Steroid receptor coactivator TAIMAN is a new modulator of
insect circadian clock

J 2023

Steroid receptor coactivator TAIMAN is a new modulator of insect circadian clock

SMYKAL, Vlastimil, Lenka CHODAKOVA, Marketa HEJNIKOVA, Kristína BRIEDIKOVÁ, Bulah Chia-Hsiang WU et. al.

Basic information

Original name

Steroid receptor coactivator TAIMAN is a new modulator of insect circadian clock

Authors

SMYKAL, Vlastimil, Lenka CHODAKOVA, Marketa HEJNIKOVA, Kristína BRIEDIKOVÁ (703 Slovakia, belonging to the institution), Bulah Chia-Hsiang WU, Hana VANECKOVA, Ping CHEN, Anna JANOVSKA, Pavlina KYJAKOVA, Martin VÁCHA (203 Czech Republic, belonging to the institution) and David DOLEZEL (guarantor)

Edition

PLoS Genetics, San Francisco, Public Library Science, 2023, 1553-7404

Other information

Language

English

Type of outcome

Článek v odborném periodiku

Field of Study

10602 Biology , Evolutionary biology

Country of publisher

United States of America

Confidentiality degree

není předmětem státního či obchodního tajemství

References:

URL

Impact factor

Impact factor: 4.500 in 2022

RIV identification code

RIV/00216224:14310/23:00133966

Organization unit

Faculty of Science

DOI

http://dx.doi.org/10.1371/journal.pgen.1010924

UT WoS

001159590000001

Keywords in English

Circadian rhythms; RNA interference; Larvae; Insects; Drosophila melanogaster; Hormones; Biological locomotion; Exon mapping

Abstract

V originále

TAIMAN (TAI), the only insect ortholog of mammalian Steroid Receptor Coactivators (SRCs), is a critical modulator of ecdysone and juvenile hormone (JH) signaling pathways, which govern insect development and reproduction. The modulatory effect is mediated by JH-dependent TAI’s heterodimerization with JH receptor Methoprene-tolerant and association with the Ecdysone Receptor complex. Insect hormones regulate insect physiology and development in concert with abiotic cues, such as photo- and thermoperiod. Here we tested the effects of JH and ecdysone signaling on the circadian clock by a combination of microsurgical operations, application of hormones and hormone mimics, and gene knockdowns in the linden bug Pyrrhocoris apterus males. Silencing taiman by each of three non-overlapping double-strand RNA fragments dramatically slowed the free-running period (FRP) to 27–29 hours, contrasting to 24 hours in controls. To further corroborate TAIMAN’s clock modulatory function in the insect circadian clock, we performed taiman knockdown in the cockroach Blattella germanica. Although Blattella and Pyrrhocoris lineages separated ~380 mya, B. germanica taiman silencing slowed the FRP by more than 2 hours, suggesting a conserved TAI clock function in (at least) some insect groups. Interestingly, the pace of the linden bug circadian clock was neither changed by blocking JH and ecdysone synthesis, by application of the hormones or their mimics nor by the knockdown of corresponding hormone receptors. Our results promote TAI as a new circadian clock modulator, a role described for the first time in insects. We speculate that TAI participation in the clock is congruent with the mammalian SRC-2 role in orchestrating metabolism and circadian rhythms, and that TAI/SRCs might be conserved components of the circadian clock in animals.

Links

QK1910286, research and development project

Name: Efektivní postupy a strategie pro zvládání včelích chorob a udržitelný chov včelstev

Investor: Ministry of Agriculture of the CR

Citovat

SMYKAL, Vlastimil, Lenka CHODAKOVA, Marketa HEJNIKOVA, Kristína BRIEDIKOVÁ, Bulah Chia-Hsiang WU, Hana VANECKOVA, Ping CHEN, Anna JANOVSKA, Pavlina KYJAKOVA, Martin VÁCHA and David DOLEZEL. Steroid receptor coactivator TAIMAN is a new modulator of insect circadian clock. PLoS Genetics. San Francisco: Public Library Science, 2023, vol. 19, No 9, p. 1-25. ISSN 1553-7404. Available from: https://dx.doi.org/10.1371/journal.pgen.1010924.

@article{2362038,
   author = {Smykal, Vlastimil and Chodakova, Lenka and Hejnikova, Marketa and Briediková, Kristína and Wu, Bulah ChiaandHsiang and Vaneckova, Hana and Chen, Ping and Janovska, Anna and Kyjakova, Pavlina and Vácha, Martin and Dolezel, David},
   article_location = {San Francisco},
   article_number = {9},
   doi = {http://dx.doi.org/10.1371/journal.pgen.1010924},
   keywords = {Circadian rhythms; RNA interference; Larvae; Insects; Drosophila melanogaster; Hormones; Biological locomotion; Exon mapping},
   language = {eng},
   issn = {1553-7404},
   journal = {PLoS Genetics},
   title = {Steroid receptor coactivator TAIMAN is a new modulator of insect circadian clock},
   url = {https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1010924},
   volume = {19},
   year = {2023}
}

TY  - JOUR
ID  - 2362038
AU  - Smykal, Vlastimil - Chodakova, Lenka - Hejnikova, Marketa - Briediková, Kristína - Wu, Bulah Chia-Hsiang - Vaneckova, Hana - Chen, Ping - Janovska, Anna - Kyjakova, Pavlina - Vácha, Martin - Dolezel, David
PY  - 2023
TI  - Steroid receptor coactivator TAIMAN is a new modulator of insect circadian clock
JF  - PLoS Genetics
VL  - 19
IS  - 9
SP  - 1-25
EP  - 1-25
PB  - Public Library Science
SN  - 15537404
KW  - Circadian rhythms
KW  - RNA interference
KW  - Larvae
KW  - Insects
KW  - Drosophila melanogaster
KW  - Hormones
KW  - Biological locomotion
KW  - Exon mapping
UR  - https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1010924
N2  - TAIMAN (TAI), the only insect ortholog of mammalian Steroid Receptor Coactivators (SRCs), is a critical modulator of ecdysone and juvenile hormone (JH) signaling pathways, which govern insect development and reproduction. The modulatory effect is mediated by JH-dependent TAI’s heterodimerization with JH receptor Methoprene-tolerant and association with the Ecdysone Receptor complex. Insect hormones regulate insect physiology and development in concert with abiotic cues, such as photo- and thermoperiod. Here we tested the effects of JH and ecdysone signaling on the circadian clock by a combination of microsurgical operations, application of hormones and hormone mimics, and gene knockdowns in the linden bug Pyrrhocoris apterus males. Silencing taiman by each of three non-overlapping double-strand RNA fragments dramatically slowed the free-running period (FRP) to 27–29 hours, contrasting to 24 hours in controls. To further corroborate TAIMAN’s clock modulatory function in the insect circadian clock, we performed taiman knockdown in the cockroach Blattella germanica. Although Blattella and Pyrrhocoris lineages separated ~380 mya, B. germanica taiman silencing slowed the FRP by more than 2 hours, suggesting a conserved TAI clock function in (at least) some insect groups. Interestingly, the pace of the linden bug circadian clock was neither changed by blocking JH and ecdysone synthesis, by application of the hormones or their mimics nor by the knockdown of corresponding hormone receptors. Our results promote TAI as a new circadian clock modulator, a role described for the first time in insects. We speculate that TAI participation in the clock is congruent with the mammalian SRC-2 role in orchestrating metabolism and circadian rhythms, and that TAI/SRCs might be conserved components of the circadian clock in animals.
ER  -

SMYKAL, Vlastimil, Lenka CHODAKOVA, Marketa HEJNIKOVA, Kristína BRIEDIKOVÁ, Bulah Chia-Hsiang WU, Hana VANECKOVA, Ping CHEN, Anna JANOVSKA, Pavlina KYJAKOVA, Martin VÁCHA and David DOLEZEL. Steroid receptor coactivator TAIMAN is a new modulator of insect circadian clock. \textit{PLoS Genetics}. San Francisco: Public Library Science, 2023, vol.~19, No~9, p.~1-25. ISSN~1553-7404. Available from: https://dx.doi.org/10.1371/journal.pgen.1010924.

Detailed Information on Publication Record