Drpiwi-1 is essential for germline cell formation during sexualization of the planarian Dugesia ryukyuensis

Haruka Nakagawa, Hirotsugu Ishizu, Reiko Hasegawa, Kazuya Kobayashi, Midori Matsumoto

Research output: Contribution to journalArticle

17 Citations (Scopus)

Abstract

A piwi homolog is required for the regulation of stem cells, formation and maintenance of germline stem cells, and gametogenesis in many metazoans. Planarians can change their reproductive mode seasonally, both asexually and sexually, and develop and maintain germ cells and sexual organs. They have many pluripotent stem cells (neoblasts) that can differentiate into both somatic and germline stem cells. Thus, we searched for a piwi subfamily in the planarian Dugesia ryukyuensis. Four piwi homologs, identified as Drpiwi-1, -2, -3, and -4, were expressed in sexually reproductive worms. We then selectively destroyed the neoblasts by irradiating the worms with X-rays. In such worms, Drpiwi-1, -2, and -3 were not expressed at all, whereas Drpiwi-4 was expressed to the same degree as that in non-irradiated controls, indicating that Drpiwi-1, -2, and -3, but not Drpiwi-4, are expressed in neoblasts. During the regeneration process, Drpiwi-2(RNAi) and -3(RNAi) worms failed to regenerate after ablation, but Drpiwi-1 and -4(RNAi) worms regenerated. During the sexualizing process, Drpiwi-1(RNAi) worms failed to develop ovaries and testes, but somatic sexual organs were unaffected. Germ cell development was normal in Drpiwi-4(RNAi) worms. Therefore, Drpiwi-2 and -3 may be related to the regulation of neoblasts important for maintaining homeostasis, and Drpiwi-1 is essential for the development of germ cells but not somatic sexual organs. DrPiwi-1 is localized in the cytoplasm of stem cells and germline cells and may be involved in regulating some gene expression. We suggest that planarian Piwi controls germline formation via RNA silencing mechanisms.

Original languageEnglish
Pages (from-to)167-176
Number of pages10
JournalDevelopmental Biology
Volume361
Issue number1
DOIs
Publication statusPublished - 2012 Jan 1

Fingerprint

Planarians
RNA Interference
Germ Cells
Stem Cells
Gametogenesis
Pluripotent Stem Cells
Adult Stem Cells
Testis
Regeneration
Ovary
Cytoplasm
Homeostasis
Maintenance
X-Rays
Gene Expression

Keywords

  • Germline cell formation
  • Piwi
  • Planarians
  • Stem cell regulation

ASJC Scopus subject areas

  • Developmental Biology
  • Cell Biology
  • Molecular Biology

Cite this

Drpiwi-1 is essential for germline cell formation during sexualization of the planarian Dugesia ryukyuensis. / Nakagawa, Haruka; Ishizu, Hirotsugu; Hasegawa, Reiko; Kobayashi, Kazuya; Matsumoto, Midori.

In: Developmental Biology, Vol. 361, No. 1, 01.01.2012, p. 167-176.

Research output: Contribution to journalArticle

@article{d4128670503e43d5b0b304cd0c791712,
title = "Drpiwi-1 is essential for germline cell formation during sexualization of the planarian Dugesia ryukyuensis",
abstract = "A piwi homolog is required for the regulation of stem cells, formation and maintenance of germline stem cells, and gametogenesis in many metazoans. Planarians can change their reproductive mode seasonally, both asexually and sexually, and develop and maintain germ cells and sexual organs. They have many pluripotent stem cells (neoblasts) that can differentiate into both somatic and germline stem cells. Thus, we searched for a piwi subfamily in the planarian Dugesia ryukyuensis. Four piwi homologs, identified as Drpiwi-1, -2, -3, and -4, were expressed in sexually reproductive worms. We then selectively destroyed the neoblasts by irradiating the worms with X-rays. In such worms, Drpiwi-1, -2, and -3 were not expressed at all, whereas Drpiwi-4 was expressed to the same degree as that in non-irradiated controls, indicating that Drpiwi-1, -2, and -3, but not Drpiwi-4, are expressed in neoblasts. During the regeneration process, Drpiwi-2(RNAi) and -3(RNAi) worms failed to regenerate after ablation, but Drpiwi-1 and -4(RNAi) worms regenerated. During the sexualizing process, Drpiwi-1(RNAi) worms failed to develop ovaries and testes, but somatic sexual organs were unaffected. Germ cell development was normal in Drpiwi-4(RNAi) worms. Therefore, Drpiwi-2 and -3 may be related to the regulation of neoblasts important for maintaining homeostasis, and Drpiwi-1 is essential for the development of germ cells but not somatic sexual organs. DrPiwi-1 is localized in the cytoplasm of stem cells and germline cells and may be involved in regulating some gene expression. We suggest that planarian Piwi controls germline formation via RNA silencing mechanisms.",
keywords = "Germline cell formation, Piwi, Planarians, Stem cell regulation",
author = "Haruka Nakagawa and Hirotsugu Ishizu and Reiko Hasegawa and Kazuya Kobayashi and Midori Matsumoto",
year = "2012",
month = "1",
day = "1",
doi = "10.1016/j.ydbio.2011.10.014",
language = "English",
volume = "361",
pages = "167--176",
journal = "Developmental Biology",
issn = "0012-1606",
publisher = "Academic Press Inc.",
number = "1",

}

TY - JOUR

T1 - Drpiwi-1 is essential for germline cell formation during sexualization of the planarian Dugesia ryukyuensis

AU - Nakagawa, Haruka

AU - Ishizu, Hirotsugu

AU - Hasegawa, Reiko

AU - Kobayashi, Kazuya

AU - Matsumoto, Midori

PY - 2012/1/1

Y1 - 2012/1/1

N2 - A piwi homolog is required for the regulation of stem cells, formation and maintenance of germline stem cells, and gametogenesis in many metazoans. Planarians can change their reproductive mode seasonally, both asexually and sexually, and develop and maintain germ cells and sexual organs. They have many pluripotent stem cells (neoblasts) that can differentiate into both somatic and germline stem cells. Thus, we searched for a piwi subfamily in the planarian Dugesia ryukyuensis. Four piwi homologs, identified as Drpiwi-1, -2, -3, and -4, were expressed in sexually reproductive worms. We then selectively destroyed the neoblasts by irradiating the worms with X-rays. In such worms, Drpiwi-1, -2, and -3 were not expressed at all, whereas Drpiwi-4 was expressed to the same degree as that in non-irradiated controls, indicating that Drpiwi-1, -2, and -3, but not Drpiwi-4, are expressed in neoblasts. During the regeneration process, Drpiwi-2(RNAi) and -3(RNAi) worms failed to regenerate after ablation, but Drpiwi-1 and -4(RNAi) worms regenerated. During the sexualizing process, Drpiwi-1(RNAi) worms failed to develop ovaries and testes, but somatic sexual organs were unaffected. Germ cell development was normal in Drpiwi-4(RNAi) worms. Therefore, Drpiwi-2 and -3 may be related to the regulation of neoblasts important for maintaining homeostasis, and Drpiwi-1 is essential for the development of germ cells but not somatic sexual organs. DrPiwi-1 is localized in the cytoplasm of stem cells and germline cells and may be involved in regulating some gene expression. We suggest that planarian Piwi controls germline formation via RNA silencing mechanisms.

AB - A piwi homolog is required for the regulation of stem cells, formation and maintenance of germline stem cells, and gametogenesis in many metazoans. Planarians can change their reproductive mode seasonally, both asexually and sexually, and develop and maintain germ cells and sexual organs. They have many pluripotent stem cells (neoblasts) that can differentiate into both somatic and germline stem cells. Thus, we searched for a piwi subfamily in the planarian Dugesia ryukyuensis. Four piwi homologs, identified as Drpiwi-1, -2, -3, and -4, were expressed in sexually reproductive worms. We then selectively destroyed the neoblasts by irradiating the worms with X-rays. In such worms, Drpiwi-1, -2, and -3 were not expressed at all, whereas Drpiwi-4 was expressed to the same degree as that in non-irradiated controls, indicating that Drpiwi-1, -2, and -3, but not Drpiwi-4, are expressed in neoblasts. During the regeneration process, Drpiwi-2(RNAi) and -3(RNAi) worms failed to regenerate after ablation, but Drpiwi-1 and -4(RNAi) worms regenerated. During the sexualizing process, Drpiwi-1(RNAi) worms failed to develop ovaries and testes, but somatic sexual organs were unaffected. Germ cell development was normal in Drpiwi-4(RNAi) worms. Therefore, Drpiwi-2 and -3 may be related to the regulation of neoblasts important for maintaining homeostasis, and Drpiwi-1 is essential for the development of germ cells but not somatic sexual organs. DrPiwi-1 is localized in the cytoplasm of stem cells and germline cells and may be involved in regulating some gene expression. We suggest that planarian Piwi controls germline formation via RNA silencing mechanisms.

KW - Germline cell formation

KW - Piwi

KW - Planarians

KW - Stem cell regulation

UR - http://www.scopus.com/inward/record.url?scp=83055186510&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=83055186510&partnerID=8YFLogxK

U2 - 10.1016/j.ydbio.2011.10.014

DO - 10.1016/j.ydbio.2011.10.014

M3 - Article

C2 - 22024321

AN - SCOPUS:83055186510

VL - 361

SP - 167

EP - 176

JO - Developmental Biology

JF - Developmental Biology

SN - 0012-1606

IS - 1

ER -