Macropinosome formation by tent pole ruffling in macrophages

Nicholas D. Condon, John M. Heddleston, Teng Leong Chew, Lin Luo, Peter S. McPherson, Maria S. Ioannou, Louis Hodgson, Jennifer L. Stow, Adam A. Wall

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

Pathogen-mediated activation of macrophages arms innate immune responses that include enhanced surface ruffling and macropinocytosis for environmental sampling and receptor internalization and signaling. Activation of macrophages with bacterial lipopolysaccharide (LPS) generates prominent dorsal ruffles, which are precursors for macropinosomes. Very rapid, high-resolution imaging of live macrophages with lattice light sheet microscopy (LLSM) reveals new features and actions of dorsal ruffles, which redefine the process of macropinosome formation and closure. We offer a new model in which ruffles are erected and supported by F-actin tent poles that cross over and twist to constrict the forming macropinosomes. This process allows for formation of large macropinosomes induced by LPS. We further describe the enrichment of active Rab13 on tent pole ruffles and show that CRISPR deletion of Rab13 results in aberrant tent pole ruffles and blocks the formation of large LPS-induced macropinosomes. Based on the exquisite temporal and spatial resolution of LLSM, we can redefine the ruffling and macropinosome processes that underpin innate immune responses.

Original languageEnglish (US)
Pages (from-to)3873-3885
Number of pages13
JournalJournal of Cell Biology
Volume217
Issue number11
DOIs
StatePublished - Nov 1 2018

Fingerprint

Lipopolysaccharides
Macrophage Activation
Macrophages
Innate Immunity
Microscopy
Clustered Regularly Interspaced Short Palindromic Repeats
Light
Actins

ASJC Scopus subject areas

  • Cell Biology

Cite this

Condon, N. D., Heddleston, J. M., Chew, T. L., Luo, L., McPherson, P. S., Ioannou, M. S., ... Wall, A. A. (2018). Macropinosome formation by tent pole ruffling in macrophages. Journal of Cell Biology, 217(11), 3873-3885. https://doi.org/10.1083/jcb.201804137

Macropinosome formation by tent pole ruffling in macrophages. / Condon, Nicholas D.; Heddleston, John M.; Chew, Teng Leong; Luo, Lin; McPherson, Peter S.; Ioannou, Maria S.; Hodgson, Louis; Stow, Jennifer L.; Wall, Adam A.

In: Journal of Cell Biology, Vol. 217, No. 11, 01.11.2018, p. 3873-3885.

Research output: Contribution to journalArticle

Condon, ND, Heddleston, JM, Chew, TL, Luo, L, McPherson, PS, Ioannou, MS, Hodgson, L, Stow, JL & Wall, AA 2018, 'Macropinosome formation by tent pole ruffling in macrophages', Journal of Cell Biology, vol. 217, no. 11, pp. 3873-3885. https://doi.org/10.1083/jcb.201804137
Condon ND, Heddleston JM, Chew TL, Luo L, McPherson PS, Ioannou MS et al. Macropinosome formation by tent pole ruffling in macrophages. Journal of Cell Biology. 2018 Nov 1;217(11):3873-3885. https://doi.org/10.1083/jcb.201804137
Condon, Nicholas D. ; Heddleston, John M. ; Chew, Teng Leong ; Luo, Lin ; McPherson, Peter S. ; Ioannou, Maria S. ; Hodgson, Louis ; Stow, Jennifer L. ; Wall, Adam A. / Macropinosome formation by tent pole ruffling in macrophages. In: Journal of Cell Biology. 2018 ; Vol. 217, No. 11. pp. 3873-3885.
@article{edb192d31bc04e88b20974b723447704,
title = "Macropinosome formation by tent pole ruffling in macrophages",
abstract = "Pathogen-mediated activation of macrophages arms innate immune responses that include enhanced surface ruffling and macropinocytosis for environmental sampling and receptor internalization and signaling. Activation of macrophages with bacterial lipopolysaccharide (LPS) generates prominent dorsal ruffles, which are precursors for macropinosomes. Very rapid, high-resolution imaging of live macrophages with lattice light sheet microscopy (LLSM) reveals new features and actions of dorsal ruffles, which redefine the process of macropinosome formation and closure. We offer a new model in which ruffles are erected and supported by F-actin tent poles that cross over and twist to constrict the forming macropinosomes. This process allows for formation of large macropinosomes induced by LPS. We further describe the enrichment of active Rab13 on tent pole ruffles and show that CRISPR deletion of Rab13 results in aberrant tent pole ruffles and blocks the formation of large LPS-induced macropinosomes. Based on the exquisite temporal and spatial resolution of LLSM, we can redefine the ruffling and macropinosome processes that underpin innate immune responses.",
author = "Condon, {Nicholas D.} and Heddleston, {John M.} and Chew, {Teng Leong} and Lin Luo and McPherson, {Peter S.} and Ioannou, {Maria S.} and Louis Hodgson and Stow, {Jennifer L.} and Wall, {Adam A.}",
year = "2018",
month = "11",
day = "1",
doi = "10.1083/jcb.201804137",
language = "English (US)",
volume = "217",
pages = "3873--3885",
journal = "Journal of Cell Biology",
issn = "0021-9525",
publisher = "Rockefeller University Press",
number = "11",

}

TY - JOUR

T1 - Macropinosome formation by tent pole ruffling in macrophages

AU - Condon, Nicholas D.

AU - Heddleston, John M.

AU - Chew, Teng Leong

AU - Luo, Lin

AU - McPherson, Peter S.

AU - Ioannou, Maria S.

AU - Hodgson, Louis

AU - Stow, Jennifer L.

AU - Wall, Adam A.

PY - 2018/11/1

Y1 - 2018/11/1

N2 - Pathogen-mediated activation of macrophages arms innate immune responses that include enhanced surface ruffling and macropinocytosis for environmental sampling and receptor internalization and signaling. Activation of macrophages with bacterial lipopolysaccharide (LPS) generates prominent dorsal ruffles, which are precursors for macropinosomes. Very rapid, high-resolution imaging of live macrophages with lattice light sheet microscopy (LLSM) reveals new features and actions of dorsal ruffles, which redefine the process of macropinosome formation and closure. We offer a new model in which ruffles are erected and supported by F-actin tent poles that cross over and twist to constrict the forming macropinosomes. This process allows for formation of large macropinosomes induced by LPS. We further describe the enrichment of active Rab13 on tent pole ruffles and show that CRISPR deletion of Rab13 results in aberrant tent pole ruffles and blocks the formation of large LPS-induced macropinosomes. Based on the exquisite temporal and spatial resolution of LLSM, we can redefine the ruffling and macropinosome processes that underpin innate immune responses.

AB - Pathogen-mediated activation of macrophages arms innate immune responses that include enhanced surface ruffling and macropinocytosis for environmental sampling and receptor internalization and signaling. Activation of macrophages with bacterial lipopolysaccharide (LPS) generates prominent dorsal ruffles, which are precursors for macropinosomes. Very rapid, high-resolution imaging of live macrophages with lattice light sheet microscopy (LLSM) reveals new features and actions of dorsal ruffles, which redefine the process of macropinosome formation and closure. We offer a new model in which ruffles are erected and supported by F-actin tent poles that cross over and twist to constrict the forming macropinosomes. This process allows for formation of large macropinosomes induced by LPS. We further describe the enrichment of active Rab13 on tent pole ruffles and show that CRISPR deletion of Rab13 results in aberrant tent pole ruffles and blocks the formation of large LPS-induced macropinosomes. Based on the exquisite temporal and spatial resolution of LLSM, we can redefine the ruffling and macropinosome processes that underpin innate immune responses.

UR - http://www.scopus.com/inward/record.url?scp=85056287515&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85056287515&partnerID=8YFLogxK

U2 - 10.1083/jcb.201804137

DO - 10.1083/jcb.201804137

M3 - Article

C2 - 30150290

AN - SCOPUS:85056287515

VL - 217

SP - 3873

EP - 3885

JO - Journal of Cell Biology

JF - Journal of Cell Biology

SN - 0021-9525

IS - 11

ER -