p38/MKP-1–regulated AKT coordinates macrophage transitions and resolution of inflammation during tissue repair
Open accessAbstract
Repair of damaged tissue requires the coordinated action of inflammatory and tissue-specific cells to restore homeostasis, but the underlying regulatory mechanisms are poorly understood. In this paper, we report new roles for MKP-1 (mitogen-activated protein kinase [MAPK] phosphatase-1) in controlling macrophage phenotypic transitions necessary for appropriate muscle stem cell–dependent tissue repair. By restricting p38 MAPK activation, MKP-1 allows the early pro- to antiinflammatory macrophage transition and the later progression into a macrophage exhaustion-like state characterized by cytokine silencing, thereby permitting resolution of inflammation as tissue fully recovers. p38 hyperactivation in macrophages lacking MKP-1 induced the expression of microRNA-21 (miR-21), which in turn reduced PTEN (phosphatase and tensin homologue) levels, thereby extending AKT activation. In the absence of MKP-1, p38-induced AKT activity anticipated the acquisition of the antiinflammatory gene program and final cytokine silencing in macrophages, resulting in impaired tissue healing. Such defects were reversed by temporally controlled p38 inhibition. Conversely, miR-21–AKT interference altered homeostasis during tissue repair. This novel regulatory mechanism involving the appropriate balance of p38, MKP-1, miR-21, and AKT activities may have implications in chronic inflammatory degenerative diseases.
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The timing of inflammatory responses can strongly influence the kinetics and extent of muscle regeneration.
“These studies showed that the timing of inflammatory responses can have profound effects on the kinetics and extent of regeneration69, findings confirmed by experiments using antibodies to block inflammatory cytokines70,71.”
From The central role of muscle stem cells in regenerative failure with aging (2015) · cites this paper as [71]
One intracellular signaling pathway controlling the phenotypic switch involves p38 and miR-21.
“One of the intracellular signaling pathways controlling the phenotypic switch involves p38 and miR-21.99,100”
From The Innate Immune System in Acute and Chronic Wounds (2016) · cites this paper as [100]
In a muscle repair system, p38 activity is controlled by MKP-1, which it induces in a feedback loop.
“In a study of a muscle repair system, Perdiguero et al. showed that the activity of p38 is controlled by mitogen-activated kinase phosphatase-1 (MKP-1), which it induces in a feedback loop.99,100”
From The Innate Immune System in Acute and Chronic Wounds (2016) · cites this paper as [100]
This process leads over some days to a general reduction in cytokine secretion that is probably important for the ultimate resolution of the macrophage phase of wound healing.
“It also leads, over some days, to a general reduction in cytokine secretion that is probably important for the ultimate resolution of the macrophage phase of wound healing.99,100”
From The Innate Immune System in Acute and Chronic Wounds (2016) · cites this paper as [100]
p38 induces miR-21, one of whose targets is PTEN.
“It also induces miR-21, one of whose targets is phosphatase with a tensin motif (PTEN).”
From The Innate Immune System in Acute and Chronic Wounds (2016) · cites this paper as [100]
In macrophages, miR-21 plays a key role in the transition from an inflammatory to an anti-inflammatory phenotype.
“In macrophages, miR-21 plays a key role in the transition from an inflammatory to an anti-inflammatory phenotype.”
From The Innate Immune System in Acute and Chronic Wounds (2016) · cites this paper as [100]
Reduction in PTEN extends the activation of AKT, which turns off the inflammatory state and promotes the anti-inflammatory state.
“The reduction in PTEN extends the activation of protein kinase B (AKT), which turns off the inflammatory state and promotes the anti-inflammatory state.”
From The Innate Immune System in Acute and Chronic Wounds (2016) · cites this paper as [100]
Either premature changes in phenotype or delayed/impaired changes in phenotype have been associated with impaired healing.
“In fact, either premature changes in phenotype or delayed/impaired changes in phenotype have been associated with impaired healing (14,29,49).”
From Sustained Inflammasome Activity in Macrophages Impairs Wound Healing in Type 2 Diabetic Humans and Mice (2014) · cites this paper as [49]
Recent studies have shown that macrophage phenotypes change over the different phases of tissue repair and that the sequential appearance of these phenotypes may be required for efficient repair.
“Recent studies have shown that Mp phenotypes change over the different phases of tissue repair and that the sequential appearance of these phenotypes may be required for efficient repair (11,14,29,49,50).”
From Sustained Inflammasome Activity in Macrophages Impairs Wound Healing in Type 2 Diabetic Humans and Mice (2014) · cites this paper as [49]
During impaired muscle healing caused by loss of MAPK-phosphatase-1, peak Mp expression of TGF-β and IL-10 is shifted to earlier time-points and occurs simultaneously with peak proinflammatory cytokine expression.
“Interestingly, during impaired muscle healing caused by loss of MAPK-phosphatase-1 [65], peak Mp expression of TGF- and IL-10 is shifted to earlier time-points and occurs simultaneously with peak proinflammatory cytokine expression, contrary to expectations of an early-M1-tolate-M2 transition.”
From Macrophage phenotypes during tissue repair (2013) · cites this paper as [65]
In murine skeletal muscle, Mp expression of TGF-β and IL-10 mRNA increases over the first few days after toxin-induced injury, peaks during the intermediate stages of healing, and then declines sharply, despite continued presence of Mp within the healing muscle.
“In murine skeletal muscle, however, Mp expression of TGF- and IL-10 mRNA increases over the first few days after toxin-induced injury, peaks during the intermediate stages of healing, and then declines sharply, despite continued presence of Mp within the healing muscle [65].”
From Macrophage phenotypes during tissue repair (2013) · cites this paper as [65]
Mp expression of mRNA and protein for these cytokines exhibits an early peak and subsequent decline after skin wounding or toxin-induced muscle injury in mice.
“Mp expression of mRNA and protein for these cytokines exhibits an early peak and subsequent decline after skin wounding [33,60] or toxin-induced muscle injury in mice [65], consistent with an early M1-like phenotype.”
From Macrophage phenotypes during tissue repair (2013) · cites this paper as [65]
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- Authors
- Perdiguero, E., Sousa-Victor, P., Ruiz-Bonilla, V., Jardí, M., Caelles, C., Serrano, A. L., & Muñoz-Cánoves, P.
- Affiliations
- Universitat Pompeu Fabra (ES)
- Cell Biology Group, Department of Experimental and Health Sciences, Pompeu Fabra University, and Centro de Investigación Biomédica en Red de Enfermedades Neurodegenerativas, 08003 Barcelona, Spain 1
- Biomedical Research Institute, Barcelona Science Park, 08028 Barcelona, Spain 2
- Venue
- Journal of Cell Biology
- Publisher
- Rockefeller University Press
- Published
- 2011-10-10
- Volume
- 195
- Issue
- 2
- Pages
- 307-322
- ISSN
- 0021-9525 (ISSN-L)
- 1540-8140
- PMC
- PMC3198158
- OpenAlex
- W2109401262
- Cited by
- 236
- References
- 50
- Citations by year
- 2026: 9 · 2025: 6 · 2024: 10 · 2023: 13 · 2022: 14 · 2021: 24 · 2020: 20 · 2019: 21 · 2018: 19 · 2017: 17 · 2016: 17 · 2015: 20 · 2014: 16 · 2013: 19 · 2012: 10
- FWCI
- 14.91
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc-sa
- Locations
- The Journal of Cell Biology (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Dipòsit Digital de la Universitat de Barcelona (Universitat de Barcelona) (publishedVersion)
- Repositori digital de la UPF (Universitat Pompeu Fabra) (submittedVersion, cc-by-nc-sa)
- RECERCAT (Consorci de Serveis Universitaris de Catalunya) (submittedVersion, other-oa)
- RECERCAT (Consorci de Serveis Universitaris de Catalunya) (submittedVersion, public-domain)
- Funders
- Muscular Dystrophy Association
- European Commission
- Ministerio de Ciencia e Innovación (PLE2009)
- Fundação para a Ciência e a Tecnologia
- Topics
- Health Sciences › Medicine › Rehabilitation › Wound Healing and Treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Tyrosine Phosphatases
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Keywords
- MKP-1, p38 MAPK, Akt signaling, macrophage polarization, inflammation resolution, tissue repair, muscle stem cells, miR-21, PTEN, chronic inflammation
- MeSH terms
- Animals, Gene Expression Regulation, Inflammation, Macrophages, Wound Healing, Cytokines, MicroRNAs, p38 Mitogen-Activated Protein Kinases, Proto-Oncogene Proteins c-akt, PTEN Phosphohydrolase, Mice, Dual Specificity Phosphatase 1
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