 45
Briegel, H., Gut, T., & Lea, A. O. (2003). Sequential deposition of yolk components during oogenesis in an insect, Aedes aegypti (Diptera: Culicidae). Journal of Insect Physiology, 49, 249–260. https://doi.org/10.1016/S0022-1910(02)00272-X
doi: 10.1016/S0022-1910(02)00272-X
pubmed: 12770000
Brown, M. R., Clark, K. D., Gulia, M., Zhao, Z., Garczynski, S. F., Crim, J. W., Suderman, R. J., & Strand, M. R. (2008). An insulin-like peptide regulates egg maturation and metabolism in the mosquito Aedes aegypti. Proceedings of the National Academy of Sciences of the United States of America, 105, 5716–5721. https://doi.org/10.1073/pnas.0800478105
doi: 10.1073/pnas.0800478105
pubmed: 18391205
pmcid: 2311378
Campos, E., Moraes, J., Façanha, A. R., Moreira, E., Valle, D., Abreu, L., Manso, P. P., Nascimento, A., Pelajo-Machado, M., Lenzi, H., & Masuda, A. (2006). Kinetics of energy source utilization in Boophilus microplus (Canestrini, 1887)(Acari: Ixodidae) embryonic development. Veterinary Parasitology, 138(3–4), 349–357.
doi: 10.1016/j.vetpar.2006.02.004
Cox, J. E., Thummel, C. S., & Tennessen, J. M. (2017). Metabolomic studies in Drosophila. Genetics, 206, 1169–1185. https://doi.org/10.1534/genetics.117.200014
doi: 10.1534/genetics.117.200014
pubmed: 28684601
pmcid: 5500124
Gonzales, K. K., et al. (2018). The effect of SkitoSnack, an artificial blood meal replacement, on Aedes aegypti life history traits and gut microbiota. Scientific Reports, 8(1), 1–14. https://doi.org/10.1038/s41598-018-29415-5
doi: 10.1038/s41598-018-29415-5
Grisi, L., Leite, R. C., Martins, J. R., Barros, A. T., Andreotti, R., Cançado, P. H., León, A. A., Pereira, J. B., & Villela, H. S. (2014). Reassessment of the potential economic impact of cattle parasites in Brazil Reavaliação do potencial impacto econômico de parasitos de bovinos no Brasil. Brazilian Journal of Veterinary Parasitology. https://doi.org/10.1590/S1984-29612014042
doi: 10.1590/S1984-29612014042
pubmed: 25054492
Gutzeit, H. O., Zissler, D., Grau, V., Liphardt, M., & Heinrich, U. R. (1994). Glycogen stores in mature ovarian follicles and young embryos of Drosophila: Ultrastructural changes and some biochemical correlates. European Journal of Cell Biology, 63, 52–60.
pubmed: 8005105
Hanson, R. W., & Patel, Y. M. (2006). Phosphoenolpyruvate carboxykinase (GTP): The gene and the enzyme. Advances in enzymology and related areas of molecular biology (pp. 203–281). Wiley.
doi: 10.1002/9780470123157.ch6
Hou, Y., Wang, X.-L., Saha, T. T., Roy, S., Zhao, B., Raikhel, A. S., & Zou, Z. (2015). Temporal coordination of carbohydrate metabolism during mosquito reproduction. PLOS Genetics, 11, e1005309. https://doi.org/10.1371/journal.pgen.1005309
doi: 10.1371/journal.pgen.1005309
pubmed: 26158648
pmcid: 4497655
Iwamoto, N., & Shimada, T. (2018). Recent advances in mass spectrometry-based approaches for proteomics and biologics: Great contribution for developing therapeutic antibodies. Pharmacology and Therapeutics, 185, 147–154. https://doi.org/10.1016/j.pharmthera.2017.12.007
doi: 10.1016/j.pharmthera.2017.12.007
pubmed: 29274706
Krisher, R. L., Schoolcraft, W. B., & Katz-Jaffe, M. G. (2015). Omics as a window to view embryo viability. Fertility and Sterility, 103, 333–341. https://doi.org/10.1016/j.fertnstert.2014.12.116
doi: 10.1016/j.fertnstert.2014.12.116
pubmed: 25639968
Lee, M. T., Bonneau, A. R., & Giraldez, A. J. (2014). Zygotic genome activation during the maternal-to-zygotic transition. Annual Review of Cell and Developmental Biology, 30, 581–613.
doi: 10.1146/annurev-cellbio-100913-013027
McDaniel, S. L., Gibson, T. J., Schulz, K. N., Fernandez Garcia, M., Nevil, M., Jain, S. U., Lewis, P. W., Zaret, K. S., & Harrison, M. M. (2019). Continued activity of the pioneer factor zelda is required to drive zygotic genome activation. Molecular Cell, 74, 185-195.e4. https://doi.org/10.1016/j.molcel.2019.01.014
doi: 10.1016/j.molcel.2019.01.014
pubmed: 30797686
pmcid: 6544384
Medina, M., & Vallejo, C. G. (1989). The contents of proteins, carbohydrates, lipids and DNA during the embryogenesis of Drosophila. International Journal of Developmental Biology, 33, 403–405. https://doi.org/10.1387/ijdb.2518452
doi: 10.1387/ijdb.2518452
Moraes, J., Galina, A., Alvarenga, P. H., Rezende, G. L., Masuda, A., da Silva Vaz, I., & Logullo, C. (2007). Glucose metabolism during embryogenesis of the hard tick Boophilus microplus. Comparative Biochemistry and Physiology Part a: Molecular & Integrative Physiology, 146, 528–533. https://doi.org/10.1016/j.cbpa.2006.05.009
doi: 10.1016/j.cbpa.2006.05.009
Nielsen, N. P. V., Carstensen, J. M., & Smedsgaard, J. (1998). Aligning of single and multiple wavelength chromatographic profiles for chemometric data analysis using correlation optimised warping. Journal of Chromatography A, 805, 17–35. https://doi.org/10.1016/S0021-9673(98)00021-1
doi: 10.1016/S0021-9673(98)00021-1
Parizi, L. F., Githaka, N. W., Logullo, C., Konnai, S., Masuda, A., Ohashi, K., & da Silva Vaz, I. (2012). The quest for a universal vaccine against ticks: Cross-immunity insights. The Veterinary Journal, 194, 158–165. https://doi.org/10.1016/j.tvjl.2012.05.023
doi: 10.1016/j.tvjl.2012.05.023
pubmed: 22766309
Pennington, J. E., Goldstrohm, D. A., & Wells, M. A. (2003). The role of hemolymph proline as a nitrogen sink during blood meal digestion by the mosquito Aedes aegypti. Journal of Insect Physiology, 49, 115–121. https://doi.org/10.1016/S0022-1910(02)00267-6
doi: 10.1016/S0022-1910(02)00267-6
pubmed: 12770004
Pinu, F. R., Beale, D. J., Paten, A. M., Kouremenos, K., Swarup, S., Schirra, H. J., & Wishart, D. (2019). Systems biology and multi-omics integration: Viewpoints from the metabolomics research community. Metabolites. https://doi.org/10.3390/metabo9040076
doi: 10.3390/metabo9040076
pubmed: 31174372
pmcid: 6631405
Pohl, P. C., Sorgine, M. H. F., Leal, A. T., Logullo, C., Oliveira, P. L., da Silva Vaz, I., & Masuda, A. (2008). An extraovarian aspartic protease accumulated in tick oocytes with vitellin-degradation activity. Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology, 151, 392–399. https://doi.org/10.1016/j.cbpb.2008.08.008
doi: 10.1016/j.cbpb.2008.08.008
pubmed: 18782630
Powers, R., & Riekeberg, E. (2017). New frontiers in metabolomics: From measurement to insight. F1000Research. https://doi.org/10.12688/f1000research.11495.1
doi: 10.12688/f1000research.11495.1
pubmed: 29225791
pmcid: 5710306
Reck, J., Berger, M., Terra, R. M. S., Marks, F. S., da Silva Vaz, I., Guimarães, J. A., & Termignoni, C. (2009). Systemic alterations of bovine hemostasis due to Rhipicephalus (Boophilus) microplus infestation. Research in Veterinary Science, 86, 56–62. https://doi.org/10.1016/j.rvsc.2008.05.007
doi: 10.1016/j.rvsc.2008.05.007
pubmed: 18571684
Santos, V. T., Ribeiro, L., Fraga, A., de Barros, C. M., Campos, E., Moraes, J., Fontenele, M. R., Araújo, H. M., Feitosa, N. M., Logullo, C., & da Fonseca, R. N. (2013). The embryogenesis of the Tick Rhipicephalus (Boophilus) microplus : The establishment of a new chelicerate model system. Genesis, 51, 803–818. https://doi.org/10.1002/dvg.22717
doi: 10.1002/dvg.22717
pubmed: 24166799
Segers, K., Declerck, S., Mangelings, D., Heyden, Y. V., & Eeckhaut, A. V. (2019). Analytical techniques for metabolomic studies: A review. Bioanalysis, 11, 2297–2318. https://doi.org/10.4155/bio-2019-0014
doi: 10.4155/bio-2019-0014
pubmed: 31845604
Seixas, A., Alzugaray, M. F., Tirloni, L., Parizi, L. F., Pinto, A. F. M., Githaka, N. W., Konnai, S., Ohashi, K., Yates, J. R., Termignoni, C., & da Silva Vaz, I. (2018). Expression profile of Rhipicephalus microplus vitellogenin receptor during oogenesis. Ticks and Tick-Borne Diseases, 9, 72–81. https://doi.org/10.1016/j.ttbdis.2017.10.006
doi: 10.1016/j.ttbdis.2017.10.006
pubmed: 29054547
Seixas, A., Oliveira, P., Termignoni, C., Logullo, C., Masuda, A., & da Silva Vaz, I. (2012). Rhipicephalus (Boophilus) microplus embryo proteins as target for tick vaccine. Veterinary Immunology and Immunopathology, 148, 149–156. https://doi.org/10.1016/j.vetimm.2011.05.011
doi: 10.1016/j.vetimm.2011.05.011
pubmed: 21620488
Tennessen, J. M., Bertagnolli, N. M., Evans, J., Sieber, M. H., Cox, J., & Thummel, C. S. (2014). Coordinated metabolic transitions during Drosophila embryogenesis and the onset of aerobic glycolysis. G3: Genes Genomes, Genetics, 4, 839–850. https://doi.org/10.1534/g3.114.010652
doi: 10.1534/g3.114.010652
Utter, M. F., & Kolenbrander, H. M. (1972). Formation of oxaloacetate by CO2 fixation on phosphoenolpyruvate. Enzymes, 6, 117–168. https://doi.org/10.1016/S1874-6047(08)60039-6
doi: 10.1016/S1874-6047(08)60039-6
Vital, W., Rezende, G. L., Abreu, L., Moraes, J., Lemos, F. J., Vaz, I. D. S., & Logullo, C. (2010). Germ band retraction as a landmark in glucose metabolism during Aedes aegypti embryogenesis. BMC Developmental Biology. https://doi.org/10.1186/1471-213X-10-25
doi: 10.1186/1471-213X-10-25
pubmed: 20184739
pmcid: 2838828
Waltero, C., De Abreu, L. A., Alonso, T., Nunes-Da-Fonseca, R., Da Silva Vaz, I., & Logullo, C. (2019). TOR as a regulatory target in Rhipicephalus microplus embryogenesis. Frontiers in Physiology. https://doi.org/10.3389/fphys.2019.00965
doi: 10.3389/fphys.2019.00965
pubmed: 31417424
pmcid: 6684781
Xavier, M. A., Tirloni, L., Pinto, A. F. M., Diedrich, J. K., Yates, J. R., Gonzales, S., Farber, M., da Silva Vaz, I., & Termignoni, C. (2019). Tick Gené’s organ engagement in lipid metabolism revealed by a combined transcriptomic and proteomic approach. Ticks and Tick-Borne Diseases, 10, 787–797. https://doi.org/10.1016/j.ttbdis.2019.03.013
doi: 10.1016/j.ttbdis.2019.03.013
pubmed: 30904537
Xavier, M. A., Tirloni, L., Pinto, A. F. M., Diedrich, J. K., Yates, J. R., Mulenga, A., Logullo, C., Da Silva Vaz, I., Seixas, A., & Termignoni, C. (2018). A proteomic insight into vitellogenesis during tick ovary maturation. Scientific Reports, 8, 1–14. https://doi.org/10.1038/s41598-018-23090-2
doi: 10.1038/s41598-018-23090-2
Yamazaki, H., & Yanagawa, S. I. (2003). Axin and the Axin/Arrow-binding protein DCAP mediate glucose-glycogen metabolism. Biochemical and Biophysical Research Communications, 304, 229–235. https://doi.org/10.1016/S0006-291X(03)00582-5
doi: 10.1016/S0006-291X(03)00582-5
pubmed: 12711303
Yang, Q., Zhang, A. H., Miao, J. H., Sun, H., Han, Y., Yan, G. L., Wu, F. F., & Wang, X. J. (2019). Metabolomics biotechnology, applications, and future trends: A systematic review. RSC Advances, 9, 37245–37257. https://doi.org/10.1039/c9ra06697g
doi: 10.1039/c9ra06697g
Ye, G., Chen, Y., Wang, H.-O., Ye, T., Lin, Y., Huang, Q., Chi, Y., & Dong, S. (2016). Metabolomics approach reveals metabolic disorders and potential biomarkers associated with the developmental toxicity of tetrabromobisphenol A and tetrachlorobisphenol A. Scientific Reports. https://doi.org/10.1038/srep35257
doi: 10.1038/srep35257
pubmed: 28009012
pmcid: 5180105
Zhang, J., Yang, P. L., & Gray, N. S. (2009). Targeting cancer with small molecule kinase inhibitors. Nature Reviews Cancer, 9, 28–39. https://doi.org/10.1038/nrc2559
doi: 10.1038/nrc2559
pubmed: 19104514
Zhou, G., Flowers, M., Friedrich, K., Horton, J., Pennington, J., & Wells, M. A. (2004b). Metabolic fate of [14C]-labeled meal protein amino acids in Aedes aegypti mosquitoes. Journal of Insect Physiology, 50, 337–349. https://doi.org/10.1016/j.jinsphys.2004.02.003
doi: 10.1016/j.jinsphys.2004.02.003
pubmed: 15081827
Zhou, G., Pennington, J. E., & Wells, M. A. (2004a). Utilization of pre-existing energy stores of female Aedes aegypti mosquitoes during the first gonotrophic cycle. Insect Biochemistry and Molecular Biology, 34, 919–925. https://doi.org/10.1016/j.ibmb.2004.05.009
doi: 10.1016/j.ibmb.2004.05.009
pubmed: 15350611