Inhibition of pro-inflammatory signaling in human primary macrophages by enhancing arginase-2 via target site blockers
The modulation of macrophage phenotype from a pro-inflammatory to an anti-inflammatory state holds therapeutic potential in the treatment of inflammatory disease. We have previously shown that arginase-2 (Arg2), a mitochondrial enzyme, is a key regulator of the macrophage anti-inflammatory response....
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| Published in | Molecular therapy. Nucleic acids Vol. 33; pp. 941 - 959 |
|---|---|
| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Elsevier Inc
12.09.2023
American Society of Gene & Cell Therapy Elsevier |
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| Online Access | Get full text |
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| Abstract | The modulation of macrophage phenotype from a pro-inflammatory to an anti-inflammatory state holds therapeutic potential in the treatment of inflammatory disease. We have previously shown that arginase-2 (Arg2), a mitochondrial enzyme, is a key regulator of the macrophage anti-inflammatory response. Here, we investigate the therapeutic potential of Arg2 enhancement via target site blockers (TSBs) in human macrophages. TSBs are locked nucleic acid antisense oligonucleotides that were specifically designed to protect specific microRNA recognition elements (MREs) in human ARG2 3′ UTR mRNA. TSBs targeting miR-155 (TSB-155) and miR-3202 (TSB-3202) MREs increased ARG2 expression in human monocyte-derived macrophages. This resulted in decreased gene expression and cytokine production of TNF-α and CCL2 and, for TSB-3202, in an increase in the anti-inflammatory macrophage marker, CD206. Proteomic analysis demonstrated that a network of pro-inflammatory responsive proteins was modulated by TSBs. In silico bioinformatic analysis predicted that TSB-3202 suppressed upstream pro-inflammatory regulators including STAT-1 while enhancing anti-inflammatory associated proteins. Proteomic data were validated by confirming increased levels of sequestosome-1 and decreased levels of phosphorylated STAT-1 and STAT-1 upon TSB treatment. In conclusion, upregulation of Arg2 by TSBs inhibits pro-inflammatory signaling and is a promising novel therapeutic strategy to modulate inflammatory signaling in human macrophages.
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Fitzsimons and colleagues demonstrated that arginase-2 is increased by IL-10 in the presence of a pro-inflammatory stimulus in human primary macrophages. We designed oligonucleotides (target site blockers) that could block microRNA binding to arginase-2 messenger RNA. This led to enhancement of arginase-2 and a decrease in pro-inflammatory signaling. |
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| AbstractList | The modulation of macrophage phenotype from a pro-inflammatory to an anti-inflammatory state holds therapeutic potential in the treatment of inflammatory disease. We have previously shown that arginase-2 (Arg2), a mitochondrial enzyme, is a key regulator of the macrophage anti-inflammatory response. Here, we investigate the therapeutic potential of Arg2 enhancement via target site blockers (TSBs) in human macrophages. TSBs are locked nucleic acid antisense oligonucleotides that were specifically designed to protect specific microRNA recognition elements (MREs) in human ARG2 3′ UTR mRNA. TSBs targeting miR-155 (TSB-155) and miR-3202 (TSB-3202) MREs increased ARG2 expression in human monocyte-derived macrophages. This resulted in decreased gene expression and cytokine production of TNF-α and CCL2 and, for TSB-3202, in an increase in the anti-inflammatory macrophage marker, CD206. Proteomic analysis demonstrated that a network of pro-inflammatory responsive proteins was modulated by TSBs. In silico bioinformatic analysis predicted that TSB-3202 suppressed upstream pro-inflammatory regulators including STAT-1 while enhancing anti-inflammatory associated proteins. Proteomic data were validated by confirming increased levels of sequestosome-1 and decreased levels of phosphorylated STAT-1 and STAT-1 upon TSB treatment. In conclusion, upregulation of Arg2 by TSBs inhibits pro-inflammatory signaling and is a promising novel therapeutic strategy to modulate inflammatory signaling in human macrophages.
[Display omitted]
Fitzsimons and colleagues demonstrated that arginase-2 is increased by IL-10 in the presence of a pro-inflammatory stimulus in human primary macrophages. We designed oligonucleotides (target site blockers) that could block microRNA binding to arginase-2 messenger RNA. This led to enhancement of arginase-2 and a decrease in pro-inflammatory signaling. The modulation of macrophage phenotype from a pro-inflammatory to an anti-inflammatory state holds therapeutic potential in the treatment of inflammatory disease. We have previously shown that arginase-2 (Arg2), a mitochondrial enzyme, is a key regulator of the macrophage anti-inflammatory response. Here, we investigate the therapeutic potential of Arg2 enhancement via target site blockers (TSBs) in human macrophages. TSBs are locked nucleic acid antisense oligonucleotides that were specifically designed to protect specific microRNA recognition elements (MREs) in human ARG2 3′ UTR mRNA. TSBs targeting miR-155 (TSB-155) and miR-3202 (TSB-3202) MREs increased ARG2 expression in human monocyte-derived macrophages. This resulted in decreased gene expression and cytokine production of TNF-α and CCL2 and, for TSB-3202, in an increase in the anti-inflammatory macrophage marker, CD206. Proteomic analysis demonstrated that a network of pro-inflammatory responsive proteins was modulated by TSBs. In silico bioinformatic analysis predicted that TSB-3202 suppressed upstream pro-inflammatory regulators including STAT-1 while enhancing anti-inflammatory associated proteins. Proteomic data were validated by confirming increased levels of sequestosome-1 and decreased levels of phosphorylated STAT-1 and STAT-1 upon TSB treatment. In conclusion, upregulation of Arg2 by TSBs inhibits pro-inflammatory signaling and is a promising novel therapeutic strategy to modulate inflammatory signaling in human macrophages. Fitzsimons and colleagues demonstrated that arginase-2 is increased by IL-10 in the presence of a pro-inflammatory stimulus in human primary macrophages. We designed oligonucleotides (target site blockers) that could block microRNA binding to arginase-2 messenger RNA. This led to enhancement of arginase-2 and a decrease in pro-inflammatory signaling. The modulation of macrophage phenotype from a pro-inflammatory to an anti-inflammatory state holds therapeutic potential in the treatment of inflammatory disease. We have previously shown that arginase-2 (Arg2), a mitochondrial enzyme, is a key regulator of the macrophage anti-inflammatory response. Here, we investigate the therapeutic potential of Arg2 enhancement via target site blockers (TSBs) in human macrophages. TSBs are locked nucleic acid antisense oligonucleotides that were specifically designed to protect specific microRNA recognition elements (MREs) in human ARG2 3' UTR mRNA. TSBs targeting miR-155 (TSB-155) and miR-3202 (TSB-3202) MREs increased ARG2 expression in human monocyte-derived macrophages. This resulted in decreased gene expression and cytokine production of TNF-α and CCL2 and, for TSB-3202, in an increase in the anti-inflammatory macrophage marker, CD206. Proteomic analysis demonstrated that a network of pro-inflammatory responsive proteins was modulated by TSBs. In silico bioinformatic analysis predicted that TSB-3202 suppressed upstream pro-inflammatory regulators including STAT-1 while enhancing anti-inflammatory associated proteins. Proteomic data were validated by confirming increased levels of sequestosome-1 and decreased levels of phosphorylated STAT-1 and STAT-1 upon TSB treatment. In conclusion, upregulation of Arg2 by TSBs inhibits pro-inflammatory signaling and is a promising novel therapeutic strategy to modulate inflammatory signaling in human macrophages.The modulation of macrophage phenotype from a pro-inflammatory to an anti-inflammatory state holds therapeutic potential in the treatment of inflammatory disease. We have previously shown that arginase-2 (Arg2), a mitochondrial enzyme, is a key regulator of the macrophage anti-inflammatory response. Here, we investigate the therapeutic potential of Arg2 enhancement via target site blockers (TSBs) in human macrophages. TSBs are locked nucleic acid antisense oligonucleotides that were specifically designed to protect specific microRNA recognition elements (MREs) in human ARG2 3' UTR mRNA. TSBs targeting miR-155 (TSB-155) and miR-3202 (TSB-3202) MREs increased ARG2 expression in human monocyte-derived macrophages. This resulted in decreased gene expression and cytokine production of TNF-α and CCL2 and, for TSB-3202, in an increase in the anti-inflammatory macrophage marker, CD206. Proteomic analysis demonstrated that a network of pro-inflammatory responsive proteins was modulated by TSBs. In silico bioinformatic analysis predicted that TSB-3202 suppressed upstream pro-inflammatory regulators including STAT-1 while enhancing anti-inflammatory associated proteins. Proteomic data were validated by confirming increased levels of sequestosome-1 and decreased levels of phosphorylated STAT-1 and STAT-1 upon TSB treatment. In conclusion, upregulation of Arg2 by TSBs inhibits pro-inflammatory signaling and is a promising novel therapeutic strategy to modulate inflammatory signaling in human macrophages. The modulation of macrophage phenotype from a pro-inflammatory to an anti-inflammatory state holds therapeutic potential in the treatment of inflammatory disease. We have previously shown that arginase-2 (Arg2), a mitochondrial enzyme, is a key regulator of the macrophage anti-inflammatory response. Here, we investigate the therapeutic potential of Arg2 enhancement via target site blockers (TSBs) in human macrophages. TSBs are locked nucleic acid antisense oligonucleotides that were specifically designed to protect specific microRNA recognition elements (MREs) in human ARG2 3′ UTR mRNA. TSBs targeting miR-155 (TSB-155) and miR-3202 (TSB-3202) MREs increased ARG2 expression in human monocyte-derived macrophages. This resulted in decreased gene expression and cytokine production of TNF-α and CCL2 and, for TSB-3202, in an increase in the anti-inflammatory macrophage marker, CD206. Proteomic analysis demonstrated that a network of pro-inflammatory responsive proteins was modulated by TSBs. In silico bioinformatic analysis predicted that TSB-3202 suppressed upstream pro-inflammatory regulators including STAT-1 while enhancing anti-inflammatory associated proteins. Proteomic data were validated by confirming increased levels of sequestosome-1 and decreased levels of phosphorylated STAT-1 and STAT-1 upon TSB treatment. In conclusion, upregulation of Arg2 by TSBs inhibits pro-inflammatory signaling and is a promising novel therapeutic strategy to modulate inflammatory signaling in human macrophages. |
| Author | Ramió-Torrentà, Lluís Nally, Frances Fitzsimons, Stephen Dillon, Eugene Strowitzki, Moritz J. McCoy, Claire E. Fashina, Ifeolutembi A. De Santi, Chiara Muñoz-San Martín, María Dowling, Jennifer K. |
| Author_xml | – sequence: 1 givenname: Stephen surname: Fitzsimons fullname: Fitzsimons, Stephen email: sfitzsimons08@gmail.com organization: School of Pharmacy and Biomolecular Science, Royal College of Surgeons in Ireland, 123 St Stephen’s Green, Dublin 2, Ireland – sequence: 2 givenname: María surname: Muñoz-San Martín fullname: Muñoz-San Martín, María organization: School of Pharmacy and Biomolecular Science, Royal College of Surgeons in Ireland, 123 St Stephen’s Green, Dublin 2, Ireland – sequence: 3 givenname: Frances surname: Nally fullname: Nally, Frances organization: School of Pharmacy and Biomolecular Science, Royal College of Surgeons in Ireland, 123 St Stephen’s Green, Dublin 2, Ireland – sequence: 4 givenname: Eugene surname: Dillon fullname: Dillon, Eugene organization: School of Biomolecular and Biomedical Science, Conway Institute, University College Dublin, Belfield, Dublin 4, Ireland – sequence: 5 givenname: Ifeolutembi A. surname: Fashina fullname: Fashina, Ifeolutembi A. organization: School of Pharmacy and Biomolecular Science, Royal College of Surgeons in Ireland, 123 St Stephen’s Green, Dublin 2, Ireland – sequence: 6 givenname: Moritz J. surname: Strowitzki fullname: Strowitzki, Moritz J. organization: Department of General, Visceral & Transplantation Surgery, University Hospital Heidelberg, Heidelberg, Germany – sequence: 7 givenname: Lluís surname: Ramió-Torrentà fullname: Ramió-Torrentà, Lluís organization: Neuroinflammation and Neurodegeneration Group, Girona Biomedical Research Institute (IDIBGI), CERCA Programme/Generalitat de Catalunya, Salt, Girona, Spain – sequence: 8 givenname: Jennifer K. surname: Dowling fullname: Dowling, Jennifer K. organization: School of Pharmacy and Biomolecular Science, Royal College of Surgeons in Ireland, 123 St Stephen’s Green, Dublin 2, Ireland – sequence: 9 givenname: Chiara surname: De Santi fullname: De Santi, Chiara email: chiaradesanti@rcsi.ie organization: School of Pharmacy and Biomolecular Science, Royal College of Surgeons in Ireland, 123 St Stephen’s Green, Dublin 2, Ireland – sequence: 10 givenname: Claire E. surname: McCoy fullname: McCoy, Claire E. organization: School of Pharmacy and Biomolecular Science, Royal College of Surgeons in Ireland, 123 St Stephen’s Green, Dublin 2, Ireland |
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| Keywords | MT: Oligonucleotides: Therapies and Applications macrophages inflammation miR-155 multiple sclerosis microRNA target site blockers arginase-2 |
| Language | English |
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| Title | Inhibition of pro-inflammatory signaling in human primary macrophages by enhancing arginase-2 via target site blockers |
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