Protein crosslinking by transglutaminase controls cuticle morphogenesis in Drosophila

Toshio Shibata, Shigeru Ariki, Naoaki Shinzawa, Ryuta Miyaji, Haruka Suyama, Miyuki Sako, Nobuyuki Inomata, Takumi Koshiba, Hirotaka Kanuka, Shun-Ichiro Kawabata

研究成果: ジャーナルへの寄稿記事

30 引用 (Scopus)

抄録

Transglutaminase (TG) plays important and diverse roles in mammals, such as blood coagulation and formation of the skin barrier, by catalyzing protein crosslinking. In invertebrates, TG is known to be involved in immobilization of invading pathogens at sites of injury. Here we demonstrate that Drosophila TG is an important enzyme for cuticle morphogenesis. Although TG activity was undetectable before the second instar larval stage, it dramatically increased in the third instar larval stage. RNA interference (RNAi) of the TG gene caused a pupal semi-lethal phenotype and abnormal morphology. Furthermore, TG-RNAi flies showed a significantly shorter life span than their counterparts, and approximately 90% of flies died within 30 days after eclosion. Stage-specific TG-RNAi before the third instar larval stage resulted in cuticle abnormality, but the TG-RNAi after the late pupal stage did not, indicating that TG plays a key role at or before the early pupal stage. Immediately following eclosion, acid-extractable protein from wild-type wings was nearly all converted to non-extractable protein due to wing maturation, whereas several proteins remained acid-extractable in the mature wings of TG-RNAi flies. We identified four proteins-two cuticular chitin-binding proteins, larval serum protein 2, and a putative C-type lectin-as TG substrates. RNAi of their corresponding genes caused a lethal phenotype or cuticle abnormality. Our results indicate that TG-dependent protein crosslinking in Drosophila plays a key role in cuticle morphogenesis and sclerotization.

元の言語英語
記事番号e13477
ジャーナルPloS one
5
発行部数10
DOI
出版物ステータス出版済み - 11 17 2010

Fingerprint

Transglutaminases
protein-glutamine gamma-glutamyltransferase
crosslinking
Morphogenesis
Crosslinking
Drosophila
morphogenesis
RNA Interference
RNA interference
Proteins
proteins
RNA
Diptera
instars
lethal genes
eclosion
Genes
C-Type Lectins
Phenotype
sclerotization

All Science Journal Classification (ASJC) codes

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

これを引用

Protein crosslinking by transglutaminase controls cuticle morphogenesis in Drosophila. / Shibata, Toshio; Ariki, Shigeru; Shinzawa, Naoaki; Miyaji, Ryuta; Suyama, Haruka; Sako, Miyuki; Inomata, Nobuyuki; Koshiba, Takumi; Kanuka, Hirotaka; Kawabata, Shun-Ichiro.

:: PloS one, 巻 5, 番号 10, e13477, 17.11.2010.

研究成果: ジャーナルへの寄稿記事

Shibata, T, Ariki, S, Shinzawa, N, Miyaji, R, Suyama, H, Sako, M, Inomata, N, Koshiba, T, Kanuka, H & Kawabata, S-I 2010, 'Protein crosslinking by transglutaminase controls cuticle morphogenesis in Drosophila', PloS one, 巻. 5, 番号 10, e13477. https://doi.org/10.1371/journal.pone.0013477
Shibata, Toshio ; Ariki, Shigeru ; Shinzawa, Naoaki ; Miyaji, Ryuta ; Suyama, Haruka ; Sako, Miyuki ; Inomata, Nobuyuki ; Koshiba, Takumi ; Kanuka, Hirotaka ; Kawabata, Shun-Ichiro. / Protein crosslinking by transglutaminase controls cuticle morphogenesis in Drosophila. :: PloS one. 2010 ; 巻 5, 番号 10.
@article{44c9120e141747c08d519d5014556ae6,
title = "Protein crosslinking by transglutaminase controls cuticle morphogenesis in Drosophila",
abstract = "Transglutaminase (TG) plays important and diverse roles in mammals, such as blood coagulation and formation of the skin barrier, by catalyzing protein crosslinking. In invertebrates, TG is known to be involved in immobilization of invading pathogens at sites of injury. Here we demonstrate that Drosophila TG is an important enzyme for cuticle morphogenesis. Although TG activity was undetectable before the second instar larval stage, it dramatically increased in the third instar larval stage. RNA interference (RNAi) of the TG gene caused a pupal semi-lethal phenotype and abnormal morphology. Furthermore, TG-RNAi flies showed a significantly shorter life span than their counterparts, and approximately 90{\%} of flies died within 30 days after eclosion. Stage-specific TG-RNAi before the third instar larval stage resulted in cuticle abnormality, but the TG-RNAi after the late pupal stage did not, indicating that TG plays a key role at or before the early pupal stage. Immediately following eclosion, acid-extractable protein from wild-type wings was nearly all converted to non-extractable protein due to wing maturation, whereas several proteins remained acid-extractable in the mature wings of TG-RNAi flies. We identified four proteins-two cuticular chitin-binding proteins, larval serum protein 2, and a putative C-type lectin-as TG substrates. RNAi of their corresponding genes caused a lethal phenotype or cuticle abnormality. Our results indicate that TG-dependent protein crosslinking in Drosophila plays a key role in cuticle morphogenesis and sclerotization.",
author = "Toshio Shibata and Shigeru Ariki and Naoaki Shinzawa and Ryuta Miyaji and Haruka Suyama and Miyuki Sako and Nobuyuki Inomata and Takumi Koshiba and Hirotaka Kanuka and Shun-Ichiro Kawabata",
year = "2010",
month = "11",
day = "17",
doi = "10.1371/journal.pone.0013477",
language = "English",
volume = "5",
journal = "PLoS One",
issn = "1932-6203",
publisher = "Public Library of Science",
number = "10",

}

TY - JOUR

T1 - Protein crosslinking by transglutaminase controls cuticle morphogenesis in Drosophila

AU - Shibata, Toshio

AU - Ariki, Shigeru

AU - Shinzawa, Naoaki

AU - Miyaji, Ryuta

AU - Suyama, Haruka

AU - Sako, Miyuki

AU - Inomata, Nobuyuki

AU - Koshiba, Takumi

AU - Kanuka, Hirotaka

AU - Kawabata, Shun-Ichiro

PY - 2010/11/17

Y1 - 2010/11/17

N2 - Transglutaminase (TG) plays important and diverse roles in mammals, such as blood coagulation and formation of the skin barrier, by catalyzing protein crosslinking. In invertebrates, TG is known to be involved in immobilization of invading pathogens at sites of injury. Here we demonstrate that Drosophila TG is an important enzyme for cuticle morphogenesis. Although TG activity was undetectable before the second instar larval stage, it dramatically increased in the third instar larval stage. RNA interference (RNAi) of the TG gene caused a pupal semi-lethal phenotype and abnormal morphology. Furthermore, TG-RNAi flies showed a significantly shorter life span than their counterparts, and approximately 90% of flies died within 30 days after eclosion. Stage-specific TG-RNAi before the third instar larval stage resulted in cuticle abnormality, but the TG-RNAi after the late pupal stage did not, indicating that TG plays a key role at or before the early pupal stage. Immediately following eclosion, acid-extractable protein from wild-type wings was nearly all converted to non-extractable protein due to wing maturation, whereas several proteins remained acid-extractable in the mature wings of TG-RNAi flies. We identified four proteins-two cuticular chitin-binding proteins, larval serum protein 2, and a putative C-type lectin-as TG substrates. RNAi of their corresponding genes caused a lethal phenotype or cuticle abnormality. Our results indicate that TG-dependent protein crosslinking in Drosophila plays a key role in cuticle morphogenesis and sclerotization.

AB - Transglutaminase (TG) plays important and diverse roles in mammals, such as blood coagulation and formation of the skin barrier, by catalyzing protein crosslinking. In invertebrates, TG is known to be involved in immobilization of invading pathogens at sites of injury. Here we demonstrate that Drosophila TG is an important enzyme for cuticle morphogenesis. Although TG activity was undetectable before the second instar larval stage, it dramatically increased in the third instar larval stage. RNA interference (RNAi) of the TG gene caused a pupal semi-lethal phenotype and abnormal morphology. Furthermore, TG-RNAi flies showed a significantly shorter life span than their counterparts, and approximately 90% of flies died within 30 days after eclosion. Stage-specific TG-RNAi before the third instar larval stage resulted in cuticle abnormality, but the TG-RNAi after the late pupal stage did not, indicating that TG plays a key role at or before the early pupal stage. Immediately following eclosion, acid-extractable protein from wild-type wings was nearly all converted to non-extractable protein due to wing maturation, whereas several proteins remained acid-extractable in the mature wings of TG-RNAi flies. We identified four proteins-two cuticular chitin-binding proteins, larval serum protein 2, and a putative C-type lectin-as TG substrates. RNAi of their corresponding genes caused a lethal phenotype or cuticle abnormality. Our results indicate that TG-dependent protein crosslinking in Drosophila plays a key role in cuticle morphogenesis and sclerotization.

UR - http://www.scopus.com/inward/record.url?scp=78149426519&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=78149426519&partnerID=8YFLogxK

U2 - 10.1371/journal.pone.0013477

DO - 10.1371/journal.pone.0013477

M3 - Article

C2 - 20976106

AN - SCOPUS:78149426519

VL - 5

JO - PLoS One

JF - PLoS One

SN - 1932-6203

IS - 10

M1 - e13477

ER -