Trophoblast apoptosis through polarization of macrophages induced by Chinese Toxoplasma gondii isolates with different virulence in pregnant mice

Parasitology Research

Volumn 112, Issue 8, 2013, Pages 3019-3027

  Liu, Tingting ^a   Zhang, Qian ^a   Liu, Lili ^a   Xu, Xiucai ^a   Chen, He ^a   Wang, Hua ^a   Kong, Lanting ^a   Wang, Weiwei ^a   Zhang, Aimei ^a   Cai, Yihong ^a   Li, Min ^a   Yu, Li ^a   Du, Jian ^a   Wang, Xuelong ^a   Luo, Qingli ^a   Lun, Zhao Rong ^b   Wang, Yong ^c   Shen, Jilong ^a  

^a ANHUI MEDICAL UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY   (China)

^c NANJING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APICOMPLEXA; APOPTOSIS; ARTICLE; BREEDING; CHINA; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; GENOTYPE; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MOUSE; NONHUMAN; PARASITE VIRULENCE; PATHOGENESIS; PLACENTAL TRANSFER; POLARIZATION; PREGNANCY OUTCOME; PRIORITY JOURNAL; SPONTANEOUS ABORTION; STRAIN DIFFERENCE; TH1 CELL; TH2 CELL; TOXOPLASMA GONDII; TROPHOBLAST;

EID: 84881128964     PISSN: 09320113     EISSN: 14321955     Source Type: Journal    
DOI: 10.1007/s00436-013-3475-3     Document Type: Article

References (34)

1. Abbasi M, Kowalewska-Grochowska K, Bahar MA, Kilani RT, Winkler-Lowen B, Guilbert LJ (2003) Infection of placental trophoblasts by Toxoplasma gondii. J Infect Dis 188(4):608-616
2. Chen ZW, Gao JM, Huo XX, Wang L, Yu L, Halm-Lai F, Xu YH, Song WJ, Hide G, Shen JL, Lun ZR (2011) Genotyping of Toxoplasma gondii isolates from cats in different geographic regions of China. Vet Parasitol 183(1-2):166-170
3. Cook T, Roos D, Morada M, Zhu G, Keithly JS, Feagin JE, Wu G, Yarlett N (2007) Divergent polyamine metabolism in the Apicomplexa. Microbiology 153(Pt 4):1123-1130
4. Dalton DK, Haynes L, Chu CQ, Swain SL, Wittmer S (2000) Interferon gamma eliminates responding CD4 T cells during mycobacterial infection by inducing apoptosis of activated CD4 T cells. J Exp Med 192(1):117-122
5. Desmonts G, Couvreur J (1974) Congenital toxoplasmosis. A prospective study of 378 pregnancies. N Engl J Med 290(20):1110-1116
6. dos Santos SA, de Andrade Junior DR, de Andrade DR (2011) TNF-alpha production and apoptosis in hepatocytes after Listeria monocytogenes and Salmonella typhimurium invasion. Rev Inst Med Trop Sao Paulo 53(2):107-112
7. El Kasmi KC, Qualls JE, Pesce JT, Smith AM, Thompson RW, Henao-Tamayo M, Basaraba RJ, Konig T, Schleicher U, Koo MS, Kaplan G, Fitzgerald KA, Tuomanen EI, Orme IM, Kanneganti TD, Bogdan C, Wynn TA, Murray PJ (2008) Toll-like receptor-induced arginase 1 in macrophages thwarts effective immunity against intracellular pathogens. Nat Immunol 9(12):1399-1406
8. Gao XJ, Zhao ZJ, He ZH, Wang T, Yang TB, Chen XG, Shen JL, Wang Y, Lv FL, Hide G, Lun ZR (2012) Toxoplasma gondii infection in pregnant women in China. Parasitology 139(2):139-147
9. Hill D, Dubey JP (2002) Toxoplasma gondii: transmission, diagnosis and prevention. Clin Microbiol Infect 8(10):634-640
10. Howe DK, Sibley LD (1995) Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease. J Infect Dis 172(6):1561-1566
11. Iniesta V, Gomez-Nieto LC, Corraliza I (2001) The inhibition of arginase by N(omega)-hydroxy-l-arginine controls the growth of Leishmania inside macrophages. J Exp Med 193(6):777-784
12. Jensen KD, Wang Y, Wojno ED, Shastri AJ, Hu K, Cornel L, Boedec E, Ong YC, Chien YH, Hunter CA, Boothroyd JC, Saeij JP (2011) Toxoplasma polymorphic effectors determine macrophage polarization and intestinal inflammation. Cell Host Microbe 9(6):472-483
13. Li Z, Zhao ZJ, Zhu XQ, Ren QS, Nie FF, Gao JM, Gao XJ, Yang TB, Zhou WL, Shen JL, Wang Y, Lu FL, Chen XG, Hide G, Ayala FJ, Lun ZR (2012) Differences in iNOS and arginase expression and activity in the macrophages of rats are responsible for the resistance against T. gondii infection. PLoS One 7(4):e35834
14. Liesenfeld O, Kosek J, Remington JS, Suzuki Y (1996) Association of CD4+ T cell-dependent, interferon-gamma-mediated necrosis of the small intestine with genetic susceptibility of mice to peroral infection with Toxoplasma gondii. J Exp Med 184(2):597-607
15. Loke P, Nair MG, Parkinson J, Guiliano D, Blaxter M, Allen JE (2002) IL-4 dependent alternatively-activated macrophages have a distinctive in vivo gene expression phenotype. BMC Immunol 3:7
16. Mantovani A (2008) From phagocyte diversity and activation to probiotics: back to Metchnikoff. Eur J Immunol 38(12):3269-3273
17. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25(12):677-686
18. Melo MB, Jensen KD, Saeij JP (2011) Toxoplasma gondii effectors are master regulators of the inflammatory response. Trends Parasitol 27(11):487-495
19. Pappas G, Roussos N, Falagas ME (2009) Toxoplasmosis snapshots: global status of Toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplasmosis. Int J Parasitol 39(12):1385-1394
20. Polgar K, Hill JA (2002) Identification of the white blood cell populations responsible for Th1 immunity to trophoblast and the timing of the response in women with recurrent pregnancy loss. Gynecol Obstet Invest 53(1):59-64
21. Raes G, Brys L, Dahal BK, Brandt J, Grooten J, Brombacher F, Vanham G, Noel W, Bogaert P, Boonefaes T, Kindt A, Van den Bergh R, Leenen PJ, De Baetselier P, Ghassabeh GH (2005) Macrophage galactose-type C-type lectins as novel markers for alternatively activated macrophages elicited by parasitic infections and allergic airway inflammation. J Leukoc Biol 77(3):321-327
22. Ramos JM, Milla A, Rodriguez JC, Padilla S, Masia M, Gutierrez F (2011) Seroprevalence of Toxoplasma gondii infection among immigrant and native pregnant women in Eastern Spain. Parasitol Res 109(5):1447-1452
23. Robben PM, Mordue DG, Truscott SM, Takeda K, Akira S, Sibley LD (2004) Production of IL-12 by macrophages infected with Toxoplasma gondii depends on the parasite genotype. J Immunol 172(6):3686-3694
24. Sibley LD, Boothroyd JC (1992) Virulent strains of Toxoplasma gondii comprise a single clonal lineage. Nature 359(6390):82-85
25. Sindrilaru A, Peters T, Wieschalka S, Baican C, Baican A, Peter H, Hainzl A, Schatz S, Qi Y, Schlecht A, Weiss JM, Wlaschek M, Sunderkotter C, Scharffetter-Kochanek K (2011) An unrestrained proinflammatory M1 macrophage population induced by iron impairs wound healing in humans and mice. J Clin Invest 121(3):985-997
26. Van den Bossche J, Bogaert P, van Hengel J, Guerin CJ, Berx G, Movahedi K, Van den Bergh R, Pereira-Fernandes A, Geuns JM, Pircher H, Dorny P, Grooten J, De Baetselier P, Van Ginderachter JA (2009) Alternatively activated macrophages engage in homotypic and heterotypic interactions through IL-4 and polyamine-induced E-cadherin/catenin complexes. Blood 114(21):4664-4674
27. Wang L, Chen H, Liu D, Huo X, Gao J, Song X, Xu X, Huang K, Liu W, Wang Y, Lu F, Lun ZR, Luo Q, Wang X, Shen J (2013) Genotypes and mouse virulence of Toxoplasma gondii isolates from animals and humans in China. PLoS One 8(1):e53483
28. Welch JS, Escoubet-Lozach L, Sykes DB, Liddiard K, Greaves DR, Glass CK (2002) TH2 cytokines and allergic challenge induce Ym1 expression in macrophages by a STAT6-dependent mechanism. J Biol Chem 277(45):42821-42829
29. Wong SY, Remington JS (1994) Toxoplasmosis in pregnancy. Clin Infect Dis 18(6):853-861, quiz 862
30. Wood KJ, Sawitzki B (2006) Interferon gamma: a crucial role in the function of induced regulatory T cells in vivo. Trends Immunol 27(4):183-187
31. Xiao W, Hong H, Kawakami Y, Lowell CA, Kawakami T (2008) Regulation of myeloproliferation and M2 macrophage programming in mice by Lyn/Hck, SHIP, and Stat5. J Clin Invest 118(3):924-934
32. Xu X, Liu T, Zhang A, Huo X, Luo Q, Chen Z, Yu L, Li Q, Liu L, Lun ZR, Shen J (2012) Reactive oxygen species-triggered trophoblast apoptosis is initiated by endoplasmic reticulum stress via activation of caspase-12, CHOP, and the JNK pathway in Toxoplasma gondii infection in mice. Infect Immun 80(6):2121-2132
33. Yu L, Shen J, Su C, Sundermann CA (2013) Genetic characterization of Toxoplasma gondii in wildlife from Alabama, USA. Parasitol Res 112(3):1333-1336
34. Zhou DH, Yuan ZG, Zhao FR, Li HL, Zhou Y, Lin RQ, Zou FC, Song HQ, Xu MJ, Zhu XQ (2011) Modulation of mouse macrophage proteome induced by Toxoplasma gondii tachyzoites in vivo. Parasitol Res 109(6):1637-1646