Conformational dynamics are a key factor in signaling mediated
by the receiver domain of a sensor histidine kinase from
Arabidopsis thaliana

J 2017

Conformational dynamics are a key factor in signaling mediated by the receiver domain of a sensor histidine kinase from Arabidopsis thaliana

OTRUSINOVÁ, Olga, Gabriel DEMO, Petr PADRTA, Zuzana JASEŇÁKOVÁ, Blanka PEKÁROVÁ et. al.

Základní údaje

Originální název

Conformational dynamics are a key factor in signaling mediated by the receiver domain of a sensor histidine kinase from Arabidopsis thaliana

Autoři

OTRUSINOVÁ, Olga (203 Česká republika, domácí), Gabriel DEMO (703 Slovensko, domácí), Petr PADRTA (203 Česká republika, domácí), Zuzana JASEŇÁKOVÁ (703 Slovensko, domácí), Blanka PEKÁROVÁ (203 Česká republika, domácí), Zuzana GELOVÁ (203 Česká republika, domácí), Agnieszka SZMITKOWSKA (616 Polsko, domácí), Pavel KADEŘÁVEK (203 Česká republika, domácí), Séverine JANSEN (250 Francie, domácí), Milan ZACHRDLA (203 Česká republika, domácí), Tomáš KLUMPLER (203 Česká republika, domácí), Jaromír MAREK (203 Česká republika, domácí), Jozef HRITZ (703 Slovensko, domácí), Lubomír JANDA (203 Česká republika, domácí), Hideo IWAI (246 Finsko), Michaela WIMMEROVÁ (203 Česká republika, domácí), Jan HEJÁTKO (203 Česká republika, domácí) a Lukáš ŽÍDEK (203 Česká republika, garant, domácí)

Vydání

Journal of Biological Chemistry, Bethesda, USA, Amer. Soc. Biochem. Mol. Biol. 2017, 0021-9258

Další údaje

Jazyk

angličtina

Typ výsledku

Článek v odborném periodiku

Obor

10600 1.6 Biological sciences

Stát vydavatele

Spojené státy

Utajení

není předmětem státního či obchodního tajemství

Odkazy

URL

Impakt faktor

Impact factor: 4.011

Kód RIV

RIV/00216224:14740/17:00095060

Organizační jednotka

Středoevropský technologický institut

DOI

http://dx.doi.org/10.1074/jbc.M117.790212

UT WoS

000414009300032

Klíčová slova anglicky

histidine kinase; nuclear magnetic resonance (NMR); protein dynamic; protein phosphorylation; X-ray crystallography; receiver domain; relaxation dispersion

Štítky

CF NMR, rivok

Příznaky

Mezinárodní význam, Recenzováno

Změněno: 12. 4. 2018 11:22, Mgr. Pavla Foltynová, Ph.D.

Anotace

V originále

Multistep phosphorelay (MSP) cascades mediate responses to a wide spectrum of stimuli, including plant hormonal signaling, but several aspects of MSP await elucidation. Here, we provide first insight into the key step of MSP- mediated phosphotransfer in a eukaryotic system, the phosphorylation of the receiver domain of the histidine kinase CYTOKININ-INDEPENDENT 1 (CKI1(RD)) from Arabidopsis thaliana. We observed that the crystal structures of free, Mg2+-bound, and beryllofluoridated CKI1(RD) (a stable analogue of the labile phosphorylated form) were identical and similar to the active state of receiver domains of bacterial response regulators. However, the three CKI1(RD) variants exhibited different conformational dynamics in solution. NMR studies revealed that Mg2+ binding and beryllofluoridation alter the conformational equilibrium of the beta 3-beta 3 loop close to the phosphorylation site. Mutations that perturbed the conformational behavior of the beta 3-beta 3 loop while keeping the active- site aspartate intact resulted in suppression of CKI1 function. Mechanistically, homology modeling indicated that the beta 3 beta 3 loop directly interacts with the ATP- binding site of the CKI1 histidine kinase domain. The functional relevance of the conformational dynamics observed in the beta 3-beta 3 loop of CKI1(RD) was supported by a comparison with another A. thaliana histidine kinase, ETR1. In contrast to the highly dynamic beta 3- beta 3 loop of CKI1(RD), the corresponding loop of the ETR1 receiver domain (ETR1(RD)) exhibited little conformational exchange and adopted a different orientation in crystals. Biochem-ical data indicated that ETR1(RD) is involved in phosphorylation-independent signaling, implying a direct link between conformational behavior and the ability of eukaryotic receiver domains to participate in MSP.

Návaznosti

GA13-25280S, projekt VaV

Název: Elucidating molecular mechanisms of cytokinins-ethylene crosstalk in the plant development

Investor: Grantová agentura ČR, Elucidating molecular mechanisms of cytokinins-ethylene crosstalk in the plant development

LM2015043, projekt VaV

Název: Česká infrastruktura pro integrativní strukturní biologii (Akronym: CIISB)

Investor: Ministerstvo školství, mládeže a tělovýchovy ČR, Czech Infrastructure for Integrative Structural Biology

LQ1601, projekt VaV

Název: CEITEC 2020 (Akronym: CEITEC2020)

Investor: Ministerstvo školství, mládeže a tělovýchovy ČR, CEITEC 2020

Citovat

OTRUSINOVÁ, Olga, Gabriel DEMO, Petr PADRTA, Zuzana JASEŇÁKOVÁ, Blanka PEKÁROVÁ, Zuzana GELOVÁ, Agnieszka SZMITKOWSKA, Pavel KADEŘÁVEK, Séverine JANSEN, Milan ZACHRDLA, Tomáš KLUMPLER, Jaromír MAREK, Jozef HRITZ, Lubomír JANDA, Hideo IWAI, Michaela WIMMEROVÁ, Jan HEJÁTKO a Lukáš ŽÍDEK. Conformational dynamics are a key factor in signaling mediated by the receiver domain of a sensor histidine kinase from Arabidopsis thaliana. Journal of Biological Chemistry. Bethesda, USA: Amer. Soc. Biochem. Mol. Biol., 2017, roč. 292, č. 42, s. 17525-17540. ISSN 0021-9258. Dostupné z: https://dx.doi.org/10.1074/jbc.M117.790212.

@article{1392278,
   author = {Otrusinová, Olga and Demo, Gabriel and Padrta, Petr and Jaseňáková, Zuzana and Pekárová, Blanka and Gelová, Zuzana and Szmitkowska, Agnieszka and Kadeřávek, Pavel and Jansen, Séverine and Zachrdla, Milan and Klumpler, Tomáš and Marek, Jaromír and Hritz, Jozef and Janda, Lubomír and Iwai, Hideo and Wimmerová, Michaela and Hejátko, Jan and Žídek, Lukáš},
   article_location = {Bethesda, USA},
   article_number = {42},
   doi = {http://dx.doi.org/10.1074/jbc.M117.790212},
   keywords = {histidine kinase; nuclear magnetic resonance (NMR); protein dynamic; protein phosphorylation; X-ray crystallography; receiver domain; relaxation dispersion},
   language = {eng},
   issn = {0021-9258},
   journal = {Journal of Biological Chemistry},
   title = {Conformational dynamics are a key factor in signaling mediated by the receiver domain of a sensor histidine kinase from Arabidopsis thaliana},
   url = {http://www.jbc.org/content/early/2017/08/31/jbc.M117.790212.short},
   volume = {292},
   year = {2017}
}

TY  - JOUR
ID  - 1392278
AU  - Otrusinová, Olga - Demo, Gabriel - Padrta, Petr - Jaseňáková, Zuzana - Pekárová, Blanka - Gelová, Zuzana - Szmitkowska, Agnieszka - Kadeřávek, Pavel - Jansen, Séverine - Zachrdla, Milan - Klumpler, Tomáš - Marek, Jaromír - Hritz, Jozef - Janda, Lubomír - Iwai, Hideo - Wimmerová, Michaela - Hejátko, Jan - Žídek, Lukáš
PY  - 2017
TI  - Conformational dynamics are a key factor in signaling mediated by the receiver domain of a sensor histidine kinase from Arabidopsis thaliana
JF  - Journal of Biological Chemistry
VL  - 292
IS  - 42
SP  - 17525-17540
EP  - 17525-17540
PB  - Amer. Soc. Biochem. Mol. Biol.
SN  - 00219258
KW  - histidine kinase
KW  - nuclear magnetic resonance (NMR)
KW  - protein dynamic
KW  - protein phosphorylation
KW  - X-ray crystallography
KW  - receiver domain
KW  - relaxation dispersion
UR  - http://www.jbc.org/content/early/2017/08/31/jbc.M117.790212.short
L2  - http://www.jbc.org/content/early/2017/08/31/jbc.M117.790212.short
N2  - Multistep phosphorelay (MSP) cascades mediate responses to a wide spectrum of stimuli, including plant hormonal signaling, but several aspects of MSP await elucidation. Here, we provide first insight into the key step of MSP- mediated phosphotransfer in a eukaryotic system, the phosphorylation of the receiver domain of the histidine kinase CYTOKININ-INDEPENDENT 1 (CKI1(RD)) from Arabidopsis thaliana. We observed that the crystal structures of free, Mg2+-bound, and beryllofluoridated CKI1(RD) (a stable analogue of the labile phosphorylated form) were identical and similar to the active state of receiver domains of bacterial response regulators. However, the three CKI1(RD) variants exhibited different conformational dynamics in solution. NMR studies revealed that Mg2+ binding and beryllofluoridation alter the conformational equilibrium of the beta 3-beta 3 loop close to the phosphorylation site. Mutations that perturbed the conformational behavior of the beta 3-beta 3 loop while keeping the active- site aspartate intact resulted in suppression of CKI1 function. Mechanistically, homology modeling indicated that the beta 3 beta 3 loop directly interacts with the ATP- binding site of the CKI1 histidine kinase domain. The functional relevance of the conformational dynamics observed in the beta 3-beta 3 loop of CKI1(RD) was supported by a comparison with another A. thaliana histidine kinase, ETR1. In contrast to the highly dynamic beta 3- beta 3 loop of CKI1(RD), the corresponding loop of the ETR1 receiver domain (ETR1(RD)) exhibited little conformational exchange and adopted a different orientation in crystals. Biochem-ical data indicated that ETR1(RD) is involved in phosphorylation-independent signaling, implying a direct link between conformational behavior and the ability of eukaryotic receiver domains to participate in MSP.
ER  -

OTRUSINOVÁ, Olga, Gabriel DEMO, Petr PADRTA, Zuzana JASEŇÁKOVÁ, Blanka PEKÁROVÁ, Zuzana GELOVÁ, Agnieszka SZMITKOWSKA, Pavel KADEŘÁVEK, Séverine JANSEN, Milan ZACHRDLA, Tomáš KLUMPLER, Jaromír MAREK, Jozef HRITZ, Lubomír JANDA, Hideo IWAI, Michaela WIMMEROVÁ, Jan HEJÁTKO a Lukáš ŽÍDEK. Conformational dynamics are a key factor in signaling mediated by the receiver domain of a sensor histidine kinase from Arabidopsis thaliana. \textit{Journal of Biological Chemistry}. Bethesda, USA: Amer. Soc. Biochem. Mol. Biol., 2017, roč.~292, č.~42, s.~17525-17540. ISSN~0021-9258. Dostupné z: https://dx.doi.org/10.1074/jbc.M117.790212.

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