Display options
Share it on

Mol Reprod Dev. 2022 Jan 12; doi: 10.1002/mrd.23555. Epub 2022 Jan 12.

Open questions on the functional biology of the yolk granules during embryo development.

Molecular reproduction and development

Isabela Ramos, Ednildo Machado, Hatisaburo Masuda, Fabio Gomes

Affiliations

  1. Instituto de Bioquímica Médica Leopoldo de Meis, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.
  2. Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular - INCT-EM/CNPq, Rio de Janeiro, Brazil.
  3. Instituto de Biofísica Carlos Chagas Filho (IBCCF), Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.

PMID: 35020238 DOI: 10.1002/mrd.23555

Abstract

Biogenesis and consumption of the yolk are well-conserved aspects of the reproductive biology in oviparous species. Most egg-laying animals accumulate yolk proteins within the oocytes thus creating the source of nutrients and energy that will feed embryo development. Yolk accumulation drives the generation of a highly specialized oocyte cytoplasm with maternal mRNAs, ribosomes, mitochondria, and, mainly, a set of organelles collectively referred to as yolk granules (Ygs). Following fertilization, the Ygs are involved in regulated mechanisms of yolk degradation to fuel the anabolic metabolism of the growing embryo. Thus, yolk accumulation and degradation are essential processes that allow successful development in many species. Nevertheless, the molecular machinery and mechanisms dedicated to the programmed yolk mobilization throughout development are still enigmatic and remain mostly unexplored. Moreover, while the Ygs functional biology as a nutritional source for the embryo has been acknowledged, several reports have suggested that Ygs cargoes and functions go far beyond yolk storage. Evidence of the role of Ygs in gene expression, microbiota harboring, and paracrine signaling has been proposed. In this study, we summarize the current knowledge of the Ygs functional biology pointing to open questions and where further investigation is needed.

© 2022 Wiley Periodicals LLC.

Keywords: development; oogenesis; yolk granules

References

  1. Abreu, L. A., Valle, D., Manso, P. P., Facanha, A. R., Pelajo-Machado, M., Masuda, H., Masuda, A., Vaz, Jr., I., Lenzi, H., Oliveira, P. L., & Logullo, C. (2004). Proteolytic activity of Boophilus microplus Yolk pro-Cathepsin D (BYC) is coincident with cortical acidification during embryogenesis. Insect Biochemistry and Molecular Biology, 34(5), 443-449. - PubMed
  2. Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K., & Walter, P. (2002). Molecular biology of the cell (4th ed.). Garland Science. - PubMed
  3. Anderson, K. L., & Woodruff, R. I. (2001). A gap junctionally transmitted epithelial cell signal regulates endocytic yolk uptake in Oncopeltus fasciatus. Developmental Biology, 239(1), 68-78. https://doi.org/10.1006/dbio.2001.0433 - PubMed
  4. Baltus, E., Hanocq-Quertier, J., & Brachet, J. (1968). Isolation of deoxyribonucleic acid from the yolk platelets of Xenopus laevis oöcyte. Proceedings of the National Academy of Sciences of the United States of America, 61(2), 469. - PubMed
  5. Bownes, M. (1982). Hormonal and genetic regulation of vitellogenesis in Drosophila. The Quarterly Review of Biology, 57(3), 247-274. https://doi.org/10.1086/412802 - PubMed
  6. Bownes, M. (1990). The yolk proteins and their genes in Drosophila. Progress in Clinical and Biological Research, 342, 336-342. - PubMed
  7. Bownes, M. (1994). Mary Bownes-The regulation of the yolk protein genes, a family of sex differentiation genes in Drosophila melanogaster. BioEssays, 16(10), 745-752. https://doi.org/10.1002/bies.950161009 - PubMed
  8. Bownes, M., Shirras, A., Blair, M., Collins, J., & Coulson, A. (1988). Evidence that insect embryogenesis is regulated by ecdysteroids released from yolk proteins. Proceedings of the National Academy of Sciences United States of America, 85(5), 1554-1557. https://doi.org/10.1073/pnas.85.5.1554 - PubMed
  9. Brawand, D., Wahli, W., & Kaessmann, H. (2008). Loss of egg yolk genes in mammals and the origin of lactation and placentation. PLoS Biology, 6(3), 0507-0517. https://doi.org/10.1371/journal.pbio.0060063 - PubMed
  10. Brooks, R. A., & Woodruff, R. I. (2004). Calmodulin transmitted through gap junctions stimulates endocytic incorporation of yolk precursors in insect oocytes. Developmental Biology, 271(2), 339-349. - PubMed
  11. Brown, M. R., & Kornberg, A. (2004). Inorganic polyphosphate in the origin and survival of species. Proceedings of the National Academy of Sciences of the United States of America, 101(46), 16085-16087. - PubMed
  12. Bruce, L., & Emanuelsson, H. (1975). Analysis of DNA isolated from intracellular yolk granules in the early chick blastoderm. Experimental Cell Research, 92(2), 462-466. https://doi.org/10.1016/0014-4827(75)90402-4 - PubMed
  13. Campos, E., Facanha, A. R., Costa, E. P., da Silva Vaz, I. J., Masuda, A., & Logullo, C. (2008). Exopolyphosphatases in nuclear and mitochondrial fractions during embryogenesis of the hard tick Rhipicephalus (Boophilus) microplus. Comparative Biochemistry and Physiology, Part B: Biochemistry & Molecular Biology, 151(3), 311-316. https://doi.org/10.1016/j.cbpb.2008.07.013 - PubMed
  14. Campos, E., Facanha, A. R., Costa, E. P., Fraga, A., Moraes, J., da Silva Vaz, I. J., Masuda, A., & Logullo, C. (2011). A mitochondrial membrane exopolyphosphatase is modulated by, and plays a role in, the energy metabolism of hard tick Rhipicephalus (Boophilus) microplus embryos. International Journal of Molecular Sciences, 12(6), 3525-3535. https://doi.org/10.3390/ijms12063525 - PubMed
  15. Chestkov, V. V., Radko, S. P., Cho, M. S., Chrambach, A., & Vogel, S. S. (1998). Reconstitution of calcium-triggered membrane fusion using “reserve” granules. Journal of Biological Chemistry, 273(4), 2445-2451. - PubMed
  16. Cho, W. L., Deitsch, K. W., & Raikhel, A. S. (1991). An extraovarian protein accumulated in mosquito oocytes is a carboxypeptidase activated in embryos. Proceedings of the National Academy of Sciences of the United States of America, 88(23), 10821-10824. - PubMed
  17. Cho, W. L., Tsao, S. M., Hays, A. R., Walter, R., Chen, J. S., Snigirevskaya, E. S., & Raikhel, A. S. (1999). Mosquito cathepsin B-like protease involved in embryonic degradation of vitellin is produced as a latent extraovarian precursor. Journal of Biological Chemistry, 274(19), 13311-13321. - PubMed
  18. Cruz, C. S., Costa, E. P., Machado, J. A., Silva, J. N., Romeiro, N. C., Moraes, J., Silva, J. R., Fonseca, R. N., Vaz, I. S. J., Logullo, C., & Campos, E. (2018). A soluble inorganic pyrophosphatase from the cattle tick Rhipicephalus microplus capable of hydrolysing polyphosphates. Insect Molecular Biology, 27(2), 260-267. https://doi.org/10.1111/imb.12369 - PubMed
  19. Docampo, R., de Souza, W., Miranda, K., Rohloff, P., & Moreno, S. N. (2005). Acidocalcisomes-Conserved from bacteria to man. Nature Reviews Microbiology, 3(3), 251-261. - PubMed
  20. Hadorn, E., & Muller, G. (1974). Has the yolk an influence on the differentiation of embryonic Drosophila blastemas? Wilhelm Roux' Archiv für Entwicklungsmechanik der Organismen. 174, 333-335. - PubMed
  21. Ezquieta, B., & Vallejo, C. G. (1986). Lipovitellin inhibition of Artemia trypsin-like proteinase: A role for a storage protein in regulating proteinase activity during development. Archives of Biochemistry and Biophysics, 250(2), 410-417. https://doi.org/10.1016/0003-9861(86)90743-5 - PubMed
  22. Fagotto, F. (1990). Yolk degradation in tick eggs: I. Occurrence of a cathepsin L-like acid proteinase in yolk spheres. Archives of Insect Biochemistry and Physiology, 14(4), 217-235. - PubMed
  23. Fagotto, F. (1991). Yolk degradation in tick eggs: III Developmentally regulated acidification of yolk spheres. Development Growth and Difference, 33, 57-66. - PubMed
  24. Fagotto, F. (1995). Regulation of yolk degradation, or how to make sleepy lysosomes. Journal of Cell Science, 108(Pt 1), 3645-3647. - PubMed
  25. Fagotto, F., & Maxfield, F. R. (1994a). Changes in yolk platelet pH during Xenopus laevis development correlate with yolk utilization. A quantitative confocal microscopy study. Journal of Cell Science, 107(Pt 1), 3325-3337. - PubMed
  26. Fagotto, F., & Maxfield, F. R. (1994b). Yolk platelets in Xenopus oocytes maintain an acidic internal pH which may be essential for sodium accumulation. Journal of Cell Biology, 125(5), 1047-1056. https://doi.org/10.1083/jcb.125.5.1047 - PubMed
  27. Fausto, A. M., Gambellini, G., Mazzini, M., Cecchettini, A., Masetti, M., & Giorgi, F. (2001). Yolk granules are differentially acidified during embryo development in the stick insect Carausius morosus. Cell and Tissue Research, 305(3), 433-443. https://doi.org/10.1007/s004410100392 - PubMed
  28. Ferenz, H.-J. (1990). Receptor-mediated endocytosis of insect yolk proteins. In H. H. Hagedorn, J. G. Hildebrand, M. G. Kidwell, & J. H. Law (Eds.), Molecular insect science (pp. 131-138). Springer. https://doi.org/10.1007/978-1-4899-3668-4_16 - PubMed
  29. Fialho, E., Nakamura, A., Juliano, L., Masuda, H., & Silva-Neto, M. A. (2005). Cathepsin D-mediated yolk protein degradation is blocked by acid phosphatase inhibitors. Archives of Biochemistry and Biophysics, 436(2), 246-253. - PubMed
  30. Fialho, E., Silveira, A. B., Masuda, H., & Silva-Neto, M. A. (2002). Oocyte fertilization triggers acid phosphatase activity during Rhodnius prolixus embryogenesis. Insect Biochemistry and Molecular Biology, 32(8), 871-880. - PubMed
  31. Gilbert, L. I. (2004). Halloween genes encode P450 enzymes that mediate steroid hormone biosynthesis in Drosophila melanogaster. Molecular and Cellular Endocrinology, 215(1-2), 1-10. https://doi.org/10.1016/j.mce.2003.11.003 - PubMed
  32. Gilbert, S. F., & Barresi, M. J. F. (2018). Developmental biology (11th ed.). Sinauer Associates, Inc. - PubMed
  33. Gomes, F. M., Oliveira, D. M. P., Motta, L. S., Ramos, I. B., Miranda, K. M., & Machado, E. a (2010). Inorganic polyphosphate inhibits an aspartic protease-like activity in the eggs of Rhodnius prolixus (Stahl) and impairs yolk mobilization in vitro. Journal of Cellular Physiology, 222(3), 606-611. https://doi.org/10.1002/jcp.21975 - PubMed
  34. Gomes, F. M., Ramos, I. B., Motta, L. M., Miranda, K., Santiago, M. F., de Souza, W., & Machado, E. A. (2008). Polyphosphate polymers during early embryogenesis of Periplaneta americana. Journal of Insect Physiology, 54(12), 1459-1466. https://doi.org/10.1016/j.jinsphys.2008.07.018 - PubMed
  35. Gomes, F. M., Ramos, I. B., Araujo, H., Miranda, K., & Ednildo, E. A. (2016). Inorganic polyphosphate functions and metabolism in insects. In T. Kulakovskaya, E. Pavlov, & E. N. Dedkova (Eds.), Inorganic polyphosphates in eukaryotic cells (pp. 123-138). Springer International Publishing. https://doi.org/10.1007/978-3-319-41073-9_9 - PubMed
  36. Grieneisen, M. L. (1994). Recent advances in our knowledge of ecdysteroid biosynthesis in insects and crustaceans. Insect Biochemistry and Molecular Biology, 24(2), 115-132. https://doi.org/10.1016/0965-1748(94)90078-7 - PubMed
  37. Guo, Y., Hoffmann, A. A., Xu, X. Q., Mo, P. W., Huang, H. J., Gong, J. T., Ju, J. F., & Hong, X. Y. (2018). Vertical transmission of Wolbachia is associated with host vitellogenin in Laodelphax striatellus. Frontiers in Microbiology, 9, 1-12. https://doi.org/10.3389/fmicb.2018.02016 - PubMed
  38. Hammer, T. J., & Moran, N. A. (2019). Links between metamorphosis and symbiosis in holometabolous insects. Philosophical Transactions of the Royal Society B, 374(1783), 20190068. - PubMed
  39. Hanocq, F., Kirsch-Volders, M., Hanocq-Quertier, J., Baltus, E., & Steinert, G. (1972). Characterization of yolk DNA from Xenopus laevis oocytes ovulated in vitro. Proceedings of the National Academy of Sciences of the United States of America, 69(5), 1322-1326. https://doi.org/10.1073/pnas.69.5.1322 - PubMed
  40. Herren, J. K., Paredes, J. C., Schüpfer, F., & Lemaitre, B. (2013). Vertical transmission of a Drosophila endosymbiont via cooption of the yolk transport and internalization machinery. MBio, 4(2), 1-8. https://doi.org/10.1128/mBio.00532-12 - PubMed
  41. Honjin, R., & Nakamura, T. (1967). A refinement of the values of the lattice parameters in the crystal structure of amphibian fresh yolk platelets by X-ray crystallography. Journal of Ultrasructure Research, 20(5-6), 400-409. https://doi.org/10.1016/S0022-5320(67)80108-4 - PubMed
  42. Honjin, R., Nakamura, T., & Shimasak, S. (1965). X-ray diffraction and electron microscopic studies on crystalline lattice structure of amphibian yolk platelets. Journal of Ultrastructure Research, 12(3-4), 404-419. - PubMed
  43. Jayasankar, V., Tomy, S., & Wilder, M. N. (2020). Insights on molecular mechanisms of ovarian development in decapod crustacea: Focus on vitellogenesis-stimulating factors and pathways. Frontiers in Endocrinology, 11, 577925. https://doi.org/10.3389/fendo.2020.577925 - PubMed
  44. Kageyama, T., Takahashi, S. Y., & Takahashi, K. (1981). Occurrence of thiol proteinases in the eggs of the silkworm, Bombyx mori. Journal of Biochemistry, 90(3), 665-671. https://doi.org/10.1093/oxfordjournals.jbchem.a133521 - PubMed
  45. Karasaki, S. (1967). An electron microscope study on crystalline stucture of yolk platelets of lamprey egg. Journal of Ultrastructure Research, 18(3-4), 377. https://doi.org/10.1016/S0022-5320(67)80125-4 - PubMed
  46. Karasaki, S., & Komoda, T. (1958). Electron micrographs of a crystalline lattice structure in yolk platelets of the amphibian embryo. Nature, 4506, 407-408. - PubMed
  47. Kaur, R., Shropshire, J. D., Cross, K. L., Leigh, B., Mansueto, A. J., Stewart, V., Bordenstein, S. R., & Bordenstein, S. R. (2021). Living in the endosymbiotic world of Wolbachia: A centennial review. Cell Host and Microbe, 29(6), 879-893. https://doi.org/10.1016/j.chom.2021.03.006 - PubMed
  48. Kelley, R. O., Nakai, G. S., & Guganig, M. E. (1971). A biochemical and ultrastructural study of RNA in yolk platelets of Xenopus gastrulae. Journal of Embryology and Experimental Morphology, 26(2), 181-193. http://www.ncbi.nlm.nih.gov/pubmed/5168215 - PubMed
  49. Kornberg, A. (1995). Inorganic polyphosphate: Toward making a forgotten polymer unforgettable. Journal of Bacteriology, 177(3), 491-496. - PubMed
  50. Kornberg, A. (1999). Inorganic polyphosphate: A molecule of many functions. Progress in Molecular and Subcellular Biology, 23, 1-18. - PubMed
  51. Krishna, P., Kennedy, B. P., Van De Sande, J. H., & McGhee, J. D. (1988). Yolk proteins from nematodes, chickens, and frogs bind strongly and preferentially to left-handed Z-DNA. Journal of Biological Chemistry, 263(35), 19066-19070. - PubMed
  52. Kulakovskaya, T., Pavlov, E., & Dedkova, E. N. (2016). Inorganic polyphosphates in eukaryotic cells. Inorganic Polyphosphates in Eukaryotic Cells, 1, 1-243. https://doi.org/10.1007/978-3-319-41073-9 - PubMed
  53. Lange, R. H. (1982). The lipoprotein crystals of cyclostome yolk platelets (Myxine glutinosa L., Lampetra planeri [Bloch], L. fluviatilis [L.]). Journal of Ultrasructure Research, 79(1), 1-17. https://doi.org/10.1016/S0022-5320(82)90048-X - PubMed
  54. Lange, R. H., Richter, H. P., Riehl, R., Zierold, K., Trandaburu, T., & Magdowski, G. (1983). Lipovitellin-phosvitin crystals with orthorhombic features: Thin-section electron microscopy, gel electrophoresis, and microanalysis in teleost and amphibian yolk platelets and a comparison with other vertebrates. Journal of Ultrasructure Research, 83(2), 122-140. https://doi.org/10.1016/S0022-5320(83)90070-9 - PubMed
  55. Lee, H. S., Lee, B. C., & Kang, D. I. (2013). Spontaneous self-assembly of DNA fragments into nucleus-like structures from yolk granules of fertilized chicken eggs: Antoine béchamp meets bong han kim via olga lepeshinskaya. Micron, 51, 54-59. https://doi.org/10.1016/j.micron.2013.06.009 - PubMed
  56. Li, H., & Zhang, S. (2017). Functions of vitellogenin in eggs. In M. Kloc (Ed.), Oocytes: Maternal information and functions (pp. 389-401). Springer International Publishing. https://doi.org/10.1007/978-3-319-60855-6_17 - PubMed
  57. Liao, Y.-D., & Wang, J.-J. (1994). Yolk granules are the major compartment for bullfrog (Rana catesbeiana) oocyte-specific ribonuclease. European Journal of Biochemistry, 222(1), 215-220. https://doi.org/10.1111/j.1432-1033.1994.tb18859.x - PubMed
  58. Mallya, S. K., Partin, J. S., Valdizan, M. C., & Lennarz, W. J. (1992). Proteolysis of the major yolk glycoproteins is regulated by acidification of the yolk platelets in sea urchin embryos. Journal of Cell Biology, 117(6), 1211-1221. - PubMed
  59. Masson, F., Calderon-Copete, S., Schüpfer, F., Vigneron, A., Rommelaere, S., Garcia-Arraez, M. G., Paredes, J. C., & Lemaitre, B. (2020). Blind killing of both male and female Drosophila embryos by a natural variant of the endosymbiotic bacterium Spiroplasma poulsonii. Cellular Microbiology, 22(5), 1-12. https://doi.org/10.1111/cmi.13156 - PubMed
  60. McNeil, P. L., Vogel, S. S., Miyake, K., & Terasaki, M. (2000). Patching plasma membrane disruptions with cytoplasmic membrane. Journal of Cell Science, 113(Pt 1), 1891-1902. - PubMed
  61. Medina, M., & Vallejo, C. G. (1989). The maternal origin of acid hydrolases in Drosophila and their relation with yolk degradation: (Drosophila/acid hydrolases/developmental regulation/yolk degradation/mitochondria). Development, Growth & Differentiation, 31(3), 241-247. https://doi.org/10.1111/j.1440-169X.1989.00241.x - PubMed
  62. Morgan, A. J. (2011). Sea urchin eggs in the acid reign. Cell Calcium, 50(2), 147-156. https://doi.org/10.1016/j.ceca.2010.12.007 - PubMed
  63. Motta, C. M., Tammaro, S., Cicale, A., Indolfi, P., Iodice, C., Spagnuolo, M. S., & Filosa, S. (2001). Storage in the yolk platelets of low MW DNA produced by the regressing follicle cells. Molecular Reproduction and Development, 59(4), 422-430. https://doi.org/10.1002/mrd.1049 - PubMed
  64. Motta, L. S., da Silva, W. S., Oliveira, D. M., de Souza, W., & Machado, E. A. (2004). A new model for proton pumping in animal cells: The role of pyrophosphate. Insect Biochemistry and Molecular Biology, 34(1), 19-27. - PubMed
  65. Motta, L. S., Ramos, I. B., Gomes, F. M., de Souza, W., Champagne, D. E., Santiago, M. F., Docampo, R., Miranda, K., & Machado, E. A. (2009). Proton-pyrophosphatase and polyphosphate in acidocalcisome-like vesicles from oocytes and eggs of Periplaneta americana. Insect Biochemistry and Molecular Biology, 39(3), 198-206. https://doi.org/10.1016/j.ibmb.2008.11.003 - PubMed
  66. Niki, Y. (1988). Ultrastructural study of the sex ratio organism(SRO) transmission into oocytes during oogenesis in Drosophila melanogaster. The Japanese Journal of Genetics, 63(1), 11-21. https://doi.org/10.1266/jjg.63.11 - PubMed
  67. Niwa, R., & Niwa, Y. S. (2014). Enzymes for ecdysteroid biosynthesis: Their biological functions in insects and beyond. Bioscience, Biotechnology, and Biochemistry, 78(8), 1283-1292. https://doi.org/10.1080/09168451.2014.942250 - PubMed
  68. Nordin Beaudoin, E. L., & Lin, X. (1991). Acidification of yolk granules in Blatella germanica eggs coincides with proteolytic processing of vitellin. Insect Biochemistry, 18, 177-192. - PubMed
  69. Nussenzveig, R. H., Oliveira, P. L., & Masuda, H. (1992). Identification of yolk platelet-associated hydrolases in the oocytes of Rhodnius prolixus. Archives of Insect Biochemistry and Physiology, 21(4), 253-262. - PubMed
  70. Ohlendorf, D. H., Barbarash, G. R., Trout, A., & Leonard, J. (1992). Lipid and polypeptide components system from Xenopus laevis. American Society of Biological Chemists, 252, 7992-8001. - PubMed
  71. Oliveira, D. M., & Machado, E. A. (2006). Characterization of a tyrosine phosphatase activity in the oogenesis of Periplaneta americana. Archives of Insect Biochemistry and Physiology, 63(1), 24-35. - PubMed
  72. Opresko, L., Wiley, H. S., & Wallace, R. A. (1979). The origin of yolk-DNA in Xenopus laevis. Journal of Experimental Zoology, 209(3), 367-376. https://doi.org/10.1002/jez.1402090303 - PubMed
  73. Pasteels, J. J. (1966). Les corps multivesiculaires de l'oeuf de Barnea candida (Mollusque bivalve) etudies au microscope electronique. Activite phosphatasique et accumulation du rouge neutre. Journal of Embryology and Experimental Morphology, 16, 301-310. - PubMed
  74. Perez, M. F., & Lehner, B. (2019). Vitellogenins-Yolk gene function and regulation in Caenorhabditis elegans. Frontiers in Physiology, 10, 1067. https://www.frontiersin.org/article/10.3389/fphys.2019.01067 - PubMed
  75. Perry, M. M., & Gilbert, A. B. (1979). Yolk transport in the ovarian follicle of the hen (Gallus domesticus): Lipoprotein-like particles at the periphery of the oocyte in the rapid growth phase. Journal of Cell Science, 39, 257-272. - PubMed
  76. Polzonetti-Magni, A. M., Mosconi, G., Soverchia, L., Kikuyama, S., & Carnevali, O. (2004). Multihormonal control of vitellogenesis in lower vertebrates. International Review of Cytology, 239, 1-46. https://doi.org/10.1016/S0074-7696(04)39001-7 - PubMed
  77. Postlethwait, J. H., & Giorgi, F. (1985). Vitellogenesis in insects. Developmental Biology (N Y 1985), 1, 85-126. - PubMed
  78. Prowse, T. A., & Byrne, M. (2012). Evolution of yolk protein genes in the Echinodermata. Evolution and Development, 14(2), 139-151. https://doi.org/10.1111/j.1525-142X.2012.00531.x - PubMed
  79. Purcell, J., Quinn, T., & Nordin, J. (1988). Correlation of yolk phosphates expression with the programed proteolysis of vitellin in Blatella germanica during embryonic development. Archives of Insect Biochemistry and Physiology, 9, 237-251. - PubMed
  80. Raikhel, A. S., & Dhadialla, T. S. (1992). Accumulation of yolk proteins in insect oocytes. Annual Review of Entomology, 37(1), 217-251. https://doi.org/10.1146/annurev.en.37.010192.001245 - PubMed
  81. Raikhel, A. S., Dhadialla, T. S., Cho, W.-L., Hays, A. R., & Koller, C. N. (1990a). Biosynthesis and endocytosis of yolk proteins in the mosquito. In H. H. Hagedorn, J. G. Hildebrand, M. G. Kidwell, & J. H. Law (Eds.), Molecular insect science (pp. 147-154). Springer. https://doi.org/10.1007/978-1-4899-3668-4_18 - PubMed
  82. Ramos, I. B., Gomes, F., Koeller, C. M., Saito, K., Heise, N., Masuda, H., Docampo, R., de Souza, W., Machado, E. A., & Miranda, K. (2011). Acidocalcisomes as calcium- and polyphosphate-storage compartments during embryogenesis of the insect Rhodnius prolixus Stahl. PLoS ONE, 6(11), e27276. https://doi.org/10.1371/journal.pone.0027276 - PubMed
  83. Ramos, I. B., Miranda, K., de Souza, W., & Machado, E. A. (2006). Calcium-regulated fusion of yolk granules during early embryogenesis of Periplaneta americana. Molecular Reproduction and Development, 73(10), 1247-1254. - PubMed
  84. Ramos, I. B., Miranda, K., de Souza, W., Oliveira, D. M. P., Lima, P. C. A, Sorgine, M. H. F., & Machado, E. A (2007). Calcium-regulated fusion of yolk granules is important for yolk degradation during early embryogenesis of Rhodnius prolixus Stahl. The Journal of Experimental Biology, 210(Pt 1), 138-148. https://doi.org/10.1242/jeb.02652 - PubMed
  85. Ramos, I. B., Miranda, K., Pace, D. A., Verbist, K. C., Lin, F. Y., Zhang, Y., Oldfield, E., Machado, E. A., de Souza, W., & Docampo, R. (2010). Calcium and polyphosphate-containing acidic granules of sea urchin eggs are similar to acidocalcisomes but are not the targets for NAADP. Biochemical Journal, 429, 485-495. - PubMed
  86. Ramos, I. B., Miranda, K., Ulrich, P., Ingram, P., LeFurgey, A., Machado, E. A., de Souza, W., & Docampo, R. (2010). Calcium- and polyphosphate-containing acidocalcisomes in chicken egg yolk. Biology of the Cell, 102(7), 421-434. - PubMed
  87. Redshaw, M. R., & Follett, B. K. (1971). The crystalline yolk-platelet proteins and their soluble plasma precursor in an amphibian, Xenopus laevis. The Biochemical Journal, 124(4), 759-766. https://doi.org/10.1042/bj1240759 - PubMed
  88. Ribolla, P. E., Bijovsky, A. T., & de Bianchi, A. G. (2001). Procathepsin and acid phosphatase are stored in Musca domestica yolk spheres. Journal of Insect Physiology, 47(3), 225-232. - PubMed
  89. 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. Journal of Insect Physiology, 47(7), 715-723. https://doi.org/10.1016/S0022-1910(00)00165-7 - PubMed
  90. Roth, T. F., Cutting, J. A., & Atlas, S. B. (1976). Protein transport: A selective membrane mechanism. Journal of Supramolecular Structure, 4(4), 527-548. - PubMed
  91. Roth, T., & Porter, K. (1964). Yolk protein uptake in the oocyte of the mosquito Aedes aegyptI. L. The Journal of Cell Biology, 20, 313-332. - PubMed
  92. Roy, S., Saha, T. T., Zou, Z., & Raikhel, A. S. (2018a). Regulatory pathways controlling female insect reproduction. Annual Review of Entomology, 63, 489-511. https://doi.org/10.1146/annurev-ento-020117-043258 - PubMed
  93. Roy, S., Saha, T. T., Zou, Z., & Raikhel, A. S. (2018b). Regulatory pathways controlling female insect reproduction. Annual Review of Entomology, 63, 489-511. https://doi.org/10.1146/annurev-ento-020117-043258 - PubMed
  94. Sappington, T. W., & Raikhel, A. S. (1998). Molecular characteristics of insect vitellogenins and vitellogenin receptors. Insect Biochemistry and Molecular Biology, 28(5-6), 277-300. https://doi.org/10.1016/s0965-1748(97)00110-0 - PubMed
  95. Schneider, W. J. (1996). Vitellogenin receptors: Oocyte-specific members of the low-density lipoprotein receptor supergene family. International Review of Cytology, 166, 103-137. https://doi.org/10.1016/S0074-7696(08)62507-3 - PubMed
  96. Takahashi, S. Y., Zhao, X., Kageyamaj, T., & Yamamoto, Y. (1992). Interferon and natural killer cell activity in patients with exanthem subitum. The Pediatric Infectious Disease Journal, 22(4), 369-377. - PubMed
  97. Takahashi, S. Y., Zhao, X., & Watabe, S. (1996). Bombyx acid cysteine proteinase. International Journal of Invertebrates Reproduction and Development, 30, 265-281. - PubMed
  98. Telfer, W. H. (1954). Immunological studies of insect metamorphosis: II. The role of a sex-limited blood protein in egg formation by the cecropia silkworm. The Journal of General Physiology, 37(4), 539-558. - PubMed
  99. Tufail, M., & Takeda, M. (2008). Molecular characteristics of insect vitellogenins. Journal of Insect Physiology, 54(12), 1447-1458. https://doi.org/10.1016/j.jinsphys.2008.08.007 - PubMed
  100. Wallace, R. A. (1985). Vitellogenesis and oocyte growth in nonmammalian vertebrates. Developmental Biology, 1, 127-177. https://doi.org/10.1007/978-1-4615-6814-8_3 - PubMed
  101. Wallace, R. A., & Karasaki, S. (1963). Studies on amphibian yolk. 2. The isolation of yolk platelets from the eggs of Rana pipiens. The Journal of Cell Biology, 18(14), 153-166. - PubMed
  102. Werren, J. H., Baldo, L., & Clark, M. E. (2008). Wolbachia: Master manipulators of invertebrate biology. Nature Reviews Microbiology, 6(10), 741-751. https://doi.org/10.1038/nrmicro1969 - PubMed
  103. Wu, Z., Yang, L., He, Q., & Zhou, S. (2021). Regulatory mechanisms of vitellogenesis in insects. Frontiers in Cell and Developmental Biology, 8, 1-11. https://doi.org/10.3389/fcell.2020.593613 - PubMed
  104. Yamada, R., Yamahama, Y., & Sonobe, H. (2005). Release of ecdysteroid-phosphates from egg yolk granules and their dephosphorylation during early embryonic development in silkworm, Bombyx mori. Zoological Science, 22(2), 187-198. https://doi.org/10.2108/zsj.22.187 - PubMed
  105. Yamahama, Y., Uto, N., Tamotsu, S., Miyata, T., Yamamoto, Y., Watabe, S., & Takahashi, S. Y. (2003). In vivo activation of pro-form Bombyx cysteine protease (BCP) in silkmoth eggs: Localization of yolk proteins and BCP, and acidification of yolk granules. Journal of Insect Physiology, 49(2), 131-140. - PubMed

Publication Types

Grant support