Phospholipase D isoforms differentially regulate leukocyte responses to acute lung injury

Phospholipase D (PLD) plays important roles in cellular responses to tissue injury that are critical to acute inflammatory diseases, such as the acute respiratory distress syndrome (ARDS). We investigated the expression of PLD isoforms and related phospholipid phosphatases in patients with ARDS, and...

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Published inJournal of leukocyte biology Vol. 103; no. 5; pp. 919 - 932
Main Authors Abdulnour, Raja‐Elie E., Howrylak, Judie A., Tavares, Alexander H., Douda, David N., Henkels, Karen M., Miller, Taylor E., Fredenburgh, Laura E., Baron, Rebecca M., Gomez‐Cambronero, Julian, Levy, Bruce D.
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Published United States 01.05.2018
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Abstract Phospholipase D (PLD) plays important roles in cellular responses to tissue injury that are critical to acute inflammatory diseases, such as the acute respiratory distress syndrome (ARDS). We investigated the expression of PLD isoforms and related phospholipid phosphatases in patients with ARDS, and their roles in a murine model of self‐limited acute lung injury (ALI). Gene expression microarray analysis on whole blood obtained from patients that met clinical criteria for ARDS and clinically matched controls (non‐ARDS) demonstrated that PLD1 gene expression was increased in patients with ARDS relative to non‐ARDS and correlated with survival. In contrast, PLD2 expression was associated with mortality. In a murine model of self‐resolving ALI, lung Pld1 expression increased and Pld2 expression decreased 24 h after intrabronchial acid. Total lung PLD activity was increased 24 h after injury. Pld1−/− mice demonstrated impaired alveolar barrier function and increased tissue injury relative to WT and Pld2−/−, whereas Pld2−/− mice demonstrated increased recruitment of neutrophils and macrophages, and decreased tissue injury. Isoform‐specific PLD inhibitors mirrored the results with isoform‐specific Pld‐KO mice. PLD1 gene expression knockdown in human leukocytes was associated with decreased phagocytosis by neutrophils, whereas reactive oxygen species production and phagocytosis decreased in M2‐macrophages. PLD2 gene expression knockdown increased neutrophil and M2‐macrophage transmigration, and increased M2‐macrophage phagocytosis. These results uncovered selective regulation of PLD isoforms after ALI, and opposing effects of selective isoform knockdown on host responses and tissue injury. These findings support therapeutic strategies targeting specific PLD isoforms for the treatment of ARDS. PLD isoforms are differentially associated with survival in patients with ARDS and regulate host responses to acute lung injury.
AbstractList Phospholipase D (PLD) plays important roles in cellular responses to tissue injury that are critical to acute inflammatory diseases, such as the acute respiratory distress syndrome (ARDS). We investigated the expression of PLD isoforms and related phospholipid phosphatases in patients with ARDS, and their roles in a murine model of self-limited acute lung injury (ALI). Gene expression microarray analysis on whole blood obtained from patients that met clinical criteria for ARDS and clinically matched controls (non-ARDS) demonstrated that PLD1 gene expression was increased in patients with ARDS relative to non-ARDS and correlated with survival. In contrast, PLD2 expression was associated with mortality. In a murine model of self-resolving ALI, lung Pld1 expression increased and Pld2 expression decreased 24 h after intrabronchial acid. Total lung PLD activity was increased 24 h after injury. Pld1 mice demonstrated impaired alveolar barrier function and increased tissue injury relative to WT and Pld2 , whereas Pld2 mice demonstrated increased recruitment of neutrophils and macrophages, and decreased tissue injury. Isoform-specific PLD inhibitors mirrored the results with isoform-specific Pld-KO mice. PLD1 gene expression knockdown in human leukocytes was associated with decreased phagocytosis by neutrophils, whereas reactive oxygen species production and phagocytosis decreased in M2-macrophages. PLD2 gene expression knockdown increased neutrophil and M2-macrophage transmigration, and increased M2-macrophage phagocytosis. These results uncovered selective regulation of PLD isoforms after ALI, and opposing effects of selective isoform knockdown on host responses and tissue injury. These findings support therapeutic strategies targeting specific PLD isoforms for the treatment of ARDS.
Phospholipase D (PLD) plays important roles in cellular responses to tissue injury that are critical to acute inflammatory diseases, such as the acute respiratory distress syndrome (ARDS). We investigated the expression of PLD isoforms and related phospholipid phosphatases in patients with ARDS, and their roles in a murine model of self-limited acute lung injury (ALI). Gene expression microarray analysis on whole blood obtained from patients that met clinical criteria for ARDS and clinically matched controls (non-ARDS) demonstrated that PLD1 gene expression was increased in patients with ARDS relative to non-ARDS and correlated with survival. In contrast, PLD2 expression was associated with mortality. In a murine model of self-resolving ALI, lung Pld1 expression increased and Pld2 expression decreased 24 h after intrabronchial acid. Total lung PLD activity was increased 24 h after injury. Pld1−/− mice demonstrated impaired alveolar barrier function and increased tissue injury relative to WT and Pld2−/−, whereas Pld2−/− mice demonstrated increased recruitment of neutrophils and macrophages, and decreased tissue injury. Isoform-specific PLD inhibitors mirrored the results with isoform-specific Pld-KO mice. PLD1 gene expression knockdown in human leukocytes was associated with decreased phagocytosis by neutrophils, whereas reactive oxygen species production and phagocytosis decreased in M2-macrophages. PLD2 gene expression knockdown increased neutrophil and M2-macrophage transmigration, and increased M2-macrophage phagocytosis. These results uncovered selective regulation of PLD isoforms after ALI, and opposing effects of selective isoform knockdown on host responses and tissue injury. These findings support therapeutic strategies targeting specific PLD isoforms for the treatment of ARDS.
Phospholipase D (PLD) plays important roles in cellular responses to tissue injury that are critical to acute inflammatory diseases, such as the acute respiratory distress syndrome (ARDS). We investigated the expression of PLD isoforms and related phospholipid phosphatases in patients with ARDS, and their roles in a murine model of self-limited acute lung injury (ALI). Gene expression microarray analysis on whole blood obtained from patients that met clinical criteria for ARDS and clinically matched controls (non-ARDS) demonstrated that PLD1 gene expression was increased in patients with ARDS relative to non-ARDS and correlated with survival. In contrast, PLD2 expression was associated with mortality. In a murine model of self-resolving ALI, lung Pld1 expression increased and Pld2 expression decreased 24 h after intrabronchial acid. Total lung PLD activity was increased 24 h after injury. Pld1 −/− mice demonstrated impaired alveolar barrier function and increased tissue injury relative to WT and Pld2 −/− , whereas Pld2 −/− mice demonstrated increased recruitment of neutrophils and macrophages, and decreased tissue injury. Isoform-specific PLD inhibitors mirrored the results with isoform-specific Pld -KO mice. PLD1 gene expression knockdown in human leukocytes was associated with decreased phagocytosis by neutrophils, whereas reactive oxygen species production and phagocytosis decreased in M2-macrophages. PLD2 gene expression knockdown increased neutrophil and M2-macrophage transmigration, and increased M2-macrophage phagocytosis. These results uncovered selective regulation of PLD isoforms after ALI, and opposing effects of selective isoform knockdown on host responses and tissue injury. These findings support therapeutic strategies targeting specific PLD isoforms for the treatment of ARDS.
Phospholipase D (PLD) plays important roles in cellular responses to tissue injury that are critical to acute inflammatory diseases, such as the acute respiratory distress syndrome (ARDS). We investigated the expression of PLD isoforms and related phospholipid phosphatases in patients with ARDS, and their roles in a murine model of self‐limited acute lung injury (ALI). Gene expression microarray analysis on whole blood obtained from patients that met clinical criteria for ARDS and clinically matched controls (non‐ARDS) demonstrated that PLD1 gene expression was increased in patients with ARDS relative to non‐ARDS and correlated with survival. In contrast, PLD2 expression was associated with mortality. In a murine model of self‐resolving ALI, lung Pld1 expression increased and Pld2 expression decreased 24 h after intrabronchial acid. Total lung PLD activity was increased 24 h after injury. Pld1−/− mice demonstrated impaired alveolar barrier function and increased tissue injury relative to WT and Pld2−/−, whereas Pld2−/− mice demonstrated increased recruitment of neutrophils and macrophages, and decreased tissue injury. Isoform‐specific PLD inhibitors mirrored the results with isoform‐specific Pld‐KO mice. PLD1 gene expression knockdown in human leukocytes was associated with decreased phagocytosis by neutrophils, whereas reactive oxygen species production and phagocytosis decreased in M2‐macrophages. PLD2 gene expression knockdown increased neutrophil and M2‐macrophage transmigration, and increased M2‐macrophage phagocytosis. These results uncovered selective regulation of PLD isoforms after ALI, and opposing effects of selective isoform knockdown on host responses and tissue injury. These findings support therapeutic strategies targeting specific PLD isoforms for the treatment of ARDS. PLD isoforms are differentially associated with survival in patients with ARDS and regulate host responses to acute lung injury.
Author Howrylak, Judie A.
Abdulnour, Raja‐Elie E.
Tavares, Alexander H.
Miller, Taylor E.
Fredenburgh, Laura E.
Baron, Rebecca M.
Gomez‐Cambronero, Julian
Douda, David N.
Henkels, Karen M.
Levy, Bruce D.
AuthorAffiliation 2 Division of Pulmonary Allergy and Critical Care Medicine, Penn State Hershey Medical Center, Hershey, Pennsylvania, USA
4 Center for Experimental Therapeutics and Reperfusion Injury, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts, USA
3 Department of Biochemistry and Molecular Biology, Wright State University, Dayton, Ohio, USA
1 Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts, USA
AuthorAffiliation_xml – name: 1 Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts, USA
– name: 3 Department of Biochemistry and Molecular Biology, Wright State University, Dayton, Ohio, USA
– name: 4 Center for Experimental Therapeutics and Reperfusion Injury, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts, USA
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Issue 5
Keywords acute respiratory distress syndrome
microarray
acute lung injury
Phospholipase D
Language English
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AUTHORSHIP
All authors concur with the submission and none of the data has been previously reported or is under consideration for publication elsewhere
R.E.A. contributed to experimental design, carried out experiments and data analyses, and wrote the manuscript; J.A.H. contributed to experimental design, carried out experiments and data analysis, and contributed to manuscript and figure preparation; A.H.T., D.N.D., K.M.H., and T.E.M. carried out experiments and data analysis and contributed to manuscript and figure preparation; L.E.F., R.M.B., and J.G.C contributed to experimental design, data analysis, and manuscript preparation; B.D.L. contributed to experimental design, carried out experiments and data analyses, contributed to manuscript preparation, and conceived the overall research plan.
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Snippet Phospholipase D (PLD) plays important roles in cellular responses to tissue injury that are critical to acute inflammatory diseases, such as the acute...
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SubjectTerms acute lung injury
Acute Lung Injury - immunology
Acute Lung Injury - metabolism
Acute Lung Injury - pathology
acute respiratory distress syndrome
Animals
Case-Control Studies
Cells, Cultured
Female
Humans
Leukocytes - immunology
Leukocytes - metabolism
Leukocytes - pathology
Lung - immunology
Lung - metabolism
Lung - pathology
Macrophages - immunology
Macrophages - metabolism
Macrophages - pathology
Male
Mice
Mice, Inbred C57BL
Mice, Knockout
microarray
Neutrophils - immunology
Neutrophils - metabolism
Neutrophils - pathology
Phagocytosis
Phospholipase D
Phospholipase D - physiology
Protein Isoforms
Respiratory Distress Syndrome, Adult - metabolism
Respiratory Distress Syndrome, Adult - pathology
Title Phospholipase D isoforms differentially regulate leukocyte responses to acute lung injury
URI https://onlinelibrary.wiley.com/doi/abs/10.1002%2FJLB.3A0617-252RR
https://www.ncbi.nlm.nih.gov/pubmed/29437245
https://search.proquest.com/docview/2001916476
https://pubmed.ncbi.nlm.nih.gov/PMC6375305
Volume 103
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