New insights into the mechanisms controlling neutrophil survival

Purpose of reviewNeutrophil survival is regulated by a complex convergence of different pathways. The present review analyzes these pathways and discusses how neutrophil survival is modulated during the course of inflammatory reactions. Recent findingsAlthough apoptosis appears to be the predominant cell death pathway in the neutrophil, recent data reveal that neutrophil survival is also regulated by a number of nonconventional pathways including NETosis, autophagic cell death, and other less characterized mechanisms. This supports an even more complex picture of the mechanisms involved in the regulation of neutrophil survival than previously thought. SummaryThe control of neutrophil survival is central to homoeostasis and resolution of inflammation. Cell death is usually discussed dichotomously in terms of apoptosis or necrosis. There are two main pathways responsible for the stimulation of apoptosis; a death receptor pathway triggered by Fas, tumor necrosis factor α, and tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) and a mitochondrial pathway stimulated by a number of stressors such as DNA damage, growth factor deprivation, and chemotherapy drugs. Nonconventional pathways of neutrophil death include NETosis and autophagic cell death as well as a number of poorly characterized mechanisms. Understanding the integrated pathways responsible for the control of neutrophil survival holds therapeutic promise in infectious and inflammatory diseases.

[1]  H. Simon,et al.  Viable neutrophils release mitochondrial DNA to form neutrophil extracellular traps , 2009, Cell Death and Differentiation.

[2]  G. Gores,et al.  Life and death by death receptors , 2009, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[3]  Z. Werb,et al.  Netting neutrophils in autoimmune small-vessel vasculitis , 2009, Nature Medicine.

[4]  G. Salvesen,et al.  Human Caspases: Activation, Specificity, and Regulation* , 2009, The Journal of Biological Chemistry.

[5]  S. de Jong,et al.  TRAIL receptor signalling and modulation: Are we on the right TRAIL? , 2009, Cancer treatment reviews.

[6]  F. Conceição-Silva,et al.  Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps , 2009, Proceedings of the National Academy of Sciences.

[7]  A. Kimchi,et al.  Life and death partners: apoptosis, autophagy and the cross-talk between them , 2009, Cell Death and Differentiation.

[8]  I. Megson,et al.  Macrophage phagocytosis of apoptotic neutrophils is critically regulated by the opposing actions of pro‐inflammatory and anti‐inflammatory agents: key role for TNF‐α , 2009, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[9]  K. Nadeau,et al.  Idiopathic neutropenia of childhood is associated with Fas/FasL expression. , 2008, Clinical immunology.

[10]  E. Morselli,et al.  Life, death and burial: multifaceted impact of autophagy. , 2008, Biochemical Society transactions.

[11]  E. Chilvers,et al.  Advances in neutrophil biology: clinical implications. , 2008, Chest.

[12]  H. Simon,et al.  Natural anti-Siglec autoantibodies mediate potential immunoregulatory mechanisms: implications for the clinical use of intravenous immunoglobulins (IVIg). , 2008, Autoimmunity reviews.

[13]  T. Kuijpers,et al.  Mitochondrial Membrane Potential in Human Neutrophils Is Maintained by Complex III Activity in the Absence of Supercomplex Organisation , 2008, PloS one.

[14]  F. Loison,et al.  Constitutive neutrophil apoptosis: Mechanisms and regulation , 2008, American journal of hematology.

[15]  Suzanne Cory,et al.  Bcl-2-regulated apoptosis: mechanism and therapeutic potential. , 2007, Current opinion in immunology.

[16]  Volker Brinkmann,et al.  Beneficial suicide: why neutrophils die to make NETs , 2007, Nature Reviews Microbiology.

[17]  You-Wen He,et al.  The antiapoptotic protein Mcl-1 is essential for the survival of neutrophils but not macrophages. , 2007, Blood.

[18]  R. Medzhitov,et al.  Innate immunity--cross-talk with adaptive immunity through pattern recognition receptors and cytokines. , 2007, Current opinion in immunology.

[19]  V. Wahn,et al.  Novel cell death program leads to neutrophil extracellular traps. , 2007, The Journal of cell biology.

[20]  K. Welte,et al.  Severe congenital neutropenia: inheritance and pathophysiology , 2007, Current opinion in hematology.

[21]  T. Kuijpers,et al.  Mitochondria in Neutrophil Apoptosis , 2006, International journal of hematology.

[22]  M. Cassatella.  On the production of TNF‐related apoptosis‐inducing ligand (TRAIL/Apo‐2L) by human neutrophils , 2006, Journal of leukocyte biology.

[23]  H. Simon,et al.  Sialic acid binding immunoglobulin‐like lectins may regulate innate immune responses by modulating the life span of granulocytes , 2006, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[24]  M. Hinds,et al.  Regulation of apoptosis: uncovering the binding determinants. , 2005, Current opinion in structural biology.

[25]  R A Knight,et al.  Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009 , 2005, Cell Death and Differentiation.

[26]  J. Takala,et al.  Siglec-9 transduces apoptotic and nonapoptotic death signals into neutrophils depending on the proinflammatory cytokine environment. , 2005, Blood.

[27]  G. Bren,et al.  Elimination of Senescent Neutrophils by TNF-Related Apoptosis-Inducing Ligand1 , 2005, The Journal of Immunology.

[28]  P. Allen,et al.  Inflammatory arthritis requires Foxo3a to prevent Fas ligand–induced neutrophil apoptosis , 2005, Nature Medicine.

[29]  David L. Vaux,et al.  IAPs, RINGs and ubiquitylation , 2005, Nature Reviews Molecular Cell Biology.

[30]  J. El Benna,et al.  Inhibition of Neutrophil Apoptosis by TLR Agonists in Whole Blood: Involvement of the Phosphoinositide 3-Kinase/Akt and NF-κB Signaling Pathways, Leading to Increased Levels of Mcl-1, A1, and Phosphorylated Bad , 2005, The Journal of Immunology.

[31]  D. Phelan,et al.  GENE EXPRESSION PROFILE OF INFLAMMATORY NEUTROPHILS: ALTERATIONS IN THE INHIBITORS OF APOPTOSIS PROTEINS DURING SPONTANEOUS AND DELAYED APOPTOSIS , 2004, Shock.

[32]  M. Fey,et al.  Inflammation-associated Cell Cycle–independent Block of Apoptosis by Survivin in Terminally Differentiated Neutrophils , 2004, The Journal of experimental medicine.

[33]  David A Hildeman,et al.  ×Phosphorylation of Bax Ser184 by Akt Regulates Its Activity and Apoptosis in Neutrophils* , 2004, Journal of Biological Chemistry.

[34]  S. Srinivasula,et al.  Functional characterization of mitochondria in neutrophils: a role restricted to apoptosis , 2004, Cell Death and Differentiation.

[35]  J. Tschopp,et al.  Induction of TNF Receptor I-Mediated Apoptosis via Two Sequential Signaling Complexes , 2003, Cell.

[36]  Andreas Villunger,et al.  Essential role for the BH3-only protein Bim but redundant roles for Bax, Bcl-2, and Bcl-w in the control of granulocyte survival. , 2003, Blood.

[37]  S. Calvano,et al.  Fas-Mediated Neutrophil Apoptosis and Associated A1 Protein Expression During Systemic Inflammation Are Regulated Independently of Both Tumor Necrosis Factor Receptors , 2003, Shock.

[38]  R. Moots,et al.  The Mitochondrial Network of Human Neutrophils: Role in Chemotaxis, Phagocytosis, Respiratory Burst Activation, and Commitment to Apoptosis 1 , 2003, The Journal of Immunology.

[39]  K. Ohta,et al.  Expression of the inhibitor of apoptosis (IAP) family members in human neutrophils: up-regulation of cIAP2 by granulocyte colony-stimulating factor and overexpression of cIAP2 in chronic neutrophilic leukemia. , 2003, Blood.

[40]  Limin Zheng,et al.  Mycobacterium tuberculosis Promotes Apoptosis in Human Neutrophils by Activating Caspase-3 and Altering Expression of Bax/Bcl-xL Via an Oxygen-Dependent Pathway1 , 2002, The Journal of Immunology.

[41]  S. Korsmeyer,et al.  The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. , 2000, Molecular cell.

[42]  P. Vogt,et al.  Cytokine-mediated Bax deficiency and consequent delayed neutrophil apoptosis: a general mechanism to accumulate effector cells in inflammation. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[43]  K. Nakayama,et al.  Accelerated Neutrophil Apoptosis in Mice Lacking A1-a, a Subtype of the bcl-2–related A1 Gene , 1998, The Journal of experimental medicine.

[44]  P. Cohen,et al.  Fas ligand (gld)‐ and Fas (lpr)‐deficient mice do not show alterations in the extravasation or apoptosis of inflammatory neutrophils , 1998, Journal of leukocyte biology.

[45]  P. Kiener,et al.  Differential expression of Fas (CD95) and Fas ligand on normal human phagocytes: implications for the regulation of apoptosis in neutrophils , 1996, The Journal of experimental medicine.

[46]  A. Kennedy,et al.  Neutrophil apoptosis and the resolution of infection , 2009, Immunologic research.

[47]  V. Duronio,et al.  Calcium pyrophosphate dihydrate crystal-induced inhibition of neutrophil apoptosis: involvement of Bcl-2 family members , 2009, Inflammation Research.

[48]  T. Kuijpers,et al.  Mitochondrial membrane potential in human neutrophils is maintained by complex III activity in the absence of supercomplex organisation , 2009 .

[49]  M. Fey,et al.  Neutrophil apoptosis mediated by nicotinic acid receptors (GPR109A) , 2008, Cell Death and Differentiation.

[50]  A. Scott,et al.  The inflammatory caspases: guardians against infections and sepsis , 2007, Cell Death and Differentiation.

[51]  A. Segal,et al.  How neutrophils kill microbes. , 2005, Annual review of immunology.

[52]  D. Green,et al.  Death receptors bind SHP-1 and block cytokine-induced anti-apoptotic signaling in neutrophils , 2002, Nature Medicine.

[53]  太郎 長谷川.  Expression of the inhibitor of apoptosis (IAP) family members in human neutrophils : up-regulation of cIAP2 by granulocyte colony-stimulating factor and overexpression of cIAP2 in chronic neutrophilic leukemia , 2002 .

[54]  J. A. Quayle,et al.  Mcl-1 expression in human neutrophils: regulation by cytokines and correlation with cell survival. , 1998, Blood.

[55]  Tumor necrosis factor (cid:1) induces a caspase-independent death pathway in human neutrophils , 2022 .