Piecemeal degranulation in human eosinophils: a distinct secretion mechanism underlying inflammatory responses.

Secretion is a fundamental cell process underlying different physiological and pathological events. In cells from the human immune system such as eosinophils, secretion of mediators generally occurs by means of piecemeal degranulation, an unconventional secretory pathway characterized by vesicular transport of small packets of materials from the cytoplasmic secretory granules to the cell surface. During piecemeal degranulation in eosinophils, a distinct transport vesicle system, which includes large, pleiomorphic vesiculo-tubular carriers is mobilized and enables regulated release of granule-stored proteins such as cytokines and major basic protein. Piecemeal degranulation underlies distinct functions of eosinophils as effector and immunoregulatory cells. This review focuses on the structural and functional advances that have been made over the last years concerning the intracellular trafficking and secretion of eosinophil proteins by piecemeal degranulation during inflammatory responses.

[1]  P. Paré,et al.  Localization of DNA and RNA in Eosinophil Secretory Granules , 2009, International Archives of Allergy and Immunology.

[2]  M. Armengot,et al.  Eosinophil Degranulation Patterns in Nasal Polyposis: An Ultrastructural Study , 2009, American journal of rhinology & allergy.

[3]  A. Dvorak,et al.  Vesicle-mediated secretion of human eosinophil granule-derived major basic protein (MBP) , 2009, Laboratory Investigation.

[4]  P. Weller,et al.  Human eosinophils constitutively express multiple Th1, Th2, and immunoregulatory cytokines that are secreted rapidly and differentially , 2008, Journal of leukocyte biology.

[5]  Xiaobing Chen,et al.  Life Inside a Thin Section: Tomography , 2008, The Journal of Neuroscience.

[6]  A. Dvorak,et al.  Electron tomography and immunonanogold electron microscopy for investigating intracellular trafficking and secretion in human eosinophils , 2008, Journal of cellular and molecular medicine.

[7]  A. Dvorak,et al.  Mechanisms of eosinophil secretion: large vesiculotubular carriers mediate transport and release of granule‐derived cytokines and other proteins , 2008, Journal of leukocyte biology.

[8]  Byung-Ho Kang,et al.  Update on Electron Tomography Analysis of Plant Golgi Stacks Nanoscale Architecture of Endoplasmic Reticulum Export Sites and of Golgi Membranes as Determined by Electron Tomography 1 , 2008 .

[9]  S. Ackerman,et al.  Mechanisms of eosinophilia in the pathogenesis of hypereosinophilic disorders. , 2007, Immunology and allergy clinics of North America.

[10]  James J. Lee,et al.  Eosinophils: singularly destructive effector cells or purveyors of immunoregulation? , 2007, The Journal of allergy and clinical immunology.

[11]  Q. Hamid,et al.  Images in allergy and immunology: role of eosinophils in airway remodeling. , 2007, The Journal of allergy and clinical immunology.

[12]  S. Phipps,et al.  Eosinophil trafficking in allergy and asthma. , 2007, The Journal of allergy and clinical immunology.

[13]  C. Lloyd,et al.  Eosinophils in the pathogenesis of allergic airways disease , 2007, Cellular and Molecular Life Sciences.

[14]  M. Saeftel,et al.  Lack of Eosinophil Peroxidase or Major Basic Protein Impairs Defense against Murine Filarial Infection , 2006, Infection and Immunity.

[15]  R. Moqbel,et al.  Differential Secretion of Cytokines , 2006, Science's STKE.

[16]  A. Dvorak,et al.  Cytokine receptor-mediated trafficking of preformed IL-4 in eosinophils identifies an innate immune mechanism of cytokine secretion. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[17]  R. Pepperkok,et al.  Biogenesis of tubular ER-to-Golgi transport intermediates. , 2005, Molecular biology of the cell.

[18]  A. Dvorak,et al.  Human Eosinophils Secrete Preformed, Granule‐Stored Interleukin‐4 Through Distinct Vesicular Compartments , 2005, Traffic.

[19]  A. Dvorak,et al.  Intragranular Vesiculotubular Compartments are Involved in Piecemeal Degranulation by Activated Human Eosinophils , 2005, Traffic.

[20]  A. Luini,et al.  Large pleiomorphic traffic intermediates in the secretory pathway. , 2005, Current opinion in cell biology.

[21]  P. Watson,et al.  ER-to-Golgi transport: form and formation of vesicular and tubular carriers. , 2005, Biochimica et biophysica acta.

[22]  A. Dvorak Ultrastructure of Mast Cells and Basophils , 2005 .

[23]  D. Adamko,et al.  The rise of the phoenix: the expanding role of the eosinophil in health and disease , 2005, Allergy.

[24]  A. Ieni,et al.  Degranulation Patterns of Eosinophils in Advanced Gastric Carcinoma: An Electron Microscopic Study , 2005, Ultrastructural pathology.

[25]  A. Dvorak Piecemeal degranulation of basophils and mast cells is effected by vesicular transport of stored secretory granule contents. , 2005, Chemical immunology and allergy.

[26]  J. Erjefält,et al.  Eosinophil degranulation status in allergic rhinitis: observations before and during seasonal allergen exposure , 2004, European Respiratory Journal.

[27]  A. Luini,et al.  Secretory traffic triggers the formation of tubular continuities across Golgi sub-compartments , 2004, Nature Cell Biology.

[28]  F. Levi-Schaffer,et al.  Eosinophils: ‘new’ roles for ‘old’ cells , 2004, Allergy.

[29]  M. Mathan,et al.  Acute dehydrating disease caused by Vibrio cholerae serogroups O1 and O139 induce increases in innate cells and inflammatory mediators at the mucosal surface of the gut , 2003, Gut.

[30]  E. Crivellato,et al.  Piecemeal degranulation as a general secretory mechanism? , 2003, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[31]  T. Makino,et al.  Localization and content of nerve growth factor in peripheral blood eosinophils of atopic dermatitis patients , 2003, Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology.

[32]  A. Bjartell,et al.  Expression and Production of the CXC Chemokine Growth-Related Oncogene-α by Human Eosinophils1 , 2003, The Journal of Immunology.

[33]  I. Ghiran,et al.  EliCell assay for the detection of released cytokines from eosinophils. , 2003, Journal of immunological methods.

[34]  R. Moqbel,et al.  Understanding exocytosis in immune and inflammatory cells: the molecular basis of mediator secretion. , 2003, The Journal of allergy and clinical immunology.

[35]  F. Qadri,et al.  Persistence of Mucosal Mast Cells and Eosinophils in Shigella-Infected Children , 2003, Infection and Immunity.

[36]  J. Malm,et al.  Expression of the neutrophil‐activating CXC chemokine ENA‐78/CXCL5 by human eosinophils , 2003, Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology.

[37]  Thorsten Lang,et al.  Membrane fusion. , 2002, Current opinion in cell biology.

[38]  H. Geuze,et al.  MHC Class II Compartments in Human Dendritic Cells Undergo Profound Structural Changes Upon Activation , 2002, Traffic.

[39]  C. Ritzenthaler,et al.  Brefeldin A: Deciphering an Enigmatic Inhibitor of Secretion , 2002, Plant Physiology.

[40]  Paige Lacy,et al.  Human eosinophils express and release IL‐13 following CD28‐dependent activation , 2002, Journal of leukocyte biology.

[41]  G. Downey,et al.  Translocation of the tetraspanin CD63 in association with human eosinophil mediator release. , 2002, Blood.

[42]  Paige Lacy,et al.  Expression of eosinophil target SNAREs as potential cognate receptors for vesicle-associated membrane protein-2 in exocytosis. , 2002, The Journal of allergy and clinical immunology.

[43]  J. Erjefält,et al.  Degranulation patterns of eosinophil granulocytes as determinants of eosinophil driven disease , 2001, Thorax.

[44]  L. J. Woods,et al.  Cutting Edge: Eotaxin Elicits Rapid Vesicular Transport-Mediated Release of Preformed IL-4 from Human Eosinophils1 , 2001, The Journal of Immunology.

[45]  Paige Lacy,et al.  Fusion protein vesicle-associated membrane protein 2 is implicated in IFN-gamma-induced piecemeal degranulation in human eosinophils from atopic individuals. , 2001, The Journal of allergy and clinical immunology.

[46]  F. Levi-Schaffer,et al.  Human peripheral blood eosinophils express stem cell factor. , 2001, Blood.

[47]  P. Venge,et al.  Piecemeal degranulation of peripheral blood eosinophils: a study of allergic subjects during and out of the pollen season. , 2000, American journal of respiratory cell and molecular biology.

[48]  A. Dvorak,et al.  Ultrastructural analysis of human eosinophils. , 2000, Chemical immunology.

[49]  J. Erjefält,et al.  New aspects of degranulation and fates of airway mucosal eosinophils. , 2000, American journal of respiratory and critical care medicine.

[50]  G. Gleich Mechanisms of eosinophil-associated inflammation. , 2000, The Journal of allergy and clinical immunology.

[51]  Paige Lacy,et al.  Eosinophil cytokines. , 2000, Chemical immunology.

[52]  Paige Lacy,et al.  Rapid mobilization of intracellularly stored RANTES in response to interferon-gamma in human eosinophils. , 1999, Blood.

[53]  Kazuhiko Yamamoto,et al.  Intracellular localization and release of eotaxin from normal eosinophils , 1998, FEBS letters.

[54]  P. Desreumaux,et al.  Similar IL-5, IL-3, and GM-CSF syntheses by eosinophils in the jejunal mucosa of patients with celiac disease and dermatitis herpetiformis. , 1998, Clinical immunology and immunopathology.

[55]  A. Dvorak A role for vesicles in human basophil secretion , 1998, Cell and Tissue Research.

[56]  F. Levi-Schaffer,et al.  Intracellular localization of interleukin-6 in eosinophils from atopic asthmatics and effects of interferon gamma. , 1998, Blood.

[57]  N. Debili,et al.  Multivesicular Bodies Are an Intermediate Stage in the Formation of Platelet α-Granules , 1998 .

[58]  N. Debili,et al.  Multivesicular bodies are an intermediate stage in the formation of platelet alpha-granules. , 1998, Blood.

[59]  T. Horiuchi,et al.  Expression of vascular endothelial growth factor by human eosinophils: upregulation by granulocyte macrophage colony-stimulating factor and interleukin-5. , 1997, American journal of respiratory cell and molecular biology.

[60]  G. Gleich,et al.  Dermal eosinophils in atopic dermatitis undergo cytolytic degeneration. , 1997, The Journal of allergy and clinical immunology.

[61]  T. H. van der Kwast,et al.  Immunolocalization of interleukin-4 in eosinophils in the bronchial mucosa of atopic asthmatics. , 1996, American journal of respiratory cell and molecular biology.

[62]  J. Calafat,et al.  Subcellular localization of transforming growth factor-alpha in human eosinophil granulocytes. , 1996, Blood.

[63]  D. Wong,et al.  Human eosinophils elaborate the lymphocyte chemoattractants. IL-16 (lymphocyte chemoattractant factor) and RANTES. , 1996, Journal of immunology.

[64]  S. Durham,et al.  Human eosinophils express messenger RNA encoding RANTES and store and release biologically active RANTES protein , 1996, European journal of immunology.

[65]  T. H. van der Kwast,et al.  Ultrastructural immunogold localization of interleukin 5 to the crystalloid core compartment of eosinophil secondary granules in patients with atopic asthma. , 1996, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[66]  F. Levi-Schaffer,et al.  Identification of interleukin-2 in human peripheral blood eosinophils. , 1996, Immunology.

[67]  S. Durham,et al.  Identification of messenger RNA for IL-4 in human eosinophils with granule localization and release of the translated product. , 1995, Journal of immunology.

[68]  F. Levi-Schaffer,et al.  Association of granulocyte-macrophage colony-stimulating factor with the crystalloid granules of human eosinophils. , 1995, Blood.

[69]  J. Tavernier,et al.  Interleukin 5 synthesis by eosinophils: association with granules and immunoglobulin-dependent secretion , 1994, The Journal of experimental medicine.

[70]  A. Dvorak,et al.  Vesicular transport of peroxidase in human eosinophilic myelocytes , 1994, Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology.

[71]  T. Fujisawa,et al.  Interferon-gamma induces interleukin-3 release from peripheral blood eosinophils. , 1994, International archives of allergy and immunology.

[72]  S. Galli,et al.  Ultrastructural immunogold localization of tumor necrosis factor-alpha to the matrix compartment of eosinophil secondary granules in patients with idiopathic hypereosinophilic syndrome. , 1993, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[73]  D. Jones The eosinophil. , 1993, Journal of comparative pathology.

[74]  G. Firestein,et al.  Eosinophils express interleukin 5 and granulocyte macrophage-colony-stimulating factor mRNA at sites of allergic inflammation in asthmatics. , 1992, The Journal of clinical investigation.

[75]  A. Dvorak,et al.  Mature eosinophils stimulated to develop in human-cord blood mononuclear cell cultures supplemented with recombinant human interleukin-5. II. Vesicular transport of specific granule matrix peroxidase, a mechanism for effecting piecemeal degranulation. , 1992, The American journal of pathology.

[76]  A. Dvorak Basophils and mast cells: piecemeal degranulation in situ and ex vivo: a possible mechanism for cytokine-induced function in disease. , 1992, Immunology series.

[77]  A. Dvorak,et al.  Mature eosinophils stimulated to develop in human cord blood mononuclear cell cultures supplemented with recombinant human interleukin-5. Part I. Piecemeal degranulation of specific granules and distribution of Charcot-Leyden crystal protein. , 1991, The American journal of pathology.

[78]  R. Todd,et al.  Human eosinophils express transforming growth factor alpha , 1990, The Journal of experimental medicine.

[79]  A. Dvorak,et al.  Ultrastructural localization of Charcot-Leyden crystal protein (lysophospholipase) and peroxidase in macrophages, eosinophils, and extracellular matrix of the skin in the hypereosinophilic syndrome. , 1990, Laboratory investigation; a journal of technical methods and pathology.

[80]  D. M. Dvorak Human Mast Cells , 1989, Advances in Anatomy Embryology and Cell Biology.

[81]  A. Capron,et al.  Eosinophilic gastroenteritis: ultrastructural evidence for a selective release of eosinophil major basic protein. , 1988, Clinical and experimental immunology.

[82]  G. Gleich,et al.  DEPOSITS OF EOSINOPHIL GRANULE PROTEINS IN CARDIAC TISSUES OF PATIENTS WITH EOSINOPHILIC ENDOMYOCARDIAL DISEASE , 1987, The Lancet.

[83]  I. Olsson,et al.  Localization of eosinophil cationic protein, major basic protein, and eosinophil peroxidase in human eosinophils by immunoelectron microscopic technique. , 1986, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[84]  Moses Rodriguez,et al.  Localization of human eosinophil granule major basic protein, eosinophil cationic protein, and eosinophil-derived neurotoxin by immunoelectron microscopy. , 1986, Laboratory investigation; a journal of technical methods and pathology.

[85]  A. Dvorak,et al.  Crohn's disease: transmission electron microscopic studies. II. Immunologic inflammatory response. Alterations of mast cells, basophils, eosinophils, and the microvasculature. , 1980, Human pathology.

[86]  A. Dvorak Ultrastructural evidence for release of major basic protein-containing crystalline cores of eosinophil granules in vivo: cytotoxic potential in Crohn's disease. , 1980, Journal of immunology.

[87]  D. Loegering,et al.  Localization of the guinea pig eosinophil major basic protein to the core of the granule , 1978, The Journal of cell biology.

[88]  S. Martínez-Cairo,et al.  [Biology of eosinophils]. , 1978, La Prensa medica mexicana.

[89]  D. Loegering,et al.  IDENTIFICATION OF A MAJOR BASIC PROTEIN IN GUINEA PIG EOSINOPHIL GRANULES , 1973, The Journal of experimental medicine.