Rat spongiotrophoblast-specific protein is predominantly a unique low sulfated chondroitin sulfate proteoglycan

Rajeshwara N. Achur, Sean T. Agbor-Enoh, Channe Gowda

Research output: Contribution to journalArticle

5 Citations (Scopus)

Abstract

We have previously demonstrated that the human placenta contains a uniquely low sulfated extracellular aggrecan family chondroitin sulfate proteoglycan (CSPG). This CSPG is a major receptor for the adherence of Plasmodium falciparum-infected red blood cells (IRBCs) in placentas, causing pregnancy-specific malaria. However, it is not known whether such low sulfated CSPGs occur in placentas of other animals and, if so, whether IRBCs bind to those CSPGs. In this study, we show that rat placenta contains a uniquely low sulfated extracellular CSPG bearing chondroitin sulfate (CS) chains, which comprise only ∼2% 4-sulfated and the remainder nonsulfated disaccharides. Surprisingly, the core protein of the rat placental CSPG, unlike that of the human placental CSPG, is a spongiotrophoblast-specific protein (SSP), which is expressed in a pregnancy stage-dependent manner. The majority of rat placental SSP is present in the CSPG form, and only ∼10% occurs without CS chain substitution. Of the total SSP-CSPG in rat placenta, ∼57% is modified with a single CS chain, and ∼43% carries two CS chains. These data together with the previous finding on human placental CSPG suggest that the expression of low sulfated CSPG is a common feature of animal placentas. Our data also show that the unique species-specific difference in the biology of the rat and human placentas is reflected in the occurrence of completely different CSPG core protein types. Furthermore, the rat SSP-CSPG binds P. falciparum IRBCs in a CS chain-dependent manner. Since IRBCs have been reported to accumulate in the placentas of malaria parasite-infected rodents, our results have important implications for exploiting pregnant rats as a model for studying chondroitin 4-sulfate-based therapeutics for human placental malaria.

Original languageEnglish (US)
Pages (from-to)32327-32334
Number of pages8
JournalJournal of Biological Chemistry
Volume281
Issue number43
DOIs
StatePublished - Oct 27 2006

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Chondroitin Sulfate Proteoglycans
Placenta
Chondroitin Sulfates
Rats
Blood
Erythrocytes
Malaria
Plasmodium falciparum
Proteins
Animals
rat Tpbp protein
Bearings (structural)
Pregnancy Proteins
Aggrecans
Pregnancy
Disaccharides
Rodentia
Parasites
Substitution reactions

All Science Journal Classification (ASJC) codes

  • Biochemistry
  • Molecular Biology
  • Cell Biology

Cite this

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title = "Rat spongiotrophoblast-specific protein is predominantly a unique low sulfated chondroitin sulfate proteoglycan",
abstract = "We have previously demonstrated that the human placenta contains a uniquely low sulfated extracellular aggrecan family chondroitin sulfate proteoglycan (CSPG). This CSPG is a major receptor for the adherence of Plasmodium falciparum-infected red blood cells (IRBCs) in placentas, causing pregnancy-specific malaria. However, it is not known whether such low sulfated CSPGs occur in placentas of other animals and, if so, whether IRBCs bind to those CSPGs. In this study, we show that rat placenta contains a uniquely low sulfated extracellular CSPG bearing chondroitin sulfate (CS) chains, which comprise only ∼2{\%} 4-sulfated and the remainder nonsulfated disaccharides. Surprisingly, the core protein of the rat placental CSPG, unlike that of the human placental CSPG, is a spongiotrophoblast-specific protein (SSP), which is expressed in a pregnancy stage-dependent manner. The majority of rat placental SSP is present in the CSPG form, and only ∼10{\%} occurs without CS chain substitution. Of the total SSP-CSPG in rat placenta, ∼57{\%} is modified with a single CS chain, and ∼43{\%} carries two CS chains. These data together with the previous finding on human placental CSPG suggest that the expression of low sulfated CSPG is a common feature of animal placentas. Our data also show that the unique species-specific difference in the biology of the rat and human placentas is reflected in the occurrence of completely different CSPG core protein types. Furthermore, the rat SSP-CSPG binds P. falciparum IRBCs in a CS chain-dependent manner. Since IRBCs have been reported to accumulate in the placentas of malaria parasite-infected rodents, our results have important implications for exploiting pregnant rats as a model for studying chondroitin 4-sulfate-based therapeutics for human placental malaria.",
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Rat spongiotrophoblast-specific protein is predominantly a unique low sulfated chondroitin sulfate proteoglycan. / Achur, Rajeshwara N.; Agbor-Enoh, Sean T.; Gowda, Channe.

In: Journal of Biological Chemistry, Vol. 281, No. 43, 27.10.2006, p. 32327-32334.

Research output: Contribution to journalArticle

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