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We conclude that the stoichiometry of differentiation factors is critical for normal epidermal development. Addition of glucose residues to the dolichol-linked oligosaccharide that will be transferred to secreted or membrane-associated proteins requires the three glycosyltransferases Alg5 Wol , Alg6 Gny and Alg8.

They eventually die after one moult without displaying any obvious phenotype. Due to the morphological defects, the cuticle of these larvae is discontinuous and their body contours are irregular.

At the edges of ruptures, the cuticle is often melanized. Specialized cuticle structures such as denticles are present.

Overall, the phenotypic analysis of these mutant larvae underlines that Wol and Gny contribute to cuticle differentiation. The piggybac insertions in wol and gny were recombined on the FRT2A chromosome by standard genetic methods.

These insertions possibly cause truncated loss-of-function proteins. In wol , the insertion disrupts translation after 80 amino acids that lack almost the entire glycosyltransferase domain of residues starting at position Mutations in genes involved in N -glycan glucosylation do not affect the larval body shape.

Light microscopy using the Nomarski optics of wild-type and homozygous wol and gny alg6 zygotic mutant larvae. The wild-type larva is covered by the cuticle that supports its spindle-like body shape A.

The body shape of larvae carrying mutations in wol wol 2 , B , alg6 alg6 P , C or both genes at the same time wol 2 , alg6 P , D is normal. Likewise, the texture of the head skeleton is normal in wol , alg6 and wol 2 , alg6 P mutant larvae insets in A—D.

Abrogation of N -glycan glucosylation causes the loss of cuticle integrity. Light microscopy using the Nomarski optics of wild-type and wol , gny alg6 and mmy mutant larvae within the egg case marked by an asterisk in each individual figure.

The wild-type larva possesses a cuticle coating the epidermis arrowhead and building up the head skeleton bracket, A. In contrast, larvae maternally and zygotically mutant for wol do not produce a proper cuticle D and F.

The cuticle including the head skeleton of strong mmy mutant larvae mmy IK63 is only poorly formed F. Larva maternally and zygotically mutant for wol or gny or double mutant for wol and gny G—J remind of the mmy IK63 mutant phenotype.

Anterior is to the left, dorsal faces up. Wild-type and maternal mutant larvae are shown in two focal planes: The egg case is about half a millimeter long.

The gene products of wol and gny are reported to act in a linear pathway to add glucose residues to the oligosaccharide.

To test whether Wol and Gny may nevertheless have other independent functions as well, we generated embryos double mutant for wol and gny.

Thus, since the defects in wol and gny mutant embryos are not additive, we assume that they function in a common pathway and do not exert other functions.

Moreover, the failure of the gny mutation to deteriorate the phenotype of wol mutant embryos indicates that mutations in wol indeed completely eliminate Wol activity.

We focus our following analyzes on the ultrastructure of the cuticle of wol mutant larvae, as the cuticles of wol and gny mutant larvae are identical.

In the most severe cases, wol maternal and zygotic mutant larvae have an expanded and spongy ECM beneath the envelope.

Traces of electron-dense material in the extracellular space suggest that some proteins are being secreted but mislocalize.

As shown by chitin detection with gold-conjugated wheat germ agglutinin WGA , this rudimentary cuticle contains chitin data not shown. Taken together, construction of the cuticle, in particular chitin orientation, depends on the dosage of Wol.

The architecture of the cuticle is sensitive to the dose of Wol. Ultrastructure of the cuticle of wild-type and wol mutant larvae by electron microscopy.

The wild-type cuticle is composed of three biochemically distinct layers: Layering of the cuticle of larvae homozygous mutant for wol is normal B.

However, procuticle homogeneity is occasionally disrupted black arrows. The cuticle of larvae lacking the maternal function of wol additionally contains electron-dense inclusions within the procuticle C.

Upon the removal of maternal as well as zygotic Wol function, the electron-dense lower sublayer of the epicuticle contacts the envelope white arrow at the expense of the electron-lucid sublayer D.

During cuticle differentiation, the apical plasma membrane of epidermal cells actively participates in organizing the cuticle Moussian, Seifarth et al.

We therefore explored whether the disorganized cuticle in wol mutant embryos may be associated with malfunctions of the apical plasma membrane.

Occasionally, in larvae with partially maternal reduced Wol function, a normal layered cuticle is separated from the surface of the epidermis by an amorph chitinous matrix.

We also assessed whether elimination or reduction in Wol activity has an impact on the so-called apical undulate, which are longitudinal corrugations of the apical plasma membrane that occur during chitin deposition Moussian, Seifarth et al.

As in the wild-type embryo at early stage 17, the apical plasma membrane of wol maternal mutant embryos elaborate the regular arrangement of apical undulate.

In contrast, the apical undulate of wol maternal and zygotic mutant embryos appear less regular. Hence, the establishment of repetitive protrusions of the epidermal apical plasma membrane during cuticle differentiation implies full Wol function as does flattening of the apical plasma membrane when cuticle differentiation ceases.

Dynamics of apical plasma membrane topology depends on Wol activity. The apical plasma membrane apm of larval epidermal cells is flat when the cuticle bracket is fully differentiated A.

In contrast, the surface of epidermal cells of larvae with reduced or eliminated Wol function protrudes into the extracellular space bracket, B and C.

During cuticle differentiation at stage 16, the apical plasma membrane of wild-type epidermal cells forms regular protrusions D.

These protrusions seem to be normal in embryos lacking maternal Wol function E. In embryos suffering complete Wol function, they are rather irregular F.

The apical plasma membrane of wild-type larval midgut epithelial cells forms an array of tightly packed microvilli called the brush border G.

Maternal reduction in Wol function has no visible effect on the brush border of midgut epithelial cells H. In wol deficient larvae, in contrast, the microvilli are less tightly packed I.

As in the epidermis, the apical plasma membrane of wild-type hindgut larval epithelial cells is flat J. Compared with the wild-type hindgut cuticle bracket , the hindgut cuticle of wol maternally mutant larvae is expanded, whereas the apical plasma membrane is flat as well K.

Complete loss of Wol function results in dramatic protrusions of the apical hindgut epithelial cells that do not produce any cuticle L.

Taken together, dynamics of plasma membrane topology in many epithelia involves Wol function. This phenotype is less severe than displayed by larvae mutant for SJ factors such as coracle and gliotactin where SJs are missing Genova and Fehon Integrity of the epidermal lateral membrane depends on Wol activity.

Ultrastructure of the lateral membrane of wild-type and wol mutant larvae by electron microscopy and immunohistochemistry with the lateral membrane marker Fas3 in wild-type and wol mutant embryos.

Fas3 white signal marks the lateral membrane of wild-type stage 16 embryos C. The Fas3 signal at the apical half is stronger than at the basal half of the lateral membrane bracket.

In respective embryos lacking maternal Wol activity, the distribution of Fas3 is normal D. In contrast, in stage 16 embryos with probably complete loss of Wol activity, the Fas3 signal is not split into two domains E.

For the examination of the molecular constitution of junctions in wol mutant embryos, we performed immunohistochemical experiments using antibodies directed against the membrane-inserted factors Crb, an apico-lateral determinant of cell polarity and fasciclin 3 Fas3 that is associated with the more baso-lateral SJ Bryant ; Assemat et al.

In spite of this, Crb amounts are elevated in wol mutant embryos. To investigate whether besides Crb, other determinants of the apical membrane show a similar wol -dependent behavior, we examined the localization and amounts of atypical protein kinase C aPKC , a cytosolic kinase Wodarz et al.

In summary, our data suggest that the proper organization of the lateral and apical plasma membrane involves full Wol function. Amounts of glycosylated proteins are perturbed in the epidermis of wol deficient embryos.

In wild-type stage 16 embryos, Crb localizes to the apical plasma membrane of epidermal cells A. Localization of Crb is normal in wol maternal B and maternal zygotic mutant embryos C.

However, compared with wild type, the amounts of Crb in the apical plasma membrane of wol mutants are elevated maternal: The aPKC is detected close to or at the apical plasma membrane in the wild-type stage 16 embryo D.

In wol maternal and maternal-zygotic mutant embryos, the apical localization of aPKC is enhanced E and F maternal: ConA marks the apical plasma membrane of wild-type stage 16 embryos J.

Some trace amounts are also found within the cell, probably representing the protein in the secretory pathway.

The light green dots are background signals also present in knk mutant embryos Moussian, Tang et al. Reduction in Fas3 in the lateral plasma membrane argues that glucosylation is controlling the amount of proteins delivered to the plasma membrane or extracellular space.

To test to what extend its activity is needed for correct trafficking of N-glycosylated proteins from the ER to the plasma membrane of epidermal cells, we monitored the behavior of secreted proteins with dye-conjugated lectins or agglutinins binding to sugar residues on glycans in wild-type and wol mutant embryos.

Despite a reduction in PSA and SBA signal intensity in wol mutant embryos, the distribution of the recognized epitopes is rather normal. WGA staining is almost normal in embryos with abolished maternal Wol contribution, but is clearly weakened in embryos with no Wol function.

Consistently, localization of Knk, a GPI-anchored and N-glycosylated protein that is involved in chitin microfibril orientation Moussian, Tang et al.

The amounts of ConA-positive proteins are however decreased in the later animals. Likewise, Knk mobility is unchanged in wol zygotic mutant larvae data not shown.

In contrast, the Knk signal from wol mutant embryos is weaker. Hence, Knk protein levels depend on Wol activity. Western blot analyzes of ConA binding N -glycans and of the cuticle-organizing factor Knk.

These experiments reveal that the total amount of mannose and glucose containing proteins is reduced in larvae with reduced or eliminated Wol function standard deviation of three independent experiments: Moreover, the pattern of protein migration is unchanged in wol mutant when compared with wild-type larvae.

Migration of Knk is identical in wild-type and wol mutant larvae, whereas Knk from EndoH-treated wild-type protein extracts migrates faster. Three independent western blots independent collection of larvae and independent blotting were analyzed, and the ratio was set to 1 for wild type.

Taking all these results together, we conclude that Wol function contributes to the normal levels of N - and O -glycans.

Assessment of transcript levels of some extracellular, glycosylation and transcription factors in wild-type and wol mutant embryos by qPCR.

A 2-fold difference in gene expression is considered as no change as it is also observed when expression levels of different wild-type samples are compared data not shown.

By trend, transcript levels are lower in wol maternal and zygotic mutant than in wild-type larvae. Especially transcripts coding for transcription factors such as grh and CrebA are affected.

Likewise, the expression of CG and CG , both encoding factors involved in the synthesis of the dolichol-anchored oligosaccharide, is down-regulated in wol maternal and zygotic mutant larvae.

Reduction in Knk amounts may result from proteasome-mediated degradation of the protein caused by the unfolded protein response pathway that occurs in wol mutant embryos Supplementary Data ; Haecker et al.

The unfolded protein response has also been reported to induce decay of mRNA associated with the ER membrane coding for proteins to be loaded into the ER Hollien and Weissman Mutations in wol reduce the expression of caudal mRNA that codes for a homeobox containing transcription factor Haecker et al.

The amounts of grh and CrebA transcripts are lowered in these embryos. Taken together, Wol activity has an influence on grh and CrebA transcript levels.

In conclusion, through downscaling of mRNA of especially transcription factors, the suppressed activities of a plethora of differentiation factors may contribute to wol -dependent defects observed in epidermal cells involved in cuticle production.

Wol is a key enzyme for glycosylation taking place in the ER. To inspect whether wol mutations have an influence on ER morphology, we examined the ultrastructure of the ER in stage 16 embryos, which have initiated cuticle production.

In the respective embryos suffering loss of maternal and zygotic Wol activity, in contrast, ER tubules are rather smooth.

Wol is associated with the ER and influences its capacity. Ultrastructure of the epidermal ER of wild-type and wol mutant stage 16 embryos by electron microscopy.

During cuticle production, the epidermal cell contains cystic ER tubules C. In the absence of Wol activity, the ER fails to form cysts and consists rather of straight tubules D.

In wol mutant embryos, N -glycans contain markedly less glucose units than in wild-type embryos, especially the second and the third Glc residues are almost undetectable in wol mutant embryos.

The significance of this observation is not obvious. Wol activity is crucial for glycan composition and amounts.

Terminal Glc residues are almost eliminated in wol mutant larvae. The addition of fucoses to the oligosaccharide is normal in wol mutant embryos.

This finding suggests that hypoglucosylated proteins are correctly passed through the secretory pathway. Modification of N -glycans in the Golgi apparatus is not affected in embryos with eliminated Wol activity.

N, N -acetylglucosamine; H, hexose mannose or galactose ; F, fucose. N -Glycan nomenclature is according to the Proglycan system http: Taken together, Wol activity is needed for full glucosylation of proteins, underlining that it is indeed the Drosophila Alg5 ortholog.

An early role of N-glycosylation in the ER is to initiate the folding reaction of proteins for correct localization and function. Recognition of the yet unfolded protein depends on a single glucose residue at the N -glycan.

The importance of glucosylation of N -glycans has mainly been investigated in yeasts and cultured cells. To understand the role of the N -glycan glucose in a multicellular organism, we have studied the role of Drosophila Wol DAlg5 and Gny DAlg6 that regulate early steps of glucosylation at the ER membrane.

Mutations in wol in Drosophila disrupt the architecture of the larval cuticle, which is an apical ECM produced by the epidermal cells.

Stepwise reduction in Wol activity results in a gradual worsening of cuticle defects ranging from small lesions in the procuticle of zygotic mutant larvae, over mislocalized cuticle proteins in maternally mutant but zygotic wild-type larvae to chitin disorganization and protein depletion upon additional removal of zygotic enzyme activity.

These observations signify that the amount of Wol activity provided by zygotic expression alone is not sufficient but nevertheless necessary to support embryogenesis, whereas maternal supply of Wol only is despite some tolerable errors adequate for development until after first moulting of the larva.

Hence, the rate of glucosylation is critical for embryogenesis and development in general and cuticle differentiation in particular.

One may postulate that hypoglucosylation yields fewer biochemically active extracellular and membrane-bound proteins, a situation that may retard especially secretion-related aspects of differentiation.

However, perturbed plasma membrane and cuticle organization cannot be satisfactorily explained by slower development.

This is a similar scenario encountered when chitin synthesis is decreased but not abrogated upon application of insecticides Gangishetti et al.

In brief, the epidermal system is unable to cope with biochemical attenuation of chitin synthesis implying that the activities of the cooperating factors are tightly adjusted and coordinated.

Full interpretation of the wol phenotypes, thus, probably also calls for the assumption of problems in coordination between effectors.

Our molecular data discussed in the following deal with these genetic arguments. N -Glycans are hypoglucosylated in wol mutant embryos that concomitantly suffer reduced glycosylation.

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