Novel strategies in the prevention and treatment of urinary tract infections

Pathogens

Volumn 5, Issue 1, 2016, Pages

  Lüthje, Petra ^a   Brauner, Annelie ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Antimicrobial peptides; Estrogen; Herbal extracts; Urinary tract infection; Vitamin D

Indexed keywords

ADHESIN; ADHESIN ANTIGEN 43; ALPHA DEFENSIN; ANTIBIOTIC AGENT; ARMORACIAE RUSTICANAE EXTRACT; BETA DEFENSIN; BETULA EXTRACT; CATHELICIDIN; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; CIPROFLOXACIN; CITRUS RETICULATA EXTRACT; ESTROGEN; GYNOSTEMMA PENTAPHYLLUM EXTRACT; IBUPROFEN; LABISIA PUMILA EXTRACT; LACTOFERRIN; LIPOPOLYSACCHARIDE; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; ORTHOSIPHON STAMINEUS EXTRACT; PLANT EXTRACT; POLYPEPTIDE ANTIBIOTIC AGENT; RIBONUCLEASE; TROPAEOLI MAJORIS EXTRACT; UNCLASSIFIED DRUG; UROPLAKIN; URTICA EXTRACT; VITAMIN D;

ANTIBIOTIC RESISTANCE; ANTIMICROBIAL ACTIVITY; BACTERIAL STRAIN; BACTERICIDAL ACTIVITY; BIOFILM; CELLULAR IMMUNITY; ESCHERICHIA COLI; EXTRACELLULAR TRAP; HERB; HUMAN; IMMUNOMODULATION; INNATE IMMUNITY; MICROBIAL COMMUNITY; NONHUMAN; QUIESCENT INTRACELLULAR RESERVOIR; REVIEW; SIGNAL TRANSDUCTION; URINARY TRACT INFECTION;

EID: 85010886615     PISSN: None     EISSN: 20760817     Source Type: Journal    
DOI: 10.3390/pathogens5010013     Document Type: Review

References (125)

1. Foxman, B.; Barlow, R.; D'Arcy, H.; Gillespie, B.; Sobel, J.D. Urinary tract infection: Self-reported incidenceand associated costs. Ann. Epidemiol. 2000, 10, 509-515. [CrossRef].
2. Foxman, B. Urinary tract infection syndromes: Occurrence, recurrence, bacteriology, risk factors, and diseaseburden. Infect. Dis. Clin. N. Am. 2014, 28, 1-13. [CrossRef] [PubMed].
3. Hoberman, A.; Chao, H.P.; Keller, D.M.; Hickey, R.; Davis, H.W.; Ellis, D. Prevalence of urinary tract infectionin febrile infants. J. Pediatr. 1993, 123, 17-23. [CrossRef].
4. Shaw, K.N.; Gorelick, M.; McGowan, K.L.; Yakscoe, N.M.; Schwartz, J.S. Prevalence of urinary tract infectionin febrile young children in the emergency department. Pediatrics 1998. [CrossRef].
5. Zorc, J.J.; Levine, D.A.; Platt, S.L.; Dayan, P.S.; Macias, C.G.; Krief, W.; Schor, J.; Bank, D.; Shaw, K.N.;Kuppermann, N.; et al. Clinical and demographic factors associated with urinary tract infection in youngfebrile infants. Pediatrics 2005, 116, 644-648. [CrossRef] [PubMed].
6. Marild, S.; Jodal, U. Incidence rate of first-time symptomatic urinary tract infection in children under 6 yearsof age. Acta Paediatr. 1998, 87, 549-552. [CrossRef] [PubMed].
7. Stokland, E.; Hellstrom, M.; Jacobsson, B.; Jodal, U.; Sixt, R. Renal damage one year after first urinary tractinfection: Role of dimercaptosuccinic acid scintigraphy. J. Pediatr. 1996, 129, 815-820. [CrossRef].
8. Stokland, E.; Hellstrom, M.; Jacobsson, B.; Jodal, U.; Sixt, R. Evaluation of DMSA scintigraphy and urographyin assessing both acute and permanent renal damage in children. Acta Radiol. 1998, 39, 447-452. [CrossRef][PubMed].
9. Saxton, H.M. Computed tomography or intravenous urography for renal damage in childhood urinaryinfection? Pediatr. Nephrol. 1995, 9, 256-257. [CrossRef] [PubMed].
10. Kavanagh, E.C.; Ryan, S.; Awan, A.; McCourbrey, S.; O'Connor, R.; Donoghue, V. Can MRI replace DMSA inthe detection of renal parenchymal defects in children with urinary tract infections? Pediatr Radiol 2005, 35,275-281. [CrossRef] [PubMed].
11. Winberg, J.; Andersen, H.J.; Bergstrom, T.; Jacobsson, B.; Larson, H.; Lincoln, K. Epidemiology ofsymptomatic urinary tract infection in childhood. Acta Paediatr. Scand. Suppl. 1974, 63, 1-20. [CrossRef].
12. Mingin, G.C.; Hinds, A.; Nguyen, H.T.; Baskin, L.S. Children with a febrile urinary tract infection anda negative radiologic workup: Factors predictive of recurrence. Urology 2004, 63, 562-565. [CrossRef][PubMed].
13. Ramos, N.L.; Dzung, D.T.; Stopsack, K.; Janko, V.; Pourshafie, M.R.; Katouli, M.; Brauner, A. Characterisationof uropathogenic Escherichia coli from children with urinary tract infection in different countries. Eur. J. Clin.Microbiol. Infect. Dis. 2011, 30, 1587-1593. [CrossRef] [PubMed].
14. Ramos, N.L.; Sekikubo, M.; Dzung, D.T.; Kosnopfel, C.; Kironde, F.; Mirembe, F.; Brauner, A. UropathogenicEscherichia coli isolates from pregnant women in different countries. J. Clin. Microbiol. 2012, 50, 3569-3574.[CrossRef] [PubMed].
15. Joo, H.S.; Otto, M. Mechanisms of resistance to antimicrobial peptides in staphylococci. Biochim. Biophys. Acta2015. [CrossRef] [PubMed].
16. Gruenheid, S.; Le Moual, H. Resistance to antimicrobial peptides in gram-negative bacteria. FEMS Microbiol. Lett.2012, 330, 81-89. [CrossRef] [PubMed].
17. Galdiero, S.; Falanga, A.; Berisio, R.; Grieco, P.; Morelli, G.; Galdiero, M. Antimicrobial peptides as anopportunity against bacterial diseases. Curr. Med. Chem. 2015, 22, 1665-1677. [CrossRef] [PubMed].
18. Niyonsaba, F.; Nagaoka, I.; Ogawa, H. Human defensins and cathelicidins in the skin: Beyond directantimicrobial properties. Crit. Rev. Immunol. 2006, 26, 545-576. [CrossRef] [PubMed].
19. Bowdish, D.M.; Davidson, D.J.; Hancock, R.E. A re-evaluation of the role of host defence peptides inmammalian immunity. Curr. Protein Pept. Sci. 2005, 6, 35-51. [CrossRef] [PubMed].
20. Heilborn, J.D.; Nilsson, M.F.; Weber, G.; Sorensen, O.; Borregaard, N.; Stahle-Backdahl, M.; Kratz, G.The cathelicidin anti-microbial peptide LL-37 is involved in re-epithelialization of human skin wounds andis lacking in chronic ulcer epithelium. J. Investig. Dermatol. 2003, 120, 379-389. [CrossRef] [PubMed].
21. Butmarc, J.; Yufit, T.; Carson, P.; Falanga, V. Human beta-defensin-2 expression is increased in chronicwounds. Wound Repair Regen. 2004, 12, 439-443. [CrossRef] [PubMed].
22. Aberg, K.M.; Man, M.Q.; Gallo, R.L.; Ganz, T.; Crumrine, D.; Brown, B.E.; Choi, E.H.; Kim, D.K.;Schroder, J.M.; Feingold, K.R.; et al. Co-regulation and interdependence of the mammalian epidermalpermeability and antimicrobial barriers. J. Investig. Dermatol. 2008, 128, 917-925. [CrossRef] [PubMed].
23. Ejrnaes, K.; Sandvang, D.; Lundgren, B.; Ferry, S.; Holm, S.; Lundholm, R.; Frimodt-Moller, N.; Monsen, T.Pulsed-field gel electrophoresis typing of Escherichia coli strains from samples collected before and afterpivmecillinam or placebo treatment of uncomplicated community-acquired urinary tract infection in women.J. Clin. Microbiol. 2006, 44, 1776-1781. [CrossRef] [PubMed].
24. Navas-Nacher, E.L.; Dardick, F.; Venegas, M.F.; Anderson, B.E.; Schaeffer, A.J.; Duncan, J.L. Relatedness ofEscherichia coli colonizing women longitudinally. Mol. Urol. 2001, 5, 31-36. [CrossRef] [PubMed].
25. Norinder, B.S.; Lüthje, P.; Yadav, M.; Kadas, L.; Fang, H.; Nord, C.E.; Brauner, A. Cellulose and papg areimportant for Escherichia coli causing recurrent urinary tract infection in women. Infection 2011, 39, 571-574.[CrossRef] [PubMed].
26. Nielsen, K.L.; Dynesen, P.; Larsen, P.; Frimodt-Moller, N. Faecal Escherichia coli from patients with E. coliurinary tract infection and healthy controls who have never had a urinary tract infection. J. Med. Microbiol.2014, 63, 582-589. [CrossRef] [PubMed].
27. Anderson, G.G.; Palermo, J.J.; Schilling, J.D.; Roth, R.; Heuser, J.; Hultgren, S.J. Intracellular bacterialbiofilm-like pods in urinary tract infections. Science 2003, 301, 105-107. [CrossRef] [PubMed].
28. Justice, S.S.; Hung, C.; Theriot, J.A.; Fletcher, D.A.; Anderson, G.G.; Footer, M.J.; Hultgren, S.J. Differentiationand developmental pathways of uropathogenic Escherichia coli in urinary tract pathogenesis. Proc. Natl. Acad.Sci. USA 2004, 101, 1333-1338. [CrossRef] [PubMed].
29. Klumpp, D.J.; Rycyk, M.T.; Chen, M.C.; Thumbikat, P.; Sengupta, S.; Schaeffer, A.J. Uropathogenic Escherichiacoli induces extrinsic and intrinsic cascades to initiate urothelial apoptosis. Infect. Immun. 2006, 74, 5106-5113.[CrossRef] [PubMed].
30. Thumbikat, P.; Berry, R.E.; Schaeffer, A.J.; Klumpp, D.J. Differentiation-induced uroplakin iii expressionpromotes urothelial cell death in response to uropathogenic E. coli. Microbes Infect. 2009, 11, 57-65. [CrossRef][PubMed].
31. Eto, D.S.; Sundsbak, J.L.; Mulvey, M.A. Actin-gated intracellular growth and resurgence of uropathogenicEscherichia coli. Cell. Microbiol. 2006, 8, 704-717. [CrossRef] [PubMed].
32. Mysorekar, I.U.; Mulvey, M.A.; Hultgren, S.J.; Gordon, J.I. Molecular regulation of urothelial renewal andhost defenses during infection with uropathogenic Escherichia coli. J. Biol. Chem. 2002, 277, 7412-7419.[CrossRef] [PubMed].
33. Mulvey, M.A.; Schilling, J.D.; Hultgren, S.J. Establishment of a persistent Escherichia coli reservoir during theacute phase of a bladder infection. Infect. Immun. 2001, 69, 4572-4579. [CrossRef] [PubMed].
34. Rosen, D.A.; Hooton, T.M.; Stamm,W.E.; Humphrey, P.A.; Hultgren, S.J. Detection of intracellular bacterialcommunities in human urinary tract infection. PLoS Med. 2007, 4, e329. [CrossRef] [PubMed].
35. Garofalo, C.K.; Hooton, T.M.; Martin, S.M.; Stamm, W.E.; Palermo, J.J.; Gordon, J.I.; Hultgren, S.J.Escherichia coli from urine of female patients with urinary tract infections is competent for intracellularbacterial community formation. Infect. Immun. 2007, 75, 52-60. [CrossRef] [PubMed].
36. Robino, L.; Scavone, P.; Araujo, L.; Algorta, G.; Zunino, P.; Pirez, M.C.; Vignoli, R. Intracellular bacteria inthe pathogenesis of Escherichia coli urinary tract infection in children. Clin. Infect. Dis. 2014, 59, e158-e164.[CrossRef] [PubMed].
37. Robino, L.; Scavone, P.; Araujo, L.; Algorta, G.; Zunino, P.; Vignoli, R. Detection of intracellular bacterialcommunities in a child with Escherichia coli recurrent urinary tract infections. Pathog. Dis. 2013, 68, 78-81.[CrossRef] [PubMed].
38. Conway, P.H.; Cnaan, A.; Zaoutis, T.; Henry, B.V.; Grundmeier, R.W.; Keren, R. Recurrent urinary tractinfections in children: Risk factors and association with prophylactic antimicrobials. JAMA 2007, 298,179-186. [CrossRef] [PubMed].
39. Nuutinen, M.; Uhari, M. Recurrence and follow-up after urinary tract infection under the age of 1 year.Pediatr. Nephrol. 2001, 16, 69-72. [CrossRef] [PubMed].
40. Godaly, G.; Ambite, I.; Svanborg, C. Innate immunity and genetic determinants of urinary tract infectionsusceptibility. Curr. Opin. Infect. Dis. 2015, 28, 88-96. [CrossRef] [PubMed].
41. Ulett, G.C.; Valle, J.; Beloin, C.; Sherlock, O.; Ghigo, J.M.; Schembri, M.A. Functional analysis of antigen 43 inuropathogenic Escherichia coli reveals a role in long-term persistence in the urinary tract. Infect. Immun. 2007,75, 3233-3244. [CrossRef] [PubMed].
42. Lüthje, P.; Brauner, A. Ag43 promotes persistence of uropathogenic Escherichia coli isolates in the urinarytract. J. Clin. Microbiol. 2010, 48, 2316-2317. [CrossRef] [PubMed].
43. Kai-Larsen, Y.; Lüthje, P.; Chromek, M.; Peters, V.;Wang, X.; Holm, Å.; Kadas, L.; Hedlund, K.O.; Johansson, J.;Chapman, M.R.; et al. Uropathogenic Escherichia coli modulates immune responses and its curli fimbriaeinteract with the antimicrobial peptide LL-37. PLoS Pathog. 2010, 6, e1001010. [CrossRef] [PubMed].
44. Albert, X.; Huertas, I.; Pereiro, I.I.; Sanfelix, J.; Gosalbes, V.; Perrota, C. Antibiotics for preventing recurrenturinary tract infection in non-pregnant women. Cochrane Database Syst. Rev. 2004. [CrossRef].
45. Eells, S.J.; Bharadwa, K.; McKinnell, J.A.; Miller, L.G. Recurrent urinary tract infections among women:Comparative effectiveness of 5 prevention and management strategies using a Markov chain Monte Carlomodel. Clin. Infect. Dis. 2014, 58, 147-160. [CrossRef] [PubMed].
46. Lorenzo-Gomez, M.F.; Padilla-Fernandez, B.; Garcia-Criado, F.J.; Miron-Canelo, J.A.; Gil-Vicente, A.;Nieto-Huertos, A.; Silva-Abuin, J.M. Evaluation of a therapeutic vaccine for the prevention of recurrenturinary tract infections versus prophylactic treatment with antibiotics. Int. Urogynecol. J. 2013, 24, 127-134.[CrossRef] [PubMed].
47. Beerepoot, M.A.; ter Riet, G.; Nys, S.; van der Wal, W.M.; de Borgie, C.A.; de Reijke, T.M.; Prins, J.M.;Koeijers, J.; Verbon, A.; Stobberingh, E.; et al. Cranberries vs antibiotics to prevent urinary tract infections:A randomized double-blind noninferiority trial in premenopausal women. Arch. Intern. Med. 2011, 171,1270-1278. [CrossRef] [PubMed].
48. Geerlings, S.E.; Beerepoot, M.A.; Prins, J.M. Prevention of recurrent urinary tract infections in women:Antimicrobial and nonantimicrobial strategies. Infect. Dis. Clin. N. Am. 2014, 28, 135-147. [CrossRef][PubMed].
49. Spencer, J.D.; Schwaderer, A.L.; Becknell, B.; Watson, J.; Hains, D.S. The innate immune response duringurinary tract infection and pyelonephritis. Pediatr. Nephrol. 2014, 29, 1139-1149. [CrossRef] [PubMed].
50. Ali, A.S.; Townes, C.L.; Hall, J.; Pickard, R.S. Maintaining a sterile urinary tract: The role of antimicrobialpeptides. J. Urol. 2009, 182, 21-28. [CrossRef] [PubMed].
51. Chromek, M.; Slamova, Z.; Bergman, P.; Kovacs, L.; Podracka, L.; Ehren, I.; Hokfelt, T.; Gudmundsson, G.H.;Gallo, R.L.; Agerberth, B.; et al. The antimicrobial peptide cathelicidin protects the urinary tract againstinvasive bacterial infection. Nat. Med. 2006, 12, 636-641. [CrossRef] [PubMed].
52. Spencer, J.D.; Schwaderer, A.L.; Dirosario, J.D.; McHugh, K.M.; McGillivary, G.; Justice, S.S.; Carpenter, A.R.;Baker, P.B.; Harder, J.; Hains, D.S. Ribonuclease 7 is a potent antimicrobial peptide within the human urinarytract. Kidney Int. 2011, 80, 174-180. [CrossRef] [PubMed].
53. Spencer, J.D.; Schwaderer, A.L.; Wang, H.; Bartz, J.; Kline, J.; Eichler, T.; DeSouza, K.R.; Sims-Lucas, S.;Baker, P.; Hains, D.S. Ribonuclease 7, an antimicrobial peptide upregulated during infection, contributes tomicrobial defense of the human urinary tract. Kidney Int. 2013, 83, 615-625. [CrossRef] [PubMed].
54. Ganz, T. Defensins in the urinary tract and other tissues. J. Infect. Dis. 2001, 183, S41-S42. [CrossRef][PubMed].
55. Semple, C.A.; Rolfe, M.; Dorin, J.R. Duplication and selection in the evolution of primate beta-defensin genes.Genome Biol. 2003, 4, R31. [CrossRef] [PubMed].
56. Zhao, C.;Wang, I.; Lehrer, R.I.Widespread expression of beta-defensin hBD-1 in human secretory glandsand epithelial cells. FEBS Lett. 1996, 396, 319-322. [CrossRef].
57. Valore, E.V.; Park, C.H.; Quayle, A.J.; Wiles, K.R.; McCray, P.B., Jr.; Ganz, T. Human beta-defensin-1:An antimicrobial peptide of urogenital tissues. J. Clin. Investig. 1998, 101, 1633-1642. [CrossRef] [PubMed].
58. Becknell, B.; Spencer, J.D.; Carpenter, A.R.; Chen, X.; Singh, A.; Ploeger, S.; Kline, J.; Ellsworth, P.; Li, B.;Proksch, E.; et al. Expression and antimicrobial function of beta-defensin 1 in the lower urinary tract.PLoS ONE 2013, 8, e77714. [CrossRef] [PubMed].
59. Hiratsuka, T.; Nakazato, M.; Ihi, T.; Minematsu, T.; Chino, N.; Nakanishi, T.; Shimizu, A.; Kangawa, K.;Matsukura, S. Structural analysis of human beta-defensin-1 and its significance in urinary tract infection.Nephron 2000, 85, 34-40. [CrossRef] [PubMed].
60. Nielsen, K.L.; Dynesen, P.; Larsen, P.; Jakobsen, L.; Andersen, P.S.; Frimodt-Moller, N. Role of urinarycathelicidin LL-37 and human beta-defensin 1 in uncomplicated Escherichia coli urinary tract infections.Infect. Immun. 2014, 82, 1572-1578. [CrossRef] [PubMed].
61. Nitschke, M.;Wiehl, S.; Baer, P.C.; Kreft, B. Bactericidal activity of renal tubular cells: The putative role ofhuman beta-defensins. Exp. Nephrol. 2002, 10, 332-337. [CrossRef] [PubMed].
62. Lehmann, J.; Retz, M.; Harder, J.; Krams, M.; Kellner, U.; Hartmann, J.; Hohgrawe, K.; Loch, T.; Raffenberg, U.;Gerber, M.; et al. Expression of human beta-defensins 1 and 2 in kidneys with chronic bacterial infection.BMC Infect. Dis. 2002, 2, 20. [CrossRef] [PubMed].
63. Spencer, J.D.; Hains, D.S.; Porter, E.; Bevins, C.L.; DiRosario, J.; Becknell, B.; Schwaderer, A.L.; Wang, H.Human alpha defensin 5 expression in the human kidney and urinary tract. PLoS ONE 2012, 7, e31712.[CrossRef] [PubMed].
64. Park, C.H.; Valore, E.V.; Waring, A.J.; Ganz, T. Hepcidin, a urinary antimicrobial peptide synthesized in theliver. J. Biol. Chem. 2001, 276, 7806-7810. [CrossRef] [PubMed].
65. Åbrink, M.; Larsson, E.; Gobl, A.; Hellman, L. Expression of lactoferrin in the kidney: Implications for innateimmunity and iron metabolism. Kidney Int. 2000, 57, 2004-2010. [CrossRef] [PubMed].
66. Paragas, N.; Kulkarni, R.; Werth, M.; Schmidt-Ott, K.M.; Forster, C.; Deng, R.; Zhang, Q.; Singer, E.;Klose, A.D.; Shen, T.H.; et al. Alpha-intercalated cells defend the urinary system from bacterial infection.J. Clin. Investig. 2014, 124, 2963-2976. [CrossRef] [PubMed].
67. Steigedal, M.; Marstad, A.; Haug, M.; Damas, J.K.; Strong, R.K.; Roberts, P.L.; Himpsl, S.D.; Stapleton, A.;Hooton, T.M.; Mobley, H.L.; et al. Lipocalin 2 imparts selective pressure on bacterial growth in the bladderand is elevated in women with urinary tract infection. J. Immunol. 2014, 193, 6081-6089. [CrossRef] [PubMed].
68. Gläser, R.; Harder, J.; Lange, H.; Bartels, J.; Christophers, E.; Schröder, J.M. Antimicrobial psoriasin (S100A7)protects human skin from Escherichia coli infection. Nat. Immunol. 2005, 6, 57-64. [CrossRef] [PubMed].
69. Lüthje, P.; Brauner, H.; Ramos, N.L.; Övregaard, A.; Gläser, R.; Hirschberg, A.L.; Aspenström, P.; Brauner, A.Estrogen supports urothelial defense mechanisms. Sci. Transl. Med. 2013, 5, 190ra180. [CrossRef] [PubMed].
70. Østergaard, M.; Wolf, H.; Orntoft, T.F.; Celis, J.E. Psoriasin (S100A7): A putative urinary marker for thefollow-up of patients with bladder squamous cell carcinomas. Electrophoresis 1999, 20, 349-354. [CrossRef].
71. Bates, J.M.; Raffi, H.M.; Prasadan, K.; Mascarenhas, R.; Laszik, Z.; Maeda, N.; Hultgren, S.J.; Kumar, S.Tamm-Horsfall protein knockout mice are more prone to urinary tract infection: Rapid communication.Kidney Int. 2004, 65, 791-797. [CrossRef] [PubMed].
72. Lehrer, R.I.; Ganz, T. Cathelicidins: A family of endogenous antimicrobial peptides. Curr. Opin. Hematol.2002, 9, 18-22. [CrossRef] [PubMed].
73. Zanetti, M. The role of cathelicidins in the innate host defenses of mammals. Curr. Issues Mol. Biol. 2005, 7,179-196. [PubMed].
74. Murakami, M.; Lopez-Garcia, B.; Braff, M.; Dorschner, R.A.; Gallo, R.L. Postsecretory processing generatesmultiple cathelicidins for enhanced topical antimicrobial defense. J. Immunol. 2004, 172, 3070-3077.[CrossRef] [PubMed].
75. Murakami, M.; Ohtake, T.; Dorschner, R.A.; Schittek, B.; Garbe, C.; Gallo, R.L. Cathelicidin anti-microbialpeptide expression in sweat, an innate defense system for the skin. J. Investig. Dermatol. 2002, 119, 1090-1095.[CrossRef] [PubMed].
76. Sorensen, O.E.; Gram, L.; Johnsen, A.H.; Andersson, E.; Bangsboll, S.; Tjabringa, G.S.; Malm, J.; Hiemstra, P.S.;Egesten, A.; Borregaard, N. Processing of seminal plasma hCAP-18 to ALL-38 by gastricsin: A novelmechanism of generating antimicrobial peptides in vagina. J. Biol. Chem. 2003, 278, 28540-28546. [CrossRef][PubMed].
77. Pestonjamasp, V.K.; Huttner, K.H.; Gallo, R.L. Processing site and gene structure for the murine antimicrobialpeptide CRAMP. Peptides 2001, 22, 1643-1650. [CrossRef].
78. Thomassin, J.L.; Brannon, J.R.; Gibbs, B.F.; Gruenheid, S.; le Moual, H. OmpT outer membrane proteases ofenterohemorrhagic and enteropathogenic Escherichia coli contribute differently to the degradation of humanLL-37. Infect. Immun. 2012, 80, 483-492. [CrossRef] [PubMed].
79. Brannon, J.R.; Thomassin, J.L.; Desloges, I.; Gruenheid, S.; le Moual, H. Role of uropathogenic Escherichia coliOmpT in the resistance against human cathelicidin LL-37. FEMS Microbiol. Lett. 2013, 345, 64-71. [CrossRef][PubMed].
80. Richards, S.M.; Strandberg, K.L.; Gunn, J.S. Salmonella-regulated lipopolysaccharide modifications.Subcell. Biochem. 2010, 53, 101-122. [PubMed].
81. Rosenfeld, Y.; Papo, N.; Shai, Y. Endotoxin (lipopolysaccharide) neutralization by innate immunityhost-defense peptides. Peptide properties and plausible modes of action. J. Biol. Chem. 2006, 281, 1636-1643.[CrossRef] [PubMed].
82. Brinkmann, V.; Reichard, U.; Goosmann, C.; Fauler, B.; Uhlemann, Y.; Weiss, D.S.; Weinrauch, Y.;Zychlinsky, A. Neutrophil extracellular traps kill bacteria. Science 2004, 303, 1532-1535. [CrossRef] [PubMed].
83. Neumann, A.; Berends, E.T.; Nerlich, A.; Molhoek, E.M.; Gallo, R.L.; Meerloo, T.; Nizet, V.; Naim, H.Y.; vonKöckritz-Blickwede, M. The antimicrobial peptide LL-37 facilitates the formation of neutrophil extracellulartraps. Biochem. J. 2014, 464, 3-11. [CrossRef] [PubMed].
84. Neumann, A.; Völlger, L.; Berends, E.T.; Molhoek, E.M.; Stapels, D.A.; Midon, M.; Friaes, A.; Pingoud, A.;Rooijakkers, S.H.; Gallo, R.L.; et al. Novel role of the antimicrobial peptide LL-37 in the protection ofneutrophil extracellular traps against degradation by bacterial nucleases. J. Innate Immun. 2014, 6, 860-868.[CrossRef] [PubMed].
85. Danka, E.S.; Hunstad, D.A. Cathelicidin augments epithelial receptivity and pathogenesis in experimentalEscherichia coli cystitis. J. Infect. Dis. 2015, 211, 1164-1173. [CrossRef] [PubMed].
86. Oottamasathien, S.; Jia,W.; McCoard, L.; Slack, S.; Zhang, J.; Skardal, A.; Job, K.; Kennedy, T.P.; Dull, R.O.;Prestwich, G.D. A murine model of inflammatory bladder disease: Cathelicidin peptide induced bladderinflammation and treatment with sulfated polysaccharides. J. Urol. 2011, 186, 1684-1692. [CrossRef][PubMed].
87. Oottamasathien, S.; Jia, W.; Roundy, L.M.; Zhang, J.; Wang, L.; Ye, X.; Hill, A.C.; Savage, J.; Lee, W.Y.;Hannon, A.M.; et al. Physiological relevance of LL-37 induced bladder inflammation and mast cells. J. Urol.2013, 190, 1596-1602. [CrossRef] [PubMed].
88. Lüthje, P.; Chromek, M.; Brauner, A. Karolinska University Hospital and Karolinska Institutet, Stockholm,Sweden. Unpublished work. 2007.
89. Overhage, J.; Campisano, A.; Bains, M.; Torfs, E.C.; Rehm, B.H.; Hancock, R.E. Human host defense peptideLL-37 prevents bacterial biofilm formation. Infect. Immun. 2008, 76, 4176-4182. [CrossRef] [PubMed].
90. Dean, S.N.; Bishop, B.M.; van Hoek, M.L. Natural and synthetic cathelicidin peptides with anti-microbialand anti-biofilm activity against Staphylococcus aureus. BMC Microbiol. 2011, 11, 114. [CrossRef] [PubMed].
91. Haisma, E.M.; de Breij, A.; van Dissel, J.T.; Drijfhout, J.W.; Hiemstra, P.S.; El Ghalbzouri, A.; Chan, H.;Nibbering, P.H. Ll-37-derived peptides eradicate multidrug-resistant Staphylococcus aureus from thermallywounded human skin equivalents. Antimicrob. Agents Chemother. 2014, 58, 4411-4419. [CrossRef] [PubMed].
92. Amer, L.S.; Bishop, B.M.; van Hoek, M.L. Antimicrobial and antibiofilm activity of cathelicidins and short,synthetic peptides against Francisella. Biochem. Biophys. Res. Commun. 2010, 396, 246-251. [CrossRef][PubMed].
93. Feng, X.; Sambanthamoorthy, K.; Palys, T.; Paranavitana, C. The human antimicrobial peptide LL-37and its fragments possess both antimicrobial and antibiofilm activities against multidrug-resistantAcinetobacter baumannii. Peptides 2013, 49, 131-137. [CrossRef] [PubMed].
94. Sol, A.; Ginesin, O.; Chaushu, S.; Karra, L.; Coppenhagen-Glazer, S.; Ginsburg, I.; Bachrach, G. Ll-37opsonizes and inhibits biofilm formation of Aggregatibacter actinomycetemcomitans at subbactericidalconcentrations. Infect. Immun. 2013, 81, 3577-3585. [CrossRef] [PubMed].
95. Tsai, P.W.; Yang, C.Y.; Chang, H.T.; Lan, C.Y. Human antimicrobial peptide LL-37 inhibits adhesion ofCandida albicans by interacting with yeast cell-wall carbohydrates. PLoS ONE 2011, 6, e17755. [CrossRef][PubMed].
96. Schwalfenberg, G.K. A review of the critical role of vitamin D in the functioning of the immune system andthe clinical implications of vitamin D deficiency. Mol. Nutr. Food. Res. 2011, 55, 96-108. [CrossRef] [PubMed].
97. Gombart, A.F.; Borregaard, N.; Koeffler, H.P. Human cathelicidin antimicrobial peptide (CAMP)gene is a direct target of the vitamin D receptor and is strongly up-regulated in myeloid cells by1,25-dihydroxyvitamin D3. FASEB J. 2005, 19, 1067-1077. [CrossRef] [PubMed].
98. Ponchon, G.; Kennan, A.L.; DeLuca, H.F. "Activation" of vitamin D by the liver. J. Clin. Investig. 1969, 48,2032-2037. [CrossRef] [PubMed].
99. Zehnder, D.; Bland, R.;Walker, E.A.; Bradwell, A.R.; Howie, A.J.; Hewison, M.; Stewart, P.M. Expression of25-hydroxyvitamin D3-1alpha-hydroxylase in the human kidney. J. Am. Soc. Nephrol. 1999, 10, 2465-2473.[PubMed].
100. Hertting, O.; Lüthje, P.; Brauner, H.; Dyrdak, R.; Jonasson, A.F.; Wiklund, P.; Chromek, M.; Holm, Å.;Brauner, A. Vitamin D induction of the human antimicrobial peptide cathelicidin in the urinary bladder.PLoS ONE 2010, 5, e15580. [CrossRef] [PubMed].
101. Tekin, M.; Konca, C.; Celik, V.; Almis, H.; Kahramaner, Z.; Erdemir, A.; Gulyuz, A.; Uckardes, F.; Turgut, M.The association between vitamin D levels and urinary tract infection in children. Horm Res Paediatr 2015, 83,198-203. [CrossRef] [PubMed].
102. Nseir, W.; Taha, M.; Nemarny, H.; Mograbi, J. The association between serum levels of vitamin D andrecurrent urinary tract infections in premenopausal women. Int. J. Infect. Dis. 2013, 17, e1121-e1124.[CrossRef] [PubMed].
103. Sonnex, C. Influence of ovarian hormones on urogenital infection. Sex. Transm. Infect. 1998, 74, 11-19.[CrossRef] [PubMed].
104. Epp, A.; Larochelle, A.; Lovatsis, D.; Walter, J.E.; Easton, W.; Farrell, S.A.; Girouard, L.; Gupta, C.;Harvey, M.A.; Robert, M.; et al. Recurrent urinary tract infection. J. Obstet. Gynaecol. Can. 2010, 32,1082-1101. [PubMed].
105. Perrotta, C.; Aznar, M.; Mejia, R.; Albert, X.; Ng, C.W. Oestrogens for preventing recurrent urinary tract infection in postmenopausal women. Cochrane Database Syst. Rev. 2008. [CrossRef].
106. Salvatore, S.; Salvatore, S.; Cattoni, E.; Siesto, G.; Serati, M.; Sorice, P.; Torella, M. Urinary tract infections inwomen. Eur. J. Obstet. Gynecol. Reprod. Biol. 2011, 156, 131-136. [CrossRef] [PubMed].
107. Eto, D.S.; Jones, T.A.; Sundsbak, J.L.; Mulvey, M.A. Integrin-mediated host cell invasion by type 1-piliated uropathogenic Escherichia coli. PLoS Pathog. 2007, 3, e100. [CrossRef] [PubMed].
108. Zhou, G.; Mo, W.J.; Sebbel, P.; Min, G.; Neubert, T.A.; Glockshuber, R.; Wu, X.R.; Sun, T.T.; Kong, X.P.Uroplakin Ia is the urothelial receptor for uropathogenic Escherichia coli: Evidence from in vitro fimH binding.J. Cell. Sci. 2001, 114, 4095-4103. [PubMed].
109. Wang, C.; Symington, J.W.; Ma, E.; Cao, B.; Mysorekar, I.U. Estrogenic modulation of uropathogenic Escherichia coli infection pathogenesis in a murine menopause model. Infect. Immun. 2013, 81, 733-739.[CrossRef] [PubMed].
110. Schnarr, J.; Smaill, F. Asymptomatic bacteriuria and symptomatic urinary tract infections in pregnancy. Eur. J. Clin. Investig. 2008, 38, 50-57. [CrossRef] [PubMed].
111. Foxman, B.; Buxton, M. Alternative approaches to conventional treatment of acute uncomplicated urinary tract infection in women. Curr. Infect. Dis. Rep. 2013, 15, 124-129. [CrossRef] [PubMed].
112. Conrad, A.; Biehler, D.; Nobis, T.; Richter, H.; Engels, I.; Biehler, K.; Frank, U. Broad spectrum antibacterial activity of a mixture of isothiocyanates from nasturtium (Tropaeoli majoris herba) and horseradish (Armoraciae rusticanae radix). Drug Res. Stuttg 2013, 63, 65-68. [CrossRef] [PubMed].
113. Liao, S.-G.; Zhang, L.-J.; Sun, F.; Zhang, J.-J.; Chen, A.Y.; Lan, Y.-Y.; Li, Y.-J.;Wang, A.-M.; He, X.; Xiong, Y.; et al. Antibacterial and anti-inflammatory effects of extracts and fractions from Polygonum capitatum. J. Ethnopharmacol. 2011, 134, 1006-1009. [CrossRef] [PubMed].
114. Peng, M.-M.; Fang, Y.; Hu,W.; Huang, Q. The pharmacological activities of compound Salvia plebeia granules on treating urinary tract infection. J. Ethnopharmacol. 2010, 129, 59-63. [CrossRef] [PubMed].
115. Albrecht, U.; Goos, K.H.; Schneider, B. A randomised, double-blind, placebo-controlled trial of a herbal medicinal product containing Tropaeoli majoris herba (nasturtium) and Armoraciae rusticanae radix (horseradish) for the prophylactic treatment of patients with chronically recurrent lower urinary tract infections. Curr. Med. Res. Opin. 2007, 23, 2415-2422. [PubMed].
116. Rafsanjany, N.; Lechtenberg, M.; Petereit, F.; Hensel, A. Antiadhesion as a functional concept for protection against uropathogenic Escherichia coli: In vitro studies with traditionally used plants with antiadhesive activity against uropathognic Escherichia coli. J. Ethnopharmacol. 2013, 145, 591-597. [CrossRef] [PubMed].
117. Chen, C.S.; Ho, D.R.; Chang, P.J.; Lin, W.Y.; Huang, Y.C. Urine post equivalent daily cranberry juice consumption may opsonize uropathogenicity of Escherichia coli. J. Infect. Chemother. 2013, 19, 812-817. [CrossRef] [PubMed].
118. Gupta, K.; Chou, M.Y.; Howell, A.; Wobbe, C.; Grady, R.; Stapleton, A.E. Cranberry products inhibit adherence of P-fimbriated Escherichia coli to primary cultured bladder and vaginal epithelial cells. J. Urol. 2007, 177, 2357-2360. [CrossRef] [PubMed].
119. Bosmans, J.E.; Beerepoot, M.A.; Prins, J.M.; ter Riet, G.; Geerlings, S.E. Cost-effectiveness of cranberries vs. antibiotics to prevent urinary tract infections in premenopausal women: A randomized clinical trial. PLoS ONE 2014, 9, e91939. [CrossRef] [PubMed].
120. Jepson, R.G.; Williams, G.; Craig, J.C. Cranberries for preventing urinary tract infections. Cochrane Database Syst. Rev. 2012, 10, CD001321. [PubMed].
121. Lüthje, P.; Dzung, D.N.; Brauner, A. Lactuca indica extract interferes with uroepithelial infection by Escherichia coli. J. Ethnopharmacol. 2011, 135, 672-677. [CrossRef] [PubMed].
122. Fazliana, M.; Ramos, N.L.; Lüthje, P.; Sekikubo, M.; Holm, Å.; Wan Nazaimoon, W.M.; Brauner, A. Labisia pumila var. alata reduces bacterial load by inducing uroepithelial cell apoptosis. J. Ethnopharmacol.2011, 136, 111-116. [PubMed].
123. Vollmerhausen, T.L.; Ramos, N.L.; Dzung, D.T.; Brauner, A. Decoctions from Citrus reticulata blanco seeds protect the uroepithelium against Escherichia coli invasion. J. Ethnopharmacol. 2013, 150, 770-774. [CrossRef][PubMed].
124. Bleidorn, J.; Gagyor, I.; Kochen, M.M.; Wegscheider, K.; Hummers-Pradier, E. Symptomatic treatment(ibuprofen) or antibiotics (ciprofloxacin) for uncomplicated urinary tract infection?-Results of a randomizedcontrolled pilot trial. BMC Med. 2010, 8, 30. [CrossRef] [PubMed].
125. Lüthje, P.; Lokman, E.F.; Sanström, C.; Östenson, C.-G.; Brauner, A. Gynostemma pentaphyllum exhibitsanti-inflammatory properties and modulates antimicrobial peptide expression in the urinary bladder. J.Funct. Foods 2015, 17, 283-292. [CrossRef].