MiR-142 Is Required for Staphylococcus aureus Clearance at Skin Wound Sites via Small GTPase-Mediated Regulation of the Neutrophil Actin Cytoskeleton

Tanaka, Katsuya; Kim, Sang Eun; Yano, Hiroki; Matsumoto, Gaku; Ohuchida, Ryoma; Ishikura, Yuhoko; Araki, Masatake; Araki, Kimi; Park, Seong Joon; Komatsu, Toshimitsu; Hayashi, Hiroko; Ikematsu, Kazuya; Tanaka, Katsumi; Hirano, Akiyoshi; Martin, Paul; Shimokawa, Isao; Mori, Ryoichi

doi:10.1016/j.jid.2016.11.018

Cited by 48 publications

(59 citation statements)

References 28 publications

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“…miR-223 regulates granulocyte development and function (Johnnidis et al, 2008), and using miR-142 À/À mice, several groups revealed that miR-142 regulates the hematopoietic development and function of mast cells, megakaryocytes, and lymphocytes (Mildner et al, 2013;Chapnik et al, 2014;Yamada et al, 2014;Sun et al, 2015). We further investigated the function of miR-142 in skin wound healing by analyzing a newly-developed miR-142 knockout mouse and showed that this miR regulates neutrophil migration at skin wound sites via the small GTPase regulation of its actin cytoskeleton (Tanaka et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

“…In vivo live imaging analysis of EGFP-expressing neutrophil recruitment and MPO activity at wound sites Neutrophil recruitment at skin wound sites was visualized and measured as previously described (Kim et al, 2008;Tanaka et al, 2017). In brief, WT:lys-EGFP mice and miR-223 Y/À :lys-EGFP mice were wounded and fluorescence intensity was monitored with IVIS Lumina II System (PerkinElmer, Waltham, MA, USA).…”

Section: Isolation Of Neutrophils and Macrophages From Skin Wounds Anmentioning

confidence: 99%

“…Wound tissues harvested at day 1 were homogenized by Tissue-Lyzer II (Qiagen) followed by total RNA and polyA + RNA purification using an RNeasy Plus Universal Mini Kit ( The 3 0 -UTRs of miR-223 targets were screened using Strand NGS software (Strand Genomics, San Francisco, CA, USA). Vectors were constructed with pmirGLO Dual-Luciferase miRNA Target Expression Vector (Promega Corp., Madison, WI, USA) according to the manufacturer's procedures and as previously described (Tanaka et al, 2017). In brief, primers consisting of the 3 0 -UTRs of predicted miR-223 family target sequences and appropriate restriction sites were synthesized, annealed, and cloned downstream of the firefly luciferase reporter (luc2) gene in pmirGLO.…”

Section: Rna-seqmentioning

confidence: 99%

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Targeting miR‐223 in neutrophils enhances the clearance of Staphylococcus aureus in infected wounds

et al. 2018

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Argonaute 2 bound mature microRNA (Ago2‐miRNA) complexes are key regulators of the wound inflammatory response and function in the translational processing of target mRNAs. In this study, we identified four wound inflammation‐related Ago2‐miRNAs (miR‐139‐5p, miR‐142‐3p, miR‐142‐5p, and miR‐223) and show that miR‐223 is critical for infection control. miR‐223 Y/− mice exhibited delayed sterile healing with prolonged neutrophil activation and interleukin‐6 expression, and markedly improved repair of Staphylococcus aureus‐infected wounds. We also showed that the expression of miR‐223 was regulated by CCAAT/enhancer binding protein alpha in human neutrophils after exposure to S. aureus peptides. Treatment with miR‐223 Y/−‐derived neutrophils, or miR‐223 antisense oligodeoxynucleotides in S. aureus‐infected wild‐type wounds markedly improved the healing of these otherwise chronic, slow healing wounds. This study reveals how miR‐223 regulates the bactericidal capacity of neutrophils at wound sites and indicates that targeting miR‐223 might be of therapeutic benefit for infected wounds in the clinic.

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Section: Discussionmentioning

confidence: 99%

Section: Isolation Of Neutrophils and Macrophages From Skin Wounds Anmentioning

confidence: 99%

Section: Rna-seqmentioning

confidence: 99%

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Targeting miR‐223 in neutrophils enhances the clearance of Staphylococcus aureus in infected wounds

et al. 2018

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“…Burroughs et al (2011) reported that miR-182, miR-222, and miR-223-5p in humans interacted with specific Ago proteins, as detected by next generation sequencing. We found inflammation-related miRNAs, including the miR-142 family, by comparing PU.1 KO and WT mouse tissues (Tanaka et al, 2017). Moreover, small RNAs (sRNAs), not yet registered in the miRNA database, were associated with Ago1 and miRNA in Epstein-Barr virus-infected cells (Yamakawa et al, 2014).…”

Section: Identifi C Ati On Of Ag O -Bound Mirna Tr Anscrip Tome Smentioning

confidence: 98%

“…These results were provided by FUJIFILM Wako Pure Chemical Corporation (Osaka, Japan) migration distance, and migration velocity (Figure 5a) (Movies S1, S2) (Tanaka et al, 2017). Ago IP RNAs or total RNAs (e.g., mRNA, tRNA, rRNA, and other ncRNA) in HeLa cell lines were purified by using monoclonal Abs specific for each Ago subfamily protein or by using standard total RNA purification procedures, followed by microarray analysis for miRNA expression.…”

Section: Staphylococcus Aureus Is An Indigenous Cutaneous Bacteriummentioning

confidence: 99%

Identification and functional analysis of inflammation‐related miRNAs in skin wound repair

2018

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Inflammation at a wound site is essential for preventing infection. However, misregulated inflammation leads to pathologies of the healing process, including chronic non-healing wounds and scarring. MicroRNAs (miRNAs) are key regulators of the inflammatory response and tissue repair, acting by translational processing of target mRNAs. In the final step of miRNA processing, Argonaute 2 (Ago2)-bound mature miRNA complexes bind to target mRNAs and inhibit their translation. A variety of wound healing-related miRNAs have been identified and their misregulation likely contributes to wound pathologies, including scarring and chronic healing. Recently, we have developed an Ago2-bound mature miRNA purification system that uses Ago2 antibody to analyze the expression of miRNAs from wound tissues by microarray and next generation sequencing. We have identified several wound inflammation-related miRNAs via Ago2-target immunoprecipitation assays and next generation sequencing of wound tissues from wild-type and PU.1 knockout mice, which exhibit no inflammatory response because of a lack of immune cell lineages. We demonstrated that miR-142, an identified inflammation-related miRNA, is essential role for neutrophilic chemotaxis via inhibition of small GTPase translation; its misregulation leads to susceptibility to infection against Staphylococcus aureus at skin wound sites. In this review, we summarize recent advances of miRNA studies in skin wound healing, introduce our miRNA purification system using an immunoprecipitation assay method, and discuss the function of miR-142 in skin wound healing.

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Role of microRNAs in Staphylococcus aureus infection: Potential biomarkers and mechanism

et al. 2020

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Staphylococcus aureus is known as a common pathogen that colonizes 30% of healthy humans. Additionally, this bacterium can cause a number of serious infections, that is, endocarditis, bacteremia, pneumonia, wound, skin infections, and tissue abscesses. A variety of cellular and molecular pathways and targets are involved in response against S. aureus. Among them, microRNAs (miRNAs) have crucial roles in response against S. aureus. In this regard, it has been shown that these molecules exert their regulatory roles via modulating a wide range of events, such as inflammatory reactions, host innate, and adaptive immunity. Current works have provided insight into the crucial involvement of miRNAs in immune defense toward Staphylococcal infections. Herein, we highlighted the current findings on the deregulation of different miRNAs in S. aureus-infected cells. Moreover, we summarized the mechanisms and targets of miRNAs in S. aureus infections.

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MiR-142 Is Required for Staphylococcus aureus Clearance at Skin Wound Sites via Small GTPase-Mediated Regulation of the Neutrophil Actin Cytoskeleton

Cited by 48 publications

References 28 publications

Targeting miR‐223 in neutrophils enhances the clearance of Staphylococcus aureus in infected wounds

Targeting miR‐223 in neutrophils enhances the clearance of Staphylococcus aureus in infected wounds

Identification and functional analysis of inflammation‐related miRNAs in skin wound repair

Role of microRNAs in Staphylococcus aureus infection: Potential biomarkers and mechanism

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