Enhancement of Muscle T Regulatory Cells and Improvement of Muscular Dystrophic Process in mdx Mice by Blockade of Extracellular ATP/P2X Axis
Infiltration of immune cells and chronic inflammation substantially affect skeletal and cardiac muscle degeneration in Duchenne muscular dystrophy. In the immune system, extracellular adenosine triphosphate (ATP) released by dying cells is sensed as a danger associated molecular pattern through P2 p...
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| Published in | The American journal of pathology Vol. 185; no. 12; pp. 3349 - 3360 |
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| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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United States
Elsevier Inc
01.12.2015
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| Abstract | Infiltration of immune cells and chronic inflammation substantially affect skeletal and cardiac muscle degeneration in Duchenne muscular dystrophy. In the immune system, extracellular adenosine triphosphate (ATP) released by dying cells is sensed as a danger associated molecular pattern through P2 purinergic receptors. Specifically, the P2X7 subtype has a prominent role in regulating immune system physiology and contributes to inflammasome activation also in muscle cells. Here, we show that in vivo blockade of the extracellular ATP/P2X purinergic signaling pathway by periodate-oxidized ATP delayed the progression of the dystrophic phenotype and dampened the local inflammatory response in mdx mice, a spontaneous mouse model of dystrophin deficiency. Reduced infiltration of leukocytes and macrophages and decreased expression of IL-6 were revealed in the muscles of periodate-oxidized ATP-treated mdx mice. Concomitantly, an increase in Foxp3+ immunosuppressive regulatory T cells was observed and correlated with enhanced myofiber regeneration. Moreover, we detected reduced concentrations of profibrotic cytokines, including transforming growth factor-β and connective tissue growth factor, in muscles of periodate-oxidized ATP-treated mdx mice. The improvement of inflammatory features was associated with increased strength and reduced necrosis, thus suggesting that pharmacologic purinergic antagonism altering the adaptive immune component in the muscle infiltrates might represent a promising therapeutic approach in Duchenne muscular dystrophy. |
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| AbstractList | Infiltration of immune cells and chronic inflammation substantially affect skeletal and cardiac muscle degeneration in Duchenne muscular dystrophy. In the immune system, extracellular adenosine triphosphate (ATP) released by dying cells is sensed as a danger associated molecular pattern through P2 purinergic receptors. Specifically, the P2X7 subtype has a prominent role in regulating immune system physiology and contributes to inflammasome activation also in muscle cells. Here, we show that in vivo blockade of the extracellular ATP/P2X purinergic signaling pathway by periodate-oxidized ATP delayed the progression of the dystrophic phenotype and dampened the local inflammatory response in mdx mice, a spontaneous mouse model of dystrophin deficiency. Reduced infiltration of leukocytes and macrophages and decreased expression of IL-6 were revealed in the muscles of periodate-oxidized ATP-treated mdx mice. Concomitantly, an increase in Foxp3+ immunosuppressive regulatory T cells was observed and correlated with enhanced myofiber regeneration. Moreover, we detected reduced concentrations of profibrotic cytokines, including transforming growth factor-β and connective tissue growth factor, in muscles of periodate-oxidized ATP-treated mdx mice. The improvement of inflammatory features was associated with increased strength and reduced necrosis, thus suggesting that pharmacologic purinergic antagonism altering the adaptive immune component in the muscle infiltrates might represent a promising therapeutic approach in Duchenne muscular dystrophy. Infiltration of immune cells and chronic inflammation substantially affect skeletal and cardiac muscle degeneration in Duchenne muscular dystrophy. In the immune system, extracellular adenosine triphosphate (ATP) released by dying cells is sensed as a danger associated molecular pattern through P2 purinergic receptors. Specifically, the P2X7 subtype has a prominent role in regulating immune system physiology and contributes to inflammasome activation also in muscle cells. Here, we show that in vivo blockade of the extracellular ATP/P2X purinergic signaling pathway by periodate-oxidized ATP delayed the progression of the dystrophic phenotype and dampened the local inflammatory response in mdx mice, a spontaneous mouse model of dystrophin deficiency. Reduced infiltration of leukocytes and macrophages and decreased expression of IL-6 were revealed in the muscles of periodate-oxidized ATP-treated mdx mice. Concomitantly, an increase in Foxp3(+) immunosuppressive regulatory T cells was observed and correlated with enhanced myofiber regeneration. Moreover, we detected reduced concentrations of profibrotic cytokines, including transforming growth factor-β and connective tissue growth factor, in muscles of periodate-oxidized ATP-treated mdx mice. The improvement of inflammatory features was associated with increased strength and reduced necrosis, thus suggesting that pharmacologic purinergic antagonism altering the adaptive immune component in the muscle infiltrates might represent a promising therapeutic approach in Duchenne muscular dystrophy.Infiltration of immune cells and chronic inflammation substantially affect skeletal and cardiac muscle degeneration in Duchenne muscular dystrophy. In the immune system, extracellular adenosine triphosphate (ATP) released by dying cells is sensed as a danger associated molecular pattern through P2 purinergic receptors. Specifically, the P2X7 subtype has a prominent role in regulating immune system physiology and contributes to inflammasome activation also in muscle cells. Here, we show that in vivo blockade of the extracellular ATP/P2X purinergic signaling pathway by periodate-oxidized ATP delayed the progression of the dystrophic phenotype and dampened the local inflammatory response in mdx mice, a spontaneous mouse model of dystrophin deficiency. Reduced infiltration of leukocytes and macrophages and decreased expression of IL-6 were revealed in the muscles of periodate-oxidized ATP-treated mdx mice. Concomitantly, an increase in Foxp3(+) immunosuppressive regulatory T cells was observed and correlated with enhanced myofiber regeneration. Moreover, we detected reduced concentrations of profibrotic cytokines, including transforming growth factor-β and connective tissue growth factor, in muscles of periodate-oxidized ATP-treated mdx mice. The improvement of inflammatory features was associated with increased strength and reduced necrosis, thus suggesting that pharmacologic purinergic antagonism altering the adaptive immune component in the muscle infiltrates might represent a promising therapeutic approach in Duchenne muscular dystrophy. Infiltration of immune cells and chronic inflammation substantially affect skeletal and cardiac muscle degeneration in Duchenne muscular dystrophy. In the immune system, extracellular adenosine triphosphate (ATP) released by dying cells is sensed as a danger associated molecular pattern through P2 purinergic receptors. Specifically, the P2X7 subtype has a prominent role in regulating immune system physiology and contributes to inflammasome activation also in muscle cells. Here, we show that in vivo blockade of the extracellular ATP/P2X purinergic signaling pathway by periodate-oxidized ATP delayed the progression of the dystrophic phenotype and dampened the local inflammatory response in mdx mice, a spontaneous mouse model of dystrophin deficiency. Reduced infiltration of leukocytes and macrophages and decreased expression of IL-6 were revealed in the muscles of periodate-oxidized ATP-treated mdx mice. Concomitantly, an increase in Foxp3(+) immunosuppressive regulatory T cells was observed and correlated with enhanced myofiber regeneration. Moreover, we detected reduced concentrations of profibrotic cytokines, including transforming growth factor-β and connective tissue growth factor, in muscles of periodate-oxidized ATP-treated mdx mice. The improvement of inflammatory features was associated with increased strength and reduced necrosis, thus suggesting that pharmacologic purinergic antagonism altering the adaptive immune component in the muscle infiltrates might represent a promising therapeutic approach in Duchenne muscular dystrophy. |
| Author | Grassi, Fabio Bruno, Claudio Perruzza, Lisa Gazzerro, Elisabetta Traggiai, Elisabetta Volpi, Stefano Panicucci, Chiara Fiorillo, Chiara Pistorio, Angela Fruscione, Floriana Assereto, Stefania Baldassari, Simona Minetti, Carlo |
| Author_xml | – sequence: 1 givenname: Elisabetta surname: Gazzerro fullname: Gazzerro, Elisabetta organization: Unit of Pediatric Neurology and Muscle Disease, Istituto Giannina Gaslini, Genova, Italy – sequence: 2 givenname: Simona surname: Baldassari fullname: Baldassari, Simona organization: Unit of Pediatric Neurology and Muscle Disease, Istituto Giannina Gaslini, Genova, Italy – sequence: 3 givenname: Stefania surname: Assereto fullname: Assereto, Stefania organization: Unit of Pediatric Neurology and Muscle Disease, Istituto Giannina Gaslini, Genova, Italy – sequence: 4 givenname: Floriana surname: Fruscione fullname: Fruscione, Floriana organization: Unit of Pediatric Neurology and Muscle Disease, Istituto Giannina Gaslini, Genova, Italy – sequence: 5 givenname: Angela surname: Pistorio fullname: Pistorio, Angela organization: Unit of Epidemiology and Statistics, Istituto Giannina Gaslini, Genova, Italy – sequence: 6 givenname: Chiara surname: Panicucci fullname: Panicucci, Chiara organization: Unit of Pediatric Neurology and Muscle Disease, Istituto Giannina Gaslini, Genova, Italy – sequence: 7 givenname: Stefano surname: Volpi fullname: Volpi, Stefano organization: Unit of Pediatrics II, Istituto Giannina Gaslini, Genova, Italy – sequence: 8 givenname: Lisa surname: Perruzza fullname: Perruzza, Lisa organization: Institute for Research in Biomedicine, Bellinzona, Switzerland – sequence: 9 givenname: Chiara surname: Fiorillo fullname: Fiorillo, Chiara organization: Neuromuscular and Molecular Medicine Unit, Stella Maris Foundation, Pisa, Italy – sequence: 10 givenname: Carlo surname: Minetti fullname: Minetti, Carlo organization: Unit of Pediatric Neurology and Muscle Disease, Istituto Giannina Gaslini, Genova, Italy – sequence: 11 givenname: Elisabetta surname: Traggiai fullname: Traggiai, Elisabetta organization: Novartis Biologics Center, Novartis Institute for Research in Biomedicine, Basel, Switzerland – sequence: 12 givenname: Fabio surname: Grassi fullname: Grassi, Fabio email: fabio.grassi@irb.unisi.ch organization: Institute for Research in Biomedicine, Bellinzona, Switzerland – sequence: 13 givenname: Claudio surname: Bruno fullname: Bruno, Claudio email: claudiobruno@ospedale-gaslini.ge.it, claudio2246@gmail.com organization: Center of Myology and Neurodegenerative Disorders, Department of Neuroscience, Istituto Giannina Gaslini, Genova, Italy |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26465071$$D View this record in MEDLINE/PubMed |
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| SubjectTerms | Adenosine Triphosphate - analogs & derivatives Adenosine Triphosphate - immunology Adenosine Triphosphate - pharmacology Adenosine Triphosphate - therapeutic use Animals Disease Progression Drug Evaluation, Preclinical - methods Male Mice, Inbred C57BL Mice, Inbred mdx Muscle, Skeletal - immunology Muscle, Skeletal - pathology Muscle, Skeletal - physiology Muscular Dystrophy, Duchenne - immunology Muscular Dystrophy, Duchenne - pathology Muscular Dystrophy, Duchenne - prevention & control Pathology Physical Conditioning, Animal Purinergic P2X Receptor Antagonists - pharmacology Purinergic P2X Receptor Antagonists - therapeutic use Receptors, Purinergic P2X - metabolism Receptors, Purinergic P2X - physiology Regeneration - drug effects Signal Transduction - drug effects T-Lymphocytes, Regulatory - drug effects T-Lymphocytes, Regulatory - immunology |
| Title | Enhancement of Muscle T Regulatory Cells and Improvement of Muscular Dystrophic Process in mdx Mice by Blockade of Extracellular ATP/P2X Axis |
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