Human Bladder Uroepithelial Cells Synergize with Monocytes to Promote IL-10 Synthesis and Other Cytokine Responses to Uropathogenic Escherichia coli

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Duell, Benjamin L ^a   Carey, Alison J ^a   Dando, Samantha J ^a   Schembri, Mark A ^b   Ulett, Glen C ^a  

^a GRIFFITH UNIVERSITY   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; EOTAXIN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 6; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PLATELET DERIVED GROWTH FACTOR BB; RANTES; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BLADDER EPITHELIUM; BLADDER UROEPITHELIAL CELL; CELL MEMBRANE; CELL TYPE; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EPITHELIUM CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; MONOCYTE; NONHUMAN; PATHOGENESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; URINARY TRACT INFECTION; UROPATHOGENIC ESCHERICHIA COLI;

BIOLOGICAL MARKERS; CELL COMMUNICATION; CELL LINE; COCULTURE TECHNIQUES; EPITHELIAL CELLS; ESCHERICHIA COLI INFECTIONS; FEMALE; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-10; MACROPHAGES; MONOCYTES; RNA, MESSENGER; SOLUBILITY; URINARY BLADDER; UROPATHOGENIC ESCHERICHIA COLI; UROTHELIUM;

EID: 84885417061     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0078013     Document Type: Article

References (64)

1. DeFrances CJ, Hall MJ, (2004) 2002 National Hospital Discharge Survey. Adv Data: pp. 1-29. PubMed: 15174387.
2. Foxman B, (2002) Epidemiology of urinary tract infections: incidence, morbidity, and economic costs. Am J Med 113 (Suppl 1A):: 5S-13S. doi:10.1016/S0002-9343(02)01054-9. PubMed: 1211386612601337.
3. Bacheller CD, Bernstein JM, (1997) Urinary tract infections. Med Clin North Am 81: 719-730. doi:10.1016/S0025-7125(05)70542-3. PubMed: 9167654.
4. Ronald A, (2002) The etiology of urinary tract infection: traditional and emerging pathogens. Am J Med 113 (Suppl 1A):: 14S-19S. doi:10.1016/S0002-9343(02)01055-0. PubMed: 12113867.
5. Ipe DS, Sundac L, Benjamin WH Jr, Moore KH, Ulett GC, (2013) Asymptomatic bacteriuria: prevalence rates of causal microbes, etiology of infection in different patient populations, and recent advances in molecular detection. FEMS Microbiol Lett 346: 1-10. doi:10.1111/1574-6968.12204. PubMed: 23808987.
6. Aboderin OA, Abdu AR, Odetoyin BW, Lamikanra A, (2009) Antimicrobial resistance in Escherichia coli strains from urinary tract infections. J Natl Med Assoc 101: 1268-1273. PubMed: 20070015.
7. Foxman B, (2010) The epidemiology of urinary tract infection. Nat. Rev Urol 7: 653-660. doi:10.1038/nrurol.2010.190.
8. Ulett GC, Totsika M, Schaale K, Carey AJ, Sweet MJ, et al. (2013) Uropathogenic Escherichia coli virulence and innate immune responses during urinary tract infection. Curr Opin Microbiol 16: 100-107. doi:10.1016/j.mib.2013.01.005. PubMed: 23403118.
9. Nielubowicz GR, Mobley HL, (2010) Host-pathogen interactions in urinary tract infection. Nat. Rev Urol 7: 430-441. doi:10.1038/nrurol.2010.101.
10. Sivick KE, Mobley HL, (2010) Waging war against uropathogenic Escherichia coli: winning back the urinary tract. Infect Immun 78: 568-585. doi:10.1128/IAI.01000-09. PubMed: 19917708.
11. Hannan TJ, Totsika M, Mansfield KJ, Moore KH, Schembri MA, et al. (2012) Host-pathogen checkpoints and population bottlenecks in persistent and intracellular uropathogenic Escherichia coli bladder infection. FEMS Microbiol Rev 36: 616-648. doi:10.1111/j.1574-6976.2012.00339.x. PubMed: 22404313.
12. Duell BL, Carey AJ, Tan CK, Cui X, Webb RI, et al. (2012) Innate transcriptional networks activated in bladder in response to uropathogenic Escherichia coli drive diverse biological pathways and rapid synthesis of IL-10 for defense against bacterial urinary tract infection. J Immunol 188: 781-792. doi:10.4049/jimmunol.1101231. PubMed: 22184725.
13. Mittal R, Sharma S, Chhibber S, Harjai K, (2009) Evaluation of interleukin-10 production in Pseudomonas aeruginosa induced acute pyelonephritis. J Infect Public Health 2: 136-140. PubMed: 20701873.
14. Kline KA, Schwartz DJ, Lewis WG, Hultgren SJ, Lewis AL, (2011) Immune activation and suppression by group B streptococcus in a murine model of urinary tract infection. Infect Immun 79: 3588-3595. doi:10.1128/IAI.00122-11. PubMed: 21690238.
15. Couper KN, Blount DG, Riley EM, (2008) IL-10: the master regulator of immunity to infection. J Immunol 180: 5771-5777. PubMed: 18424693.
16. Duell BL, Tan CK, Carey AJ, Wu F, Cripps AW, et al. (2012) Recent insights into microbial triggers of interleukin-10 production in the host and the impact on infectious disease pathogenesis. FEMS Immunol Med Microbiol 64: 295-313. doi:10.1111/j.1574-695X.2012.00931.x. PubMed: 22268692.
17. Stanley AC, Lieu ZZ, Wall AA, Venturato J, Khromykh T, et al. (2012) Recycling endosome-dependent and-independent mechanisms for IL-10 secretion in LPS-activated macrophages. J Leukoc Biol 92: 1227-1239. doi:10.1189/jlb.0412191. PubMed: 23012430.
18. Chan CY, St John AL, Abraham SN, (2013) Mast cell interleukin-10 drives localized tolerance in chronic bladder infection. Immunity 38: 349-359. doi:10.1016/j.immuni.2012.10.019. PubMed: 23415912.
19. Mulvey MA, Schilling JD, Hultgren SJ, (2001) Establishment of a persistent Escherichia coli reservoir during the acute phase of a bladder infection. Infect Immun 69: 4572-4579. doi:10.1128/IAI.69.7.4572-4579.2001. PubMed: 11402001.
20. Andersen TE, Khandige S, Madelung M, Brewer J, Kolmos HJ, et al. (2012) Escherichia coli uropathogenesis in vitro: invasion, cellular escape, and secondary infection analyzed in a human bladder cell infection model. Infect Immun 80: 1858-1867. doi:10.1128/IAI.06075-11. PubMed: 22354025.
21. Klumpp DJ, Weiser AC, Sengupta S, Forrestal SG, Batler RA, et al. (2001) Uropathogenic Escherichia coli potentiates type 1 pilus-induced apoptosis by suppressing NF-kappaB. Infect Immun 69: 6689-6695. doi:10.1128/IAI.69.11.6689-6695.2001. PubMed: 11598039.
22. Blango MG, Mulvey MA, (2010) Persistence of uropathogenic Escherichia coli in the face of multiple antibiotics. Antimicrob Agents Chemother 54: 1855-1863. doi:10.1128/AAC.00014-10. PubMed: 20231390.
23. Thumbikat P, Berry RE, Zhou G, Billips BK, Yaggie RE, et al. (2009) Bacteria-induced uroplakin signaling mediates bladder response to infection. PLOS Pathog 5: e1000415. PubMed: 19412341.
24. Eto DS, Jones TA, Sundsbak JL, Mulvey MA, (2007) Integrin-mediated host cell invasion by type 1-piliated uropathogenic Escherichia coli. PLOS Pathog 3: e100. doi:10.1371/journal.ppat.0030100. PubMed: 17630833.
25. Svanborg C, Bergsten G, Fischer H, Godaly G, Gustafsson M, et al. (2006) Uropathogenic Escherichia coli as a model of host-parasite interaction. Curr Opin Microbiol 9: 33-39. doi:10.1016/j.mib.2005.12.012. PubMed: 16406777.
26. Fazliana M, Ramos NL, Lüthje P, Sekikubo M, Holm A, et al. (2011) Labisia pumila var. alata reduces bacterial load by inducing uroepithelial cell apoptosis. J Ethnopharmacol 136: 111-116. doi:10.1016/j.jep.2011.04.018. PubMed: 21524700.
27. Martinez JJ, Mulvey MA, Schilling JD, Pinkner JS, Hultgren SJ, (2000) Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. EMBO J 19: 2803-2812. doi:10.1093/emboj/19.12.2803. PubMed: 10856226.
28. Hilbert DW, Paulish-Miller TE, Tan CK, Carey AJ, Ulett GC, et al. (2012) Clinical Escherichia coli isolates utilize alpha-hemolysin to inhibit in vitro epithelial cytokine production. Microbes Infect 14: 628-638. doi:10.1016/j.micinf.2012.01.010. PubMed: 22326301.
29. Hilbert DW, Pascal KE, Libby EK, Mordechai E, Adelson ME, et al. (2008) Uropathogenic Escherichia coli dominantly suppress the innate immune response of bladder epithelial cells by a lipopolysaccharide- and Toll-like receptor 4-independent pathway. Microbes Infect 10: 114-121. doi:10.1016/j.micinf.2007.10.012. PubMed: 18248759.
30. Billips BK, Forrestal SG, Rycyk MT, Johnson JR, Klumpp DJ, et al. (2007) Modulation of host innate immune response in the bladder by uropathogenic Escherichia coli. Infect Immun 75: 5353-5360. doi:10.1128/IAI.00922-07. PubMed: 17724068.
31. Barrila J, Radtke AL, Crabbé A, Sarker SF, Herbst-Kralovetz MM, et al. (2010) Organotypic 3D cell culture models: using the rotating wall vessel to study host-pathogen interactions. Nat Rev Microbiol 8: 791-801. doi:10.1038/nrmicro2423. PubMed: 20948552.
32. Duell BL, Cripps AW, Schembri MA, Ulett GC, (2011) Epithelial cell coculture models for studying infectious diseases: benefits and limitations. J Biomed Biotechnol(2011): pp. 852419. PubMed: 22007147.
33. Smith YC, Grande KK, Rasmussen SB, O'Brien AD, (2006) Novel three-dimensional organoid model for evaluation of the interaction of uropathogenic Escherichia coli with terminally differentiated human urothelial cells. Infect Immun 74: 750-757. doi:10.1128/IAI.74.1.750-757.2006. PubMed: 16369034.
34. Ulett GC, Adderson EE, (2005) Nitric oxide is a key determinant of group B streptococcus-induced murine macrophage apoptosis. J Infect Dis 191: 1761-1770. doi:10.1086/429693. PubMed: 15838805.
35. Mobley HL, Green DM, Trifillis AL, Johnson DE, Chippendale GR, et al. (1990) Pyelonephritogenic Escherichia coli and killing of cultured human renal proximal tubular epithelial cells: role of hemolysin in some strains. Infect Immun 58: 1281-1289. PubMed: 2182540.
36. Khalil A, Brauner A, Bakhiet M, Burman LG, Jaremko G, et al. (1997) Cytokine gene expression during experimental Escherichia coli pyelonephritis in mice. J Urol 158: 1576-1580. doi:10.1016/S0022-5347(01)64282-4. PubMed: 9302176.
37. Lloyd AL, Smith SN, Eaton KA, Mobley HL, (2009) Uropathogenic Escherichia coli suppresses the host inflammatory response via pathogenicity island genes sisA and sisB. Infect Immun 77: 5322-5333. doi:10.1128/IAI.00779-09. PubMed: 19797063.
38. Ulett GC, Valle J, Beloin C, Sherlock O, Ghigo JM, et al. (2007) Functional analysis of antigen 43 in uropathogenic Escherichia coli reveals a role in long-term persistence in the urinary tract. Infect Immun 75: 3233-3244. doi:10.1128/IAI.01952-06. PubMed: 17420234.
39. Yadav M, Zhang J, Fischer H, Huang W, Lutay N, et al. (2010) Inhibition of TIR domain signaling by TcpC: MyD88-dependent and independent effects on Escherichia coli virulence. PLOS Pathog 6: e1001120. PubMed: 20886104.
40. Pfaffl MW, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45. doi:10.1093/nar/29.9.e45. PubMed: 11328886.
41. Pfaffl MW, Horgan GW, Dempfle L, (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30: e36. doi:10.1093/nar/30.9.e36. PubMed: 11972351.
42. Ulett GC, Webb RI, Ulett KB, Cui X, Benjamin WH, et al. (2010) Group B Streptococcus (GBS) urinary tract infection involves binding of GBS to bladder uroepithelium and potent but GBS-specific induction of interleukin 1alpha. J Infect Dis 201: 866-870. doi:10.1086/650696. PubMed: 20132033.
43. Benjamin D, Knobloch TJ, Dayton MA, (1992) Human B-cell interleukin-10: B-cell lines derived from patients with acquired immunodeficiency syndrome and Burkitt's lymphoma constitutively secrete large quantities of interleukin-10. Blood 80: 1289-1298. PubMed: 1325212.
44. Cavaillon JM, Fitting C, Haeffner-Cavaillon N, Kirsch SJ, Warren HS, (1990) Cytokine response by monocytes and macrophages to free and lipoprotein-bound lipopolysaccharide. Infect Immun 58: 2375-2382. PubMed: 2114366.
45. Hannan TJ, Riehl T, Schwartz D, Binkley J, Roberts P, et al. (2013) Inflammatory monocyte recruitment and cyclooxygenase 2-dependent inflammation contribute to severe acute, chronic and recurrent cystitis. Clinical and Scientific Advances in Urinary Tract Infections Conference. Columbus, Ohio.
46. Tan CK, Carey AJ, Cui X, Webb RI, Ipe D, et al. (2012) Genome-wide mapping of cystitis due to Streptococcus agalactiae and Escherichia coli in mice identifies a unique bladder transcriptome that signifies pathogen-specific antimicrobial defense against urinary tract infection. Infect Immun 80: 3145-3160. doi:10.1128/IAI.00023-12. PubMed: 22733575.
47. Bokil NJ, Totsika M, Carey AJ, Stacey KJ, Hancock V, et al. (2011) Intramacrophage survival of uropathogenic Escherichia coli: differences between diverse clinical isolates and between mouse and human macrophages. Immunobiology 216: 1164-1171. doi:10.1016/j.imbio.2011.05.011. PubMed: 21802164.
48. Gardiner RA, Seymour GJ, Lavin MF, Strutton GM, Gemmell E, et al. (1986) Immunohistochemical analysis of the human bladder. Br J Urol 58: 19-25. doi:10.1111/j.1464-410X.1986.tb05420.x. PubMed: 2936415.
49. Sunderkötter C, Nikolic T, Dillon MJ, Van Rooijen N, Stehling M, et al. (2004) Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J Immunol 172: 4410-4417. PubMed: 15034056.
50. Ingersoll MA, Platt AM, Potteaux S, Randolph GJ, (2011) Monocyte trafficking in acute and chronic inflammation. Trends Immunol 32: 470-477. doi:10.1016/j.it.2011.05.001. PubMed: 21664185.
51. Shi C, Pamer EG, (2011) Monocyte recruitment during infection and inflammation. Nat Rev Immunol 11: 762-774. doi:10.1038/nri3070. PubMed: 21984070.
52. Herold S, von Wulffen W, Steinmueller M, Pleschka S, Kuziel WA, et al. (2006) Alveolar epithelial cells direct monocyte transepithelial migration upon influenza virus infection: impact of chemokines and adhesion molecules. J Immunol 177: 1817-1824. PubMed: 16849492.
53. Eghtesad M, Jackson HE, Cunningham AC, (2001) Primary human alveolar epithelial cells can elicit the transendothelial migration of CD14+ monocytes and CD3+ lymphocytes. Immunology 102: 157-164. doi:10.1046/j.1365-2567.2001.01172.x. PubMed: 11260320.
54. Mäkelä SM, Strengell M, Pietilä TE, Osterlund P, Julkunen I, (2009) Multiple signaling pathways contribute to synergistic TLR ligand-dependent cytokine gene expression in human monocyte-derived macrophages and dendritic cells. J Leukoc Biol 85: 664-672. doi:10.1189/jlb.0808503. PubMed: 19164128.
55. Ting Tan RS, Lin B, Liu Q, Tucker-Kellogg L, Ho B, et al. (2013) The synergy in cytokine production through MyD88-TRIF pathways is co-ordinated with ERK phosphorylation in macrophages. Immunol Cell Biol 91: 377-387. doi:10.1038/icb.2013.13. PubMed: 23567895.
56. Gouwy M, Struyf S, Proost P, Van Damme J, (2005) Synergy in cytokine and chemokine networks amplifies the inflammatory response. Cytokine Growth Factor Rev 16: 561-580. doi:10.1016/j.cytogfr.2005.03.005. PubMed: 16023396.
57. Bien J, Sokolova O, Bozko P, (2012) Role of Uropathogenic Escherichia coli virulence factors in development of urinary tract infection and kidney damage. Int J Nephrol(2012): pp. 681473. PubMed: 22506110.
58. Ingersoll MA, Kline KA, Nielsen HV, Hultgren SJ, (2008) G-CSF induction early in uropathogenic Escherichia coli infection of the urinary tract modulates host immunity. Cell Microbiol 10: 2568-2578. doi:10.1111/j.1462-5822.2008.01230.x. PubMed: 18754853.
59. Andersson M, Lutay N, Hallgren O, Westergren-Thorsson G, Svensson M, et al. (2012) Mycobacterium bovis bacilli Calmette-Guerin regulates leukocyte recruitment by modulating alveolar inflammatory responses. Innate Immun 18: 531-540. doi:10.1177/1753425911426591. PubMed: 22058091.
60. Sawant KV, McMurray DN, (2007) Guinea pig neutrophils infected with Mycobacterium tuberculosis produce cytokines which activate alveolar macrophages in noncontact cultures. Infect Immun 75: 1870-1877. doi:10.1128/IAI.00858-06. PubMed: 17283104.
61. Fedele G, Bianco M, Debrie AS, Locht C, Ausiello CM, (2011) Attenuated Bordetella pertussis vaccine candidate BPZE1 promotes human dendritic cell CCL21-induced migration and drives a Th1/Th17 response. J Immunol 186: 5388-5396. doi:10.4049/jimmunol.1003765. PubMed: 21430219.
62. Vargas-Inchaustegui DA, Hogg AE, Tulliano G, Llanos-Cuentas A, Arevalo J, et al. (2010) CXCL10 production by human monocytes in response to Leishmania braziliensis infection. Infect Immun 78: 301-308. doi:10.1128/IAI.00959-09. PubMed: 19901067.
63. Krueger S, Kuester D, Bernhardt A, Wex T, Roessner A, (2009) Regulation of cathepsin X overexpression in H. pylori-infected gastric epithelial cells and macrophages. J Pathol 217: 581-588. doi:10.1002/path.2485. PubMed: 19090485.
64. Ulett GC, Ketheesan N, Hirst RG, (1998) Macrophage-lymphocyte interactions mediate anti-Burkholderia pseudomallei activity. FEMS Immunol Med Microbiol 21: 283-286. doi:10.1111/j.1574-695X.1998.tb01175.x. PubMed: 9753000.