Phospholipase D family member 4, a transmembrane glycoprotein with no phospholipase D activity, expression in spleen and early postnatal microglia

Fumio Yoshikawa, Yoshiko Banno, Yoshinori Otani, Yoshihide Yamaguchi, Yuko Nagakura-Takagi, Noriyuki Morita, Yumi Sato, Chihiro Saruta, Hirozumi Nishibe, Tetsushi Sadakata, Yo Shinoda, Kanehiro Hayashi, Yuriko Mishima, Hiroko Baba, Teiichi Furuichi

Research output: Contribution to journalArticle

31 Citations (Scopus)

Abstract

Background: Phospholipase D (PLD) catalyzes conversion of phosphatidylcholine into choline and phosphatidic acid, leading to a variety of intracellular signal transduction events. Two classical PLDs, PLD1 and PLD2, contain phosphatidylinositide-binding PX and PH domains and two conserved His-x-Lys-(x)4-Asp (HKD) motifs, which are critical for PLD activity. PLD4 officially belongs to the PLD family, because it possesses two HKD motifs. However, it lacks PX and PH domains and has a putative transmembrane domain instead. Nevertheless, little is known regarding expression, structure, and function of PLD4. Methodology/Principal Findings: PLD4 was analyzed in terms of expression, structure, and function. Expression was analyzed in developing mouse brains and non-neuronal tissues using microarray, in situ hybridization, immunohistochem-istry, and immunocytochemistry. Structure was evaluated using bioinformatics analysis of protein domains, biochemical analyses of transmembrane property, and enzymatic deglycosylation. PLD activity was examined by choline release and transphosphatidylation assays. Results demonstrated low to modest, but characteristic, PLD4 mRNA expression in a subset of cells preferentially localized around white matter regions, including the corpus callosum and cerebellar white matter, during the first postnatal week. These PLD4 mRNA-expressing cells were identified as Iba1-positive microglia. In nonneuronal tissues, PLD4 mRNA expression was widespread, but predominantly distributed in the spleen. Intense PLD4 expression was detected around the marginal zone of the splenic red pulp, and splenic PLD4 protein recovered from subcellular membrane fractions was highly N-glycosylated. PLD4 was heterologously expressed in cell lines and localized in the endoplasmic reticulum and Golgi apparatus. Moreover, heterologously expressed PLD4 proteins did not exhibit PLD enzymatic activity. Conclusions/Significance: Results showed that PLD4 is a non-PLD, HKD motif-carrying, transmembrane glycoprotein localized in the endoplasmic reticulum and Golgi apparatus. The spatiotemporally restricted expression patterns suggested that PLD4 might play a role in common function(s) among microglia during early postnatal brain development and splenic marginal zone cells.

Original languageEnglish
Article numbere13932
JournalPLoS One
Volume5
Issue number11
DOIs
Publication statusPublished - 2010
Externally publishedYes

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Phospholipase D
phospholipase D
neuroglia
Microglia
glycoproteins
Glycoproteins
spleen
Spleen
Golgi Apparatus
choline
Choline
Golgi apparatus
Endoplasmic Reticulum
endoplasmic reticulum
Messenger RNA
Brain
Tissue
brain
Signal transduction
Phosphatidic Acids

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Phospholipase D family member 4, a transmembrane glycoprotein with no phospholipase D activity, expression in spleen and early postnatal microglia. / Yoshikawa, Fumio; Banno, Yoshiko; Otani, Yoshinori; Yamaguchi, Yoshihide; Nagakura-Takagi, Yuko; Morita, Noriyuki; Sato, Yumi; Saruta, Chihiro; Nishibe, Hirozumi; Sadakata, Tetsushi; Shinoda, Yo; Hayashi, Kanehiro; Mishima, Yuriko; Baba, Hiroko; Furuichi, Teiichi.

In: PLoS One, Vol. 5, No. 11, e13932, 2010.

Research output: Contribution to journalArticle

Yoshikawa, F, Banno, Y, Otani, Y, Yamaguchi, Y, Nagakura-Takagi, Y, Morita, N, Sato, Y, Saruta, C, Nishibe, H, Sadakata, T, Shinoda, Y, Hayashi, K, Mishima, Y, Baba, H & Furuichi, T 2010, 'Phospholipase D family member 4, a transmembrane glycoprotein with no phospholipase D activity, expression in spleen and early postnatal microglia', PLoS One, vol. 5, no. 11, e13932. https://doi.org/10.1371/journal.pone.0013932
Yoshikawa, Fumio ; Banno, Yoshiko ; Otani, Yoshinori ; Yamaguchi, Yoshihide ; Nagakura-Takagi, Yuko ; Morita, Noriyuki ; Sato, Yumi ; Saruta, Chihiro ; Nishibe, Hirozumi ; Sadakata, Tetsushi ; Shinoda, Yo ; Hayashi, Kanehiro ; Mishima, Yuriko ; Baba, Hiroko ; Furuichi, Teiichi. / Phospholipase D family member 4, a transmembrane glycoprotein with no phospholipase D activity, expression in spleen and early postnatal microglia. In: PLoS One. 2010 ; Vol. 5, No. 11.
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AU - Yoshikawa, Fumio

AU - Banno, Yoshiko

AU - Otani, Yoshinori

AU - Yamaguchi, Yoshihide

AU - Nagakura-Takagi, Yuko

AU - Morita, Noriyuki

AU - Sato, Yumi

AU - Saruta, Chihiro

AU - Nishibe, Hirozumi

AU - Sadakata, Tetsushi

AU - Shinoda, Yo

AU - Hayashi, Kanehiro

AU - Mishima, Yuriko

AU - Baba, Hiroko

AU - Furuichi, Teiichi

PY - 2010

Y1 - 2010

N2 - Background: Phospholipase D (PLD) catalyzes conversion of phosphatidylcholine into choline and phosphatidic acid, leading to a variety of intracellular signal transduction events. Two classical PLDs, PLD1 and PLD2, contain phosphatidylinositide-binding PX and PH domains and two conserved His-x-Lys-(x)4-Asp (HKD) motifs, which are critical for PLD activity. PLD4 officially belongs to the PLD family, because it possesses two HKD motifs. However, it lacks PX and PH domains and has a putative transmembrane domain instead. Nevertheless, little is known regarding expression, structure, and function of PLD4. Methodology/Principal Findings: PLD4 was analyzed in terms of expression, structure, and function. Expression was analyzed in developing mouse brains and non-neuronal tissues using microarray, in situ hybridization, immunohistochem-istry, and immunocytochemistry. Structure was evaluated using bioinformatics analysis of protein domains, biochemical analyses of transmembrane property, and enzymatic deglycosylation. PLD activity was examined by choline release and transphosphatidylation assays. Results demonstrated low to modest, but characteristic, PLD4 mRNA expression in a subset of cells preferentially localized around white matter regions, including the corpus callosum and cerebellar white matter, during the first postnatal week. These PLD4 mRNA-expressing cells were identified as Iba1-positive microglia. In nonneuronal tissues, PLD4 mRNA expression was widespread, but predominantly distributed in the spleen. Intense PLD4 expression was detected around the marginal zone of the splenic red pulp, and splenic PLD4 protein recovered from subcellular membrane fractions was highly N-glycosylated. PLD4 was heterologously expressed in cell lines and localized in the endoplasmic reticulum and Golgi apparatus. Moreover, heterologously expressed PLD4 proteins did not exhibit PLD enzymatic activity. Conclusions/Significance: Results showed that PLD4 is a non-PLD, HKD motif-carrying, transmembrane glycoprotein localized in the endoplasmic reticulum and Golgi apparatus. The spatiotemporally restricted expression patterns suggested that PLD4 might play a role in common function(s) among microglia during early postnatal brain development and splenic marginal zone cells.

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