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Murine macrophage response from peritoneal cavity requires signals mediated by chemokine receptor CCR-2 during Staphylococcus aureus infection

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Abstract

C–C chemokine receptor-2 (CCR-2) is a cognate receptor for monocyte chemotactic protein-1 (MCP-1), and recent studies revealed that MCP-1–CCR-2 signaling is involved in several inflammatory diseases characterized by macrophage infiltration. Currently, there is no study on the involvement of CCR-2 in the killing of S. aureus by macrophages of Swiss albino mice, and its substantial role in host defense against S. aureus infection in murine macrophages is still unclear. Therefore, the present study was aimed to investigate the functional and interactive role of CCR-2 and MCP-1 in regulating peritoneal macrophage responses with respect to acute S. aureus infection. We found that phagocytosis of S. aureus can serve as an important stimulus for MCP-1 production by peritoneal macrophages, which is dependent directly or indirectly on cytokines, reactive oxygen species and nitric oxide. Neutralization of CCR-2 in macrophages leads to increased production of IL-10 and decreased production of IFN-γ and IL-6. In CCR-2 blocked macrophages, pretreatment with specific blocker of NF-κB or p38-MAPK causes elevation in MCP-1 level and subsequent downregulation of CCR-2 itself. We speculate that CCR-2 is involved in S. aureus-induced MCP-1 production via NF-κB or p38-MAPK signaling. We also hypothesized that unnaturally high level of MCP-1 that build up upon CCR-2 neutralization might allow promiscuous binding to one or more other chemokine receptors, a situation that would not occur in CCR-2 non-neutralized condition. This may be the plausible explanation for such observed Th-2 response in CCR-2 blocked macrophages infected with S. aureus in the present study.

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Abbreviations

ATZ:

Amino triazole

CPCSEA:

Committee for the Purpose of Control and Supervision of Experiments on Animal

CCL-2:

C–C chemokine ligand-2

CCR-2:

C–C chemokine receptor-2

DDC:

Diethyl dithio carbamic acid

DTH:

Delayed type hypersensitivity

FBS:

Foetal bovine serum

LPS:

Lipopolysaccharide

MAPK:

Mitogen-activated protein kinase

MCP:

Monocyte chemotactic protein-1

NaNO3 :

Sodium nitrate

NF-κB:

Nuclear factor kappa beta

PAMPs:

Pathogen-associated molecular patterns

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Acknowledgments

The authors are thankful to the Department of Science and Technology, Government of India, for providing the DST-INSPIRE fellowship to Mrs. Ajeya Nandi [Grant Number: DST INSPIRE Fellowship/2013/1118, dated June 23, 2014] for funding this project. Part of this work was also supported by the Department of Science and Technology (DST), Science and Engineering Research Board (SERB), Ministry of Science and Technology, Government of India, New Delhi, India [Grant Number: SR/SO/HS/0013/2012, dated May 21, 2013, to Biswadev Bishayi]. The author (BB) is indebted to Department of Science and Technology, Government of India, for providing them with the instruments procured under the DST-PURSE programme to the Department of Physiology, University of Calcutta.

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  1. Immunology Laboratory, Department of Physiology, University Colleges of Science and Technology, University of Calcutta, 92 APC Road, Calcutta, West Bengal, 700009, India

    Ajeya Nandi & Biswadev Bishayi

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  1. Ajeya Nandi
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Correspondence to Biswadev Bishayi.

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For the manuscript entitled “Murine macrophage response from peritoneal cavity requires signals mediated by chemokine receptor CCR-2 during Staphylococcus aureus infection” by Ajeya Nandi and Biswadev Bishayi, authors declared that they have no conflict of interest for this manuscript toward submission in Immunol. Res. The authors also state that they do not have a direct financial relation with the commercial identities mentioned in this manuscript that might lead to a conflict of interest for any of the authors.

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Nandi, A., Bishayi, B. Murine macrophage response from peritoneal cavity requires signals mediated by chemokine receptor CCR-2 during Staphylococcus aureus infection. Immunol Res 64, 213–232 (2016). https://doi.org/10.1007/s12026-015-8739-9

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