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Original Article

Proliferation of Toxoplasma gondii Suppresses Host Cell Autophagy

Youn-Jin Lee1,†, Hyun-Ouk Song2,†, Young-Ha Lee3, Jae-Sook Ryu1, Myoung-Hee Ahn1
The Korean Journal of Parasitology 2013;51(3):279-287.
Published online: June 30, 2013

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Corresponding author (mhahn@hanyang.ac.kr)

†Joint first authors.

• Received: March 8, 2013   • Revised: May 10, 2013   • Accepted: May 10, 2013

© 2013, Korean Society for Parasitology and Tropical Medicine

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Proliferation of Toxoplasma gondii Suppresses Host Cell Autophagy
Korean J Parasitol. 2013;51(3):279-287.   Published online June 30, 2013
DOI: https://doi.org/10.3347/kjp.2013.51.3.279
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Proliferation of Toxoplasma gondii Suppresses Host Cell Autophagy
Korean J Parasitol. 2013;51(3):279-287.   Published online June 30, 2013
DOI: https://doi.org/10.3347/kjp.2013.51.3.279
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Proliferation of Toxoplasma gondii Suppresses Host Cell Autophagy
Image Image Image Image Image Image
Fig. 1 Cell death and cell viability were assessed by the LDH and MTT assay. HeLa cells were exposed to T. gondii or rapamycin or combination for 6-48 hr. Control cells were treated with rapamycin only for 24 hr. (A) Cell death increased due to T. gondii or T. gondii plus rapamycin treatment at 36 hr and 48 hr post-infction as shown by the LDH assay. (B) The MTT assay showed gradually decreasing cell viability following exposure to T. gondii or T. gondii plus rapamycin after 24 hr. C, control. aP<0.05.
Fig. 2 Autophagic marker LC3 II, measured by Western blotting. HeLa cells were exposed to T. gondii (cell: T. gondii ratio=1:5) or rapamycin (24 hr) or the combination for 6-36 hr. Cells were pre-treated with an autophagic inhibitor, 3-MA (10 nM), a pan-caspase inhibitor (20 µM) or a calpain inhibitor (100 µM) for 2 hr. (A) Over-expression of LC3 II was observed in T. gondii-infected HeLa cells with rapamycin treatment at 18-24 hr post-infection. (B) The 3-MA and pan-caspase inhibitor suppressed LC3 II expressison. C, control; H, HeLa cells; R, rapamycin; T, T. gondii; RT, rapamycin and T. gondii; 3MA, 3- methyladenine; Pan, pan-caspase inhibitor; Cal, calpain inhibitor.
Fig. 3 Beclin 1 expression in HeLa cells treated with T. gondii and rapamycin detected by Western blotting and RT-PCR. HeLa cells were exposed to T. gondii (cell: T. gondii ratio=1:5) or rapamycin or the combination for 1-48 hr or for 6-36 hr. Cells were pre-treated with 3-MA (10 nM), pan-caspase inhibitor (20 µM) or a calpain inhibitor (100 µM) for 2 hr followed by T. gondii and rapamycin treatment. (A and C) Increased expression of Beclin 1 mRNA and protein was observed in HeLa cells treated with T. gondii or T. gondii plus rapamycin at 18 hr and 24 hr post-infection. (B) Beclin 1 expression was suppressed in cells pre-treated with 3-MA and a calpain inhibitor for 2 hr. C, control; H, HeLa cells; R, rapamycin; T, T. gondii; RT, rapamycin and T. gondii; 3-MA, 3-methladenine; Pan, pan-caspase inhibitor; Cal, calpain inhibitor.
Fig. 4 Fluorescence micrographs of MDC-labeled autophagic vesicles (AVs). HeLa cells were exposed to T. gondii (cell: T. gondii ratio= 1:5) and rapamycin for 6, 18, and 24 hr. The cells were incubated with MDC (0.05 mM) for 1 hr and treated with a fixation-permeabilization solution for 15 min. Untreated cells or cells treated with rapamycin for 18 hr were used as controls (A, B; ×400). Distinct fluorescent dots were observed in the cytoplasm of the cells infected with T. gondii and exposed to rapamycin for 18 hr. Decreased fluorescence was noted at 24 hr post-infection (C, D; × 200). Arrows indicate the MDC positive AVs.
Fig. 5 Ultrastructural observation of T. gondii-infected and rapamycin-treated HeLa cells. (A) Control cells treated with rapamycin for 18 hr showing numerous AVs containing damaged organelles. (B) Cells infected with T. gondii for 18 hr showing tachyzoite proliferation in PVs. (C) HeLa cells exposed to T. gondii and rapamycin showing numerous AVs at 6 hr post-infection. (D) Proliferation of T. gondii accompanied by a decline in the numbers of Avs, observed at 18 hr post-infection. (E, F) Cells pre-treated 3-MA for 2 hr and exposed to T. gondii with rapamycin for 18 hr had reduced numbers of AVs. Cells pre-treated with wortmannin did not show this effect. Scale bar: 2 µm (A-D), 500 nm (E, F).
Fig. 6 Flow cytometry to detect apoptosis in HeLa cells treated with T. gondii and rapamycin. (Aa, b) Control cells with no treatment or actinomycin D (5 µg/ml) had apoptosis rates of 14.7 % and 58.3%, respectively. (Ac, d) Low level apoptosis was observed in HeLa cells treated with rapamycin with or without T. gondii infection (13.4% and 10.1%, respectively). (Be, f, g) Cells pre-treated with inhibitors of autophagy or apoptosis and exposed to T. gondii and rapamycin did not show apoptosis (15.9% in cells pre-treated with 3-MA; 13.7% in cells pre-treated with a pan-caspase inhibitor; 16.0% in cells pre-treated with calpeptin).

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Proliferation of Toxoplasma gondii Suppresses Host Cell Autophagy
PHD : Parasites, Hosts and Diseases

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