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Articles

Canonical and Noncanonical G-Protein Signaling Helps Coordinate Actin Dynamics To Promote Macrophage Phagocytosis of Zymosan

Ning-Na Huang, Steven Becker, Cedric Boularan, Olena Kamenyeva, Ali Vural, Il-Young Hwang, Chong-Shan Shi, John H. Kehrl
Ning-Na Huang
B-Cell Molecular Immunology Section, Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, USA
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Steven Becker
Biological Imaging Facility, Research Technologies Branch, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, USA
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Cedric Boularan
B-Cell Molecular Immunology Section, Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, USA
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Olena Kamenyeva
B-Cell Molecular Immunology Section, Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, USA
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Ali Vural
B-Cell Molecular Immunology Section, Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, USA
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Il-Young Hwang
B-Cell Molecular Immunology Section, Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, USA
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Chong-Shan Shi
B-Cell Molecular Immunology Section, Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, USA
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John H. Kehrl
B-Cell Molecular Immunology Section, Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, USA
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DOI: 10.1128/MCB.00325-14
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ABSTRACT

Both chemotaxis and phagocytosis depend upon actin-driven cell protrusions and cell membrane remodeling. While chemoattractant receptors rely upon canonical G-protein signaling to activate downstream effectors, whether such signaling pathways affect phagocytosis is contentious. Here, we report that Gαi nucleotide exchange and signaling helps macrophages coordinate the recognition, capture, and engulfment of zymosan bioparticles. We show that zymosan exposure recruits F-actin, Gαi proteins, and Elmo1 to phagocytic cups and early phagosomes. Zymosan triggered an increase in intracellular Ca2+ that was partially sensitive to Gαi nucleotide exchange inhibition and expression of GTP-bound Gαi recruited Elmo1 to the plasma membrane. Reducing GDP-Gαi nucleotide exchange, decreasing Gαi expression, pharmacologically interrupting Gβγ signaling, or reducing Elmo1 expression all impaired phagocytosis, while favoring the duration that Gαi remained GTP bound promoted it. Our studies demonstrate that targeting heterotrimeric G-protein signaling offers opportunities to enhance or retard macrophage engulfment of phagocytic targets such as zymosan.

FOOTNOTES

    • Received 7 March 2014.
    • Returned for modification 21 May 2014.
    • Accepted 5 September 2014.
    • Accepted manuscript posted online 15 September 2014.
  • Supplemental material for this article may be found at http://dx.doi.org/10.1128/MCB.00325-14.

  • Copyright © 2014, American Society for Microbiology. All Rights Reserved.
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Canonical and Noncanonical G-Protein Signaling Helps Coordinate Actin Dynamics To Promote Macrophage Phagocytosis of Zymosan
Ning-Na Huang, Steven Becker, Cedric Boularan, Olena Kamenyeva, Ali Vural, Il-Young Hwang, Chong-Shan Shi, John H. Kehrl
Molecular and Cellular Biology Oct 2014, 34 (22) 4186-4199; DOI: 10.1128/MCB.00325-14

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Canonical and Noncanonical G-Protein Signaling Helps Coordinate Actin Dynamics To Promote Macrophage Phagocytosis of Zymosan
Ning-Na Huang, Steven Becker, Cedric Boularan, Olena Kamenyeva, Ali Vural, Il-Young Hwang, Chong-Shan Shi, John H. Kehrl
Molecular and Cellular Biology Oct 2014, 34 (22) 4186-4199; DOI: 10.1128/MCB.00325-14
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