Human placental syncytiotrophoblasts restrict toxoplasma gondii attachment and replication and respond to infection by producing immunomodulatory chemokines

mBio

Volumn 9, Issue 1, 2018, Pages

  Ander, Stephanie E ^a,b   Rudzki, Elizabeth N ^c   Arora, Nitin ^a,b   Sadovsky, Yoel ^a,d   Coyne, Carolyn B ^a,b   Boyle, Jon P ^c  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

^d UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

CCL22; Placenta; Syncytiotrophoblast; Toxoplasma gondii

Indexed keywords

CHEMOKINE; MACROPHAGE DERIVED CHEMOKINE; TRANSCRIPTOME;

ARTICLE; CELL ADHESION; CHORION VILLUS; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEVELOPMENTAL STAGE; FEMALE; GENE; GESTATIONAL AGE; HOST PARASITE INTERACTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNITY RELATED GENE; IMMUNOMODULATION; MATERNAL BLOOD; MICROBIAL ACTIVITY; MULTINUCLEAR CELL; NONHUMAN; PARASITE DEVELOPMENT; PARASITE TRANSMISSION; PLACENTA TISSUE; PRIORITY JOURNAL; RNA SEQUENCE; RNA TRANSCRIPTION; SECOND TRIMESTER PREGNANCY; SYNCYTIOTROPHOBLAST CELL; THIRD TRIMESTER PREGNANCY; TOXOPLASMA GONDII; TOXOPLASMOSIS; UPREGULATION; VERTICAL TRANSMISSION; CELL CULTURE; GENE EXPRESSION PROFILING; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; METABOLISM; ORGAN CULTURE TECHNIQUE; PARASITOLOGY; PLACENTA; PREGNANCY; TOXOPLASMA; TROPHOBLAST;

CELLS, CULTURED; CHEMOKINES; FEMALE; GENE EXPRESSION PROFILING; HUMANS; ORGAN CULTURE TECHNIQUES; PLACENTA; PREGNANCY; TOXOPLASMA; TROPHOBLASTS;

EID: 85043453861     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01678-17     Document Type: Article

References (33)

1. Torgerson PR, Mastroiacovo P. 2013. The global burden of congenital toxoplasmosis: a systematic review. Bull World Health Organ 91: 501–508. https://doi.org/10.2471/BLT.12.111732.
2. Olariu TR, Remington JS, McLeod R, Alam A, Montoya JG. 2011. Severe congenital toxoplasmosis in the United States: clinical and serologic findings in untreated infants. Pediatr Infect Dis J 30:1056–1061. https://doi.org/10.1097/INF.0b013e3182343096.
3. Bayer A, Lennemann NJ, Ouyang Y, Bramley JC, Morosky S, Marques ET, Jr, Cherry S, Sadovsky Y, Coyne CB. 2016. Type III interferons produced by human placental trophoblasts confer protection against Zika virus infection. Cell Host Microbe 19:705–712. https://doi.org/10.1016/j.chom.2016.03.008.
4. Delorme-Axford E, Sadovsky Y, Coyne CB. 2013. Lipid raft- and SRC family kinase-dependent entry of coxsackievirus B into human placental trophoblasts. J Virol 87:8569–8581. https://doi.org/10.1128/JVI.00708-13.
5. Bayer A, Delorme-Axford E, Sleigher C, Frey TK, Trobaugh DW, Klim-stra WB, Emert-Sedlak LA, Smithgall TE, Kinchington PR, Vadia S, Seveau S, Boyle JP, Coyne CB, Sadovsky Y. 2015. Human trophoblasts confer resistance to viruses implicated in perinatal infection. Am J Obstet Gynecol 212:71.e1–71.e8. https://doi.org/10.1016/j.ajog.2014.07.060.
6. Robbins JR, Zeldovich VB, Poukchanski A, Boothroyd JC, Bakardjiev AI. 2012. Tissue barriers of the human placenta to infection with Toxoplasma gondii. Infect Immun 80:418– 428. https://doi.org/10.1128/IAI.05899-11.
7. McConkey CA, Delorme-Axford E, Nickerson CA, Kim KS, Sadovsky Y, Boyle JP, Coyne CB. 2016. A three-dimensional culture system recapitulates placental syncytiotrophoblast development and microbial resistance. Sci Adv 2:e1501462. https://doi.org/10.1126/sciadv.1501462.
8. Kamau E, Meehan T, Lavine MD, Arrizabalaga G, Mustata Wilson G, Boyle J. 2011. A novel benzodioxole-containing inhibitor of Toxoplasma gondii growth alters the parasite cell cycle. Antimicrob Agents Chemother 55:5438–5451. https://doi.org/10.1128/AAC.00455-11.
9. Kafsack BF, Carruthers VB, Pineda FJ. 2007. Kinetic modeling of Toxoplasma gondii invasion. J Theor Biol 249:817– 825. https://doi.org/10.1016/j.jtbi.2007.09.008.
10. Coffey MJ, Sleebs BE, Uboldi AD, Garnham A, Franco M, Marino ND, Panas MW, Ferguson DJ, Enciso M, O’Neill MT, Lopaticki S, Stewart RJ, Dewson G, Smyth GK, Smith BJ, Masters SL, Boothroyd JC, Boddey JA, Tonkin CJ. 2015. An aspartyl protease defines a novel pathway for export of Toxoplasma proteins into the host cell. Elife 4:e10809. https://doi.org/10.7554/eLife.10809.
11. Freier CP, Kuhn C, Rapp M, Endres S, Mayr D, Friese K, Anz D, Jeschke U. 2015. Expression of CCL22 and infiltration by regulatory T cells are increased in the decidua of human miscarriage placentas. Am J Reprod Immunol 74:216–227. https://doi.org/10.1111/aji.12399.
12. Holtan SG, Chen Y, Kaimal R, Creedon DJ, Enninga EA, Nevala WK, Markovic SN. 2015. Growth modeling of the maternal cytokine milieu throughout normal pregnancy: macrophage-derived chemokine decreases as inflammation/counterregulation increases. J Immunol Res 2015:952571. https://doi.org/10.1155/2015/952571.
13. Franco M, Panas MW, Marino ND, Lee MC, Buchholz KR, Kelly FD, Bednarski JJ, Sleckman BP, Pourmand N, Boothroyd JC. 2016. A novel secreted protein, MYR1, is central to toxoplasma’s manipulation of host cells. mBio 7:e02231-15. https://doi.org/10.1128/mBio.02231-15.
14. Braun L, Brenier-Pinchart MP, Yogavel M, Curt-Varesano A, Curt-Bertini RL, Hussain T, Kieffer-Jaquinod S, Coute Y, Pelloux H, Tardieux I, Sharma A, Belrhali H, Bougdour A, Hakimi MA. 2013. A Toxoplasma dense granule protein, GRA24, modulates the early immune response to infection by promoting a direct and sustained host p38 MAPK activation. J Exp Med 210:2071–2086. https://doi.org/10.1084/jem.20130103.
15. Reid AJ, Vermont SJ, Cotton JA, Harris D, Hill-Cawthorne GA, Könen-Waisman S, Latham SM, Mourier T, Norton R, Quail MA, Sanders M, Shanmugam D, Sohal A, Wasmuth JD, Brunk B, Grigg ME, Howard JC, Parkinson J, Roos DS, Trees AJ, Berriman M, Pain A, Wastling JM. 2012. Comparative genomics of the apicomplexan parasites Toxoplasma gondii and Neospora caninum: coccidia differing in host range and transmission strategy. PLoS Pathog 8:e1002567. https://doi.org/10.1371/journal.ppat.1002567.
16. Landmann JK, Jillella D, O’Donoghue PJ, McGowan MR. 2002. Confirmation of the prevention of vertical transmission of Neospora caninum in cattle by the use of embryo transfer. Aust Vet J 80:502–503. https://doi.org/10.1111/j.1751-0813.2002.tb12475.x.
17. Davison HC, Otter A, Trees AJ. 1999. Estimation of vertical and horizontal transmission parameters of Neospora caninum infections in dairy cattle. Int J Parasitol 29:1683–1689. https://doi.org/10.1016/S0020-7519(99) 00129-0.
18. English ED, Adomako-Ankomah Y, Boyle JP. 2015. Secreted effectors in Toxoplasma gondii and related species: determinants of host range and pathogenesis? Parasite Immunol 37:127–140. https://doi.org/10.1111/pim.12166.
19. Bougdour A, Durandau E, Brenier-Pinchart MP, Ortet P, Barakat M, Kieffer S, Curt-Varesano A, Curt-Bertini RL, Bastien O, Coute Y, Pelloux H, Hakimi MA. 2013. Host cell subversion by Toxoplasma GRA16, an exported dense granule protein that targets the host cell nucleus and alters gene expression. Cell Host Microbe 13:489–500. https://doi.org/10.1016/j.chom.2013.03.002.
20. Shastri AJ, Marino ND, Franco M, Lodoen MB, Boothroyd JC. 2014. GRA25 is a novel virulence factor of Toxoplasma gondii and influences the host immune response. Infect Immun 82:2595–2605. https://doi.org/10.1128/IAI.01339-13.
21. Håkansson S, Morisaki H, Heuser J, Sibley LD. 1999. Time-lapse video microscopy of gliding motility in Toxoplasma gondii reveals a novel, biphasic mechanism of cell locomotion. Mol Biol Cell 10:3539–3547. https://doi.org/10.1091/mbc.10.11.3539.
22. Carruthers VB, Håkansson S, Giddings OK, Sibley LD. 2000. Toxoplasma gondii uses sulfated proteoglycans for substrate and host cell attachment. Infect Immun 68:4005–4011. https://doi.org/10.1128/IAI.68.7.4005 -4011.2000.
23. Pfefferkorn ER. 1984. Interferon-g blocks the growth of Toxoplasma gondii in human fibroblasts by inducing the host cell to degrade tryp-tophan. Proc Natl Acad Sci U S A 81:908–912. https://doi.org/10.1073/pnas.81.3.908.
24. Selleck EM, Fentress SJ, Beatty WL, Degrandi D, Pfeffer K, Virgin HW, IV, Macmicking JD, Sibley LD. 2013. Guanylate-binding protein 1 (Gbp1) contributes to cell-autonomous immunity against Toxoplasma gondii. PLoS Pathog 9:e1003320. https://doi.org/10.1371/journal.ppat.1003320.
25. Foltz C, Napolitano A, Khan R, Clough B, Hirst EM, Frickel EM. 2017. TRIM21 is critical for survival of Toxoplasma gondii infection and loca-lises to GBP-positive parasite vacuoles. Sci Rep 7:5209. https://doi.org/10.1038/s41598-017-05487-7.
26. Choi J, Park S, Biering SB, Selleck E, Liu CY, Zhang X, Fujita N, Saitoh T, Akira S, Yoshimori T, Sibley LD, Hwang S, Virgin HW. 2014. The parasi-tophorous vacuole membrane of Toxoplasma gondii is targeted for disruption by ubiquitin-like conjugation systems of autophagy. Immunity 40:924–935. https://doi.org/10.1016/j.immuni.2014.05.006.
27. Lavine MD, Arrizabalaga G. 2011. The antibiotic monensin causes cell cycle disruption of Toxoplasma gondii mediated through the DNA repair enzyme TgMSH-1. Antimicrob Agents Chemother 55:745–755. https://doi.org/10.1128/AAC.01092-10.
28. Chtanova T, Schaeffer M, Han SJ, van Dooren GG, Nollmann M, Herzmark P, Chan SW, Satija H, Camfield K, Aaron H, Striepen B, Robey EA. 2008. Dynamics of neutrophil migration in lymph nodes during infection. Immunity 29:487– 496. https://doi.org/10.1016/j.immuni.2008.07.012.
29. Laudanski P, Lemancewicz A, Kuc P, Charkiewicz K, Ramotowska B, Kretowska M, Jasinska E, Raba G, Karwasik-Kajszczarek K, Kraczkowski J, Laudanski T. 2014. Chemokines profiling of patients with preterm birth. Mediators Inflamm 2014:185758. https://doi.org/10.1155/2014/185758.
30. Arenas-Hernandez M, Romero R, St Louis D, Hassan SS, Kaye EB, Gomez-Lopez N. 2016. An imbalance between innate and adaptive immune cells at the maternal-fetal interface occurs prior to endotoxin-induced preterm birth. Cell Mol Immunol 13:462– 473. https://doi.org/10.1038/cmi.2015.22.
31. Rowe JH, Ertelt JM, Aguilera MN, Farrar MA, Way SS. 2011. Foxp3(<) regulatory T cell expansion required for sustaining pregnancy compromises host defense against prenatal bacterial pathogens. Cell Host Microbe 10:54– 64. https://doi.org/10.1016/j.chom.2011.06.005.
32. Rausch K, Hackett BA, Weinbren NL, Reeder SM, Sadovsky Y, Hunter CA, Schultz DC, Coyne CB, Cherry S. 2017. Screening bioactives reveals nanchangmycin as a broad spectrum antiviral active against Zika virus. Cell Rep 18:804– 815. https://doi.org/10.1016/j.celrep.2016.12.068.
33. Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550. https://doi.org/10.1186/s13059-014-0550-8.