Juvenile hormone signaling promotes ovulation and maintains egg shape by inducing expression of extracellular matrix genes

Wei Luo; Suning Liu; Wenqiang Zhang; Liu Yang; Jianhua Huang; Shutang Zhou; Qili Feng; Subba Reddy Palli; Jian Wang; Siegfried Roth; Sheng Li

doi:10.1073/pnas.2104461118

Juvenile hormone signaling promotes ovulation and maintains egg shape by inducing expression of extracellular matrix genes

Wei Luo, Suning Liu, Wenqiang Zhang, Liu Yang, Jianhua Huang, Shutang Zhou, Qili Feng, Subba Reddy Palli, Jian Wang, Siegfried Roth, Sheng Li

Research output: Contribution to journal › Article › peer-review

17 Scopus citations

Abstract

It is well documented that the juvenile hormone (JH) can function as a gonadotropic hormone that stimulates vitellogenesis by activating the production and uptake of vitellogenin in insects. Here, we describe a phenotype associated with mutations in the Drosophila JH receptor genes, Met and Gce: The accumulation of mature eggs with reduced egg length in the ovary. JH signaling is mainly activated in ovarian muscle cells and induces laminin gene expression in these cells. Meanwhile, JH signaling induces collagen IV gene expression in the adult fat body, from which collagen IV is secreted and deposited onto the ovarian muscles. Laminin locally and collagen IV remotely contribute to the assembly of ovarian muscle extracellular matrix (ECM); moreover, the ECM components are indispensable for ovarian muscle contraction. Furthermore, ovarian muscle contraction externally generates a mechanical force to promote ovulation and maintain egg shape. This work reveals an important mechanism for JHregulated insect reproduction.

Original language	English
Article number	e2104461118
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	118
Issue number	39
DOIs	https://doi.org/10.1073/pnas.2104461118
State	Published - Sep 28 2021

Bibliographical note

Funding Information:
ACKNOWLEDGMENTS. We greatly appreciate Dr. Marek Jindra and Dr. Sally Horne-Badovinac for their great comments and suggestions to improve this paper. This study was supported by the National Science Foundation of China (Grant Nos. 31620103917, 31970459, 32070441, 31702054, and 31930014) to S. Li, J.W., and S. Liu; the Shenzhen Science and Technology Program (Grant No. 20180411143628272) to S. Li; and the Natural Science Foundation of Guangdong Province (Grant No. 2019A1515011899) to S. Liu.

Publisher Copyright:
© 2021 National Academy of Sciences. All rights reserved.

Keywords

Collagen IV
Egg chamber elongation
Laminin
Ovarian contraction
Visceral muscle

ASJC Scopus subject areas

General

Access to Document

10.1073/pnas.2104461118

Cite this

Luo, W., Liu, S., Zhang, W., Yang, L., Huang, J., Zhou, S., Feng, Q., Palli, S. R., Wang, J., Roth, S., & Li, S. (2021). Juvenile hormone signaling promotes ovulation and maintains egg shape by inducing expression of extracellular matrix genes. Proceedings of the National Academy of Sciences of the United States of America, 118(39), [e2104461118]. https://doi.org/10.1073/pnas.2104461118

@article{71fe9c4be8d44a1aac81ad0ed4d0a8b8,

title = "Juvenile hormone signaling promotes ovulation and maintains egg shape by inducing expression of extracellular matrix genes",

abstract = "It is well documented that the juvenile hormone (JH) can function as a gonadotropic hormone that stimulates vitellogenesis by activating the production and uptake of vitellogenin in insects. Here, we describe a phenotype associated with mutations in the Drosophila JH receptor genes, Met and Gce: The accumulation of mature eggs with reduced egg length in the ovary. JH signaling is mainly activated in ovarian muscle cells and induces laminin gene expression in these cells. Meanwhile, JH signaling induces collagen IV gene expression in the adult fat body, from which collagen IV is secreted and deposited onto the ovarian muscles. Laminin locally and collagen IV remotely contribute to the assembly of ovarian muscle extracellular matrix (ECM); moreover, the ECM components are indispensable for ovarian muscle contraction. Furthermore, ovarian muscle contraction externally generates a mechanical force to promote ovulation and maintain egg shape. This work reveals an important mechanism for JHregulated insect reproduction.",

keywords = "Collagen IV, Egg chamber elongation, Laminin, Ovarian contraction, Visceral muscle",

author = "Wei Luo and Suning Liu and Wenqiang Zhang and Liu Yang and Jianhua Huang and Shutang Zhou and Qili Feng and Palli, {Subba Reddy} and Jian Wang and Siegfried Roth and Sheng Li",

note = "Funding Information: ACKNOWLEDGMENTS. We greatly appreciate Dr. Marek Jindra and Dr. Sally Horne-Badovinac for their great comments and suggestions to improve this paper. This study was supported by the National Science Foundation of China (Grant Nos. 31620103917, 31970459, 32070441, 31702054, and 31930014) to S. Li, J.W., and S. Liu; the Shenzhen Science and Technology Program (Grant No. 20180411143628272) to S. Li; and the Natural Science Foundation of Guangdong Province (Grant No. 2019A1515011899) to S. Liu. Publisher Copyright: {\textcopyright} 2021 National Academy of Sciences. All rights reserved.",

year = "2021",

month = sep,

day = "28",

doi = "10.1073/pnas.2104461118",

language = "English",

volume = "118",

number = "39",

}

Luo, W, Liu, S, Zhang, W, Yang, L, Huang, J, Zhou, S, Feng, Q, Palli, SR, Wang, J, Roth, S & Li, S 2021, 'Juvenile hormone signaling promotes ovulation and maintains egg shape by inducing expression of extracellular matrix genes', Proceedings of the National Academy of Sciences of the United States of America, vol. 118, no. 39, e2104461118. https://doi.org/10.1073/pnas.2104461118

TY - JOUR

T1 - Juvenile hormone signaling promotes ovulation and maintains egg shape by inducing expression of extracellular matrix genes

AU - Luo, Wei

AU - Liu, Suning

AU - Zhang, Wenqiang

AU - Yang, Liu

AU - Huang, Jianhua

AU - Zhou, Shutang

AU - Feng, Qili

AU - Palli, Subba Reddy

AU - Wang, Jian

AU - Roth, Siegfried

AU - Li, Sheng

N1 - Funding Information: ACKNOWLEDGMENTS. We greatly appreciate Dr. Marek Jindra and Dr. Sally Horne-Badovinac for their great comments and suggestions to improve this paper. This study was supported by the National Science Foundation of China (Grant Nos. 31620103917, 31970459, 32070441, 31702054, and 31930014) to S. Li, J.W., and S. Liu; the Shenzhen Science and Technology Program (Grant No. 20180411143628272) to S. Li; and the Natural Science Foundation of Guangdong Province (Grant No. 2019A1515011899) to S. Liu. Publisher Copyright: © 2021 National Academy of Sciences. All rights reserved.

PY - 2021/9/28

Y1 - 2021/9/28

N2 - It is well documented that the juvenile hormone (JH) can function as a gonadotropic hormone that stimulates vitellogenesis by activating the production and uptake of vitellogenin in insects. Here, we describe a phenotype associated with mutations in the Drosophila JH receptor genes, Met and Gce: The accumulation of mature eggs with reduced egg length in the ovary. JH signaling is mainly activated in ovarian muscle cells and induces laminin gene expression in these cells. Meanwhile, JH signaling induces collagen IV gene expression in the adult fat body, from which collagen IV is secreted and deposited onto the ovarian muscles. Laminin locally and collagen IV remotely contribute to the assembly of ovarian muscle extracellular matrix (ECM); moreover, the ECM components are indispensable for ovarian muscle contraction. Furthermore, ovarian muscle contraction externally generates a mechanical force to promote ovulation and maintain egg shape. This work reveals an important mechanism for JHregulated insect reproduction.

AB - It is well documented that the juvenile hormone (JH) can function as a gonadotropic hormone that stimulates vitellogenesis by activating the production and uptake of vitellogenin in insects. Here, we describe a phenotype associated with mutations in the Drosophila JH receptor genes, Met and Gce: The accumulation of mature eggs with reduced egg length in the ovary. JH signaling is mainly activated in ovarian muscle cells and induces laminin gene expression in these cells. Meanwhile, JH signaling induces collagen IV gene expression in the adult fat body, from which collagen IV is secreted and deposited onto the ovarian muscles. Laminin locally and collagen IV remotely contribute to the assembly of ovarian muscle extracellular matrix (ECM); moreover, the ECM components are indispensable for ovarian muscle contraction. Furthermore, ovarian muscle contraction externally generates a mechanical force to promote ovulation and maintain egg shape. This work reveals an important mechanism for JHregulated insect reproduction.

KW - Collagen IV

KW - Egg chamber elongation

KW - Laminin

KW - Ovarian contraction

KW - Visceral muscle

UR - http://www.scopus.com/inward/record.url?scp=85116066115&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85116066115&partnerID=8YFLogxK

U2 - 10.1073/pnas.2104461118

DO - 10.1073/pnas.2104461118

M3 - Article

C2 - 34544864

AN - SCOPUS:85116066115

VL - 118

IS - 39

M1 - e2104461118

ER -

Juvenile hormone signaling promotes ovulation and maintains egg shape by inducing expression of extracellular matrix genes

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Cite this