Apoptosis in the lung: induction, clearance and detection.

Apoptosis and other forms of programmed cell death are important contributors to lung pathophysiology. In this brief review, we discuss some of the implications of finding apoptotic cells in the lung and methods for their detection. The balance between induction of apoptosis and the normally highly efficient clearance of such cells shows that these are highly dynamic processes and suggests that abnormalities of apoptotic cell clearance may be an alternative explanation for their detection. Because recognition of apoptotic cells by other lung cells has additional effects on inflammation, immunity, and tissue repair, local responses to the dying cells may also have important consequences in addition to the cell death itself.

[1]  J. Roa,et al.  Histologic Sectioning Produces TUNEL Reactivity , 2009 .

[2]  A. Mb Morphologic criteria and detection of apoptosis , 2009, Herz.

[3]  W. Cioffi,et al.  Fas-induced pulmonary apoptosis and inflammation during indirect acute lung injury. , 2007, American journal of respiratory and critical care medicine.

[4]  G. Perkins,et al.  BUB1 mediation of caspase-independent mitotic death determines cell fate , 2007, The Journal of cell biology.

[5]  L. Zitvogel,et al.  Cell death modalities: classification and pathophysiological implications , 2007, Cell Death and Differentiation.

[6]  P. Kirkham Oxidative stress and macrophage function: a failure to resolve the inflammatory response. , 2007, Biochemical Society transactions.

[7]  I. Komuro,et al.  p53-induced inhibition of Hif-1 causes cardiac dysfunction during pressure overload , 2007, Nature.

[8]  W. Schiemann,et al.  Apoptotic Cells, through Transforming Growth Factor-β, Coordinately Induce Anti-inflammatory and Suppress Pro-inflammatory Eicosanoid and NO Synthesis in Murine Macrophages* , 2006, Journal of Biological Chemistry.

[9]  Seamus J. Martin,et al.  Mitochondrial membrane remodeling in apoptosis: an inside story , 2006, Cell Death and Differentiation.

[10]  Dmitri V. Krysko,et al.  Clearance of apoptotic and necrotic cells and its immunological consequences , 2006, Apoptosis.

[11]  S. Pervaiz,et al.  TNF receptor superfamily‐induced cell death: redox‐dependent execution , 2006, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[12]  J. Levine,et al.  Specific Recognition of Apoptotic Cells Reveals a Ubiquitous and Unconventional Innate Immunity* , 2006, Journal of Biological Chemistry.

[13]  R. Bowler,et al.  Lovastatin Enhances Clearance of Apoptotic Cells (Efferocytosis) with Implications for Chronic Obstructive Pulmonary Disease1 , 2006, The Journal of Immunology.

[14]  J. Horowitz,et al.  Evolving concepts of apoptosis in idiopathic pulmonary fibrosis. , 2006, Proceedings of the American Thoracic Society.

[15]  D. Green,et al.  Dissecting p53-dependent apoptosis , 2006, Cell Death and Differentiation.

[16]  P. Henson,et al.  Recognition ligands on apoptotic cells: a perspective , 2006, Journal of leukocyte biology.

[17]  B. Ma,et al.  Role of CCR5 in the Pathogenesis of IL-13-Induced Inflammation and Remodeling1 , 2006, The Journal of Immunology.

[18]  D. Hyde,et al.  Design-Based Sampling and Quantitation of the Respiratory Airways , 2006, Toxicologic pathology.

[19]  G. Joos,et al.  Role of apoptosis in the pathogenesis of COPD and pulmonary emphysema , 2006, Respiratory research.

[20]  W. Janssen,et al.  Cell-Surface Calreticulin Initiates Clearance of Viable or Apoptotic Cells through trans-Activation of LRP on the Phagocyte , 2005, Cell.

[21]  Richard,et al.  Role of cathepsin S-dependent epithelial cell apoptosis in IFN-γ-induced alveolar remodeling and pulmonary emphysema , 2005, The Journal of Immunology.

[22]  J. Erjefält Transepithelial migration, necrosis and apoptosis as silent and pro-inflammatory fates of airway granulocytes. , 2005, Current drug targets. Inflammation and allergy.

[23]  R. Flavell,et al.  Role of Cathepsin S-Dependent Epithelial Cell Apoptosis in IFN-γ-Induced Alveolar Remodeling and Pulmonary Emphysema1 , 2005, The Journal of Immunology.

[24]  D. Green,et al.  Apoptotic Pathways: Ten Minutes to Dead , 2005, Cell.

[25]  I. Petrache,et al.  Ceramide upregulation causes pulmonary cell apoptosis and emphysema-like disease in mice , 2005, Nature Medicine.

[26]  B. Cookson,et al.  Apoptosis, Pyroptosis, and Necrosis: Mechanistic Description of Dead and Dying Eukaryotic Cells , 2005, Infection and Immunity.

[27]  S. Hodge,et al.  Increased airway epithelial and T-cell apoptosis in COPD remains despite smoking cessation , 2005, European Respiratory Journal.

[28]  Andrea Vondracek,et al.  Interaction between Phosphatidylserine and the Phosphatidylserine Receptor Inhibits Immune Responses In Vivo1 , 2005, The Journal of Immunology.

[29]  M. Neville,et al.  Epithelial cells as phagocytes: apoptotic epithelial cells are engulfed by mammary alveolar epithelial cells and repress inflammatory mediator release , 2005, Cell Death and Differentiation.

[30]  N. Hagimoto,et al.  Apoptosis and epithelial injury in the lungs. , 2005, Proceedings of the American Thoracic Society.

[31]  C. Thompson,et al.  Death by design: apoptosis, necrosis and autophagy. , 2004, Current opinion in cell biology.

[32]  T. Welte,et al.  Life after corpse engulfment: phagocytosis of apoptotic cells leads to VEGF secretion and cell growth , 2004, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[33]  Irina Petrache,et al.  Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. , 2004, The Journal of clinical investigation.

[34]  J. Milbrandt,et al.  Early Growth Response Gene 1–mediated Apoptosis Is Essential for Transforming Growth Factor β1–induced Pulmonary Fibrosis , 2004, The Journal of experimental medicine.

[35]  Tak W. Mak,et al.  Pathways of apoptotic and non-apoptotic death in tumour cells , 2004, Nature Reviews Cancer.

[36]  N. Palaniyar,et al.  Nucleic Acid Is a Novel Ligand for Innate, Immune Pattern Recognition Collectins Surfactant Proteins A and D and Mannose-binding Lectin* , 2004, Journal of Biological Chemistry.

[37]  M. Fessler,et al.  Phospholipid Flip-Flop and Phospholipid Scramblase 1 (PLSCR1) Co-localize to Uropod Rafts in Formylated Met-Leu-Phe-stimulated Neutrophils* , 2004, Journal of Biological Chemistry.

[38]  P. Thompson,et al.  Comparison of the morphological and biochemical changes in normal human lung fibroblasts and fibroblasts derived from lungs of patients with idiopathic pulmonary fibrosis during FasL‐induced apoptosis , 2004, The Journal of pathology.

[39]  F. Harrisson,et al.  Histochemical Demonstration of Apoptotic Cells in the Chicken Embryo Using Annexin V , 1998, The Histochemical Journal.

[40]  J. Buyon,et al.  Clearance of apoptotic cells: TGF‐β in the balance between inflammation and fibrosis , 2003, Journal of leukocyte biology.

[41]  C. Haslett,et al.  Eat Me or Die , 2003, Science.

[42]  P. Henson,et al.  The final step in programmed cell death: phagocytes carry apoptotic cells to the grave. , 2003, Essays in biochemistry.

[43]  N. Voelkel,et al.  Methylprednisolone causes matrix metalloproteinase-dependent emphysema in adult rats. , 2003, American journal of respiratory and critical care medicine.

[44]  N. Voelkel,et al.  Oxidative stress and apoptosis interact and cause emphysema due to vascular endothelial growth factor receptor blockade. , 2003, American journal of respiratory cell and molecular biology.

[45]  C. Haslett,et al.  Cell biology. Eat me or die. , 2003, Science.

[46]  John Savill,et al.  A blast from the past: clearance of apoptotic cells regulates immune responses , 2002, Nature Reviews Immunology.

[47]  K. Brown,et al.  Elastase-mediated phosphatidylserine receptor cleavage impairs apoptotic cell clearance in cystic fibrosis and bronchiectasis. , 2002, The Journal of clinical investigation.

[48]  V. Fadok,et al.  Phosphatidylserine-dependent ingestion of apoptotic cells promotes TGF-beta1 secretion and the resolution of inflammation. , 2002, The Journal of clinical investigation.

[49]  D. Romberger,et al.  Cigarette smoke inhibits human bronchial epithelial cell repair processes. , 2001, American journal of respiratory cell and molecular biology.

[50]  Louise P. Cramer,et al.  An epithelial cell destined for apoptosis signals its neighbors to extrude it by an actin- and myosin-dependent mechanism , 2001, Current Biology.

[51]  R. Scott,et al.  Phagocytosis and clearance of apoptotic cells is mediated by MER , 2001, Nature.

[52]  H. Yamamoto,et al.  Alveolar macrophages that phagocytose apoptotic neutrophils produce hepatocyte growth factor during bacterial pneumonia in mice. , 2001, American journal of respiratory cell and molecular biology.

[53]  M. Cosio,et al.  Lymphocyte population and apoptosis in the lungs of smokers and their relation to emphysema. , 2001, The European respiratory journal.

[54]  D A Lynch,et al.  Endothelial cell death and decreased expression of vascular endothelial growth factor and vascular endothelial growth factor receptor 2 in emphysema. , 2001, American journal of respiratory and critical care medicine.

[55]  P. Hirth,et al.  Inhibition of the VEGF receptor 2 combined with chronic hypoxia causes cell death‐dependent pulmonary endothelial cell proliferation and severe pulmonary hypertension , 2001, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[56]  P. Matzinger,et al.  Danger signals: SOS to the immune system. , 2001, Current opinion in immunology.

[57]  P. Hirth,et al.  Inhibition of VEGF receptors causes lung cell apoptosis and emphysema. , 2000, The Journal of clinical investigation.

[58]  Adrian M Heilbut,et al.  Complete reversal of fatal pulmonary hypertension in rats by a serine elastase inhibitor , 2000, Nature Medicine.

[59]  H. Katus,et al.  Decreased apoptosis and increased activation of alveolar neutrophils in bacterial pneumonia. , 2000, Chest.

[60]  P. Jusuf,et al.  A semi-quantitative PCR method for the detection of low levels of apoptotic DNA fragmentation in a heart failure model. , 2000, The Japanese journal of physiology.

[61]  Gerard I. Evan,et al.  The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant , 2000, Nature Cell Biology.

[62]  E. Marchi,et al.  Mesothelial cell apoptosis is confirmed in vivo by morphological change in cytokeratin distribution. , 2000, American journal of physiology. Lung cellular and molecular physiology.

[63]  P. Doevendans,et al.  Markers of apoptosis in cardiovascular tissues: focus on Annexin V. , 2000, Cardiovascular research.

[64]  C. Haslett Granulocyte apoptosis and its role in the resolution and control of lung inflammation. , 1999, American journal of respiratory and critical care medicine.

[65]  J. Roa,et al.  Histologic sectioning produces TUNEL reactivity. A potential cause of false-positive staining. , 1999, Archives of pathology & laboratory medicine.

[66]  S. Nagata,et al.  Apoptotic nuclear morphological change without DNA fragmentation , 1999, Current Biology.

[67]  K. Roth,et al.  In situ immunodetection of activated caspase-3 in apoptotic neurons in the developing nervous system , 1998, Cell Death and Differentiation.

[68]  G. D. De Meyer,et al.  RNA synthesis and splicing interferes with DNA in situ end labeling techniques used to detect apoptosis. , 1998, The American journal of pathology.

[69]  E. Brambilla,et al.  TUNEL Apoptotic Cell Detection in Tissue Sections: Critical Evaluation and Improvement , 1998, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[70]  V. Fadok,et al.  Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. , 1998, The Journal of clinical investigation.

[71]  I. Darby,et al.  Cautionary note on the use of end‐labelling DNA fragments for detection of apoptosis , 1998, Pathology.

[72]  C. Reutelingsperger,et al.  Annexin V-affinity assay: a review on an apoptosis detection system based on phosphatidylserine exposure. , 1998, Cytometry.

[73]  M. Prevost,et al.  Strategies for phenotyping apoptotic peripheral human lymphocytes comparing ISNT, annexin-V and 7-AAD cytofluorometric staining methods. , 1997, Journal of immunological methods.

[74]  C. D. De Zeeuw,et al.  In situ detection of apoptosis during embryogenesis with annexin V: from whole mount to ultrastructure. , 1997, Cytometry.

[75]  J. Erenpreisa,et al.  Apoptotic cell nuclei favour aggregation and fluorescence quenching of DNA dyes , 1997, Histochemistry and Cell Biology.

[76]  Postmortem delay and temperature conditions affect the in situ end-labeling (ISEL) assay in brain tissue of mice. , 1997, Clinical neuropathology.

[77]  S. Muller,et al.  An ELISA for detection of apoptosis. , 1997, Nucleic acids research.

[78]  P. Hornsby,et al.  Presence of double-strand breaks with single-base 3' overhangs in cells undergoing apoptosis but not necrosis , 1996, The Journal of cell biology.

[79]  E. Brambilla,et al.  In situ apoptotic cell labeling by the TUNEL method: improvement and evaluation on cell preparations. , 1996, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[80]  J. Robb,et al.  Monoclonal antibody to single-stranded DNA is a specific and sensitive cellular marker of apoptosis. , 1996, Experimental cell research.

[81]  M. Vitale,et al.  Supravital exposure to propidium iodide identifies apoptotic cells in the absence of nucleosomal DNA fragmentation. , 1996, Cytometry.

[82]  B. Piqueras,et al.  Detection of apoptosis at the single-cell level by direct incorporation of fluorescein-dUTP in DNA strand breaks. , 1996, BioTechniques.

[83]  P. Olive,et al.  The comet assay: a comprehensive review. , 1995, Mutation research.

[84]  A. Wyllie,et al.  Apoptosis: A Basic Biological Phenomenon with Wide-ranging Implications in Tissue Kinetics , 1972, British Journal of Cancer.

[85]  J. Mitchison Cell Biology , 1964, Nature.