Apoptosis, inflammatory response and parasite load in skin of Leishmania (Leishmania) chagasi naturally infected dogs: A histomorphometric analysis

Veterinary Parasitology - Tập 189 Số 2-4 - Trang 162-170 - 2012
Bárbara Laurice Araújo Verçosa1, Mariano Domingo2, Helen L. Del Puerto1, Ivete Lopes de Mendonça3, A.C. Vasconcelos1
1Laboratory of Apoptosis, Department of General Pathology, Institute of Biological Sciences, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil.
2Laboratory of Leishmania Biology, Department of Parasitology, Institute of Biological Sciences, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
3Department of Veterinary Clinics and Surgery, Universidade Federal do Piauí, Teresina, Piauí, Brazil

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Afonso, 2008, Interactions with apoptotic but not necrotic neutrophils increase parasite burden in human macrophages infected with Leishmania amazonensis, J. Leukoc. Biol., 8, 389, 10.1189/jlb.0108018

Baneth, 2008, Canine leishmaniasis – new concepts and insights on an expanding zoonosis: part one, Trends Parasitol., 24, 324, 10.1016/j.pt.2008.04.001

Carmen, 2007, Suicide prevention: disruption of apoptotic pathways by protozoan parasites, Mol. Microbiol., 64, 904, 10.1111/j.1365-2958.2007.05714.x

Carrero, 2004, Type I interferon sensitizes lymphocytes to apoptosis and reduce resistances to Listeria infection, J. Exp. Med., 200, 535, 10.1084/jem.20040769

Cochran, 1957

Cohen, 2002, Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase, J. Exp. Med., 196, 135, 10.1084/jem.20012094

Conceição-Silva, 1998, The resolution of lesions induced by Leishmania major in mice requires a functional Fas (APO-1, CD95) pathway of cytotoxicity, Eur. J. Immunol., 28, 237, 10.1002/(SICI)1521-4141(199801)28:01<237::AID-IMMU237>3.0.CO;2-O

Das, 1999, Leishmania donovani infection of a susceptible host results in CD4+ T-cell apoptosis and decreased Th1 cytokine production, Scand. J. Immunol., 49, 307, 10.1046/j.1365-3083.1999.00486.x

Das, 2001, Hydrogen peroxide induces apoptosis-like death in Leishmania donovani promastigotes, J. Cell Sci., 114, 2461, 10.1242/jcs.114.13.2461

Deane, 1955, Leishmaniose visceral urbana (no cão e no homem) em Sobral, Ceará. O Hosp., 47, 75

Dos-Santos, 2004, Association between skin parasitism and granulomatous inflammatory pattern in canine visceral leishmaniasis, Parasitol. Res., 94, 84

Eda, 2004, Carbohydrate-mediated phagocytic recognition of early apoptotic cells undergoing transient capping of CD43 glycoprotein, J. Biol. Chem., 279, 5967, 10.1074/jbc.M310805200

Fadok, 1998, Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta PGE2, and PAF, J. Clin. Invest., 101, 890, 10.1172/JCI1112

Giunchetti, 2006, Relationship between canine visceral leishmaniasis and the Leishmania (Leishmania) chagasi burden in dermal inflammatory foci, J. Comp. Pathol., 135, 100, 10.1016/j.jcpa.2006.06.005

Gramiccia, 2005, The current status of zoonotic leishmaniasis and approaches to disease control, Int. J. Parasitol., 35, 1169, 10.1016/j.ijpara.2005.07.001

Huang, 1998, Mice defective in Fas are highly susceptible to Leishmania major infection despite elevated IL-12 synthesis, strong Th1 responses, and enhanced nitric oxide production, J. Immunol., 160, 4143, 10.4049/jimmunol.160.9.4143

Huynh, 2002, Phosphatidylserine-dependent ingestion of apoptotic cells promotes TGF-beta 1 secretion and the resolution of inflammation, J. Clin. Invest., 109, 41, 10.1172/JCI0211638

Kerr, 1993, Definition of apoptosis and overview of its incidence, 1

Knight, 2002, The archaeology of apoptosis, Cell Death Differ., 9, 1, 10.1038/sj.cdd.4400980

Krysko, 2006, Macrophages use different internalization mechanisms to clear apoptotic and necrotic cells, Cell Death Differ., 18, 781

Lanzaro, 1995, Genetic variability in phlebotomine sandflies: possible implications for leishmaniasis epidemiology, Parasitol. Today, 11, 151, 10.1016/0169-4758(95)80137-5

Lee, 2002, Programmed cell death in the unicellular protozoan parasite Leishmania, Cell Death Differ., 9, 53, 10.1038/sj.cdd.4400952

Lindoso, 2004, Apoptosis of Leishmania (Leishmania) chagasi amastigotes in hamsters infected with visceral leishmaniasis, Int. J. Parasitol., 34, 1, 10.1016/j.ijpara.2003.09.010

Luna, 1968

Maderna, 2003, Phagocytosis of apoptotic cells and the resolution of inflammation, Biochim. Biophys. Acta, 1639, 141, 10.1016/j.bbadis.2003.09.004

Mauricio, 2000, The strange case of Leishmania chagasi, Parasitol. Today, 16, 188, 10.1016/S0169-4758(00)01637-9

Mikel, 1994

Moreira, 1996, Heat shock induction of apoptosis in promastigotes of the unicellular organism Leishmania (Leishmania) amazonensis, J. Cell Physiol., 167, 305, 10.1002/(SICI)1097-4652(199605)167:2<305::AID-JCP15>3.0.CO;2-6

Moro, 2004, Determination of the minimal representative number of microscopic fields to quantify apoptosis in canine lymph nodes, Arq. Bras. Med. Vet. Zootech., 56, 408, 10.1590/S0102-09352004000300020

Peters, 2008, In vivo imaging revealed an essential role for neutrophils in leishmaniasis transmitted by sand flies, Science, 321, 970, 10.1126/science.1159194

Piarroux, 1993, Isolation and characterization of a repetitive DNA sequence from Leishmania infantum: development of s visceral leishmaniasis Polymerase Chain Reaction, Am. J. Trop. Med. Hyg., 49, 364, 10.4269/ajtmh.1993.49.364

Pozio, 1981, Leishmaniasis in Tuscany (Italy): VI. Canine leishmaniasis in the focus of Monte Argentario (Grosseto), Acta Trop., 38, 383

Reed, 1996, Diagnosis of leishmaniasis, Clin. Dermatol., 14, 471, 10.1016/0738-081X(96)00038-7

Reynolds, 1963, The use of lead citrate at high pH as an electron opaque stain in electron microscopy, J. Cell Biol., 17, 208, 10.1083/jcb.17.1.208

Ribeiro-Gomes, 2005, Macrophage interactions with neutrophils regulate Leishmania major infection, J. Immunol., 172, 454

Rousseau, 2001, In vivo involvement of polymorphonuclear neutrophils in Leishmania infantum infection, BMC Microbiol., 1

Savill, 2002, A blast from the past: clearance of apoptotic cells regulates immune responses, Nat. Rev. Immunol., 2, 965, 10.1038/nri957

Solano-Gallego, 2004, Histological and immunohistochemical study of clinically normal skin of Leishmania infantum-infected dogs, J. Comp. Pathol., 130, 7, 10.1016/S0021-9975(03)00063-X

Solano-Gallego, 2001, Prevalence of Leishmania infantum infection in dogs living in an area of canine leishmaniasis endemicity using PCR on several tissues and serology, J. Clin. Microbiol., 39, 560, 10.1128/JCM.39.2.560-563.2001

Tacchini-Cottier, 2000, An immunomodulatory function for neutrophils during the induction of a CD4_Th2 response in BALB/c mice infected with Leishmania major, J. Immunol., 165, 26, 10.4049/jimmunol.165.5.2628

Tafuri, 2004, An alternative immunohistochemical method for detecting Leishmania amastigotes in paraffin-embedded canine tissues, J. Immunol. Method, 292, 17, 10.1016/j.jim.2004.05.009

Van Zandbergen, 2006, Leishmania disease development depends on the presence of apoptotic promastigotes in the virulent inoculum, Proc. Natl. Acad. Sci., 103, 13837, 10.1073/pnas.0600843103

Van Zandbergen, 2004, Cutting edge: neutrophil granulocyte serves as a vector for Leishmania entry into macrophages, J. Immunol., 173, 6521, 10.4049/jimmunol.173.11.6521

Verçosa, 2008, Transmission potential, skin inflammatory response and parasitism of symptomatic and asymptomatic dogs with visceral leishmaniasis, BMC Vet. Res., 4, 1, 10.1186/1746-6148-4-45

Verçosa, 2011, Inflammatory response, parasite load and AgNOR expression in ear skin of symptomatic and asymptomatic Leishmania (Leishmania) chagasi infected dogs, J. Venom. Anim. Toxins Incl. Trop. Dis., 17, 308, 10.1590/S1678-91992011000300011

Wanderley, 2009, Cooperation between apoptotic and viable metacyclics enhances the pathogenesis of leishmaniasis, PLoS One, 4, 1, 10.1371/journal.pone.0005733

Watson, 1958, Staining of tissue sections for electron microscopy with heavy metals, J. Biophys. Biochem. Cytol., 4, 475, 10.1083/jcb.4.4.475

Weinrauch, 1999, The induction of apoptosis by bacterial pathogens, Annu. Rev. Microbiol., 53, 155, 10.1146/annurev.micro.53.1.155

Welburn, 1997, Control of 473 Trypanosoma brucei brucei infections in tse-tse, Glossina morsitans, Med. Vet. Entomol., 11, 286, 10.1111/j.1365-2915.1997.tb00408.x

Xavier, 2006, Comparison of paraffin-embedded skin biopsies from different anatomical regions as sampling methods for detecting Leishmania infection in dogs using histological, immunohistochemical and PCR methods, BMC Vet. Res., 2, 17, 10.1186/1746-6148-2-17