Cargando…

Diversity of function and higher-order structure within HWE sensor histidine kinases

Integral to the protein structure/function paradigm, oligomeric state is typically conserved along with function across evolution. However, notable exceptions such as the hemoglobins show how evolution can alter oligomerization to enable new regulatory mechanisms. Here, we examine this linkage in hi...

Descripción completa

Detalles Bibliográficos
Autores principales: Dikiy, Igor, Swingle, Danielle, Toy, Kaitlyn, Edupuganti, Uthama R., Rivera-Cancel, Giomar, Gardner, Kevin H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Biochemistry and Molecular Biology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10359499/
https://www.ncbi.nlm.nih.gov/pubmed/37331599
http://dx.doi.org/10.1016/j.jbc.2023.104934
_version_ 1785075896583979008
author Dikiy, Igor
Swingle, Danielle
Toy, Kaitlyn
Edupuganti, Uthama R.
Rivera-Cancel, Giomar
Gardner, Kevin H.
author_facet Dikiy, Igor
Swingle, Danielle
Toy, Kaitlyn
Edupuganti, Uthama R.
Rivera-Cancel, Giomar
Gardner, Kevin H.
author_sort Dikiy, Igor
collection PubMed
description Integral to the protein structure/function paradigm, oligomeric state is typically conserved along with function across evolution. However, notable exceptions such as the hemoglobins show how evolution can alter oligomerization to enable new regulatory mechanisms. Here, we examine this linkage in histidine kinases (HKs), a large class of widely distributed prokaryotic environmental sensors. While the majority of HKs are transmembrane homodimers, members of the HWE/HisKA2 family can deviate from this architecture as exemplified by our finding of a monomeric soluble HWE/HisKA2 HK (EL346, a photosensing light-oxygen-voltage [LOV]-HK). To further explore the diversity of oligomerization states and regulation within this family, we biophysically and biochemically characterized multiple EL346 homologs and found a range of HK oligomeric states and functions. Three LOV-HK homologs are primarily dimeric with differing structural and functional responses to light, while two Per-ARNT-Sim–HKs interconvert between differentially active monomers and dimers, suggesting dimerization might control enzymatic activity for these proteins. Finally, we examined putative interfaces in a dimeric LOV-HK, finding that multiple regions contribute to dimerization. Our findings suggest the potential for novel regulatory modes and oligomeric states beyond those traditionally defined for this important family of environmental sensors.
format Online
Article
Text
id pubmed-10359499
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher American Society for Biochemistry and Molecular Biology
record_format MEDLINE/PubMed
spelling pubmed-103594992023-07-22 Diversity of function and higher-order structure within HWE sensor histidine kinases Dikiy, Igor Swingle, Danielle Toy, Kaitlyn Edupuganti, Uthama R. Rivera-Cancel, Giomar Gardner, Kevin H. J Biol Chem Research Article Integral to the protein structure/function paradigm, oligomeric state is typically conserved along with function across evolution. However, notable exceptions such as the hemoglobins show how evolution can alter oligomerization to enable new regulatory mechanisms. Here, we examine this linkage in histidine kinases (HKs), a large class of widely distributed prokaryotic environmental sensors. While the majority of HKs are transmembrane homodimers, members of the HWE/HisKA2 family can deviate from this architecture as exemplified by our finding of a monomeric soluble HWE/HisKA2 HK (EL346, a photosensing light-oxygen-voltage [LOV]-HK). To further explore the diversity of oligomerization states and regulation within this family, we biophysically and biochemically characterized multiple EL346 homologs and found a range of HK oligomeric states and functions. Three LOV-HK homologs are primarily dimeric with differing structural and functional responses to light, while two Per-ARNT-Sim–HKs interconvert between differentially active monomers and dimers, suggesting dimerization might control enzymatic activity for these proteins. Finally, we examined putative interfaces in a dimeric LOV-HK, finding that multiple regions contribute to dimerization. Our findings suggest the potential for novel regulatory modes and oligomeric states beyond those traditionally defined for this important family of environmental sensors. American Society for Biochemistry and Molecular Biology 2023-06-17 /pmc/articles/PMC10359499/ /pubmed/37331599 http://dx.doi.org/10.1016/j.jbc.2023.104934 Text en © 2023 The Authors https://creativecommons.org/licenses/by/4.0/This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Research Article
Dikiy, Igor
Swingle, Danielle
Toy, Kaitlyn
Edupuganti, Uthama R.
Rivera-Cancel, Giomar
Gardner, Kevin H.
Diversity of function and higher-order structure within HWE sensor histidine kinases
title Diversity of function and higher-order structure within HWE sensor histidine kinases
title_full Diversity of function and higher-order structure within HWE sensor histidine kinases
title_fullStr Diversity of function and higher-order structure within HWE sensor histidine kinases
title_full_unstemmed Diversity of function and higher-order structure within HWE sensor histidine kinases
title_short Diversity of function and higher-order structure within HWE sensor histidine kinases
title_sort diversity of function and higher-order structure within hwe sensor histidine kinases
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10359499/
https://www.ncbi.nlm.nih.gov/pubmed/37331599
http://dx.doi.org/10.1016/j.jbc.2023.104934
work_keys_str_mv AT dikiyigor diversityoffunctionandhigherorderstructurewithinhwesensorhistidinekinases
AT swingledanielle diversityoffunctionandhigherorderstructurewithinhwesensorhistidinekinases
AT toykaitlyn diversityoffunctionandhigherorderstructurewithinhwesensorhistidinekinases
AT edupugantiuthamar diversityoffunctionandhigherorderstructurewithinhwesensorhistidinekinases
AT riveracancelgiomar diversityoffunctionandhigherorderstructurewithinhwesensorhistidinekinases
AT gardnerkevinh diversityoffunctionandhigherorderstructurewithinhwesensorhistidinekinases