Chemoattractant receptors activate, recruit and capture G proteins for wide range chemotaxis

Yukihiro Miyanaga, Yoichiro Kamimura, Hidekazu Kuwayama, Peter N Devreotes, Masahiro Ueda

Research output: Contribution to journalArticle

Abstract

The wide range sensing of extracellular signals is a common feature of various sensory cells. Eukaryotic chemotactic cells driven by GPCRs and their cognate G proteins are one example. This system endows the cells directional motility towards their destination over long distances. There are several mechanisms to achieve the long dynamic range, including negative regulation of the receptors upon ligand interaction and spatial regulation of G proteins, as we found recently. However, these mechanisms are insufficient to explain the 105-fold range of chemotaxis seen in Dictyostelium. Here, we reveal that the receptor-mediated activation, recruitment, and capturing of G proteins mediate chemotactic signaling at the lower, middle and higher concentration ranges, respectively. These multiple mechanisms of G protein dynamics can successfully cover distinct ranges of ligand concentrations, resulting in seamless and broad chemotaxis. Furthermore, single-molecule imaging analysis showed that the activated Gα subunit forms an unconventional complex with the agonist-bound receptor. This complex formation of GPCR-Gα increased the membrane-binding time of individual Gα molecules and therefore resulted in the local accumulation of Gα. Our findings provide an additional chemotactic dynamic range mechanism in which multiple G protein dynamics positively contribute to the production of gradient information.

Original languageEnglish (US)
Pages (from-to)304-310
Number of pages7
JournalBiochemical and Biophysical Research Communications
Volume507
Issue number1-4
DOIs
StatePublished - Dec 9 2018

Fingerprint

Formyl Peptide Receptor
Chemotaxis
GTP-Binding Proteins
Ligands
Molecules
Dictyostelium
Eukaryotic Cells
Cell Movement
Chemical activation
Membranes
Imaging techniques

Keywords

  • Dynamic range extension
  • Eukaryotic chemotaxis
  • G protein-coupled receptor
  • Gradient sensing
  • Single-molecule analysis

ASJC Scopus subject areas

  • Biophysics
  • Biochemistry
  • Molecular Biology
  • Cell Biology

Cite this

Chemoattractant receptors activate, recruit and capture G proteins for wide range chemotaxis. / Miyanaga, Yukihiro; Kamimura, Yoichiro; Kuwayama, Hidekazu; Devreotes, Peter N; Ueda, Masahiro.

In: Biochemical and Biophysical Research Communications, Vol. 507, No. 1-4, 09.12.2018, p. 304-310.

Research output: Contribution to journalArticle

Miyanaga, Yukihiro ; Kamimura, Yoichiro ; Kuwayama, Hidekazu ; Devreotes, Peter N ; Ueda, Masahiro. / Chemoattractant receptors activate, recruit and capture G proteins for wide range chemotaxis. In: Biochemical and Biophysical Research Communications. 2018 ; Vol. 507, No. 1-4. pp. 304-310.
@article{78563bc8fcb14cec82abb1758870232a,
title = "Chemoattractant receptors activate, recruit and capture G proteins for wide range chemotaxis",
abstract = "The wide range sensing of extracellular signals is a common feature of various sensory cells. Eukaryotic chemotactic cells driven by GPCRs and their cognate G proteins are one example. This system endows the cells directional motility towards their destination over long distances. There are several mechanisms to achieve the long dynamic range, including negative regulation of the receptors upon ligand interaction and spatial regulation of G proteins, as we found recently. However, these mechanisms are insufficient to explain the 105-fold range of chemotaxis seen in Dictyostelium. Here, we reveal that the receptor-mediated activation, recruitment, and capturing of G proteins mediate chemotactic signaling at the lower, middle and higher concentration ranges, respectively. These multiple mechanisms of G protein dynamics can successfully cover distinct ranges of ligand concentrations, resulting in seamless and broad chemotaxis. Furthermore, single-molecule imaging analysis showed that the activated Gα subunit forms an unconventional complex with the agonist-bound receptor. This complex formation of GPCR-Gα increased the membrane-binding time of individual Gα molecules and therefore resulted in the local accumulation of Gα. Our findings provide an additional chemotactic dynamic range mechanism in which multiple G protein dynamics positively contribute to the production of gradient information.",
keywords = "Dynamic range extension, Eukaryotic chemotaxis, G protein-coupled receptor, Gradient sensing, Single-molecule analysis",
author = "Yukihiro Miyanaga and Yoichiro Kamimura and Hidekazu Kuwayama and Devreotes, {Peter N} and Masahiro Ueda",
year = "2018",
month = "12",
day = "9",
doi = "10.1016/j.bbrc.2018.11.029",
language = "English (US)",
volume = "507",
pages = "304--310",
journal = "Biochemical and Biophysical Research Communications",
issn = "0006-291X",
publisher = "Academic Press Inc.",
number = "1-4",

}

TY - JOUR

T1 - Chemoattractant receptors activate, recruit and capture G proteins for wide range chemotaxis

AU - Miyanaga, Yukihiro

AU - Kamimura, Yoichiro

AU - Kuwayama, Hidekazu

AU - Devreotes, Peter N

AU - Ueda, Masahiro

PY - 2018/12/9

Y1 - 2018/12/9

N2 - The wide range sensing of extracellular signals is a common feature of various sensory cells. Eukaryotic chemotactic cells driven by GPCRs and their cognate G proteins are one example. This system endows the cells directional motility towards their destination over long distances. There are several mechanisms to achieve the long dynamic range, including negative regulation of the receptors upon ligand interaction and spatial regulation of G proteins, as we found recently. However, these mechanisms are insufficient to explain the 105-fold range of chemotaxis seen in Dictyostelium. Here, we reveal that the receptor-mediated activation, recruitment, and capturing of G proteins mediate chemotactic signaling at the lower, middle and higher concentration ranges, respectively. These multiple mechanisms of G protein dynamics can successfully cover distinct ranges of ligand concentrations, resulting in seamless and broad chemotaxis. Furthermore, single-molecule imaging analysis showed that the activated Gα subunit forms an unconventional complex with the agonist-bound receptor. This complex formation of GPCR-Gα increased the membrane-binding time of individual Gα molecules and therefore resulted in the local accumulation of Gα. Our findings provide an additional chemotactic dynamic range mechanism in which multiple G protein dynamics positively contribute to the production of gradient information.

AB - The wide range sensing of extracellular signals is a common feature of various sensory cells. Eukaryotic chemotactic cells driven by GPCRs and their cognate G proteins are one example. This system endows the cells directional motility towards their destination over long distances. There are several mechanisms to achieve the long dynamic range, including negative regulation of the receptors upon ligand interaction and spatial regulation of G proteins, as we found recently. However, these mechanisms are insufficient to explain the 105-fold range of chemotaxis seen in Dictyostelium. Here, we reveal that the receptor-mediated activation, recruitment, and capturing of G proteins mediate chemotactic signaling at the lower, middle and higher concentration ranges, respectively. These multiple mechanisms of G protein dynamics can successfully cover distinct ranges of ligand concentrations, resulting in seamless and broad chemotaxis. Furthermore, single-molecule imaging analysis showed that the activated Gα subunit forms an unconventional complex with the agonist-bound receptor. This complex formation of GPCR-Gα increased the membrane-binding time of individual Gα molecules and therefore resulted in the local accumulation of Gα. Our findings provide an additional chemotactic dynamic range mechanism in which multiple G protein dynamics positively contribute to the production of gradient information.

KW - Dynamic range extension

KW - Eukaryotic chemotaxis

KW - G protein-coupled receptor

KW - Gradient sensing

KW - Single-molecule analysis

UR - http://www.scopus.com/inward/record.url?scp=85056735802&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85056735802&partnerID=8YFLogxK

U2 - 10.1016/j.bbrc.2018.11.029

DO - 10.1016/j.bbrc.2018.11.029

M3 - Article

C2 - 30454895

AN - SCOPUS:85056735802

VL - 507

SP - 304

EP - 310

JO - Biochemical and Biophysical Research Communications

JF - Biochemical and Biophysical Research Communications

SN - 0006-291X

IS - 1-4

ER -