Androgens enhance male urinary tract infection severity in a new model

Journal of the American Society of Nephrology

Volumn 27, Issue 6, 2016, Pages 1625-1634

  Olson, Patrick D ^a   Hruska, Keith A ^a   Hunstad, David A ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 1ALPHA; INTERLEUKIN 5; INTERLEUKIN 6; KERATINOCYTE DERIVED CHEMOKINE; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; TESTOSTERONE; TUMOR NECROSIS FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL LOAD; C3H/HE MOUSE; C57BL 6 MOUSE; COLONY FORMING UNIT; CYSTITIS; CYTOKINE RESPONSE; DISEASE PREDISPOSITION; DISEASE SEVERITY; EX VIVO STUDY; FEMALE; GONADECTOMY; IMMUNE RESPONSE; INOCULATION; KIDNEY ABSCESS; MALE; MICROBIAL COMMUNITY; MORBIDITY; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PYELONEPHRITIS; SEX DIFFERENCE; SURGICAL APPROACH; URINARY TRACT INFECTION; URINE SAMPLING; UROPATHOGENIC ESCHERICHIA COLI; ANIMAL; C3H MOUSE; C57BL MOUSE; DISEASE MODEL; ESCHERICHIA COLI INFECTIONS; MICROBIOLOGY; PHYSIOLOGY; SEVERITY OF ILLNESS INDEX; URINARY TRACT INFECTIONS;

ANDROGENS; ANIMALS; CYSTITIS; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; ESCHERICHIA COLI INFECTIONS; FEMALE; MALE; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; SEVERITY OF ILLNESS INDEX; SEX FACTORS; URINARY TRACT INFECTIONS; UROPATHOGENIC ESCHERICHIA COLI;

EID: 84992757666     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2015030327     Document Type: Article

References (66)

1. Foxman B: Epidemiology of urinary tract infections: incidence, morbidity, and economic costs. Dis Mon 49: 53-70, 2003
2. Foxman B, Klemstine KL, Brown PD: Acute pyelonephritis in US hospitals in 1997: hospitalization and in-hospital mortality. Ann Epidemiol 13: 144-150, 2003
3. Efstathiou SP, Pefanis AV, Tsioulos DI, Zacharos ID, Tsiakou AG, Mitromaras AG, Mastorantonakis SE, Kanavaki SN, Mountokalakis TD: Acute pyelonephritis in adults: prediction of mortality and failure of treatment. Arch Intern Med 163: 1206-1212, 2003
4. Nicolle LE, Friesen D, Harding GK, Roos LL: Hospitalization for acute pyelonephritis in Manitoba, Canada, during the period from 1989 to 1992; impact of diabetes, pregnancy, and aboriginal origin. Clin Infect Dis 22: 1051-1056, 1996
5. Ki M, Park T, Choi B, Foxman B: The epidemiology of acute pyelonephritis in South Korea, 1997-1999. Am J Epidemiol 160: 985-993, 2004
6. Wenninger K,Heiman JR, Rothman I, Berghuis JP, Berger RE: Sickness impact of chronic nonbacterial prostatitis and its correlates.JUrol 155: 965-968, 1996
7. Benway BM,Moon TD: Bacterial prostatitis. Urol Clin North Am35: 23-32, v, 2008
8. Domingue GJ Sr, HellstromWJ: Prostatitis. Clin Microbiol Rev 11: 604-613, 1998
9. Foxman B: The epidemiology of urinary tract infection. Nat Rev Urol 7: 653-660, 2010
10. Ulleryd P, Zackrisson B, Aus G, Bergdahl S, Hugosson J, Sandberg T: Selective urological evaluation in men with febrile urinary tract infection. BJU Int 88: 15-20, 2001
11. Hooton TM: Recurrent urinary tract infection in women. Int J Antimicrob Agents 17: 259-268, 2001
12. Hooton TM, Stapleton AE, Roberts PL,Winter C, Scholes D, Bavendam T, Stamm WE: Perineal anatomy and urine-voiding characteristics of young women with and without recurrent urinary tract infections. Clin Infect Dis 29: 1600-1601, 1999
13. Hung CS, Dodson KW, Hultgren SJ: A murine model of urinary tract infection. Nat Protoc 4: 1230-1243, 2009
14. Carey AJ, Tan CK, Ipe DS, SullivanMJ, Cripps AW, SchembriMA, Ulett GC: Urinary tract infection of mice to model human disease: Practicalities, implications and limitations. Crit Rev Microbiol 26: 1-20, 2015
15. Song J, Bishop BL, Li G, Duncan MJ, Abraham SN: TLR4-initiated and cAMP-mediated abrogation of bacterial invasion of the bladder. Cell Host Microbe 1: 287-298, 2007
16. Wright KJ, Seed PC, Hultgren SJ: Development of intracellular bacterial communities of uropathogenic Escherichia coli depends on type 1 pili. Cell Microbiol 9: 2230-2241, 2007
17. Eto DS, Gordon HB, Dhakal BK, Jones TA, Mulvey MA: Clathrin, AP-2, and the NPXY-binding subset of alternate endocytic adaptors facilitate FimH-mediated bacterial invasion of host cells. Cell Microbiol 10: 2553-2567, 2008
18. Schilling JD,MulveyMA, Vincent CD, Lorenz RG, Hultgren SJ: Bacterial invasion augments epithelial cytokine responses to Escherichia coli through a lipopolysaccharide-dependent mechanism. J Immunol 166: 1148-1155, 2001
19. Berry RE, Klumpp DJ, Schaeffer AJ: Urothelial cultures support intracellular bacterial community formation by uropathogenic Escherichia coli. Infect Immun 77: 2762-2772, 2009
20. Martinez JJ, Mulvey MA, Schilling JD, Pinkner JS, Hultgren SJ: Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. EMBO J 19: 2803-2812, 2000
21. Anderson GG, Palermo JJ, Schilling JD, Roth R, Heuser J, Hultgren SJ: Intracellular bacterial biofilm-like pods in urinary tract infections. Science 301: 105-107, 2003
22. Mulvey MA, Schilling JD, Hultgren SJ: Establishment of a persistent Escherichia coli reservoir during the acute phase of a bladder infection. Infect Immun 69: 4572-4579, 2001
23. Eto DS, Jones TA, Sundsbak JL, Mulvey MA: Integrin-mediated host cell invasion by type 1-piliated uropathogenic Escherichia coli. PLoS Pathog 3: e100, 2007
24. Duncan MJ, Li G, Shin JS, Carson JL, Abraham SN: Bacterial penetration of bladder epithelium through lipid rafts. J Biol Chem279: 18944-18951, 2004
25. Bishop BL, DuncanMJ, Song J, Li G, Zaas D, AbrahamSN: Cyclic AMPregulated exocytosis of Escherichia coli from infected bladder epithelial cells. Nat Med 13: 625-630, 2007
26. Eto DS, Sundsbak JL,MulveyMA: Actin-gated intracellular growth and resurgence of uropathogenic Escherichia coli. Cell Microbiol 8: 704-717, 2006
27. Rosen DA, Hooton TM, Stamm WE, Humphrey PA, Hultgren SJ: Detection of intracellular bacterial communities in human urinary tract infection. PLoS Med 4: e329, 2007
28. Robino L, Scavone P, Araujo L, AlgortaG, Zunino P, Vignoli R: Detection of intracellular bacterial communities in a child with Escherichia coli recurrent urinary tract infections. Pathog Dis 68: 78-81, 2013
29. Hannan TJ,Mysorekar IU, Hung CS, Isaacson-SchmidML, Hultgren SJ: Early severe inflammatory responses to uropathogenic E. coli predispose to chronic and recurrent urinary tract infection. PLoS Pathog 6: e1001042, 2010
30. Hannan TJ, Totsika M, Mansfield KJ, Moore KH, Schembri MA, Hultgren SJ: Host-pathogen checkpoints and population bottlenecks in persistent and intracellular uropathogenic Escherichia coli bladder infection. FEMS Microbiol Rev 36: 616-648, 2012
31. O'Brien VP, Hannan TJ, Schaeffer AJ, Hultgren SJ: Are you experienced? Understanding bladder innate immunity in the context of recurrent urinary tract infection. Curr Opin Infect Dis 28: 97-105, 2015
32. Schwartz DJ, Conover MS, Hannan TJ, Hultgren SJ: Uropathogenic Escherichia coli superinfection enhances the severity of mouse bladder infection. PLoS Pathog 11: e1004599, 2015
33. Boehm BJ, Colopy SA, Jerde TJ, Loftus CJ, Bushman W: Acute bacterial inflammation of the mouse prostate. Prostate 72: 307-317, 2012
34. Rudick CN, Berry RE, Johnson JR, Johnston B, Klumpp DJ, Schaeffer AJ, Thumbikat P: Uropathogenic Escherichia coli induces chronic pelvic pain. Infect Immun 79: 628-635, 2011
35. Schwartz DJ, Chen SL, Hultgren SJ, Seed PC: Population dynamics and niche distribution of uropathogenic Escherichia coli during acute and chronic urinary tract infection. Infect Immun 79: 4250-4259, 2011
36. Mysorekar IU, Hultgren SJ: Mechanisms of uropathogenic Escherichia coli persistence and eradication from the urinary tract. Proc Natl Acad Sci U S A 103: 14170-14175, 2006
37. Bowen SE, Watt CL, Murawski IJ, Gupta IR, Abraham SN: Interplay between vesicoureteric reflux and kidney infection in the development of reflux nephropathy in mice. Dis Model Mech 6: 934-941, 2013
38. Chan CY, St John AL, Abraham SN: Mast cell interleukin-10 drives localized tolerance in chronic bladder infection. Immunity 38: 349-359, 2013
39. Nicholson TF, Watts KM, Hunstad DA: OmpA of uropathogenic Escherichia coli promotes postinvasion pathogenesis of cystitis. Infect Immun 77: 5245-5251, 2009
40. Justice SS, Lauer SR, Hultgren SJ, Hunstad DA: Maturation of intracellular Escherichia coli communities requires SurA. Infect Immun 74: 4793-4800, 2006
41. TotsikaM, Kostakioti M, Hannan TJ, UptonM, Beatson SA, Janetka JW, Hultgren SJ, Schembri MA: A FimH inhibitor prevents acute bladder infection and treats chronic cystitis caused by multidrug-resistant uropathogenic Escherichia coli ST131. J Infect Dis 208: 921-928, 2013
42. Murawski IJ, Maina RW, Malo D, Guay-Woodford LM, Gros P, Fujiwara M, Morgan K, Gupta IR: The C3H/HeJ inbred mouse is a model of vesico-ureteric reflux with a susceptibility locus on chromosome 12 Kidney Int 78: 269-278, 2010
43. Robinson DP, Lorenzo ME, Jian W, Klein SL: Elevated 17b-estradiol protects females from influenza A virus pathogenesis by suppressing inflammatory responses. PLoS Pathog 7: e1002149, 2011
44. Kadioglu A, Cuppone AM, Trappetti C, List T, Spreafico A, Pozzi G, Andrew PW, Oggioni MR: Sex-based differences in susceptibility to respiratory and systemic pneumococcal disease in mice. J Infect Dis 204: 1971-1979, 2011
45. Klein SL: The effects of hormones on sex differences in infection: from genes to behavior. Neurosci Biobehav Rev 24: 627-638, 2000
46. Billington WD: The immunological problem of pregnancy: 50 years with the hope of progress. A tribute to Peter Medawar. J Reprod Immunol 60: 1-11, 2003
47. Gleicher N, Barad DH: Gender as risk factor for autoimmune diseases. J Autoimmun 28: 1-6, 2007
48. Jacobson DL, Gange SJ, Rose NR, Graham NM: Epidemiology and estimated population burden of selected autoimmune diseases in the United States. Clin Immunol Immunopathol 84: 223-243, 1997
49. Whittam TS, Wolfe ML, Wilson RA: Genetic relationships among Escherichia coli isolates causing urinary tract infections in humans and animals. Epidemiol Infect 102: 37-46, 1989
50. Johnson JR, Johnston B, Clabots CR, Kuskowski MA, Roberts E, DebRoy C: Virulence genotypes and phylogenetic background of Escherichia coli serogroup O6 isolates from humans, dogs, and cats. J ClinMicrobiol 46: 417-422, 2008
51. Bélanger L, Garenaux A, Harel J, Boulianne M, Nadeau E, Dozois CM: Escherichia coli from animal reservoirs as a potential source of human extraintestinal pathogenic E. coli. FEMS ImmunolMedMicrobiol 62: 1-10, 2011
52. Stamm WE, Raz R: Factors contributing to susceptibility of postmenopausal women to recurrent urinary tract infections. Clin Infect Dis 28: 723-725, 1999
53. Wang C, Symington JW, Ma E, Cao B, Mysorekar IU: Estrogenic modulation of uropathogenic Escherichia coli infection pathogenesis in a murine menopause model. Infect Immun 81: 733-739, 2013
54. Lüthje P, Brauner H, Ramos NL, Ovregaard A, Gläser R, Hirschberg AL, Aspenström P, Brauner A: Estrogen supports urothelial defense mechanisms. Sci Transl Med 5: 190ra80, 2013
55. Svensson M, Yadav M, Holmqvist B, Lutay N, Svanborg C, Godaly G: Acute pyelonephritis and renal scarring are caused by dysfunctional innate immunity in mCxcr2 heterozygous mice. Kidney Int 80: 1064-1072, 2011
56. Jaillon S,Moalli F, Ragnarsdottir B, Bonavita E, PuthiaM, Riva F, Barbati E, Nebuloni M, Cvetko Krajinovic L, Markotic A, Valentino S, Doni A, Tartari S, Graziani G, Montanelli A, Delneste Y, Svanborg C, Garlanda C, Mantovani A: The humoral pattern recognition molecule PTX3 is a key component of innate immunity against urinary tract infection. Immunity 40: 621-632, 2014
57. Clayton JA, Collins FS: Policy: NIH to balance sex in cell and animal studies. Nature 509: 282-283, 2014
58. Pollitzer E: Biology: Cell sex matters. Nature 500: 23-24, 2013
59. Miller VM: Why are sex and gender important to basic physiology and translational and individualized medicine? Am J Physiol Heart Circ Physiol 306: H781-H788, 2014
60. Cahill L: A half-truth is a whole lie: on the necessity of investigating sex influences on the brain. Endocrinology 153: 2541-2543, 2012
61. Drekonja DM, Rector TS, Cutting A, Johnson JR: Urinary tract infection in male veterans: treatment patterns and outcomes. JAMA Intern Med 173: 62-68, 2013
62. den Heijer CDJ, Penders J, Donker GA, Bruggeman CA, Stobberingh EE: The importance of gender-stratified antibiotic resistance surveillance of unselected uropathogens: A Dutch Nationwide Extramural Surveillance study. PLoS One 8: e60497, 2013
63. Chen SL, Hung CS, Pinkner JS, Walker JN, Cusumano CK, Li Z, Bouckaert J, Gordon JI, Hultgren SJ: Positive selection identifies an in vivo role for FimH during urinary tract infection in addition to mannose binding. Proc Natl Acad Sci U S A 106: 22439-22444, 2009
64. Mobley HL, Green DM, Trifillis AL, Johnson DE, Chippendale GR, Lockatell CV, Jones BD, Warren JW: Pyelonephritogenic Escherichia coli and killing of cultured human renal proximal tubular epithelial cells: role of hemolysin in some strains. Infect Immun 58: 1281-1289, 1990
65. Mulvey MA, Lopez-Boado YS, Wilson CL, Roth R, Parks WC, Heuser J, Hultgren SJ: Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science 282: 1494-1497, 1998
66. Ingersoll MA, Kline KA, Nielsen HV, Hultgren SJ: G-CSF induction early in uropathogenic Escherichia coli infection of the urinary tract modulates host immunity. Cell Microbiol 10: 2568-2578, 2008