Differential effects of three canonical Toxoplasma strains on gene expression in human neuroepithelial cells

Infection and Immunity

Volumn 79, Issue 3, 2011, Pages 1363-1373

  Xiao, Jianchun ^a   Jones Brando, Lorraine ^a   Talbot Jr , C Conover ^a   Yolken, Robert H ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL STRAIN; CENTRAL NERVOUS SYSTEM; GENE EXPRESSION; NEUROEPITHELIUM; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; TOXOPLASMOSIS;

CELL LINE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMANS; NEUROEPITHELIAL CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TOXOPLASMA; TOXOPLASMOSIS;

EID: 79952301066     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00947-10     Document Type: Article

References (60)

1. Ajioka, J. W., and D. Soldati. 2007. Toxoplasma: molecular and cellular biology. Horizon Bioscience, Norfolk, United Kingdom.
2. Barnes, E. N., J. L. Biedler, B. A. Spengler, and K. M. Lyser. 1981. The fine structure of continuous human neuroblastoma lines SK-N-SH, SK-N-BE(2), and SK-N-MC. In Vitro 17:619-631.
3. Benedetto, N., A. Folgore, M. Galdiero, R. Meli, and R. Di Carlo. 1995. Effect of prolactin, rIFN-gamma or rTNF-alpha in murine toxoplasmosis. Pathol. Biol. (Paris) 43:395-400.
4. Berdoy, M., J. P. Webster, and D. W. Macdonald. 2000. Fatal attraction in rats infected with Toxoplasma gondii. Proc. Biol. Sci. 267:1591-1594.
5. Blader, I. J., I. D. Manger, and J. C. Boothroyd. 2001. Microarray analysis reveals previously unknown changes in Toxoplasma gondii-infected human cells. J. Biol. Chem. 276:24223-24231.
6. Bole-Feysot, C., V. Goffin, M. Edery, N. Binart, and P. A. Kelly. 1998. Prolactin (PRL) and its receptor: actions signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocr. Rev. 19:225-268.
7. Butcher, B. A., L. Kim, P. F. Johnson, and E. Y. Denkers. 2001. Toxoplasma gondii tachyzoites inhibit proinflammatory cytokine induction in infected macrophages by preventing nuclear translocation of the transcription factor NF-kappa B. J. Immunol. 167:2193-2201.
8. Chaussabel, D., et al. 2003. Unique gene expression profiles of human macrophages and dendritic cells to phylogenetically distinct parasites. Blood 102:672-681. (Pubitemid 36841991)
9. Cunha-Reis, D., A. M. Sebastião, K. Wirkner, P. Illes, and J. A. Ribeiro. 2004. VIP enhances both pre- and postsynaptic GABAergic transmission to hippocampal interneurones leading to increased excitatory synaptic transmission to CA1 pyramidal cells. Br. J. Pharmacol. 143:733-744.
10. Datta, R., et al. 1993. Reactive oxygen intermediates target CC(A/T)6GG sequences to mediate activation of the early growth response 1 transcription factor gene by ionizing radiation. Proc. Natl. Acad. Sci. U. S. A. 90:2419-2422.
11. El Gazzar, M. 2007. HMGB1 modulates inflammatory responses in LPS-activated macrophages. Inflamm. Res. 56:162-167.
12. Flegr, J., J. Havlícek, P. Kodym, M. Malý, and Z. Smahel. 2002. Increased risk of traffic accidents in subjects with latent toxoplasmosis: a retrospective case-control study. BMC Infect. Dis. 2:11.
13. Frank, O., L. Jones-Brando, C. Leib-Mosch, R. Yolken, and W. Seifarth. 2006. Altered transcriptional activity of human endogenous retroviruses in neuroepithelial cells after infection with Toxoplasma gondii. J. Infect. Dis. 194:1447-1449. (Pubitemid 44706514)
14. Garcia, L. S., and D. A. Bruckner (ed.). 1997. Parasitic infections in the compromised host (Toxoplasma gondii), p. 111-121. In Diagnostic medical parasitology, 3rd ed. American Society for Microbiology, Washington, DC.
15. Garénaux, E., et al. 2008. The dual origin of Toxoplasma gondii N-glycans. Biochemistry 47:12270-12276.
16. Goto, Y., C. R. Yang, and S. Otani. 2010. Functional and dysfunctional synaptic plasticity in prefrontal cortex: roles in psychiatric disorders. Biol. Psychiatry 67:199-207.
17. Grigg, M. E., J. Ganatra, J. C. Boothroyd, and T. P. Margolis. 2001. Unusual abundance of atypical strains associated with human ocular toxoplasmosis. J. Infect. Dis. 184:633-639.
18. Guiry, A., et al. 2010. Testes and brain gene expression in precocious male and adult maturing Atlantic salmon (Salmo salar). BMC Genomics 11:211.
19. Hashimoto, R., et al. 2007. Pituitary adenylate cyclase-activating polypeptide is associated with schizophrenia. Mol. Psychiatry 12:1026-1032. (Pubitemid 350006203)
20. Hendriks, J., Y. Xiao, and J. Borst. 2003. CD27 promotes survival of activated T cells and complements CD28 in generation and establishment of the effector T cell pool. J. Exp. Med. 198:1369-1380.
21. Hintzen, R. Q., et al. 1995. Engagement of CD27 with its ligand CD70 provides a second signal for T cell activation. J. Immunol. 154:2612-2623.
22. Howe, D. K., S. Honoré, F. Derouin, and L. D. Sibley. 1997. Determination of genotypes of Toxoplasma gondii strains isolated from patients with toxoplasmosis. J. Clin. Microbiol. 35:1411-1414.
23. Howe, D. K., and L. D. Sibley. 1995. Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease. J. Infect. Dis. 172:1561-1566.
24. Irizarry, R. A., et al. 2003. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31:e15.
25. Janssen, T., et al. 2008. Discovery of a cholecystokinin-gastrin-like signaling system in nematodes. Endocrinology 149:2826-2839. (Pubitemid 351724514)
26. Joynson, D. H., and T. J. Wreghitt. 2001. Toxoplasmosis: a comprehensive clinical guide. Cambridge University Press, Cambridge, United Kingdom.
27. Kafsack, B. F., V. B. Carruthers, and F. J. Pineda. 2007. Kinetic modeling of Toxoplasma gondii invasion. J. Theor. Biol. 249:817-825.
28. Kim, L., B. A. Butcher, and E. Y. Denkers. 2004. Toxoplasma gondii interferes with lipopolysaccharide-induced mitogen-activated protein kinase activation by mechanisms distinct from endotoxin tolerance. J. Immunol. 172: 3003-3010.
29. Kim, S. K., A. E. Fouts, and J. C. Boothroyd. 2007. Toxoplasma gondii dysregulates IFN-gamma-inducible gene expression in human fibroblasts: insights from a genome-wide transcriptional profiling. J. Immunol. 178:5154-5165.
30. Knight, B. C., C. L. Brunton, N. C. Modi, G. R. Wallace, and M. R. Stanford. 2005. The effect of Toxoplasma gondii infection on expression of chemokines by rat retinal vascular endothelial cells. J. Neuroimmunol. 160:41-47.
31. Kong, J. T., M. E. Grigg, L. Uyetake, S. Parmley, and J. C. Boothroyd. 2003. Serotyping of Toxoplasma gondii infections in humans using synthetic peptides. J. Infect. Dis. 187:1484-1495.
32. Leng, J., B. A. Butcher, C. E. Egan, D. S. Abdallah, and E. Y. Denkers. 2009. Toxoplasma gondii prevents chromatin remodeling initiated by TLR-triggered macrophage activation. J. Immunol. 182:489-497.
33. Levy, S., et al. 2007. Strategy of transcription regulation in the budding yeast. PLoS One 2:e250.
34. Losavio, A. S., et al. 1993. Functional changes of the sciatic nerve in mice chronically infected with Trypanosoma cruzi. Medicina (B. Aires) 53:129-132.
35. Luk, F. C., T. M. Johnson, and C. J. Beckers. 2008. N-linked glycosylation of proteins in the protozoan parasite Toxoplasma gondii. Mol. Biochem. Parasitol. 157:169-178.
36. Marder, S. R., et al. 2004. Physical health monitoring of patients with schizophrenia. Am. J. Psychiatry 161:1334-1349. (Pubitemid 38989085)
37. Marvanová, M., M. Lakso, and G. Wong. 2004. Identification of genes regulated by memantine and MK-801 in adult rat brain by cDNA microarray analysis. Neuropsychopharmacology 29:1070-1079. (Pubitemid 38670045)
38. Mechta-Grigoriou, F., D. Gerald, and M. Yaniv. 2001. The mammalian Jun proteins: redundancy and specificity. Oncogene 20:2378-2389. (Pubitemid 32531296)
39. Moyes, K. M., et al. 2009. Gene network and pathway analysis of bovine mammary tissue challenged with Streptococcus uberis reveals induction of cell proliferation and inhibition of PPARgamma signaling as potential mechanism for the negative relationships between immune response and lipid metabolism. BMC Genomics 10:542.
40. Noel, G. L., H. K. Suh, J. G. Stone, and A. G. Frantz. 1972. Human prolactin and growth hormone release during surgery and other conditions of stress. J. Clin. Endocrinol. Metab. 35:840-851.
41. Pereira, R. M., et al. 2010. Novel role for the double-stranded RNA-activated protein kinase PKR: modulation of macrophage infection by the protozoan parasite Leishmania. FASEB J. 24:617-626.
42. Robben, P. M., et al. 2004. Production of IL-12 by macrophages infected with Toxoplasma gondii depends on the parasite genotype. J. Immunol. 172:3686-3694.
43. Saeij, J. P., J. P. Boyle, and J. C. Boothroyd. 2005. Differences among the three major strains of Toxoplasma gondii and their specific interactions with the infected host. Trends Parasitol. 21:476-481.
44. Saeij, J. P., et al. 2007. Toxoplasma co-opts host gene expression by injection of a polymorphic kinase homologue. Nature 445:324-327.
45. Sassin, J. F., A. G. Frantz, E. D. Weitzman, and S. Kapen. 1972. Human prolactin: 24-hour pattern with increased release during sleep. Science 177: 1205-1207.
46. Senaldi, G., et al. 1999. Novel neurotrophin-1/B cell-stimulating factor-3: a cytokine of the IL-6 family. Proc. Natl. Acad. Sci. U. S. A. 96:11458-11463.
47. Sever, J. L., et al. 1988. Toxoplasmosis: maternal and pediatric findings in 23,000 pregnancies. Pediatrics 82:181-192.
48. Sibley, L. D., D. G. Mordue, C. Su, P. M. Robben, and D. K. Howe. 2002. Genetic approaches to studying virulence and pathogenesis in Toxoplasma gondii. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357:81-88.
49. Staines, D. R., E. W. Brenu, and S. Marshall-Gradisnik. 2008. Postulated role of vasoactive neuropeptide-related immunopathology of the blood brain barrier and Virchow-Robin spaces in the aetiology of neurological-related conditions. Mediators Inflamm. 2008:792428.
50. Suzuki, Y., et al. 1996. Evidence for genetic regulation of susceptibility to toxoplasmic encephalitis in AIDS patients. J. Infect. Dis. 173:265-268.
51. Tavazoie, S., J. D. Hughes, M. J. Campbell, R. J. Cho, and G. M. Church. 1999. Systematic determination of genetic network architecture. Nat. Genet. 22:281-285.
52. Tekiel, V., A. Losavio, M. Jones, S. Muchnik, and S. M. González-Cappa. 2001. Changes in the mouse sciatic nerve action potential after epineural injection of sera from Trypanosoma cruzi infected mice. Parasite Immunol. 23:533-539.
53. Vyas, A., S. K. Kim, N. Giacomini, J. C. Boothroyd, and R. M. Sapolsky. 2007. Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors. Proc. Natl. Acad. Sci. U. S. A. 104:6442-6447.
54. Wang, Y., et al. 2006. Large scale real-time PCR validation on gene expression measurements from two commercial long-oligonucleotide microarrays. BMC Genomics 7:59.
55. Webster, J. P. 2001. Rats, cats, people and parasites: the impact of latent toxoplasmosis on behaviour. Microbes Infect. 3:1037-1045. (Pubitemid 32913702)
56. Weis, S., et al. 2007. Quality control for microarray analysis of human brain samples: the impact of postmortem factors, RNA characteristics, and histopathology. J. Neurosci. Methods 165:198-209. (Pubitemid 47212459)
57. Xiao, J., et al. 2009. Serological pattern consistent with infection with type I Toxoplasma gondii in mothers and risk of psychosis among adult offspring. Microbes Infect. 11:1011-1018.
58. Zentella, R., et al. 2007. Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19:3037-3057. (Pubitemid 350276710)
59. Zhao, H., et al. 2009. ben functions with Scamp during synaptic transmission and long-term memory formation in Drosophila. J. Neurosci. 29:414-424.
60. Zhao, Y. O., A. Khaminets, J. P. Hunn, and J. C. Howard. 2009. Disruption of the Toxoplasma gondii parasitophorous vacuole by IFNgamma-inducible immunity-related GTPases (IRG proteins) triggers necrotic cell death. PLoS Pathog. 5:e1000288.