Molecular characterization, developmental expression and immunolocalization of clathrin heavy chain in the ovary of the American cockroach, Periplaneta americana during oogenesis

Authors

  • Mohamed Elmogy Department of Entomology, Faculty of Science, Biotechnology Program, Cairo University, Giza, Egypt.
  • Azza M. Elgendy Department of Entomology, Faculty of Science, Biotechnology Program, Cairo University, Giza, Egypt.
  • Wael M. Alamodi Department of Biology, Faculty of Applied Science, Umm Al-Qura University, Makkah, Saudi Arabia.
  • Makio Takeda Insect Science Laboratory, Graduate School of Science and Technology, Kobe University, Kobe, Japan.

Keywords:

Clathrin, Receptor-mediated endocytosis, Vitellogenin, Insect oocyte, Periplaneta americana

Abstract

Clathrin is the principal protein involved in receptor mediate endocytosis and the main component of the coated vesicles. It is composed of three identical clathrin heavy chains (CHC), each with an attached light chain. We characterized the deduced amino acid sequence of the partial cDNA clone of the American cockroach, Periplaneta americana (Pam) CHC. The analysis showed that this sequence is represented as multiple alpha helical repeats occurred in the arm region of the CHC and displayed a high level of identity and similarity to mosquitoes and Drosophila melanogaster CHCs. This is the first report on CHC from a hemimetabolous insect. The amplified CHC probe could hybridize two CHC transcripts in the current preparations, 6.3 kb and 7.3 kb. The Northern blot analysis confirmed that a 6.3 kb transcript is specifically expressed in ovarian tissues at high levels throughout the ovarian development, especially in previtellogenic ovaries (Days 1-4) but dropped during the vitellogenic period (days 5-7) and ultimately no transcript was detected in fully vitellogenic ovaries (days 9-13). Immunoblot analysis detected an ovary specific CHC protein of ~175 kDa that was present in previtellogenic ovaries on the day of female emergence and after initiation of vitellogenesis and onset of Vg uptake. Immunocytochemistry localized CHC protein to germ-line derived cells, oocytes, and revealed that CHC translation begins very early during oocyte differentiation in the germarium. The present work suggested a possible role for clathrin in the early fluid phase endocytosis (pinocytosis) in addition to its role in receptor-mediated endocytosis.

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References

Schneider, W.J. (1995). Yolk precursor transport in the laying hen. Curr. Opin. Lipidol., 6(2): 92–96. https://doi.org/10.1097/00041433-199504000-00006.

Jha, A., Watkins, S.C. & Traub, L.M. (2012). The apoptotic engulfment protein Ced-6 participates in clathrin-mediated yolk uptake in Drosophila egg chambers. Mol. Biol. Cell., 23(9): 1742–1764. https://doi.org/10.1091/mbc.E11-11-0939.

Raikhel, A.S. & Dhadialla, T.S. (1992). Accumulation of yolk proteins in insect oocytes. Annu. Rev. Entomol., 37: 217–251. https://doi.org/10.1146/annurev.en.37.010192.001245.

Richard, D.S., Gilbert, M., Crum, B., Hollinshead, D.M., Schelble, S. & Scheswohl, D. (2001). Yolk protein endocytosis by oocytes in Drosophila melanogaster: immunofluorescent localization of clathrin, adaptin and the yolk protein receptor. J. Insect Physiol., 47(7): 715–723. https://doi.org/10.1016/s0022-1910(00)00165-7.

Keen, J.H. (1990). Clathrin and associated assembly and disassembly proteins. Annu. Rev. Biochem., 59: 415–438. https://doi.org/10.1146/annurev.bi.59.070190.002215.

Pearse, B.M. (1988). Receptors compete for adaptors found in plasma membrane coated pits. EMBO J., 7(11): 3331–3336.

Sappington, T.W. & Raikhel, A.S. (1998). Molecular characteristics of insect vitellogenins and vitellogenin receptors. Insect Biochem. Mol. Biol., 28(5-6): 277–300. https://doi.org/10.1016/s0965-1748(97)00110-0.

Van-Antwerpen, R., Pham, D.Q.D. & Ziegler, R. (2005). Accumulation of lipids 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. pp. 265–288.

Richard, D.S., Jones, J.M., Barbarito, M.R., Cerula, S., Detweiler, J.P., Fisher, S.J., Brannigan, D.M. & Scheswohl, D.M. (2001). Vitellogenesis in diapausing and mutant Drosophila melanogaster: further evidence for the relative roles of ecdysteroids and juvenile hormones. J. Insect Physiol., 47(8): 905–913. https://doi.org/10.1016/S0022-1910(01)00063-4.

Kokoza, V.A. & Raikhel, A.S. (1997). Ovarian- and somatic-specific transcripts of the mosquito clathrin heavy chain gene generated by alternative 5'-exon splicing and polyadenylation. J. Biol. Chem., 272(2): 1164–1170. https://doi.org/10.1074/jbc.272.2.1164.

Kokoza, V.A., Snigirevskaya, E.S. & Raikhel, A.S. (1997). Mosquito clathrin heavy chain: analysis of protein structure and developmental expression in the ovary during vitellogenesis. Insect Mol. Biol., 6(4): 357–368. https://doi.org/10.1046/j.1365-2583.1997.00191.x.

Tufail, M., Lee, J.M., Hatakeyama, M., Oishi, K. & Takeda, M. (2000). Cloning of vitellogenin cDNA of the American cockroach, Periplaneta americana (Dictyoptera), and its structural and expression analyses. Arch. Insect Biochem. Physiol., 45(1): 37–46. https://doi.org/10.1002/1520-6327(200009)45:1<37::AID-ARCH4>3.0.CO;2-8.

Tufail, M., Hatakeyama, M. & Takeda, M. (2001). Molecular evidence for two vitellogenin genes and processing of vitellogenins in the American cockroach, Periplaneta americana. Arch. Insect Biochem. Physiol., 48(2): 72–80. https://doi.org/10.1002/arch.1059.

Tufail, M., Raikhel, A.S. & Takeda, M. (2005). Biosynthesis and processing of insect vitellogenins. 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. pp. 1–32.

Tufail, M. & Takeda, M. (2005). Molecular cloning, characterization and regulation of the cockroach vitellogenin receptor during oogenesis. Insect Mol. Biol., 14: 389–401.

Tufail, M. & Takeda, M. (2008). Molecular characteristics of insect vitellogenins. J. Insect Physiol., 54(12): 1447–1458. https://doi.org/10.1016/j.jinsphys.2008.08.007.

Elgendy, A.M., Elmogy, M., Tufail, M. & Takeda, M. (2009). Developmental expression profile of cockroach vitellogenin genes Vg1 and 2. Animal Biol. J., 1: 39-48.

Laemmli, U.K. (1970). Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4. Nature, 227: 680–685. https://doi.org/10.1038/227680a0.

Liu, S.-H., Wong, M.L., Craik, C.S. & Brodsky, F.M. (1995). Regulation of clathrin assembly and trimerization defined using recombinant triskelion hubs. Cell, 83(2): 257–267. https://doi.org/10.1016/0092-8674(95)90167-1.

Koller, C.N., Dhadialla, T.S. & Raikhel, A.S. (1989). Selective endocytosis of vitellogenin by oocytes of the mosquito, Aedes aegypti: An in vitro study. Insect Biochem., 19(7): 693–702. https://doi.org/10.1016/0020-1790(89)90106-6.

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Published

2012-10-01

How to Cite

Elmogy, M., Elgendy, A. M., Alamodi, W. M., & Takeda, M. (2012). Molecular characterization, developmental expression and immunolocalization of clathrin heavy chain in the ovary of the American cockroach, Periplaneta americana during oogenesis. Advances in BioScience, 3(4), 313–318. Retrieved from https://journals.sospublication.co.in/ab/article/view/104

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Vol. 3 No. 4 (2012): October

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