Essential roles of 3′-phosphoadenosine 5′-phoshosulfate synthase in embryonic and larval development of the nematode Caenorhabditis elegans

Katsufumi Dejima, Akira Seko, Katsuko Yamashita, Keiko Gengyo-Ando, Shohei Mitani, Tomomi Izumikawa, Hiroshi Kitagawa, Kazuyuki Sugahara, Souhei Mizuguchi, Kazuya Nomura

Research output: Contribution to journalArticle

18 Citations (Scopus)

Abstract

Sulfation of biomolecules, which is widely observed from bacteria to humans, plays critical roles in many biological processes. All sulfation reactions in all organisms require activated sulfate, 3′-phosphoadenosine 5′-phosphosulfate (PAPS), as a universal donor. In animals, PAPS is synthesized from ATP and inorganic sulfate by the bifunctional enzyme, PAPS synthase. In mammals, genetic defects in PAPS synthase 2, one of two PAPS synthase isozymes, cause dwarfism disorder, but little is known about the consequences of the complete loss of PAPS synthesis. To define the developmental role of sulfation, we cloned a Caenorhabditis elegans PAPS synthase-homologous gene, pps-1, and depleted expression of its product by isolating the deletion mutant and by RNA-mediated interference. PPS-1 protein exhibits specific activity to form PAPS in vitro, and disruption of the pps-1 gene by RNAi causes pleiotropic developmental defects in muscle patterning and epithelial cell shape changes with a decrease in glycosaminoglycan sulfation. Additionally, the pps-1 null mutant exhibits larval lethality. These data suggest that sulfation is essential for normal growth and integrity of epidermis in C. elegans. Furthermore, reporter analysis showed that pps-1 is expressed in the epidermis and several gland cells but not in neurons and muscles, indicating that PAPS in the neurons and muscles is provided by other cells.

Original languageEnglish
Pages (from-to)11431-11440
Number of pages10
JournalJournal of Biological Chemistry
Volume281
Issue number16
DOIs
Publication statusPublished - Apr 21 2006

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Phosphoadenosine Phosphosulfate
Caenorhabditis elegans
Embryonic Development
Muscle
Sulfates
Neurons
Genes
Defects
Mammals
Biomolecules
Glycosaminoglycans
Isoenzymes
Bacteria
Animals
Adenosine Triphosphate
RNA
RNA Interference
Epidermis
Enzymes
Biological Phenomena

All Science Journal Classification (ASJC) codes

  • Biochemistry
  • Molecular Biology
  • Cell Biology

Cite this

Essential roles of 3′-phosphoadenosine 5′-phoshosulfate synthase in embryonic and larval development of the nematode Caenorhabditis elegans. / Dejima, Katsufumi; Seko, Akira; Yamashita, Katsuko; Gengyo-Ando, Keiko; Mitani, Shohei; Izumikawa, Tomomi; Kitagawa, Hiroshi; Sugahara, Kazuyuki; Mizuguchi, Souhei; Nomura, Kazuya.

In: Journal of Biological Chemistry, Vol. 281, No. 16, 21.04.2006, p. 11431-11440.

Research output: Contribution to journalArticle

Dejima, K, Seko, A, Yamashita, K, Gengyo-Ando, K, Mitani, S, Izumikawa, T, Kitagawa, H, Sugahara, K, Mizuguchi, S & Nomura, K 2006, 'Essential roles of 3′-phosphoadenosine 5′-phoshosulfate synthase in embryonic and larval development of the nematode Caenorhabditis elegans', Journal of Biological Chemistry, vol. 281, no. 16, pp. 11431-11440. https://doi.org/10.1074/jbc.M601509200
Dejima, Katsufumi ; Seko, Akira ; Yamashita, Katsuko ; Gengyo-Ando, Keiko ; Mitani, Shohei ; Izumikawa, Tomomi ; Kitagawa, Hiroshi ; Sugahara, Kazuyuki ; Mizuguchi, Souhei ; Nomura, Kazuya. / Essential roles of 3′-phosphoadenosine 5′-phoshosulfate synthase in embryonic and larval development of the nematode Caenorhabditis elegans. In: Journal of Biological Chemistry. 2006 ; Vol. 281, No. 16. pp. 11431-11440.
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