Biosynthesis of sulfated glycosaminoglycans in the hemipteran Rhodnius prolixus: Enhancement of chondroitin sulfate synthesis by phenylxyloside

doi:10.1016/0020-1790(86)90046-6

Insect Biochemistry

Volume 16, Issue 2, 1986, Pages 347-352

https://doi.org/10.1016/0020-1790(86)90046-6 Get rights and content

Abstract

The insect Rhodnius prolixus synthesizes chondroitin sulfate and heparan sulfate after a blood meal containing radioactive ³⁵S-inorganic sulfate. A 3.5-fold enhancement of chondroitin sulfate synthesis was obtained when the meal was supplemented with 10⁻³ M $p- nitrophenyl-β- d -xyloside$ whereas no significant changes were observed for heparan sulfate. Time course experiments have shown that the synthesis of chondroitin sulfate in the presence of phenylxyloside is maximum 2 days after feeding and decreases slowly after 10 days, whereas heparan sulfate remains constant during the whole period. The analysis of this chondroitin sulfate has shown that its structure is similar to the chondroitin sulfate synthesized by mammalian cells in culture in the presence of phenylxyloside. It is concluded that the synthesis of these compounds follows the same pattern of mammals and that their structures are maintained through evolution.

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Cited by (10)

Identification of chondroitin/dermatan sulfotransferases in the protochordate, Ciona intestinalis
2010, Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology
Sulfated glycosaminoglycans are important components of connective tissues. The pattern of sulfation is important for their biological functions. Ascidians, the closest relatives of vertebrates, have a simple chordate body plan. In the present study, we identified an almost complete set of genes encoding proteins homologous to chondroitin/dermatan sulfotransferases in the genome of the ascidian Ciona intestinalis. We found eight genes encoding 4-O-sulfotransferases, eight genes encoding 6-O-sulfotransferases, and three genes encoding uronyl 2-O-sulfotransferases. The number of sulfotransferase genes was unexpectedly large, considering that ascidians do not have a well-developed endoskeleton. In addition, most of the genes within each sub-family seemed to have arisen by gene duplication events that occurred in the ascidian lineage after divergence from the main chordate lineage. This suggests that a unique pattern of sulfation independently developed during ascidian evolution. Some of the genes identified in the present study showed tissue-specific expression in the epidermis, notochord, muscle, and central nervous system. Region-specific expression in the epidermis was also observed. The present study provides useful information for further comparative and functional analyses of sulfotransferases and proteoglycans in chordate embryos.
Sulfated glycosaminoglycans in two hematophagous arthropod vectors of Chagas disease, Triatoma brasiliensis and Rhodnius prolixus (Hemiptera: Reduviidae)
2004, Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology
The characterization of sulfated glycosaminoglycans (GAGs) in hematophagous arthropod vectors in general has been limited, with the exception of the studies in the triatomine Rhodnius prolixus. Heparan sulfate (HS) and chondroitin sulfate (CS) were previously identified and structurally characterized in extracts of whole bodies of fourth instar larvae of R. prolixus. Recently, we showed the expression of these two sulfated GAGs in specific body tissues of adult males and females and in embryos of R. prolixus. In the present work, we identified and compared the sulfated GAG composition in specific tissues of adult insects and in embryos of another triatomine species, Triatoma brasiliensis. Sulfated GAGs were isolated from the fat body, intestinal tract, and the reproductive tracts of adult insects and from embryos. Only HS and CS were found in the tissues analyzed. The present results extend the initial observations on the sulfated GAG composition in R. prolixus by showing that these molecules are widely distributed among internal organs of triatomines. These observations may be useful for future investigations aiming to evaluate the possible implication of these compounds in physiological events that take place in a specific organ(s) in these insects.
Identification and tissue-specific distribution of sulfated glycosaminoglycans in the blood-sucking bug Rhodnius prolixus (Linnaeus)
2004, Insect Biochemistry and Molecular Biology
We have previously characterized heparan sulfate (HS) as the major ovarian sulfated glycosaminoglycan (GAG) in females of Rhodnius prolixus, while chondroitin sulfate (CS) was the minor component. Using histochemical procedures we found that GAGs were concentrated in the ovarian tissue but not found inside the oocytes. Here, we extend our initial observations of GAG expression in R. prolixus by characterizing these molecules in other organs: the fat body, intestinal tract, and the reproductive tracts. Only HS and CS were found in the three organs analyzed, however CS was the major GAG species in these tissues. We also determined the compartmental distribution of GAGs in these organs by histochemical analysis using 1,9-dimethylmethylene blue, and evaluated the specific distribution of CS within both male and female reproductive tracts by immunohistochemistry using an anti-CS antibody. We also determined the GAG composition in eggs at days 0 and 6 of embryonic development. Only HS and CS were found in eggs at day 6, while no sulfated GAGs were detected at day 0. Our results demonstrate that HS and CS are the only sulfated GAG species expressed in the fat body and in the intestinal and reproductive tracts of Rhodnius male and female adults. Both sulfated GAGs were also identified in Rhodnius embryos. Altogether, these results show no qualitative differences in the sulfated GAG composition regarding tissue-specific or development-specific distribution.
A novel heparan sulphate with high degree of N-sulphation and high heparin cofactor-II activity from the brine shrimp Artemia franciscana
2000, International Journal of Biological Macromolecules
With the aid of heparinase and heparitinases from Flavobacterium heparinum and ¹³C and ^IH NMR spectroscopy it was shown that the heparan sulphate isolated from the brine shrimp Artemia franciscana exhibits structural features intermediate between those of mammalian heparins and heparan sulphates. These include an unusually high degree of N-sulphation (with corresponding very low degree of N-acetylation), a relatively high content of iduronic acid residues (both unsulphated and 2-O-sulphated) and a relatively low degree of 6-O-sulphation of the glucosamine residues. The major sequences (glucuronic acid→N-sulphated glucosamine and glucuronic acid→N,6-disulphated glucosamine) are most probably arranged in blocks. Although exhibiting negligible anticlotting activity in the APTT and anti-factor Xa assays the A. franciscana heparan sulphate has a high heparin cofactor-II activity (about 1/3 that of heparin).
The glycosaminoglycans of midgut connective sheath during development of the mealworm Tenebrio molitor L.
1989, Comparative Biochemistry and Physiology -- Part B: Biochemistry and
- 1.
  1. Modifications in the constitution of the glycosaminoglycans of the mesenteric connective sheath of beetle Tenebrio molitor L. during larval, pupal and imaginal stages were analysed by means of histochemical studies and electrophoresis characterization.
- 2.
  2. The results indicated that in the early larval instars hyaluronic acid is the major component and is associated with heparan sulfate.
- 3.
  3. In the last larval instar as well as in nymphal and imaginal stages, dermatan sulfate, heparan sulfate and chondroitin-4-sulfate were detected, with a high quantity of heparan sulfate and a rapid increase of chondroitin sulfate in adults.
- 4.
  4. The possible reasons for these variations are discussed.
A relationship between the inhibition of heparan sulfate and chondroitin sulfate synthesis and the inhibition of molting by selenate in the hemipteran Rhodnius prolixus
1987, Biochemical and Biophysical Research Communications
The insect Rhodnius prolixus synthesizes heparan sulfate and chondroitin sulfate after a blood meal containing [³⁵S]-inorganic sulfate. A 40 to 80 % inhibition of heparan sulfate synthesis was obtained when the meal was supplemented with 10⁻⁵ and 10⁻⁴ M sodium selenate respectively. Likewise an inhibition of the molting in the order of 30 to 60% was observed when the insects were fed with blood containing 10⁻⁵ and 10⁻⁴ M selenate respectively. The insects after a subsequent meal without selenate molted normally. Except for the inhibition of the ecdysis no gross physiological or morphological changes could be observed in the insects. Based on these and other findings the possible role of sulfated glycosaminoglycans in the control of cell growth is discussed.

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Insect Biochemistry

Abstract

References (13)

Distribution of sulfated mucopolysaccharides in invertebrates

J. biol. Chem.

Turnover, change of composition with rate of cell growth and effect of phenylxyloside on synthesis and structure of cell surface sulfated glycosaminoglycans of normal and transformed cells

Biochim. biophys. Acta

Purification and characterization of a SH-dependent protease from Rhodnius prolixus midgut

Archs Biochem. Biophys.

Distribution of heparin and other sulfated glycosaminoglycans and vertebrates

Comp. Biochem. Physiol.

Glycosaminoglycans in Calliphora erythrocephala

Comp. Biochem. Physiol.

A correlation between the sulfated glycosaminoglycan concentration and degree of salinity of the “habitat” in fifteen species of the classes Crustacea, Pelecypoda and Gastropoda

Comp. Biochem. Physiol.

Cited by (10)

Identification of chondroitin/dermatan sulfotransferases in the protochordate, Ciona intestinalis

Sulfated glycosaminoglycans in two hematophagous arthropod vectors of Chagas disease, Triatoma brasiliensis and Rhodnius prolixus (Hemiptera: Reduviidae)

Identification and tissue-specific distribution of sulfated glycosaminoglycans in the blood-sucking bug Rhodnius prolixus (Linnaeus)

A novel heparan sulphate with high degree of N-sulphation and high heparin cofactor-II activity from the brine shrimp Artemia franciscana

The glycosaminoglycans of midgut connective sheath during development of the mealworm Tenebrio molitor L.

A relationship between the inhibition of heparan sulfate and chondroitin sulfate synthesis and the inhibition of molting by selenate in the hemipteran Rhodnius prolixus