Coxiella burnetii, the agent of Q fever, replicates within trophoblasts and induces a unique transcriptional response

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Ben Amara, Amira ^a   Ghigo, Eric ^a   Le Priol, Yannick ^b   Lépolard, Catherine ^a   Salcedo, Suzana P ^c   Lemichez, Emmanuel ^d   Bretelle, Florence ^a   Capo, Christian ^a   Mege, Jean Louis ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b SERVICE DE SANTÉ DES ARMÉES   (France)

^c CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^d INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN D; EARLY GROWTH RESPONSE FACTOR 1; GELATINASE B; INTERLEUKIN 4 RECEPTOR; TRANSCRIPTOME;

ANIMAL TISSUE; ARTICLE; BACTERIAL CELL; BINDING AFFINITY; BONE MARROW CELL; CELL DIVISION; CONTROLLED STUDY; COXIELLA BURNETII; CYTOSKELETON; DENSITOMETRY; DOWN REGULATION; GENE CLUSTER; GENE REPLICATION; HUMAN; HUMAN CELL; MACROPHAGE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGOLYSOSOME; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; Q FEVER; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TROPHOBLAST; UPREGULATION;

ANIMALS; COXIELLA BURNETII; EARLY GROWTH RESPONSE PROTEIN 1; GENE EXPRESSION PROFILING; INFLAMMATION; INTERLEUKIN-13; INTERLEUKIN-6; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHAGOSOMES; PHENOTYPE; Q FEVER; STAT3 TRANSCRIPTION FACTOR; TRANSCRIPTION, GENETIC; TROPHOBLASTS;

BACTERIA (MICROORGANISMS); BOS; COXIELLA BURNETII;

EID: 78650773565     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015315     Document Type: Article

References (60)

1. Raoult D, Marrie T, Mege JL (2005) Natural history and pathophysiology of Q fever. Lancet Infect Dis 5: 219-226.
2. Carcopino X, Raoult D, Bretelle F, Boubli L, Stein A (2007) Managing Q fever during pregnancy: the benefits of long-term cotrimoxazole therapy. Clin Infect Dis 45: 548-555.
3. Stein A, Lepidi H, Mege JL, Marrie TJ, Raoult D (2000) Repeated pregnancies in BALB/c mice infected with Coxiella burnetii cause disseminated infection, resulting in stillbirth and endocarditis. J Infect Dis 181: 188-194.
4. Lang G, Waltner-Toews D, Menzies P (1991) The seroprevalence of coxiellosis (Q fever) in Ontario sheep flocks. Can J Vet Res 55: 139-142.
5. Arricau-Bouvery N, Rodolakis A (2005) Is Q fever an emerging or re-emerging zoonosis? Vet Res 36: 327-349.
6. Parisi A, Fraccalvieri R, Cafiero M, Miccolupo A, Padalino I, et al. (2006) Diagnosis of Coxiella burnetii-related abortion in Italian domestic ruminants using single-tube nested PCR. Vet Microbiol 118: 101-106.
7. Langley JM (1990) Perinatal Q fever: is Coxiella burnetii a human perinatal pathogen? In: Marrie TJ, ed. Q fever, Vol I: the disease. Boca Raton: CRC Press, FL. pp 201-212.
8. Tissot-Dupont H, Amadei MA, Nezri M, Raoult D (2004) Wind in november, Q fever in december. Emerg Infect Dis 10: 1264-1269.
9. Benoit M, Ghigo E, Capo C, Raoult D, Mege JL (2008) The uptake of apoptotic cells drives Coxiella burnetii replication and macrophage polarization: a model for Q fever endocarditis. PLoS Pathog 4: e1000066.
10. Meghari S, Bechah Y, Capo C, Lepidi H, Raoult D, et al. (2008) Persistent Coxiella burnetii infection in mice overexpressing IL-10: an efficient model for chronic Q fever pathogenesis. PLoS Pathog 4: e23.
11. van Moll P, Baumgartner W, Eskens U, Hanichen T (1993) Immunocytochemical demonstration of Coxiella burnetii antigen in the fetal placenta of naturally infected sheep and cattle. J Comp Pathol 109: 295-301.
12. Jensen TK, Montgomery DL, Jaeger PT, Lindhardt T, Agerholm JS, et al. (2007) Application of fluorescent in situ hybridisation for demonstration of Coxiella burnetii in placentas from ruminant abortions. Apmis 115: 347-353.
13. Sanchez J, Souriau A, Buendia AJ, Arricau-Bouvery N, Martinez CM, et al. (2006) Experimental Coxiella burnetii infection in pregnant goats: a histopathological and immunohistochemical study. J Comp Pathol 135: 108-115.
14. Maidji E, Genbacev O, Chang HT, Pereira L (2007) Developmental regulation of human cytomegalovirus receptors in cytotrophoblasts correlates with distinct replication sites in the placenta. J Virol 81: 4701-4712.
15. Ferro EA, Mineo JR, Ietta F, Bechi N, Romagnoli R, et al. (2008) Macrophage migration inhibitory factor is up-regulated in human first-trimester placenta stimulated by soluble antigen of Toxoplasma gondii, resulting in increased monocyte adhesion on villous explants. Am J Pathol 172: 50-58.
16. Carvalho Neta AV, Stynen AP, Paixao TA, Miranda KL, Silva FL, et al. (2008) Modulation of the bovine trophoblastic innate immune response by Brucella abortus. Infect Immun 76: 1897-1907.
17. Haider S, Knofler M (2009) Human tumour necrosis factor: physiological and pathological roles in placenta and endometrium. Placenta 30: 111-123.
18. Lee BN, Ordonez N, Popek EJ, Lu JG, Helfgott A, et al. (1997) Inflammatory cytokine expression is correlated with the level of human immunodeficiency virus (HIV) transcripts in HIV-infected placental trophoblastic cells. J Virol 71: 3628-3635.
19. Bental T, Fejgin M, Keysary A, Rzotkiewicz S, Oron C, et al. (1995) Chronic Q fever of pregnancy presenting as Coxiella burnetii placentitis: successful outcome following therapy with erythromycin and rifampin. Clin Infect Dis 21: 1318-1321.
20. Ghigo E, Capo C, Tung CH, Raoult D, Gorvel JP, et al. (2002) Coxiella burnetii survival in THP-1 monocytes involves the impairment of phagosome maturation: IFN-c mediates its restoration and bacterial killing. J Immunol 169: 4488-4495.
21. Capo C, Lindberg FP, Meconi S, Zaffran Y, Tardei G, et al. (1999) Subversion of monocyte functions by Coxiella burnetii: impairment of the cross-talk between avb3 integrin and CR3. J Immunol 163: 6078-6085.
22. McArthur SJ, Leigh D, Marshall JT, Gee AJ, De Boer KA, et al. (2008) Blastocyst trophectoderm biopsy and preimplantation genetic diagnosis for familial monogenic disorders and chromosomal translocations. Prenat Diagn 28: 434-442.
23. Renaud SJ, Sullivan R, Graham CH (2009) Tumour necrosis factor alpha stimulates the production of monocyte chemoattractants by extravillous trophoblast cells via differential activation of MAPK pathways. Placenta 30: 313-319.
24. Ghigo E, Capo C, Raoult D, Mege JL (2001) Interleukin-10 stimulates Coxiella burnetii replication in human monocytes through tumor necrosis factor downmodulation: role in microbicidal defect of Q fever. Infect Immun 69: 2345-2352.
25. King A, Thomas L, Bischof P (2000) Cell culture models of trophoblast II: trophoblasts cell lines-a workshop report. Placenta 21(Suppl A): S113-119.
26. Pospechova K, Rozehnal V, Stejskalova L, Vrzal R, Pospisilova N, et al. (2009) Expression and activity of vitamin D receptor in the human placenta and in choriocarcinoma BeWo and JEG-3 cell lines. Mol Cell Endocrinol 299: 178-187.
27. Voth DE, Heinzen RA (2007) Lounging in a lysosome: the intracellular lifestyle of Coxiella burnetii. Cell Microbiol 9: 829-840.
28. Gorvel JP (2008) Brucella: a Mr "Hide" converted into Dr Jekyll. Microbes Infect 10: 1010-1013.
29. Naroeni A, Jouy N, Ouahrani-Bettache S, Liautard JP, Porte F (2001) Brucella suis-impaired specific recognition of phagosomes by lysosomes due to phagosomal membrane modifications. Infect Immun 69: 486-493.
30. Philips JA (2008) Mycobacterial manipulation of vacuolar sorting. Cell Microbiol 10: 2408-2415.
31. van der Wel N, Hava D, Houben D, Fluitsma D, van Zon M, et al. (2007) M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 129: 1287-1298.
32. de Chastelier C (2009) The many niches and strategies used by pathogenic mycobacteria for survival within host macrophages. Immunobiol 214: 526-42.
33. Babior BM (1999) NADPH oxidase: an update. Blood 93: 1464-1476.
34. Munn DH, Zhou M, Attwood JT, Bondarev I, Conway SJ, et al. (1998) Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281: 1191-1193.
35. Miwa N, Hayakawa S, Miyazaki S, Myojo S, Sasaki Y, et al. (2005) IDO expression on decidual and peripheral blood dendritic cells and monocytes/ macrophages after treatment with CTLA-4 or interferon-c increase in normal pregnancy but decrease in spontaneous abortion. Mol Hum Reprod 11: 865-870.
36. Benoit M, Desnues B, Mege JL (2008) Macrophage polarization in bacterial infections. J Immunol 181: 3733-3739.
37. de la Torre E, Mulla MJ, Yu AG, Lee SJ, Kavathas PB, et al. (2009) Chlamydia trachomatis infection modulates trophoblast cytokine/chemokine production. J Immunol 182: 3735-3745.
38. Straszewski-Chavez SL, Abrahams VM, Mor G (2005) The role of apoptosis in the regulation of trophoblast survival and differentiation during pregnancy. Endocr Rev 26: 877-897.
39. Dellacasagrande J, Ghigo E, Raoult D, Capo C, Mege JL (2002) IFN-c-induced apoptosis and microbicidal activity in monocytes harboring the intracellular bacterium Coxiella burnetii require membrane TNF and homotypic cell adherence. J Immunol 169: 6309-6315.
40. McArthur SJ, Leigh D, Marshall JT, Gee AJ, De Boer KA, et al. (2008) Blastocyst trophectoderm biopsy and preimplantation genetic diagnosis for familial monogenic disorders and chromosomal translocations. Prenat Diagn 28: 434-442.
41. Akutagawa O, Nishi H, Kyo S, Higuma C, Inoue M, et al. (2007) Early growth response-1 mediates up-regulation of telomerase in placenta. Placenta 28: 920-927.
42. Kenzel S, Santos-Sierra S, Deshmukh SD, Moeller I, Ergin B, et al. (2009) Role of p38 and early growth response factor 1 in the macrophage response to group B streptococcus. Infect Immun 77: 2474-2481.
43. Jiang SJ, Kuo CC, Berry MW, Lee AW, Campbell LA (2008) Identification and characterization of Chlamydia pneumoniae-specific proteins that activate tumor necrosis factor alpha production in RAW 264.7 murine macrophages. Infect Immun 76: 1558-1564.
44. Xu B, Lin L, Rote NS (1999) Identification of a stress-induced protein during human trophoblast differentiation by differential display analysis. Biol Reprod 61: 681-686.
45. Chen CP, Wang KG, Chen CY, Yu C, Chuang HC, et al. (2006) Altered placental syncytin and its receptor ASCT2 expression in placental development and pre-eclampsia. Bjog 113: 152-158.
46. Jones RL, Stoikos C, Findlay JK, Salamonsen LA (2006) TGF-b superfamily expression and actions in the endometrium and placenta. Reproduction 132: 217-232.
47. Caron PL, Frechette-Frigon G, Shooner C, Leblanc V, Asselin E (2009) Transforming growth factor beta isoforms regulation of Akt activity and XIAP levels in rat endometrium during estrous cycle, in a model of pseudopregnancy and in cultured decidual cells. Reprod Biol Endocrinol 7: 80-93.
48. Fitzgerald JS, Poehlmann TG, Schleussner E, Markert UR (2008) Trophoblast invasion: the role of intracellular cytokine signalling via signal transducer and activator of transcription 3 (STAT3). Hum Reprod Update 14: 335-344.
49. Ernst M, Inglese M, Waring P, Campbell IK, Bao S, et al. (2001) Defective gp130-mediated signal transducer and activator of transcription (STAT) signaling results in degenerative joint disease, gastrointestinal ulceration, and failure of uterine implantation. J Exp Med 194: 189-203.
50. Jiang K, Chen Y, Jarvis JN (2007) Soluble factors from LPS-and PHA-activated PBMC induce MAPK, Stat1 and Stat3 phosphorylation in primary cultures of human term placental trophoblasts: implications for infection and prematurity. Placenta 28: 538-542.
51. Catalano RD, Johnson MH, Campbell EA, Charnock-Jones DS, Smith SK, et al. (2005) Inhibition of Stat3 activation in the endometrium prevents implantation: a nonsteroidal approach to contraception. ProcNatl Acad SciUS A 102: 8585-8590.
52. Daines MO, Tabata Y, Walker BA, Chen W, Warrier MR, et al. (2006) Level of expression of IL-13Ra2 impacts receptor distribution and IL-13 signaling. J Immunol 176: 7495-7501.
53. Chiaramonte MG, Mentink-Kane M, Jacobson BA, Cheever AW, Whitters MJ, et al. (2003) Regulation and function of the interleukin 13 receptor a2 during a T helper cell type 2-dominant immune response. J Exp Med 197: 687-701.
54. Rahaman SO, Vogelbaum MA, Haque SJ (2005) Aberrant Stat3 signaling by interleukin-4 in malignant glioma cells: involvement of IL-13Ra2. Cancer Res 65: 2956-2963.
55. Andrews AL, Nasir T, Bucchieri F, Holloway JW, Holgate ST, et al. (2006) IL-13 receptor a2: a regulator of IL-13 and IL-4 signal transduction in primary human fibroblasts. J Allergy Clin Immunol 118: 858-865.
56. Glazunova O, Roux V, Freylikman O, Sekeyova Z, Fournous G, et al. (2005) Coxiella burnetii genotyping. Emerg Infect Dis 121: 1211-1217.
57. Meghari S, Berruyer C, Lepidi H, Galland F, Naquet P, et al. (2007) Vanin-1 controls granuloma formation and macrophage polarization in Coxiella burnetii infection. Eur J Immunol 37: 24-32.
58. Benoit M, Barbarat B, Bernard A, Olive D, Mege JL (2008) Coxiella burnetii, the agent of Q fever, stimulates an atypical M2 activation program in human macrophages. Eur J Immunol 38: 1065-1070.
59. Bastonero S, Le Priol Y, Armand M, Bernard CS, Reynaud-Gaubert M, et al. (2009) New microbicidal functions of tracheal glands: defective anti-infectious response to Pseudomonas aeruginosa in cystic fibrosis. PLoS ONE 4: e5357.
60. Meconi S, Capo C, Remacle-Bonnet M, Pommier G, Raoult D, et al. (2001) Activation of protein tyrosine kinases by Coxiella burnetii: role in actin cytoskeleton reorganization and bacterial phagocytosis. Infect Immun 69: 2520-2526.