Entamoeba histolytica: immunohistochemical study of hepatic amoebiasis in mouse. Neutrophils and nitric oxide as possible factors of resistance

Jarillo-Luna, Rosa Adriana; Campos-Rodrı́guez, Rafael; Tsutsumi, Vı́ctor

doi:10.1016/s0014-4894(02)00021-8

Cited by 48 publications

(64 citation statements)

References 85 publications

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“…Third, IFN-␥ and functional NKT cells are required to mediate primary resistance in female mice. In previous studies of mice the workers used cultured E. histolytica trophozoites that had been passaged through livers of hamsters or SCID mice (17,18,26,28). However, a strain adapted to immunocompetent mice was not established, and gender differences were not addressed.…”

Section: Discussionmentioning

confidence: 99%

Sexual Dimorphism in the Control of Amebic Liver Abscess in a Mouse Model of Disease

Lotter¹,

Jacobs

Gaworski

et al. 2006

Infect Immun

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Amebic liver abscess (ALA) is the most common extraintestinal manifestation of human infection by the enteric protozoan parasite Entamoeba histolytica. In contrast to intestinal infection, ALA greatly predominates in males but is rare in females. Since humans are the only relevant host for E. histolytica, experimental studies concerning this sexual dimorphism have been hampered by the lack of a suitable animal model. By serial liver passage of cultured E. histolytica trophozoites in gerbils and mice, we generated amebae which reproducibly induce ALA in C57BL/6 mice. Interestingly, all animals developed ALA, but the time courses of abscess formation differed significantly between the genders. Female mice were able to clear the infection within 3 days, whereas in male mice the parasite could be recovered for at least 14 days. Accordingly, male mice showed a prolonged time of recovery from ALA. Immunohistology of abscesses revealed that polymorphonuclear leukocytes and macrophages were the dominant infiltrates, but in addition, ␥,␦-T cells, NK cells, and natural killer T (NKT) cells were also present at early times during abscess development, whereas conventional ␣,␤-T cells appeared later, when female mice had already cleared the parasite. Interestingly, male and female mice differed in early cytokine production in response to ameba infection. Enzyme-linked immunospot assays performed with spleen cells of infected animals revealed significantly higher numbers of interleukin-4-producing cells in male mice but significantly higher numbers of gamma interferon (IFN-␥)-producing cells in female mice. Early IFN-␥ production and the presence of functional NKT cells were found to be important for the control of hepatic amebiasis as application of an IFN-␥-neutralizing monoclonal antibody or the use of NKT knockout mice (V␣14iNKT, J␣ 18؊/؊ ) dramatically increased the size of ALA in female mice. In addition, E. histolytica trophozoites could be reisolated from liver abscesses of J␣18 ؊/؊ mice on day 7 postinfection, when wild-type mice had already cleared the parasite. These data suggest that the sexual dimorphism in the control of ALA is due to gender-specific differences in early cytokine production mediated at least in part by NKT cells in response to E. histolytica infection of the liver.Entamoeba histolytica, the causative agent of human amebiasis, is endemic in most tropical and subtropical countries and is considered to be responsible for tens of millions of cases of dysentery and liver abscesses each year (32, 33). Following fecal-oral transmission, the parasite colonizes the large bowel, where it multiplies and may persist for months or even years as an asymptomatic luminal gut infection (3). Only in about 10% of infected individuals does the parasite penetrate the intestinal mucosa and induce colitis or disseminate to other organs, and it most commonly disseminates to the liver, where it induces abscess formation (13). At present, the factors that trigger ameba invasion are largely unknown.Another unresolved enig...

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Section: Discussionmentioning

confidence: 99%

Sexual Dimorphism in the Control of Amebic Liver Abscess in a Mouse Model of Disease

Lotter¹,

Jacobs

Gaworski

et al. 2006

Infect Immun

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“…Although 0.5 mM SNAP showed toxicity to the ciliates, the level of NO generated was still higher than physiological ranges. NO produced by activated phagocytes expressing iNOS has been shown to function as a cytotoxic or cytostatic molecule and to inhibit the growth of pathogenic protozoa in mammals (Lin & Chadee 1992, Oswald et al 1994, Romao et al 1999, Jarillo-Luna et al 2002 and fish (Saeij et al 2000, Scharsack et al 2003a. It has been reported that exogenous NO released from the NO donors kill Trypanosoma cruzi (Vespa et al 1994, Petray et al 1995, Gobert et al 1998 and Plasmodium falciparum (Rockett et al 1991, Balmer et al 2000 in a dose-and time-dependent fashion.…”

Section: Discussionmentioning

confidence: 99%

“…Intracellular parasites such as Leishmania (Liew et al 1990) and extracellular parasites such as Entamoeba histolytica (Jarillo-Luna et al 2002) or Giardia lamblia (Eckmann et al 2000) can be killed or controlled by NO. However, Trypanosoma cruzi (Denicola et al 1993) and Brugia malayi (Thomas et al 1997) have been shown to be more susceptible to peroxynitrite than NO.…”

Section: Introductionmentioning

confidence: 99%

Comparison of toxic effects of nitric oxide and peroxynitrite on Uronema marinum (Ciliata: Scuticociliatida)

Lee¹,

Kim²,

Kwon³

et al. 2004

Dis. Aquat. Org.

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To discover the effects of nitric oxide (NO) and peroxynitrite on Uronema marinum (a ciliate responsible for systemic scuticociliatosis in cultured olive flounder Paralichthys olivaceus), the dose-dependent inhibitory effect of NO donors, S-nitroso-N-acetylpenicillamine (SNAP) and 3-morpholinosydnonimine (SIN-1) on the proliferation and survival of U. marinum was investigated. The inhibitory effects of exogenous superoxide dismutase (SOD) and catalase on the toxicity of SIN-1 were also investigated. After 24 h of incubation in the presence of 0.2 mM SNAP, the number of ciliates was not statistically different from that of the controls, whereas incubation in the presence of 0.5 mM SNAP reduced the number of parasites significantly to 59.1% of controls. Concentrations of SNAP higher than 0.5 mM resulted in greater reductions in the number of ciliates, but levels of generated NO far exceeded physiological ranges. The number of viable ciliates incubated for 24 h with 0.2 mM SIN-1 was reduced significantly to 25.0%, and all ciliates were killed by incubation in concentrations above 0.5 mM SIN-1. Although SOD decreased the toxic effect of SIN-1 on U. marinum, protection was not complete and did not improve after increasing the SOD concentration from 50 to 400 U ml -1 . Addition of catalase ranging from 500 to 10 000 U ml -1 completely protected U. marinum from SIN-1 toxicity. Ciliates exposed to catalase alone or catalase plus SIN-1 showed significantly higher and dose-dependent proliferation rates compared to controls. Addition of haemoglobin, ranging from 0.5 to 2.0 mg ml -1 , also protected U. marinum from SIN-1 toxicity, and increased the proliferation rate dose-dependently. In conclusion, resistance of U. marinum to oxidative and nitrative stress may allow this pathogen to withstand the NO-and oxygen-radical-dependent killing mechanisms of phagocytic cells. KEY WORDS: Uronema marinum · Scuticociliatosis · Nitric oxide · Peroxynitrite · CytotoxicityResale or republication not permitted without written consent of the publisher

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“…However, another study reported that NK cells activated by lipopeptidophosphoglicane from E. histolytica reduce the size of AHA (Lotter et al, 2009). Moreover, eosinophils and mast cells are also implicated in the cellular response and have been found to be involved in the reduction of amebic damage in various in vivo models (Houpt, 2002;Jarillo-Luna, 2002;López-Osuna et al, 1997. By using histochemical techniques in human intestinal tissue with FAC, eosinophils were stained with eritrosine B 1.5% (Benítez et al, 1987) and mast cells with toluidine blue 0.7% (Enerback, 1986;VenturaJuárez et al, 1990).…”

Section: Role Of the Cellular Immune Responsementioning

confidence: 99%

Fulminant Amoebic Colitis: Role of the Innate and Adaptive Immune Responses

Ventura‐Juárez¹,

Rosario²,

Martin-H³

et al. 2012

Colitis

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Entamoeba histolytica: immunohistochemical study of hepatic amoebiasis in mouse. Neutrophils and nitric oxide as possible factors of resistance

Cited by 48 publications

References 85 publications

Sexual Dimorphism in the Control of Amebic Liver Abscess in a Mouse Model of Disease

Sexual Dimorphism in the Control of Amebic Liver Abscess in a Mouse Model of Disease

Comparison of toxic effects of nitric oxide and peroxynitrite on Uronema marinum (Ciliata: Scuticociliatida)

Fulminant Amoebic Colitis: Role of the Innate and Adaptive Immune Responses

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