Estrogen supports urothelial defense mechanisms

Science Translational Medicine

Volumn 5, Issue 190, 2013, Pages

  Lüthje, Petra ^a   Brauner, Hanna ^a   Ramos, Nubia L ^a   Övregaard, Amanda ^a   Gläser, Regine ^b   Hirschberg, Angelica Lindén ^c   Aspenström, Pontus ^a   Brauner, Annelie ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; CELL PROTEIN; ESTRADIOL; ESTROGEN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBACTERIAL ACTIVITY; ARTICLE; CELL CONTACT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EPITHELIUM CELL; ESTRADIOL BLOOD LEVEL; ESTROGEN THERAPY; FEMALE; HORMONAL REGULATION; HORMONE ACTION; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; MENSTRUATION; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PATHOGENESIS; POSTMENOPAUSE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RECURRENT INFECTION; TREATMENT DURATION; URINARY TRACT INFECTION; UROPATHOGENIC ESCHERICHIA COLI; UROTHELIUM;

ADOLESCENT; ADULT; AGED; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; CELL COMMUNICATION; CELL LINE; CELL PROLIFERATION; DIETARY SUPPLEMENTS; EPITHELIAL CELLS; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESTRADIOL; ESTROGENS; FEMALE; HUMANS; INTERCELLULAR JUNCTIONS; MICE; MICE, INBRED C57BL; MIDDLE AGED; URINARY BLADDER; UROTHELIUM; YOUNG ADULT;

EID: 84880550601     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3005574     Document Type: Article

References (56)

1. B. Foxman, R. Barlow, H. D'Arcy, B. Gillespie, J. D. Sobel, Urinary tract infection: Self-reported incidence and associated costs. Ann. Epidemiol. 10, 509-515 (2000).
2. B. Foxman, Recurring urinary tract infection: Incidence and risk factors. Am. J. Public Health 80, 331-333 (1990).
3. E. J. Dielubanza, A. J. Schaeffer, Urinary tract infections in women. Med. Clin. North Am. 95, 27-41 (2011).
4. P. L. Dwyer, M. O'Reilly, Recurrent urinary tract infection in the female. Curr. Opin. Obstet. Gynecol. 14, 537-543 (2002).
5. T. M. Hooton, Recurrent urinary tract infection in women. Int. J. Antimicrob. Agents 17, 259-268 (2001).
6. C. Sonnex, Influence of ovarian hormones on urogenital infection. Sex. Transm. Infect. 74, 11-19 (1998).
7. W. E. Stamm, R. Raz, Factors contributing to susceptibility of postmenopausal women to recurrent urinary tract infections. Clin. Infect. Dis. 28, 723-725 (1999).
8. A. Epp, A. Larochelle, D. Lovatsis, J. E. Walter, W. Easton, S. A. Farrell, L. Girouard, C. Gupta, M. A. Harvey, M. Robert, S. Ross, J. Schachter, J. A. Schulz, D.Wilkie, W. Ehman, S. Domb, A. Gagnon, O. Hughes, J. Konkin, J. Lynch, C. Marshall; Society of Obstetricians and Gynaecologists of Canada, Recurrent urinary tract infection. J. Obstet. Gynaecol. Can. 32, 1082-1101 (2010).
9. S. Salvatore, S. Salvatore, E. Cattoni, G. Siesto, M. Serati, P. Sorice, M. Torella, Urinary tract infections in women. Eur. J. Obstet. Gynecol. Reprod. Biol. 156, 131-136 (2011).
10. C. Perrotta, M. Aznar, R. Mejia, X. Albert, C. W. Ng, Oestrogens for preventing recurrent urinary tract infection in postmenopausal women. Cochrane Database Syst. Rev. 2, CD005131 (2008).
11. G. G. Anderson, J. J. Palermo, J. D. Schilling, R. Roth, J. Heuser, S. J. Hultgren, Intracellular bacterial biofilm-like pods in urinary tract infections. Science 301, 105-107 (2003).
12. S. S. Justice, C. Hung, J. A. Theriot, D. A. Fletcher, G. G. Anderson, M. J. Footer, S. J. Hultgren, Differentiation and developmental pathways of uropathogenic Escherichia coli in urinary tract pathogenesis. Proc. Natl. Acad. Sci. U.S.A. 101, 1333-1338 (2004).
13. I. U. Mysorekar, S. J. Hultgren, Mechanisms of uropathogenic Escherichia coli persistence and eradication from the urinary tract. Proc. Natl. Acad. Sci. U.S.A. 103, 14170-14175 (2006).
14. M. A. Mulvey, J. D. Schilling, S. J. Hultgren, Establishment of a persistent Escherichia coli reservoir during the acute phase of a bladder infection. Infect. Immun. 69, 4572-4579 (2001).
15. P. Veranic, R. Romih, K. Jezernik, What determines differentiation of urothelial umbrella cells? Eur. J. Cell Biol. 83, 27-34 (2004).
16. R. Romih, P. Veranic, K. Jezernik, Actin filaments during terminal differentiation of urothelial cells in the rat urinary bladder. Histochem. Cell Biol. 112, 375-380 (1999).
17. D. S. Eto, J. L. Sundsbak, M. A. Mulvey, Actin-gated intracellular growth and resurgence of uropathogenic Escherichia coli. Cell. Microbiol. 8, 704-717 (2006).
18. M. Chromek, Z. Slamová, P. Bergman, L. Kovács, L. Podracká, I. Ehrén, T. Hökfelt, G. H. Gudmundsson, R. L. Gallo, B. Agerberth, A. Brauner, The antimicrobial peptide cathelicidin protects the urinary tract against invasive bacterial infection. Nat. Med. 12, 636-641 (2006).
19. J. D. Spencer, A. L. Schwaderer, J. D. Dirosario, K. M. McHugh, G. McGillivary, S. S. Justice, A. R. Carpenter, P. B. Baker, J. Harder, D. S. Hains, Ribonuclease 7 is a potent antimicrobial peptide within the human urinary tract. Kidney Int. 80, 174-180 (2011).
20. J. D. Spencer, A. L. Schwaderer, H. Wang, J. Bartz, J. Kline, T. Eichler, K. R. Desouza, S. Sims-Lucas, P. Baker, D. S. Hains, Ribonuclease 7, an antimicrobial peptide upregulated during infection, contributes to microbial defense of the human urinary tract. Kidney Int. 83, 615-625 (2013).
21. T. Ganz, Defensins in the urinary tract and other tissues. J. Infect. Dis. 183 (Suppl. 1), S41-S42 (2001).
22. M. Østergaard, H. Wolf, T. F. Ørntoft, J. E. Celis, Psoriasin (S100A7): A putative urinary marker for the follow-up of patients with bladder squamous cell carcinomas. Electrophoresis 20, 349-354 (1999).
23. C. A. Semple, M. Rolfe, J. R. Dorin, Duplication and selection in the evolution of primate b-defensin genes. Genome Biol. 4, R31 (2003).
24. E. V. Valore, C. H. Park, A. J. Quayle, K. R. Wiles, P. B. McCray Jr., T. Ganz, Human b-defensin-1: An antimicrobial peptide of urogenital tissues. J. Clin. Invest. 101, 1633-1642 (1998).
25. D. J. Klumpp, M. T. Rycyk, M. C. Chen, P. Thumbikat, S. Sengupta, A. J. Schaeffer, Uropathogenic Escherichia coli induces extrinsic and intrinsic cascades to initiate urothelial apoptosis. Infect. Immun. 74, 5106-5113 (2006).
26. M. A. Mulvey, Y. S. Lopez-Boado, C. L. Wilson, R. Roth, W. C. Parks, J. Heuser, S. J. Hultgren, Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science 282, 1494-1497 (1998).
27. P. Thumbikat, R. E. Berry, A. J. Schaeffer, D. J. Klumpp, Differentiation-induced uroplakin III expression promotes urothelial cell death in response to uropathogenic E. coli. Microbes Infect. 11, 57-65 (2009).
28. V. Braniste, M. Leveque, C. Buisson-Brenac, L. Bueno, J. Fioramonti, E. Houdeau, Oestradiol decreases colonic permeability through oestrogen receptor b-mediated up-regulation of occludin and junctional adhesion molecule-A in epithelial cells. J. Physiol. 587, 3317-3328 (2009).
29. M. Looijer-van Langen, N. Hotte, L. A. Dieleman, E. Albert, C. Mulder, K. L. Madsen, Estrogen receptor-b signaling modulates epithelial barrier function. Am. J. Physiol. Gastrointest. Liver Physiol. 300, G621-G626 (2011).
30. J. S. Brown, E. Vittinghoff, A. M. Kanaya, S. K. Agarwal, S. Hulley, B. Foxman; Heart and Estrogen/Progestin Replacement Study Research Group, Urinary tract infections in postmenopausal women: Effect of hormone therapy and risk factors. Obstet. Gynecol. 98, 1045-1052 (2001).
31. E.M. Curran, A. H. V. Tassell, B. M. Judy, B. Nowicki, V. Montgomery-Rice,D. M. Estes, S. Nowicki, Estrogen increases menopausal host susceptibility to experimental ascending urinary-tract infection. J. Infect. Dis. 195, 680-683 (2007).
32. C. S. de Ruiz, M. R. Rey, A. P. de Ruiz Holgado, M. E. Nader-Macías, Experimental administration of estradiol on the colonization of Lactobacillus fermentum and Escherichia coli in the urogenital tract of mice. Biol. Pharm. Bull. 24, 127-134 (2001).
33. D. Robinson, L. Cardozo, Oestrogens and the lower urinary tract. BJOG 111 (Suppl. 1), 10-14 (2004).
34. R. Raz, W. E. Stamm, A controlled trial of intravaginal estriol in postmenopausal women with recurrent urinary tract infections. N. Engl. J. Med. 329, 753-756 (1993).
35. J. V. Fahey, R. M. Rossoll, C. R. Wira, Sex hormone regulation of anti-bacterial activity in rat uterine secretions and apical release of anti-bacterial factor(s) by uterine epithelial cells in culture. J. Steroid Biochem. Mol. Biol. 93, 59-66 (2005).
36. C. R. Wira, K. Merritt, Effect of the estrous cycle, castration and pseudopregnancy on E. coli in the uterus and uterine secretions of the rat. Biol. Reprod. 17, 519-522 (1977).
37. J. H. Han, M. S. Kim, M. Y. Lee, T. H. Kim, M. K. Lee, H. R. Kim, S. C. Myung, Modulation of human b-defensin-2 expression by 17b-estradiol and progesterone in vaginal epithelial cells. Cytokine 49, 209-214 (2010).
38. J. V. Fahey, T. M. Schaefer, C. R. Wira, Sex hormone modulation of human uterine epithelial cell immune responses. Integr. Comp. Biol. 46, 1082-1087 (2006).
39. T. M. Schaefer, J. V. Fahey, J. A. Wright, C. R. Wira, Innate immunity in the human female reproductive tract: Antiviral response of uterine epithelial cells to the TLR3 agonist poly(I:C). J. Immunol. 174, 992-1002 (2005).
40. S. Tang, H. Han, V. B. Bajic, ERGDB: Estrogen Responsive Genes Database. Nucleic Acids Res. 32, D533-D536 (2004).
41. C. Wang, J. W. Symington, E. Ma, B. Cao, I. U. Mysorekar, Estrogenic modulation of uropathogenic Escherichia coli infection pathogenesis in a murine menopause model. Infect. Immun. 81, 733-739 (2013).
42. L. A. Helguero, K. Lindberg, C. Gardmo, T. Schwend, J. A. Gustafsson, L. A. Haldosén, Different roles of estrogen receptors a and b in the regulation of E-cadherin protein levels in a mouse mammary epithelial cell line. Cancer Res. 68, 8695-8704 (2008).
43. J. Butmarc, T. Yufit, P. Carson, V. Falanga, Human b-defensin-2 expression is increased in chronic wounds. Wound Repair Regen. 12, 439-443 (2004).
44. J. D. Heilborn, M. F. Nilsson, G. Kratz, G. Weber, O. Sørensen, N. Borregaard, M. Ståhle-Bäckdahl, The cathelicidin anti-microbial peptide LL-37 is involved in re-epithelialization of human skin wounds and is lacking in chronic ulcer epithelium. J. Invest. Dermatol. 120, 379-389 (2003).
45. F. Niyonsaba, I. Nagaoka, H. Ogawa, Human defensins and cathelicidins in the skin: Beyond direct antimicrobial properties. Crit. Rev. Immunol. 26, 545-576 (2006).
46. K. M. Aberg, M. Q. Man, R. L. Gallo, T. Ganz, D. Crumrine, B. E. Brown, E. H. Choi, D. K. Kim, J. M. Schröder, K. R. Feingold, P. M. Elias, Co-regulation and interdependence of the mammalian epidermal permeability and antimicrobial barriers. J. Invest. Dermatol. 128, 917-925 (2008).
47. M. Kim, M. Jung, S. P. Hong, H. Jeon, M. J. Kim, M. Y. Cho, S. H. Lee, M. Q. Man, P. M. Elias, E. H. Choi, Topical calcineurin inhibitors compromise stratum corneum integrity, epidermal permeability and antimicrobial barrier function. Exp. Dermatol. 19, 501-510 (2010).
48. F. J. Byfield, M. Kowalski, K. Cruz, K. Leszczyńska, A. Namiot, P. B. Savage, R. Bucki, P. A. Janmey, Cathelicidin LL-37 increases lung epithelial cell stiffness, decreases transepithelial permeability, and prevents epithelial invasion by Pseudomonas aeruginosa. J. Immunol. 187, 6402-6409 (2011).
49. T. M. Hooton, C. Winter, F. Tiu, W. E. Stamm, Association of acute cystitis with the stage of the menstrual cycle in young women. Clin. Infect. Dis. 23, 635-636 (1996).
50. J. D. Sobel, D. Kaye, Enhancement of Escherichia coli adherence to epithelial cells derived from estrogen-stimulated rats. Infect. Immun. 53, 53-56 (1986).
51. B. Sugarman, L. R. Epps, Effect of estrogens on bacterial adherence to HeLa cells. Infect. Immun. 35, 633-638 (1982).
52. L. Hagberg, I. Engberg, R. Freter, J. Lam, S. Olling, C. Svanborg Edén, Ascending, unobstructed urinary tract infection in mice caused by pyelonephritogenic Escherichia coli of human origin. Infect. Immun. 40, 273-283 (1983).
53. Y. Kai-Larsen, P. Lüthje, M. Chromek, V. Peters, X. Wang, Å. Holm, L. Kádas, K. O. Hedlund, J. Johansson, M. R. Chapman, S. H. Jacobson, U. Römling, B. Agerberth, A. Brauner, Uropathogenic Escherichia coli modulates immune responses and its curli fimbriae interact with the antimicrobial peptide LL-37. PLoS Pathog. 6, e1001010 (2010).
54. O. Hertting, Å. Holm, P. Lüthje, H. Brauner, R. Dyrdak, A. F. Jonasson, P. Wiklund, M. Chromek, A. Brauner, Vitamin D induction of the human antimicrobial peptide cathelicidin in the urinary bladder. PLoS One 5, e15580 (2010).
55. B. Köten, M. Simanski, R. Gläser, R. Podschun, J. M. Schröder, J. Harder, RNase 7 contributes to the cutaneous defense against Enterococcus faecium. PLoS One 4, e6424 (2009).
56. F. Fortin, T. Anghel, P. Brochu, N. Lemieux, Optimizing urothelial cell preparation for the human urinary micronucleus assay. Toxicol. In Vitro 24, 1821-1827 (2010).