The impact of vector‐mediated neutrophil recruitment on cutaneous leishmaniasis

The dynamic process of pathogen transmission by the bite of an insect vector combines several biological processes that have undergone extensive co‐evolution. Whereas the host response to an insect bite is only occasionally confronted with the parasitic pathogens that competent vectors might transmit, the transmitted parasites will always be confronted with the acute, wound‐healing response that is initiated by the bite itself. Invariably, this response involves neutrophils. In the case of Leishmania, infection is initiated in the skin following the bite of an infected sand fly, suggesting that Leishmania must possess some means to survive their early encounter with recruited neutrophils at the bite site. Here, we review the literature regarding the impact of neutrophils on the outcome of infection with Leishmania, with special attention to the role of the sand fly bite.

[1]  S. Kamhawi,et al.  Vector Transmission of Leishmania Abrogates Vaccine-Induced Protective Immunity , 2009, PLoS pathogens.

[2]  G. Berton Faculty Opinions recommendation of Critical role of phospholipase Cgamma2 in integrin and Fc receptor-mediated neutrophil functions and the effector phase of autoimmune arthritis. , 2009 .

[3]  D. Frommhold,et al.  Critical role of phospholipase Cγ2 in integrin and Fc receptor-mediated neutrophil functions and the effector phase of autoimmune arthritis , 2009, The Journal of experimental medicine.

[4]  L. Ng,et al.  Migratory Dermal Dendritic Cells Act as Rapid Sensors of Protozoan Parasites , 2008, PLoS pathogens.

[5]  M. Fay,et al.  In Vivo Imaging Reveals an Essential Role for Neutrophils in Leishmaniasis Transmitted by Sand Flies , 2008, Science.

[6]  C. Brodskyn,et al.  Interactions with apoptotic but not with necrotic neutrophils increase parasite burden in human macrophages infected with Leishmania amazonensis , 2008, Journal of leukocyte biology.

[7]  W. Solbach,et al.  Neutrophil granulocytes as host cells and transport vehicles for intracellular pathogens: apoptosis as infection-promoting factor. , 2008, Immunobiology.

[8]  N. Setterblad,et al.  Mycobacterium bovis BCG‐infected neutrophils and dendritic cells cooperate to induce specific T cell responses in humans and mice , 2008, European journal of immunology.

[9]  F. Tacchini-Cottier,et al.  Neutrophils Contribute to Development of a Protective Immune Response during Onset of Infection with Leishmania donovani , 2007, Infection and Immunity.

[10]  L. Allen,et al.  To activate or not to activate: distinct strategies used by Helicobacter pylori and Francisella tularensis to modulate the NADPH oxidase and survive in human neutrophils , 2007, Immunological reviews.

[11]  W. Nauseef How human neutrophils kill and degrade microbes: an integrated view , 2007, Immunological reviews.

[12]  M. S. Alexandre-Moreira,et al.  Neutrophils Activate Macrophages for Intracellular Killing of Leishmania major through Recruitment of TLR4 by Neutrophil Elastase1 , 2007, The Journal of Immunology.

[13]  V. García,et al.  Neutrophil elastase converts human immature dendritic cells into transforming growth factor-beta1-secreting cells and reduces allostimulatory ability. , 2007, The American journal of pathology.

[14]  F. Tacchini-Cottier,et al.  Leishmania major induces distinct neutrophil phenotypes in mice that are resistant or susceptible to infection , 2007, Journal of leukocyte biology.

[15]  Qilong Xu,et al.  Increasing the Recruitment of Neutrophils to the Site of Infection Dramatically Attenuates Borrelia burgdorferi Infectivity1 , 2007, The Journal of Immunology.

[16]  W. Solbach,et al.  Apoptosis driven infection , 2007, Autoimmunity.

[17]  Michael Loran Dustin,et al.  Innate Response to Focal Necrotic Injury Inside the Blood-Brain Barrier1 , 2006, The Journal of Immunology.

[18]  Amnon Peled,et al.  A streptococcal protease that degrades CXC chemokines and impairs bacterial clearance from infected tissues , 2006, The EMBO journal.

[19]  A. Lacy-Hulbert,et al.  Requirements for Apoptotic Cell Contact in Regulation of Macrophage Responses1 , 2006, The Journal of Immunology.

[20]  A. Roberts,et al.  Granulocyte colony-stimulating factor and neutrophils—forgotten mediators of inflammatory disease , 2006, Nature Clinical Practice Rheumatology.

[21]  R. Levy,et al.  Impaired neutrophil functions in the pathogenesis of an outbreak of recurrent furunculosis caused by methicillin-resistant Staphylococcus aureus among mentally retarded adults. , 2006, Microbes and infection.

[22]  J. Gluckman,et al.  Polymorphonuclear neutrophils deliver activation signals and antigenic molecules to dendritic cells: a new link between leukocytes upstream of T lymphocytes , 2006, Journal of leukocyte biology.

[23]  R. Terkeltaub,et al.  The inflammatory process of gout and its treatment , 2006, Arthritis research & therapy.

[24]  F. Ribeiro-Gomes,et al.  Neutrophils, apoptosis and phagocytic clearance: an innate sequence of cellular responses regulating intramacrophagic parasite infections , 2006, Parasitology.

[25]  E. Fikrig,et al.  Mechanisms of evasion of neutrophil killing by Anaplasma phagocytophilum , 2006, Current opinion in hematology.

[26]  J. C. Miranda,et al.  Saliva from Lutzomyia longipalpis Induces CC Chemokine Ligand 2/Monocyte Chemoattractant Protein-1 Expression and Macrophage Recruitment1 , 2005, The Journal of Immunology.

[27]  P. Bozza,et al.  Turnover of neutrophils mediated by Fas ligand drives Leishmania major infection. , 2005, The Journal of infectious diseases.

[28]  Lin Chen,et al.  The involvement of neutrophils in the resistance to Leishmania major infection in susceptible but not in resistant mice. , 2005, Parasitology international.

[29]  A. Gebert,et al.  Cutting Edge: Neutrophil Granulocyte Serves as a Vector for Leishmania Entry into Macrophages1 , 2004, The Journal of Immunology.

[30]  F. Ribeiro-Gomes,et al.  Macrophage Interactions with Neutrophils Regulate Leishmania major Infection1 , 2004, The Journal of Immunology.

[31]  T. Curiel,et al.  Cross-Talk in the Innate Immune System: Neutrophils Instruct Recruitment and Activation of Dendritic Cells during Microbial Infection 1 , 2003, The Journal of Immunology.

[32]  M. Drayson,et al.  Dendritic cell uptake of human apoptotic and necrotic neutrophils inhibits CD40, CD80, and CD86 expression and reduces allogeneic T cell responses: relevance to systemic vasculitis. , 2003, Arthritis and rheumatism.

[33]  W. Solbach,et al.  Neutrophil granulocytes--Trojan horses for Leishmania major and other intracellular microbes? , 2003, Trends in microbiology.

[34]  Helmut Laufs,et al.  Inhibition of the Spontaneous Apoptosis of Neutrophil Granulocytes by the Intracellular Parasite Leishmania major1 , 2002, The Journal of Immunology.

[35]  S. Shapiro,et al.  Neutrophil elastase targets virulence factors of enterobacteria , 2002, Nature.

[36]  J. Lamb,et al.  Inhibitory Effects of Apoptotic Cell Ingestion upon Endotoxin-Driven Myeloid Dendritic Cell Maturation1 , 2002, The Journal of Immunology.

[37]  H. Laufs,et al.  Intracellular Survival of Leishmania major in Neutrophil Granulocytes after Uptake in the Absence of Heat-Labile Serum Factors , 2002, Infection and Immunity.

[38]  Y. Belkaid,et al.  An Immunomodulatory Function for Neutrophils During the Induction of a CD4+ Th2 Response in BALB/c Mice Infected with Leishmania major1 , 2000, The Journal of Immunology.

[39]  Y. Belkaid,et al.  A Natural Model of Leishmania major Infection Reveals a Prolonged “Silent” Phase of Parasite Amplification in the Skin Before the Onset of Lesion Formation and Immunity , 2000, The Journal of Immunology.

[40]  R. Steinman,et al.  The Induction of Tolerance by Dendritic Cells That Have Captured Apoptotic Cells , 2000, The Journal of experimental medicine.

[41]  H. Castro-Faria-Neto,et al.  Uptake of apoptotic cells drives the growth of a pathogenic trypanosome in macrophages , 2000, Nature.

[42]  E. Bevilacqua,et al.  The role of polymorphonuclear leukocytes in the resistance to cutaneous Leishmaniasis. , 1998, Immunology letters.

[43]  H. Goto,et al.  The role of complement in the acute inflammatory process in the skin and in host–parasite interaction in hamsters inoculated with Leishmania (Leishmania) chagasi , 1996, International journal of experimental pathology.

[44]  M. Goebeler,et al.  Resistance of mice to experimental leishmaniasis is associated with more rapid appearance of mature macrophages in vitro and in vivo. , 1993, Journal of immunology.

[45]  W. Beil,et al.  Differences in the onset of the inflammatory response to cutaneous leishmaniasis in resistant and susceptible mice , 1992, Journal of leukocyte biology.

[46]  I. A. Al Mofleh,et al.  Effect of Leishmania major on human polymorphonuclear leucocyte function in vitro. , 1990, Journal of medical microbiology.

[47]  I. Sarov,et al.  Leishmania major: inhibition of the chemiluminescent response of human polymorphonuclear leukocytes by promastigotes and their excreted factors , 1990, Parasite immunology.

[48]  W. de Souza,et al.  Fine structure and cytochemistry of the interaction between Leishmania mexicana amazonensis and rat neutrophils and eosinophils. , 1987, Journal of submicroscopic cytology.

[49]  R. Pearson,et al.  Early histopathology of experimental infection with Leishmania donovani in hamsters. , 1987, The Journal of parasitology.

[50]  A. Remaley,et al.  Leishmanial phosphatase blocks neutrophil O-2 production. , 1984, The Journal of biological chemistry.

[51]  M. J. Soares,et al.  Tissue eosinophilia and Leishmania mexicana mexicana eosinophil interactions in murine cutaneous leishmaniasis , 1984, Parasite immunology.

[52]  R. Pearson,et al.  Phagocytosis and killing of the protozoan Leishmania donovani by human polymorphonuclear leukocytes. , 1981, Journal of immunology.

[53]  K. Chang Leishmanicidal mechanisms of human polymorphonuclear phagocytes. , 1981, The American journal of tropical medicine and hygiene.

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

[55]  S. Reed,et al.  Immunopathology of experimental cutaneous leishmaniasis. , 1984, The American journal of pathology.