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Co-infection: the outcome of Plasmodium infection differs according to the time of pre-existing helminth infection

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Abstract

Although helminth-Plasmodium coinfections are common in tropical regions, the implications of this co-existence for the host immune response are poorly understood. In order to understand the effect of helminth infection at different times of coinfection on the immune response against Plasmodium infection, BALB/c mice were intraperitoneally infected with Taenia crassiceps (Tc). At 2 (Tc2) or 8 (Tc8) weeks post-infection, mice were intravenously infected with 1 × 103 Plasmodium yoelii (Py) 17XL-parasitized red blood cells. Py 17XL-single-infected mice developed cachexia, splenomegaly, and anemia, and died at 11 days post-infection. Importantly, Tc2 + Py-coinfected mice showed increased survival of 58% on day 11, but developed pathology (cachexia and splenomegaly) and succumbed on day 18 post-coinfection, this latter associated with high levels of IL-1β and IL-12, and reduced IFN-γ in serum compared with Py 17XL-single-infected mice. Interestingly, Tc8 + Py-coinfected mice showed increased survival up to 80% on day 11 and succumbed on day 30 post-coinfection. This increased survival rate conferred by chronic helminth infection was associated with a decreased pathology and mixed inflammatory-type 1/anti-inflammatory-type 2 immune profile as evidenced by the production of high levels of IL-12 and IL-10, and reduced TNF-α from macrophages, high levels of IL-4 and IL-10, and low levels of IFN-γ from spleen cells. Also high serum levels of IL-1β, TNF-α, IL-12, IL-4, and IL-10, but a significant reduction of IFN-γ were observed. Together, these data indicate that polarization of the cell-mediated response modulated by a pre-existing helminth infection differentially impacts on the host immune response to Py 17XL in a time-dependent manner.

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Acknowledgments

This work is part of the requirements to obtain a PhD degree in the Programa de Doctorado en Ciencias Biomédicas, Universidad Nacional Autónoma de México (UNAM), for Victor H. Salazar Castañon, who received a fellowship No. 0443480 from the National Council of Science and Technology of Mexico (CONACyT). This study was supported in part by grants from the “Support Program for Research Projects and Technological Innovation” (PAPIIT) No. IN-209718 and IN-220417 to MRS and MLH, respectively.

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Correspondence to Miriam Rodriguez-Sosa.

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The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in these studies were in accordance with the ethical standards approved and carried out under strict accordance with the guidelines for the Care and Use of Laboratory Animals adopted by the U.S. National Institutes of Health, and the Mexican Regulation of Animal Care and maintenance (NOM-062-ZOO-1999, 2001). And it was revised and approved by the Ethics Committee at FES-Iztacala, UNAM (CE/FESI/032017/1154).

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Fig. S1

Late Taenia crassiceps-Plasmodium yoelii 17XL coinfection promotes IL-1β, TNF-α, IL-12 and IL-10 production by macrophages stimulated with the TcPyAg. Peritoneal Mφ from Py 17XL-single-infected, Tc2, Tc8, Tc2 + Py, Tc8 + Py experimental groups were isolated at 7 days post-coinfection and stimulated with TcPyAg (25 μg/mL, for each antigen). Supernatants were collected 48 h later and cytokine production IL-1β (a), TNF-α (b), IL-12 (c) and IL-10 (d) was measured by ELISA. Data are expressed as the mean ± SEM and are representative of 3 independent experiments with at least 3–5 mice per group. Values of p < 0.05 were considered statistically significant, (a) compared with the non-infected group, (b) compared with the Tc2 group, (c) compared with the Tc8 group, (*) compared with the Py 17XL group, and (&) compared with the Tc2 + Py group. (GIF 56 kb)

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Fig. S2

Late Taenia crassiceps-Plasmodium yoelii 17XL coinfection decreases the proliferative response. Mice infected with Taenia crassiceps for 2 (Tc2) or 8 (Tc8) weeks were coinfected with Py 17XL (Tc2 + Py or Tc8 + Py, respectively). Seven days post-Py 17XL coinfection, the spleen cell proliferation was assayed in freshly isolated spleen cells upon stimulation with Con-A for 72 h. The bars represent the mean incorporation of 3H-TDR ± SEM from triplicate assays. Data are expressed as the mean ± SEM and are representative of 3 independent experiments with at least 3–5 mice per group. Values of p < 0.05 were considered statistically significant, (a) compared with the non-infected group, (b) compared with the Tc2 group, (c) compared with the Tc8 group, (*) compared with the Py 17XL group, and (&) compared with the Tc2 + Py group. (GIF 17 kb)

High resolution image (TIF 154 kb)

Fig. S3

Late Taenia crassiceps-Plasmodium yoelii 17XL coinfection promotes IL-4 and IL-10 production by spleen cells after Con-A stimulation. Spleen cells from Py 17XL-single-infected, Tc2, Tc8, Tc2 + Py, Tc8 + Py experimental groups were isolated at 7 days post-coinfection after stimulation with Con-A for 72 h the cytokines were quantified in supernatants, a) IL-4, b) IL- 10 and c) IFN-γ. The bars represent the mean ± SEM and are representative of from 3 independent experiments with at least 3–5 mice per group. Values of p < 0.05 were considered statistically significant, (a) compared with the non-infected group, (b) compared with the Tc2 group, (c) compared with the Tc8 group, (*) compared with the Py 17XL group, and (&) compared with the Tc2 + Py group. (GIF 41 kb)

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Salazar-Castañón, V.H., Juárez-Avelar, I., Legorreta-Herrera, M. et al. Co-infection: the outcome of Plasmodium infection differs according to the time of pre-existing helminth infection. Parasitol Res 117, 2767–2784 (2018). https://doi.org/10.1007/s00436-018-5965-9

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  • DOI: https://doi.org/10.1007/s00436-018-5965-9

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