Receptor-Mediated Endocytosis of Insect Yolk Proteins

Ferenz, Hans‐Jörg

doi:10.1007/978-1-4899-3668-4_16

Cited by 14 publications

(7 citation statements)

References 29 publications

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“…Our data indicate that all three YPPs are labeled along the oocyte surface and within the endocytotic vesicles. Within the oocyte, these proteins clearly follow the pathway of receptor-mediated endocytosis, which is characteristic of oocytes of oviparous animals (Ferenz 1990(Ferenz , 1993Schneider 1992;Yoshizaki 1992; and somatic cells (Dini et al 1992;Kimura et al 1992;Segretain et al 1992;Bu and Schwartz 1994). In mosquito oocytes, all three ligands (Vg, VCP, 44KP) are bound to microdomains of the oocyte plasma membrane, located at the base and between microvilli and internalized by the oocyte via coated pits/coated vesicles.…”

Section: Discussionmentioning

confidence: 97%

Secretory and internalization pathways of mosquito yolk protein precursors

Snigirevskaya

Hays

Raikhel

1997

Cell and Tissue Research

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The vitellogenic female fat body of the mosquito Aedes aegypti produces three yolk protein precursors that are deposited in the yolk bodies of developing oocytes: vitellogenin, vitellogenic carboxypeptidase (VCP), and 44-kDa protein (44KP). We have used gold immunocytochemistry to investigate the pathways of their secretion in fat body trophocytes and their internalization by oocytes. In fat body trophocytes, all three yolk protein precursors are co-localized in the Golgi complex and secretory granules, indicating that they proceed simultaneously through the secretory pathway. The lysosomal system plays an important role in the termination of vitellogenesis in mosquito trophocytes, by degrading biosynthetic organelles and secretory granules. At this time, VCP and 44KP are found together with vitellogenin in trophocyte autophagolysosomes, suggesting that all three yolk protein precusors are redirected from the secretory to the lysosomal degradative pathway. Localization of VCP and 44KP in developing mosquito oocytes clearly shows that the internalization of these yolk protein precursors by oocytes occurs via the same endocytotic route as vitellogenin: all three yolk protein precursors are found on the oocyte microvillus membrane, in coated vesicles, and early endosomes. They are observed intermixed with one another in the late endosomes or in transitional yolk bodies. In mature yolk bodies, however, 44KP and VCP are segregated from vitellin, the crystallized storage form of vitellogenin; 44KP and VCP reside in the non-crystalline cortex, surrounding the vitellin core in nature yolk bodies.

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Section: Discussionmentioning

confidence: 97%

Secretory and internalization pathways of mosquito yolk protein precursors

Snigirevskaya

Hays

Raikhel

1997

Cell and Tissue Research

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“…Plus, as previously observed for the silencing of ATG6/Beclin1, the lack of that signal molecule is likely the reason why silenced oocytes were not able to properly uptake the yolk proteins. The participation of endocytosis in the yolk uptake is not disputed and have been previously described in the oocytes of other insects [37][38][39][40][41][42][43][44][45]. Because PI3P is typically highly concentrated in early endosomes [83], and the mature yolk organelles are notably not formed in the oocytes of silenced females (Fig 5 ), it is likely that the silencing of the ATG6-PI3K complexes impair the endocytic flux at early steps of endosomal sorting.…”

Section: Discussionmentioning

confidence: 73%

“…The participation of receptor mediated endocytosis in the yolk uptake and biogenesis of the yolk organelles have been investigated in oocytes of many species. In insects, the internalization of yolk proteins through the presence of a specialized endocytic cortex in the oocytes, which includes prominent microvilli, coated pits, coated vesicles, and endosomes have been shown in several species [37][38][39][40][41][42][43][44]. Immunodetection of the internalization of yolk proteins and markers of endocytosis (such as clathrin, α-adaptin, and yolk protein receptors) have been performed in Drosophila [44] and mosquito [45].…”

Section: Introductionmentioning

confidence: 99%

VPS38/UVRAG and ATG14, the variant regulatory subunits of the ATG6/Beclin1-PI3K complexes, are crucial for the biogenesis of the yolk organelles and are transcriptionally regulated in the oocytes of the vector Rhodnius prolixus

et al. 2021

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In insects the reserve proteins are stored in the oocytes into endocytic-originated vesicles named yolk organelles. VPS38/UVRAG and ATG14 are the variant regulatory subunits of two class-III ATG6/Beclin1 PI3K complexes that regulate the recruitment of the endocytic (complex II) and autophagic (complex I) machineries. In a previous work from our group, we found that the silencing of ATG6/Beclin1 resulted in the formation of yolk-deficient oocytes due to defects in the endocytosis of the yolk proteins. Because ATG6/Beclin1 is present in the two above-described PI3K complexes, we could not identify the contributions of each complex to the yolk defective phenotypes. To address this, here we investigated the role of the variant subunits VPS38/UVRAG (complex II, endocytosis) and ATG14 (complex I, autophagy) in the biogenesis of the yolk organelles in the insect vector of Chagas Disease Rhodnius prolixus. Interestingly, the silencing of both genes phenocopied the silencing of ATG6/Beclin1, generating 1) accumulation of yolk proteins in the hemolymph; 2) white, smaller, and yolk-deficient oocytes; 3) abnormal yolk organelles in the oocyte cortex; and 4) unviable F1 embryos. However, we found that the similar phenotypes were the result of a specific cross-silencing effect among the PI3K subunits where the silencing of VPS38/UVRAG and ATG6/Beclin1 resulted in the specific silencing of each other, whereas the silencing of ATG14 triggered the silencing of all three PI3K components. Because the silencing of VPS38/UVRAG and ATG6/Beclin1 reproduced the yolk-deficiency phenotypes without the cross silencing of ATG14, we concluded that the VPS38/UVRAG PI3K complex II was the major contributor to the previously observed phenotypes in silenced insects. Altogether, we found that class-III ATG6/Beclin1 PI3K complex II (VPS38/UVRAG) is essential for the yolk endocytosis and that the subunits of both complexes are under an unknown transcriptional regulatory system.

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“…The number and molecular weight of these subunits vary from species to species, depending on their taxonomical position and evolutionary relatedness (Harnish and White, 1982). Vg is transferred from the hemolymph to the oocyte by receptor-mediated endocytosis (Postlethwait and Giorgi, 1985;Kulakosky and Telfer, 1987;Ferenz, 1990;Sappinton et al, 1995) and stored in the yolk granules as vitellin(s) (Vt) (Raikhel and Dhadialla, 1992). Since Vg and Vt appear immunologically identical when tested with anti-yolk sera (Hagedorn and Kunkel, 1979), it is currently believed that no major structural changes occur during Vg transfer from the hemolymph to the oocyte (Kunkel and Nordin, 1985).…”

Section: Introductionmentioning

confidence: 99%

Native vitellins are modified during ovarian development in the stick insectCarausius morosus (Br.)

Giorgi

Cecchettini

Locci

et al. 1997

Arch. Insect Biochem. Physiol.

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Vitellins from ovarian follicles and newly laid eggs of the stick insect Carausius morosus were examined by ion exchange chromatography on a HPLC Mono Q column. Under these conditions, vitellins from newly laid eggs resolved as two distinct peaks, referred to as VtA and VtB, that eluted at 8.5 and 12.0 min, respectively. On native gels, both VtA and VtB separated into two different variant forms (VtA′ and VtA′, VtB′ and VtB′). By two‐dimensional gel electrophoresis, VtA′ and VtA′ were shown to contain polypeptides A1, A2 and A3. On the other hand, VtB′ and VtB′ appeared to comprise polypeptides B1 and B2 and B1, A1, A2, B2 and A3*, respectively. A similar Vt polypeptide composition was also observed by size‐exclusion chromatography of vitellins from newly laid eggs. Vitellins from early vitellogenic ovarian follicles resolved into a single chromatographic peak at 7.5 min that coeluted with a major peak from the hemolymph of egg‐laying females. Ovarian follicles progressively more advanced in development exhibited a more complex chromatographic profile, consisting of three separate peaks. By two‐dimensional gel immunoelectrophoresis, vitellins from ovarian follicles appeared to consist of two closely related, immunologically cross‐reacting antigens that gradually shifted apart as ovarian development proceeded to completion. By size‐exclusion chromatography, each Vt from ovarian follicles was shown to consist of a unique set of polypeptides different from those listed above. Single ovarian follicles were fractionated into yolk granules and yolk fluid ooplasm and tested by immunoblotting against Mab 12. Under these conditions, VtA variant forms in yolk granules and yolk fluid ooplasm reacted differently. Sections from ovarian follicles in different developmental stages were exposed to Mab 12 and stained with a peroxidase‐conjugated, goat anti‐mouse antibody. Regardless of the developmental stage attained, staining for peroxidase was restricted to free yolk granules, suggesting that native vitellins in stick insects are structurally modified upon fusion into the yolk fluid ooplasm. Arch. Insect Biochem. Physiol. 36:335–348, 1997. © 1997 Wiley‐Liss, Inc.

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Receptor-Mediated Endocytosis of Insect Yolk Proteins

Cited by 14 publications

References 29 publications

Secretory and internalization pathways of mosquito yolk protein precursors

Secretory and internalization pathways of mosquito yolk protein precursors

VPS38/UVRAG and ATG14, the variant regulatory subunits of the ATG6/Beclin1-PI3K complexes, are crucial for the biogenesis of the yolk organelles and are transcriptionally regulated in the oocytes of the vector Rhodnius prolixus

Native vitellins are modified during ovarian development in the stick insectCarausius morosus (Br.)

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