American Journal of BioScience

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Detection of Small GTP Binding Proteins Showing GTPase and GTP/ATP Binding Activities in the Ovary of the American Cockroach, Periplaneta Americana, during Oogenesis

Received: 12 April 2014    Accepted: 28 April 2014    Published: 30 May 2014
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Abstract

In the present study, the small GTP binding proteins involved in the regulatory mechanism of vitellogenin (Vg) endocytotic vesicles trafficking were detected, for the first time, in ovaries of the most basal hemimetabolus insect, Periplaneta americana during oogenesis. The ovarian GTPase activities were peaked during previtellogenic and early vitellogenic periods. Such activity coincides with vitellogenin receptors (VgRs) and clathrin early expression during these developmental periods, suggesting the importance of GTPases not only in the process of vesicle formation and fusion but also in the process of early fluid phase endocytosis. Two small peaks of activities were monitored during the late vitellogenic period (days 8 and 10), suggesting a possible role of GTPases in VgRs and clathrin recycling process. The [α32P]-GTP binding assay analysis in different tissues revealed the presence of small GTP binding proteins of molecular weights 25, 23 and 21 kDa in ovaries and head. However, a single binding signal band of 21 and 25 kDa was each detected in the fat bodies and muscles, respectively. No binding was detected in the midgut and Malpighian tubules. However, the 23 kDa protein detected was suggested as a probable cytosolic form of the 25 kDa protein. The competition assay results indicated that the small ovarian GTP binding proteins could also bind ATP, suggesting that like GTP, ATP is a regulatory nucleotide for the ovarian small proteins detected during oogenesis. The present study will pave the way for more understanding of the mechanisms that regulate Vg transport machinery in hemimetabolous insects.

DOI 10.11648/j.ajbio.20140203.15
Published in American Journal of BioScience (Volume 2, Issue 3, May 2014)
Page(s) 106-110
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This is an Open Access article, distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium or format, provided the original work is properly cited.

Copyright

Copyright © The Author(s), 2024. Published by Science Publishing Group

Keywords

GTP/ATP Binding, GTPase, Vitellogenesis, Endocytosis, American Cockroach

References
[1] E.S., Snigirevskaya, and A.S., Raikhel, “Receptor mediated endocytosis of yolk proteins in insect oocytes. In: Raikhel A. S., Sappington T. W. (Eds.), Progress in vitellogenesis. Reproductive Biology of Invertebrates, vol. XII. Part B. Science Publishers, Inc., Enfield, USA-Plymouth UK,2005, pp. 199-228.
[2] A.S., Raikhel, and T.S. Dhadialla, “Accumulation of yolk proteins in insect oocytes. Ann. Rev. Entomol., vol. 73 pp. 217-251, 1992.
[3] K. G. Davey, “Hormonal integration of egg production in Rhodnius prolixus,” American Zoologist, vol.33, pp.397-402. 1993.
[4] M., Tufail, M., Takeda, “Molecular characteristics of insect vitellogenins. J. Insect Physiol, vol. 54, pp.1447–1458, 2008.
[5] M., Tufail, and M., Takeda, “Insect vitellogenin/lipophorin receptors: Molecular structures, role in oogenesis, and regulatory mechanisms. J. Insect Physiol., vol. 55, pp. 88–104, 2009.
[6] R. Diaz, L.S. Mayorga, L.E. Mayorga, and P. Stahl, “In vitro clustering and multiple fusion among macrophage endosomes,” Journal of Biological Chemistry, vol.264, no.22, 13171-13180, 1989.
[7] P. D`Adamo, M. Masetti, V. Bianchi, L. More`, M. Mignogna, and S. Gatti, “RAB GTPases and RAB-interacting proteins and their role in the control of cognitive functions”, Journal of neurobiology review, Doi.org/10.1016/J.neubiorev.2013.12.009, 2014.
[8] M., Zerial, and H., McBride H., “Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol., vol. 2, pp. 107-117, 2001.
[9] J. Armstrong, “How do Rab proteins function in membrane traffic?” International Journal of Biochemistry and Cell Biology, vol.32, pp. 303-307, 2000.
[10] Y., Takai, T., Sasaki, and T., Matozaki, “Small GTP-binding proteins. Physiol. Rev., vol. 81, no.1, pp. 153-208, 2001.
[11] I. Jordens, M. Marsman, C. Kuijl, and J. Neefjes, “Rab pro-teins connecting transport and vesicle fusion,” Traffic, vol.6, pp. 1070-1077, 2005.
[12] M.T. Handley, and R.D. Burgoyne, “The Rab27 effector Rabphilin, unlike Granuphilin and Noc2, rapidly exchanges between secretory granules and cytosol in PC12 cells,” Biochemical Biophysical Research Communication, vol.373, pp. 275-281, 2008.
[13] T., Uno, T., Moriwaki, Y., Isoyama, Y., Uno, K., Kanamaru, H., Yamagata, M., Nakamura and M., Takagi, “Rab14 from Bombyx mori (Lepidoptera: Bombycidae) shows ARPase activity. Biol. Lett. (doi: 10.1098/rsbl.2009.0878), 2010.
[14] J. Blumer, Y. W. Wu, R. S. Goody, and A. Itzen, “Specific localization of Rabs at intracellular membranes”, Biochemical Society Transactions, Vol.40, no. 6, pp.1421- 1425, 2012.
[15] P., Liu, R., Bartz, J.K., Zehmer, Y.S., Ying, M., Zhu, G.M., Serrero, and R/G., Anderson. Rab-regulated interaction of early endosomes with lipid droplets. Biochem. Biophys. Acta., vol. 1773, pp. 784-793, 2007.
[16] R., Van Antwerpen, D.Q.D., Pham, and R., Ziegler, Accumulation of lipids in insect oocytes. In Progress in Vitellogenesis (Raikhel A.S., Sappington, T.W. eds); Reproductive Biology of Invertebrates (Adiyodi, K.G., Adiyodi R.G., Series Editors), Science Publishers, Inc., Enfield, NH; Plymouth UK, Vol XII. Part B, 2005, pp. 265–288.
[17] M., Tufail, J. M., Lee, M., Hatakeyama, K., Oishi, and M., Takeda, Cloning of vitellogenin cDNA of the american cockroach, Periplaneta americana (Dictyoptera), and its structural and expression analyses. Arch. Insect Biochem. Physiol., vol. 45, pp. 37–46, 2000.
[18] M., Tufail, M., Hatakeyama, and M. Takeda. Molecular evidence for two vitellogenin genes and processing of vitellogenins in the american cockroach, Periplaneta americana. Arch. Insect Biochem. Physiol., vol. 48, pp. 72–80, 2001.
[19] M., Tufail, A.S., Raikhel, M. Takeda. Biosynthesis and processing of insect vitellogenins. In Progress in Vitellogenesis (Raikhel A.S. and Sappington T.W. eds); Reproductive Biology of Invertebrates (Adiyodi K.G. and Adiyodi R.G., Series Editors), Science Publishers, Inc., Enfield, NH; Plymouth, UK., Vol XII. Part B, 2004, pp. 1–32.
[20] M., Tufail, and M., Takeda M. Molecular cloning, characterization and regulation of the cockroach vitellogenin receptor during oogenesis. Insect Mol. Biol., vol. 14, pp. 389–401, 2005.
[21] M., Tufail, and M., Takeda. Molecular characteristics of insect vitellogenins. J. Insect Physiol., vol. 54, pp. 1447–1458, 2008.
[22] A. M. Elgendy, M. Elmogy, M. Tufail, and M. Takeda, “Developmental expression profile of cockroach vitellogenin genes Vg1 and2,” Animal Biology Journal, vol.1, pp. 39–48, 2009.
[23] M. Elmogy, A.M. Elgendy, W.M. Alamodi, and M. Takeda, “Molecular characterization, developmental expression and immunolocalization of clathrin heavy chain in the ovary of the american cockroach, Periplaneta americana during oogenesis,” Journal of Advanced laboratory Research in Biology, vol.3, no.4, pp. 313-318, 2012.
[24] Y., Shirai, N., Sakai, and N., Saito. 1998. Subspecies-specific targeting mechanism of protein kinase C. Jpn. J. Pharmacol., vol. 78, no. 4, pp. 411-418, 1998.
[25] E. Anderson, “Oocyte differentiation and vitellogenesis in the roach Periplaneta americana,” Journal of Cell Biology, vol.20, pp.131-153, 1964.
[26] A. Itzen, and R.S. Goody, “GTPases involved in vesicular trafficking: structures and mechanisms,” Seminar of Cell and Developmantal Biology, vol.22, no.1, pp. 48-56, 2011.
[27] G. Dollar, E. Struckhoff, J. Michaud, and R.S. Cohen, “Rab11 polarization of the Drosophila oocyte: a novel link between membrane trafficking, microtubule organization, and oskar mRNA localization and translation,” Development, vol.129, pp. 517-526, 2002.
[28] X.B., Li, A.K., Satoh, and D.F., Ready. Myosin V, Rab11, and dRip11 direct apical secretion and cellular morphogenesis in developing Drosophila photoreceptors. J. Cell. Biol., vol.177, pp. 659-669, 2007.
[29] A.K. Satoh, F., Tokunaga, S., Kawamura, and K., Ozaki. In situ inhibition vesicle transport protein processing in the dominant negative Rab1 mutant of Drosophila. J. Cell Sci., vol. 110, pp. 2943-2953, 1997.
[30] K. M., Shetty, P., Kurada, and J.E., Otousa. Rab6 regulation rhodopsin transport in Drosophila. J. Biol. Chem., vol. 273, pp. 20425-20430, 1998.
[31] T., Wucherpfennig, M., Wilsch-Brauninger, and M., Gonzalez-Gaitan. Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J. Cell Biol., vol. 161, pp. 609-624, 2003.
[32] T. Uno, A. Nakao, and C. Katsurauma. Phosphorylation of Rab proteins from the brain of Bombyx mori. Arch. Insect Biochem. Physiol., vol. 57, pp. 68-77, 2004.
[33] T., Uno, T. Moriwaki, M. Nakamura, M. Matsubara, H. Yamagata, K., Kanamaru, and M. Takagi. Biochemical characterization of Rab proteins from Bombyx mori. Arch. Insect Biochem. Physiol. 2008 (doi: 10.1002/arch.20273).
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    Mohamed Elmogy, Azza M. Elgendy, Makio Takeda. (2014). Detection of Small GTP Binding Proteins Showing GTPase and GTP/ATP Binding Activities in the Ovary of the American Cockroach, Periplaneta Americana, during Oogenesis. American Journal of BioScience, 2(3), 106-110. https://doi.org/10.11648/j.ajbio.20140203.15

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    Mohamed Elmogy; Azza M. Elgendy; Makio Takeda. Detection of Small GTP Binding Proteins Showing GTPase and GTP/ATP Binding Activities in the Ovary of the American Cockroach, Periplaneta Americana, during Oogenesis. Am. J. BioScience 2014, 2(3), 106-110. doi: 10.11648/j.ajbio.20140203.15

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    AMA Style

    Mohamed Elmogy, Azza M. Elgendy, Makio Takeda. Detection of Small GTP Binding Proteins Showing GTPase and GTP/ATP Binding Activities in the Ovary of the American Cockroach, Periplaneta Americana, during Oogenesis. Am J BioScience. 2014;2(3):106-110. doi: 10.11648/j.ajbio.20140203.15

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  • @article{10.11648/j.ajbio.20140203.15,
      author = {Mohamed Elmogy and Azza M. Elgendy and Makio Takeda},
      title = {Detection of Small GTP Binding Proteins Showing GTPase and GTP/ATP Binding Activities in the Ovary of the American Cockroach, Periplaneta Americana, during Oogenesis},
      journal = {American Journal of BioScience},
      volume = {2},
      number = {3},
      pages = {106-110},
      doi = {10.11648/j.ajbio.20140203.15},
      url = {https://doi.org/10.11648/j.ajbio.20140203.15},
      eprint = {https://article.sciencepublishinggroup.com/pdf/10.11648.j.ajbio.20140203.15},
      abstract = {In the present study, the small GTP binding proteins involved in the regulatory mechanism of vitellogenin (Vg) endocytotic vesicles trafficking were detected, for the first time, in ovaries of the most basal hemimetabolus insect, Periplaneta americana during oogenesis. The ovarian GTPase activities were peaked during previtellogenic and early vitellogenic periods. Such activity coincides with vitellogenin receptors (VgRs) and clathrin early expression during these developmental periods, suggesting the importance of GTPases not only in the process of vesicle formation and fusion but also in the process of early fluid phase endocytosis. Two small peaks of activities were monitored during the late vitellogenic period (days 8 and 10), suggesting a possible role of GTPases in VgRs and clathrin recycling process. The [α32P]-GTP binding assay analysis in different tissues revealed the presence of small GTP binding proteins of molecular weights 25, 23 and 21 kDa in ovaries and head. However, a single binding signal band of 21 and 25 kDa was each detected in the fat bodies and muscles, respectively. No binding was detected in the midgut and Malpighian tubules. However, the 23 kDa protein detected was suggested as a probable cytosolic form of the 25 kDa protein. The competition assay results indicated that the small ovarian GTP binding proteins could also bind ATP, suggesting that like GTP, ATP is a regulatory nucleotide for the ovarian small proteins detected during oogenesis. The present study will pave the way for more understanding of the mechanisms that regulate Vg transport machinery in hemimetabolous insects.},
     year = {2014}
    }
    

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  • TY  - JOUR
    T1  - Detection of Small GTP Binding Proteins Showing GTPase and GTP/ATP Binding Activities in the Ovary of the American Cockroach, Periplaneta Americana, during Oogenesis
    AU  - Mohamed Elmogy
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    JF  - American Journal of BioScience
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    UR  - https://doi.org/10.11648/j.ajbio.20140203.15
    AB  - In the present study, the small GTP binding proteins involved in the regulatory mechanism of vitellogenin (Vg) endocytotic vesicles trafficking were detected, for the first time, in ovaries of the most basal hemimetabolus insect, Periplaneta americana during oogenesis. The ovarian GTPase activities were peaked during previtellogenic and early vitellogenic periods. Such activity coincides with vitellogenin receptors (VgRs) and clathrin early expression during these developmental periods, suggesting the importance of GTPases not only in the process of vesicle formation and fusion but also in the process of early fluid phase endocytosis. Two small peaks of activities were monitored during the late vitellogenic period (days 8 and 10), suggesting a possible role of GTPases in VgRs and clathrin recycling process. The [α32P]-GTP binding assay analysis in different tissues revealed the presence of small GTP binding proteins of molecular weights 25, 23 and 21 kDa in ovaries and head. However, a single binding signal band of 21 and 25 kDa was each detected in the fat bodies and muscles, respectively. No binding was detected in the midgut and Malpighian tubules. However, the 23 kDa protein detected was suggested as a probable cytosolic form of the 25 kDa protein. The competition assay results indicated that the small ovarian GTP binding proteins could also bind ATP, suggesting that like GTP, ATP is a regulatory nucleotide for the ovarian small proteins detected during oogenesis. The present study will pave the way for more understanding of the mechanisms that regulate Vg transport machinery in hemimetabolous insects.
    VL  - 2
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Author Information
  • Department of Entomology, Faculty of Science, Biotechnology program, Cairo University, Giza, Egypt; Department of Biology, Faculty of Applied Science, Umm Al-Qura University, Makkah, Saudi Arabia

  • Department of Entomology, Faculty of Science, Biotechnology program, Cairo University, Giza, Egypt

  • Insect Science Laboratory, Graduate School of Agricultural, Kobe University, Kobe, Japan

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