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. 2005 Jul;73(7):4155-60.
doi: 10.1128/IAI.73.7.4155-4160.2005.

Trichomonas vaginalis-induced epithelial monolayer disruption and human immunodeficiency virus type 1 (HIV-1) replication: implications for the sexual transmission of HIV-1

Patricia C Guenthner  1 , W Evan Secor, Charlene S Dezzutti
Affiliations

Trichomonas vaginalis-induced epithelial monolayer disruption and human immunodeficiency virus type 1 (HIV-1) replication: implications for the sexual transmission of HIV-1

Patricia C Guenthner et al. Infect Immun. 2005 Jul.

Abstract

The objective of this study was to evaluate potential mechanisms of Trichomonas vaginalis involvement in human immunodeficiency virus type 1 (HIV-1) transmission. Polarized monolayer integrity of primary cervical and prostate epithelial cells or cell lines cultured with T. vaginalis was measured by monitoring transepithelium resistance. The effect of T. vaginalis isolates on HIV-1 passage through polarized epithelial cell monolayers was evaluated for HIV-1 p24gag in the basolateral supernatants. Coincubation with T. vaginalis isolates induced disruption of monolayer integrity and resulted in passage of virus to the basolateral side of the monolayer. Furthermore, there was isolate variability in which two isolates induced greater monolayer damage and increased HIV-1 passage than did the other two isolates. Coincubation of T. vaginalis isolates with acutely HIV-1-infected peripheral blood mononuclear cells enhanced HIV-1 replication. This enhancement was associated with cellular proliferation and activation, as well as with tumor necrosis factor alpha production. In contrast to the monolayer disruption, the effect of T. vaginalis on HIV-1 replication was not isolate dependent. Thus, two mechanisms have been identified that could contribute to the epidemiologic association of trichomoniasis with the sexual transmission of HIV-1. (i) T. vaginalis disruption of urogenital epithelial monolayers could facilitate passage of HIV-1 to underlying layers. (ii) Activation of local immune cells by T. vaginalis in the presence of infectious HIV-1 might lead to increased viral replication. Collectively, these data suggest the need for more vigilant efforts in the diagnosis and treatment of T. vaginalis in women and men, especially in countries with a high prevalence of HIV-1.

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Figures

FIG. 1.
FIG. 1.
Deterioration of polarized primary monolayers of A) prostate (PrEC) epithelial cells and B) cervical (CerEC) epithelial cells after culturing with T. vaginalis strains Balt42 and JH31. Deterioration was determined by a decrease in the resistance of a polarized monolayer of cells. Ratios given are protozoan to cell. Black bar, 0 h; grey bar, 4 h; white bar, 18 h after T. vaginalis addition. Data presented are representative of two independent experiments. T0, time zero.
FIG. 2.
FIG. 2.
Deterioration of a polarized monolayer of an endometrial epithelial cell line (HEC1A) after exposure to T. vaginalis. A) Resistance across the HEC1A monolayer at 0, 24, 48, and 72 h after treatment with T. vaginalis (1 protozoan to 5 cells). Resistance presented as a percentage of the resistance at time zero (T0) and is the mean of three independent experiments. Light grey bar, 0 h; dark grey bar, 24 h; black bar, 48 h; white bar, 72 h. B) HIV-1 p24 levels in the basolateral supernatants at 24, 48, and 72 h of culture. Data presented are the means ± standard errors of the means (error bars) from three independent experiments. Dark grey bar, 24 h; black bar, 48 h; white bar, 72 h. Values that were significantly different (P < 0.05) from the value for the culture of HEC1A cells alone are indicated by asterisks. C) Correlation between resistance across the HEC1A monolayer and HIV-1 p24 levels at all time points. There is an inverse relationship between resistance and p24 levels (Spearman rank correlation of r = −0.88 [P < 0.0001]). Circles represent 24 h, squares represent 48 h, and triangles represent 72 h time points.
FIG. 3.
FIG. 3.
T. vaginalis-induced HIV-1 replication and TNF-α in resting PBMCs. A) HIV-1 p24 levels on days 4 (grey bar), 6 (black bar), and 8 (white bar) in HIV-1-infected, resting PBMCs incubated with T. vaginalis (1 protozoan to 100 cells). Cells stimulated with 0.5 μg/ml of phytohemagglutinin (positive control) produced 852,600 pg/ml of TNF-α on day 6. B) TNF-α levels on days 2 (light grey bar), 4 (dark grey bar), and 6 (black bar) in the experiment described above. Cells stimulated with 0.5 μg/ml of phytohemagglutinin (positive control) produced 1,483 pg/ml of TNF-α and peaked on day 2. Data presented are the means ± standard errors of the means (error bars) from three independent experiments. Values that were significantly different (P < 0.05) from the values for cultures with HIVLAI alone on the same day are indicated by asterisks.
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