α-Intercalated cells defend the urinary system from bacterial infection

Journal of Clinical Investigation

Volumn 124, Issue 7, 2014, Pages 2963-2976

  Paragas, Neal ^a   Kulkarni, Ritwij ^a,b   Werth, Max ^a   Schmidt Ott, Kai M ^c   Forster, Catherine ^a   Deng, Rong ^a   Zhang, Qingyin ^a   Singer, Eugenia ^c   Klose, Alexander D ^a   Shen, Tian Huai ^a   Francis, Kevin P ^d   Ray, Sunetra ^d   Vijayakumar, Soundarapandian ^e   Seward, Samuel ^a   Bovino, Mary E ^a   Xu, Katherine ^a   Takabe, Yared ^a   Amaral, Fábio E ^a   Mohan, Sumit ^a   Wax, Rebecca ^a   Corbin, Kaitlyn ^a   Sanna Cherchi, Simone ^a   Mori, Kiyoshi ^f   Johnson, Lynne ^a   Nickolas, Thomas ^a   D'Agati, Vivette ^a   Lin, Chyuan Sheng ^a   Qiu, Andong ^a   Al Awqati, Qais ^a   Ratner, Adam J ^a   Barasch, Jonathan ^a   more..

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b LOUISIANA STATE UNIVERSITY   (United States)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^d Preclinical Imaging PerkinElmer   (United States)

^e UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^f KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; LIPOPOLYSACCHARIDE; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; TOLL LIKE RECEPTOR 4;

ALPHA INTERCALATED CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC THERAPY; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL GROWTH; BACTERIAL INFECTION; BACTERIAL LOAD; CELLULAR IMMUNITY; COHORT ANALYSIS; COLONY FORMING UNIT; CONTROLLED STUDY; EXPERIMENTAL INFECTION; EXPERIMENTAL UROGENITAL DISEASE; FEMALE; GROWTH INHIBITION; HUMAN; KIDNEY CELL; KIDNEY CONCENTRATING CAPACITY; KIDNEY MEDULLA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; URINARY TRACT INFECTION; URINE ACIDIFICATION; UROPATHOGENIC ESCHERICHIA COLI;

ACID-BASE EQUILIBRIUM; ACUTE-PHASE PROTEINS; ANIMALS; DISEASE MODELS, ANIMAL; ESCHERICHIA COLI INFECTIONS; FEMALE; HUMANS; HYDROGEN-ION CONCENTRATION; IRON; KIDNEY TUBULES, COLLECTING; LIPOCALINS; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS; TOLL-LIKE RECEPTOR 4; URINARY TRACT INFECTIONS; UROPATHOGENIC ESCHERICHIA COLI;

EID: 84903752904     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI71630     Document Type: Article

References (120)

1. Litwin MS, et al. Urologic diseases in America Project: analytical methods and principal findings. J Urol. 2005;173(3):933-937. (Pubitemid 40239368)
2. Freedman AL, et al. Urologic diseases in North America Project: trends in resource utilization for urinary tract infections in children. J Urol. 2005;173(3):949-954. (Pubitemid 40239372)
3. Brzuszkiewicz E, et al. How to become a uropathogen: comparative genomic analysis of extraintestinal pathogenic Escherichia coli strains. Proc Natl Acad Sci U S A. 2006;103(34):12879-12884. (Pubitemid 44298655)
4. Foxman B. Epidemiology of urinary tract infections: incidence, morbidity, and economic costs. Am J Med. 2002;113(suppl 1A):5S-13S.
5. Spencer JD, et al. Ribonuclease 7 is a potent antimicrobial peptide within the human urinary tract. Kidney Int. 2011;80(2):174-180.
6. Chromek M, et al. The antimicrobial peptide cathelicidin protects the urinary tract against invasive bacterial infection. Nat Med. 2006;12(6):636-641. (Pubitemid 43865231)
7. Yang J, et al. An iron delivery pathway mediated by a lipocalin. Mol Cell. 2002;10(5):1045-1056. (Pubitemid 35453824)
8. Mori K, et al. Endocytic delivery of lipocalinsiderophore-iron complex rescues the kidney from ischemia-reperfusion injury. J Clin Invest. 2005;115(3):610-621. (Pubitemid 40322235)
9. Mishra J, et al. Identification of neutrophil gelatinase-associated lipocalin as a novel early urinary biomarker for ischemic renal injury. J Am Soc Nephrol. 2003;14(10):2534-2543. (Pubitemid 37169339)
10. Parravicini E, Lorenz JM, Nemerofsky SL, O'Rourke M, Barasch J, Bateman D. Reference range of urinary neutrophil gelatinase-associated lipocalin in very low-birth-weight infants: preliminary data. Am J Perinatol. 2009;26(6):437-440.
11. Bagshaw SM, et al. Plasma and urine neutrophil gelatinase-associated lipocalin in septic versus non-septic acute kidney injury in critical illness. Intensive Care Med. 2010;36(3):452-461.
12. Kümpers P, et al. Serum neutrophil gelatinaseassociated lipocalin at inception of renal replacement therapy predicts survival in critically ill patients with acute kidney injury. Crit Care. 2010; 14(1):R9.
13. Cruz DN, et al. Plasma neutrophil gelatinaseassociated lipocalin is an early biomarker for acute kidney injury in an adult ICU population. Intensive Care Med. 2010;36(3):444-451.
14. Wheeler DS, et al. Serum neutrophil gelatinaseassociated lipocalin (NGAL) as a marker of acute kidney injury in critically ill children with septic shock. Crit Care Med. 2008;36(4):1297-1303. (Pubitemid 351482681)
15. Paragas N, et al. The Ngal reporter mouse detects the response of the kidney to injury in real time. Nat Med. 2011;17(2):216-222.
16. Bennett M, et al. Urine NGAL predicts severity of acute kidney injury after cardiac surgery: a prospective study. Clin J Am Soc Nephrol. 2008;3(3):665-673.
17. McIlroy DR, Wagener G, Lee HT. Neutrophil gelatinase-associated lipocalin and acute kidney injury after cardiac surgery: the effect of baseline renal function on diagnostic performance. Clin J Am Soc Nephrol. 2010;5(2):211-219.
18. Mishra J, et al. Neutrophil gelatinase-associated lipocalin (NGAL) as a biomarker for acute renal injury after cardiac surgery. Lancet. 2005; 365(9466):1231-1238. (Pubitemid 40469655)
19. Niemann CU, et al. Acute kidney injury during liver transplantation as determined by neutrophil gelatinase-associated lipocalin. Liver Transpl. 2009;15(12):1852-1860.
20. Capuano F, et al. Neutrophil gelatinase-associated lipocalin levels after use of mini-cardiopulmonary bypass system. Interact Cardiovasc Thorac Surg. 2009;9(5):797-801.
21. Haase-Fielitz A, et al. The predictive performance of plasma neutrophil gelatinase-associated lipocalin (NGAL) increases with grade of acute kidney injury. Nephrol Dial Transplant. 2009;24(11):3349-3354.
22. Tuladhar SM, Puntmann VO, Soni M, Punjabi PP, Bogle RG. Rapid detection of acute kidney injury by plasma and urinary neutrophil gelatinaseassociated lipocalin after cardiopulmonary bypass. J Cardiovasc Pharmacol. 2009;53(3):261-266.
23. Wan X, et al. [Association between urinary neutrophil gelatinase-associated lipocalin and acute kidney injury after cardiac surgery]. Zhonghua Yi Xue Za Zhi. 2008;88(19):1318-1322.
24. Xin C, Yulong X, Yu C, Changchun C, Feng Z, Xinwei M. Urine neutrophil gelatinase-associated lipocalin and interleukin-18 predict acute kidney injury after cardiac surgery. Ren Fail. 2008;30(9):904-913.
25. Koyner JL, et al. Urinary cystatin C as an early biomarker of acute kidney injury following adult cardiothoracic surgery. Kidney Int. 2008;74(8):1059-1069.
26. Wagener G, Gubitosa G, Wang S, Borregaard N, Kim M, Lee HT. Increased incidence of acute kidney injury with aprotinin use during cardiac surgery detected with urinary NGAL. Am J Nephrol. 2008;28(4):576-582. (Pubitemid 351832444)
27. Dent CL, et al. Plasma neutrophil gelatinase-associated lipocalin predicts acute kidney injury, morbidity and mortality after pediatric cardiac surgery: a prospective uncontrolled cohort study. Crit Care. 2007;11(6):R127.
28. Kuwabara T, et al. Urinary neutrophil gelatinaseassociated lipocalin levels reflect damage to glomeruli, proximal tubules, and distal nephrons. Kidney Int. 2009;75(3):285-294.
29. Mishra J, Mori K, Ma Q, Kelly C, Barasch J, Devarajan P. Neutrophil gelatinase-associated lipocalin: a novel early urinary biomarker for cisplatin nephrotoxicity. Am J Nephrol. 2004;24(3):307-315. (Pubitemid 39070114)
30. Malyszko J, Bachorzewska-Gajewska H, Poniatowski B, Malyszko JS, Dobrzycki S. Urinary and serum biomarkers after cardiac catheterization in diabetic patients with stable angina and without severe chronic kidney disease. Ren Fail. 2009;31(10):910-919.
31. Vaidya VS, et al. Urinary biomarkers for sensitive and specific detection of acute kidney injury in humans. Clin Transl Sci. 2008;1(3):200-208. (Pubitemid 352831522)
32. Hirsch R, et al. NGAL is an early predictive biomarker of contrast-induced nephropathy in children. Pediatr Nephrol. 2007;22(12):2089- 2095. (Pubitemid 350090716)
33. Ling W, et al. Urinary IL-18 and NGAL as early predictive biomarkers in contrast-induced nephropathy after coronary angiography. Nephron Clin Pract. 2008;108(3):c176-c181. (Pubitemid 351588109)
34. Makris K, et al. Urinary neutrophil gelatinaseassociated lipocalin (NGAL) as an early marker of acute kidney injury in critically ill multiple trauma patients. Clin Chem Lab Med. 2009;47(1):79-82.
35. Lebkowska U, et al. Neutrophil gelatinase-associated lipocalin and cystatin C could predict renal outcome in patients undergoing kidney allograft transplantation: a prospective study. Transplant Proc. 2009;41(1):154-157.
36. Parikh CR, et al. Urine NGAL and IL-18 are predictive biomarkers for delayed graft function following kidney transplantation. Am J Transplant. 2006;6(7):1639-1645. (Pubitemid 43945804)
37. Ferguson MA, et al. Urinary liver-type fatty acidbinding protein predicts adverse outcomes in acute kidney injury. Kidney Int. 2010;77(8):708-714.
38. Nickolas TL, et al. Sensitivity and specificity of a single emergency department measurement of urinary neutrophil gelatinase-associated lipocalin for diagnosing acute kidney injury. Ann Intern Med. 2008;148(11):810-819. (Pubitemid 351786928)
39. Flower DR, North AC, Sansom CE. The lipocalin protein family: structural and sequence overview. Biochim Biophys Acta. 2000;1482(1-2):9-24.
40. Goetz DH, Holmes MA, Borregaard N, Bluhm ME, Raymond KN, Strong RK. The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition. Mol Cell. 2002;10(5):1033-1043. (Pubitemid 36001971)
41. Barasch J, Mori K. Cell biology: iron thievery. Nature. 2004;432(7019):811-813.
42. Abergel RJ, et al. The siderocalin/enterobactin interaction: a link between mammalian immunity and bacterial iron transport. J Am Chem Soc. 2008;130(34):11524-11534.
43. Berger T, et al. Lipocalin 2-deficient mice exhibit increased sensitivity to Escherichia coli infection but not to ischemia-reperfusion injury. Proc Natl Acad Sci U S A. 2006;103(6):1834-1839. (Pubitemid 43228779)
44. Holmes MA, Paulsene W, Jide X, Ratledge C, Strong RK. Siderocalin (Lcn 2) also binds carboxymycobactins, potentially defending against mycobacterial infections through iron sequestration. Structure. 2005;13(1):29-41. (Pubitemid 40092472)
45. Flo TH, et al. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature. 2004;432(7019):917-921. (Pubitemid 40037155)
46. Zhou G, et al. Uroplakin Ia is the urothelial receptor for uropathogenic Escherichia coli: evidence from in vitro FimH binding. J Cell Sci. 2001; 114(pt 22):4095-4103. (Pubitemid 33115030)
47. Hiratsuka T, et al. Structural analysis of human β-defensin-1 and its significance in urinary tract infection. Nephron. 2000;85(1):34-40. (Pubitemid 30242827)
48. Valore EV, Park CH, Quayle AJ, Wiles KR, McCray PB, Ganz T. Human β-defensin-1: an antimicrobial peptide of urogenital tissues. J Clin Invest. 1998;101(8):1633-1642. (Pubitemid 28198492)
49. Serafini-Cessi F, Malagolini N, Cavallone D. Tamm-Horsfall glycoprotein: biology and clinical relevance. Am J Kidney Dis. 2003;42(4):658-676. (Pubitemid 37187366)
50. Bates JM, et al. Tamm-Horsfall protein knockout mice are more prone to urinary tract infection: rapid communication. Kidney Int. 2004;65(3):791-797.
51. Mulvey MA, Schilling JD, Martinez JJ, Hultgren SJ. Bad bugs and beleaguered bladders: interplay between uropathogenic Escherichia coli and innate host defenses. Proc Natl Acad Sci U S A. 2000;97(16):8829-8835. (Pubitemid 30626633)
52. Wright KJ, Seed PC, Hultgren SJ. Uropathogenic Escherichia coli flagella aid in efficient urinary tract colonization. Infect Immun. 2005;73(11):7657- 7668. (Pubitemid 41587672)
53. Abrink M, Larsson E, Gobl A, Hellman L. Expression of lactoferrin in the kidney: implications for innate immunity and iron metabolism. Kidney Int. 2000;57(5):2004-2010. (Pubitemid 30252292)
54. Zasloff M. Antimicrobial peptides, innate immunity, and the normally sterile urinary tract. J Am Soc Nephrol. 2007;18(11):2810-2816. (Pubitemid 350058386)
55. Reinhart H, Obedeanu N, Hooton T, Stamm W, Sobel J. Urinary excretion of Tamm-Horsfall protein in women with recurrent urinary tract infections. J Urol. 1990;144(5):1185-1187. (Pubitemid 20388069)
56. Zasloff M. Antimicrobial peptides of multicellular organisms. Nature. 2002;415(6870):389-395. (Pubitemid 34100944)
57. Perron GG, Zasloff M, Bell G. Experimental evolution of resistance to an antimicrobial peptide. Proc Biol Sci. 2006;273(1583):251-256. (Pubitemid 46768100)
58. Spencer JD, et al. An endogenous ribonuclease inhibitor regulates the antimicrobial activity of ribonuclease 7 in the human urinary tract. Kidney Int. 2013;85(5):1179-1191.
59. Raffi HS, Bates JJM, Laszik Z, Kumar S. Tamm-Horsfall protein acts as a general host-defense factor against bacterial cystitis. Am J Nephrol. 2005; 25(6):570-578. (Pubitemid 41816050)
60. Nickolas TL, et al. Diagnostic and prognostic stratification in the emergency department using urinary biomarkers of nephron damage: a multicenter prospective cohort study. J Am Coll Cardiol. 2012;59(3):246-255.
61. Gupta K, et al. International clinical practice guidelines for the treatment of acute uncomplicated cystitis and pyelonephritis in women: a 2010 update by the infectious diseases society of america and the European society for microbiology and infectious diseases. Clin Infect Dis. 2011;52(5):e103-e120.
62. Mobley HL, et al. Pyelonephritogenic Escherichia coli and killing of cultured human renal proximal tubular epithelial cells: role of hemolysin in some strains. Infect Immun. 1990;58(5):1281-1289. (Pubitemid 20151789)
63. Welch RA, et al. Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci U S A. 2002;99(26):17020-17024. (Pubitemid 36034091)
64. Hopkins WJ, Gendron-Fitzpatrick A, Balish E, Uehling DT. Time course and host responses to Escherichia coli urinary tract infection in genetically distinct mouse strains. Infect Immun. 1998; 66(6):2798-2802. (Pubitemid 28261786)
65. Lakso M, et al. Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc Natl Acad Sci U S A. 1996;93(12):5860-5865. (Pubitemid 26190768)
66. Torres AG, Redford P, Welch RA, Payne SM. TonBdependent systems of uropathogenic Escherichia coli: aerobactin and heme transport and TonB are required for virulence in the mouse. Infect Immun. 2001;69(10):6179-6185. (Pubitemid 32885180)
67. Hvidberg H, Struve C, Krogfelt KA, Christensen N, Rasmussen SN, Frimodt-Moller N. Development of a long-term ascending urinary tract infection mouse model for antibiotic treatment studies. Antimicrob Agents Chemother. 2000;44(1):156-163. (Pubitemid 30010687)
68. Garcia EC, Brumbaugh AR, Mobley HL. Redundancy specificity of Escherichia coli iron acquisition systems during urinary tract infection. Infect Immun. 2011;79(3):1225-1235.
69. Carbonetti NH, Boonchai S, Parry SH, Vaisanen-Rhen V, Korhonen TK, Williams PH. Aerobactinmediated iron uptake by Escherichia coli isolates from human extraintestinal infections. Infect Immun. 1986;51(3):966-968. (Pubitemid 16163006)
70. Johnson Jr. Virulence factors in Escherichia coli urinary tract infection. Clin Microbiol Rev. 1991;4(1):80-128. (Pubitemid 21920389)
71. Buchanan SK, et al. Crystal structure of the outer membrane active transporter FepA from Escherichia coli. Nat Struct Biol. 1999;6(1):56-63. (Pubitemid 29232425)
72. Russo TA, McFadden CD, Carlino-MacDonald UB, Beanan JM, Olson R, Wilding GE. The Siderophore receptor IroN of extraintestinal pathogenic Escherichia coli is a potential vaccine candidate. Infect Immun. 2003;71(12):7164-7169. (Pubitemid 37475350)
73. Alteri CJ, Hagan EC, Sivick KE, Smith SN, Mobley HL. Mucosal immunization with iron receptor antigens protects against urinary tract infection. PLoS Pathog. 2009;5(9):e1000586.
74. Ehmann DE, Shaw-Reid CA, Losey HC, Walsh CT. The EntF and EntE adenylation domains of Escherichia coli enterobactin synthetase: Sequestration and selectivity in acyl-AMP transfers to thiolation domain cosubstrates. Proc Natl Acad Sci U S A. 2000;97(6):2509-2514. (Pubitemid 30159201)
75. Russo TA, McFadden CD, Carlino-MacDonald UB, Beanan JM, Barnard TJ, Johnson Jr. IroN functions as a siderophore receptor and is a urovirulence factor in an extraintestinal pathogenic isolate of Escherichia coli. Infect Immun. 2002;70(12):7156-7160. (Pubitemid 35387956)
76. Strong RK. Siderocalins. In: Åkerström B, Borregard N, Flower DR, Salier JP, eds. Lipocalins. Georgetown, Texas, USA: Landes Bioscience; 2006: 83-98.
77. Hung C-S, Dodson KW, Hultgren SJ. A murine model of urinary tract infection. Nat Protoc. 2009;4(8):1230-1243.
78. Nelson AL, Barasch JM, Bunte RM, Weiser JN. Bacterial colonization of nasal mucosa induces expression of siderocalin, an iron-sequestering component of innate immunity. Cell Microbiol. 2005;7(10):1404-1417. (Pubitemid 41335245)
79. Cowland JB, Sorensen OE, Sehested M, Borregaard N. Neutrophil gelatinase-associated lipocalin is upregulated in human epithelial cells by IL-1β, but not by TNF-α. J Immunol. 2003;171(12):6630-6639. (Pubitemid 37532095)
80. Bando M, et al. Interleukin-1α regulates antimicrobial peptide expression in human keratinocytes. Immunol Cell Biol. 2007;85(7):532-537. (Pubitemid 47530586)
81. Chan YR, et al. Lipocalin 2 is required for pulmonary host defense against Klebsiella infection. J Immunol. 2009;182(8):4947-4956.
82. Lysenko ES, Ratner AJ, Nelson AL, Weiser JN. The role of innate immune responses in the outcome of interspecies competition for colonization of mucosal surfaces. PLoS Pathog. 2005;1(1):e1.
83. Murawski IJ, et al. The C3H/HeJ inbred mouse is a model of vesico-ureteric reflux with a susceptibility locus on chromosome 12. Kidney Int. 2010;78(3):269-278.
84. Murawski IJ, Watt CL, Gupta IR. Vesico-ureteric reflux: using mouse models to understand a common congenital urinary tract defect. Pediatr Nephrol. 2011;26(9):1513-1522.
85. van Adelsberg J, Edwards JC, Takito J, Kiss B, al-Awqati Q. An induced extracellular matrix protein reverses the polarity of band 3 in intercalated epithelial cells. Cell. 1994;76(6):1053-1061.
86. Xie Y, et al. Identification of N-(quinolin-8-yl) benzenesulfonamides as agents capable of downregulating NFκB activity within two separate highthroughput screens of NFκB activation. Bioorg Med Chem Lett. 2008;18(1):329-335.
87. Schmidt-Ott KM, et al. β-Catenin/TCF/Lef controls a differentiation-associated transcriptional program in renal epithelial progenitors. Development. 2007;134(17):3177-3190. (Pubitemid 47506156)
88. Poltorak A, et al. Defective LPS signaling in C3H/ HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science. 1998;282(5396):2085-2088. (Pubitemid 29001265)
89. Chassin C, et al. Renal collecting duct epithelial cells react to pyelonephritis-associated Escherichia coli by activating distinct TLR4-dependent and-independent inflammatory pathways. J Immunol. 2006;177(7):4773-4784. (Pubitemid 44469812)
90. Schwartz GJ, Barasch J, Alawqati Q. Plasticity of functional epithelial polarity. Nature 1985;318(6044):368-371. (Pubitemid 16198492)
91. Wagner CA, et al. Regulation of the expression of the Cl-/anion exchanger pendrin in mouse kidney by acid-base status. Kidney Int. 2002;62(6):2109-2117. (Pubitemid 35366165)
92. Shohl AT, Janney JH. The growth of Bacillus coli in urine at varying hydrogen ion concentrations. J Urol. 1917;1(2):211-229.
93. Martinez JJ, Mulvey MA, Schilling JD, Pinkner JS, Hultgren SJ. Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. EMBO J. 2000;19(12):2803-2812. (Pubitemid 30386753)
94. Nielubowicz GR, Mobley HLT. Host-pathogen interactions in urinary tract infection. Nat Rev Urol. 2010;7(8):430-441.
95. Ramanathan B, Davis EG, Ross CR, Blecha F. Cathelicidins: microbicidal activity, mechanisms of action, and roles in innate immunity. Microbes Infect. 2002;4(3):361-372. (Pubitemid 34293642)
96. Ganz T. Defensins: antimicrobial peptides of innate immunity. Nat Rev Immunol. 2003;3(9):710-720. (Pubitemid 41070812)
97. Gauer S, et al. IL-18 is expressed in the intercalated cell of human kidney. Kidney Int. 2007;72(9):1081-1087. (Pubitemid 47609039)
98. Barasch J, et al. Mesenchymal to epithelial conversion in rat metanephros is induced by LIF. Cell. 1999;99(4):377-386.
99. Shao X, Somlo S, Igarashi P. Epithelial-specific Cre/lox recombination in the developing kidney and genitourinary tract. J Am Soc Nephrol. 2002;13(7):1837-1846. (Pubitemid 34700608)
100. Yamaguchi Y, Yonemura S, Takada S. Grainyheadrelated transcription factor is required for duct maturation in the salivary gland and the kidney of the mouse. Development. 2006;133(23):4737-4748. (Pubitemid 46063086)
101. Watts RE, et al. Contribution of siderophore systems to growth and urinary tract colonization of asymptomatic bacteriuria Escherichia coli. Infect Immun. 2012;80(1):333-344.
102. Bachman MA, Miller VL, Weiser JN. Mucosal lipocalin 2 has pro-inflammatory and iron-sequestering effects in response to bacterial enterobactin. PLoS Pathog. 2009;5(10):e1000622.
103. Bao G, et al. Iron traffics in circulation bound to a siderocalin (Ngal)-catechol complex. Nat Chem Biol. 2010;6(8):602-609.
104. Devireddy LR, Gazin C, Zhu X, Green MR. A cellsurface receptor for lipocalin 24p3 selectively mediates apoptosis and iron uptake. Cell. 2005; 123(7):1293-1305. (Pubitemid 41821786)
105. Subcommittee on Urinary Tract Infection, Steering Committee on Quality Improvement Management, Roberts KB. Urinary tract infection: clinical practice guideline for the diagnosis and management of the initial UTI in febrile infants and children 2 to 24 months. Pediatrics. 2011;128(3):595-610.
106. Hagberg L, Hull R, Hull S, McGhee JR, Michalek SM, Svanborg Eden C. Difference in susceptibility to gram-negative urinary tract infection between C3H/HeJ and C3H/HeN mice. Infect Immun. 1984;46(3):839-844. (Pubitemid 15211093)
107. Schilling JD, Martin SM, Hung CS, Lorenz RG, Hultgren SJ. Toll-like receptor 4 on stromal hematopoietic cells mediates innate resistance to uropathogenic Escherichia coli. Proc Natl Acad Sci U S A. 2003;100(7):4203-4208. (Pubitemid 36418181)
108. Karoly E, et al. Heat shock protein 72 (HSPA1B) gene polymorphism Toll-like receptor (TLR) 4 mutation are associated with increased risk of urinary tract infection in children. Pediatr Res. 2007;61(3):371-374.
109. Hopkins WJ, Gendron-Fitzpatrick A, Balish E, Uehling DT. Time course and host responses to Escherichia coli urinary tract infection in genetically distinct mouse strains. Infect Immun. 1998; 66(6):2798-2802. (Pubitemid 28261786)
110. Schilling JD, Mulvey MA, Vincent CD, Lorenz RG, Hultgren SJ. Bacterial invasion augments epithelial cytokine responses to Escherichia coli through a lipopolysaccharide-dependent mechanism. J Immunol. 2001;166(2):1148-1155. (Pubitemid 32060274)
111. Nelson AL, Ratner AJ, Barasch J, Weiser JN. Interleukin-8 secretion in response to aferric enterobactin is potentiated by siderocalin. Infect Immun. 2007;75(6):3160-3168. (Pubitemid 46870202)
112. Agace W, Hedges S, Andersson U, Andersson J, Ceska M, Svanborg C. Selective cytokine production by epithelial cells following exposure to Escherichia coli. Infect Immun. 1993;61(2):602-609. (Pubitemid 23030850)
113. Ko YC, et al. Elevated interleukin-8 levels in the urine of patients with urinary tract infections. Infect Immun. 1993;61(4):1307-1314.
114. Heyman SN, Rosenberger C, Rosen S. Experimental ischemia-reperfusion: biases and myths-the proximal vs. distal hypoxic tubular injury debate revisited. Kidney Int. 2010;77(1):9-16.
115. di Mari JF, Davis R, Safirstein RL. MAPK activation determines renal epithelial cell survival during oxidative injury. Am J Physiol. 1999;277(2 pt 2):F195-F203. (Pubitemid 29415137)
116. Arany I, Faisal A, Nagamine Y, Safirstein RL. p66shc inhibits pro-survival epidermal growth factor receptor/ERK signaling during severe oxidative stress in mouse renal proximal tubule cells. J Biol Chem. 2008;283(10):6110-6117.
117. Rosenberger C, et al. Adaptation to hypoxia in the diabetic rat kidney. Kidney Int. 2008;73(1):34-42. (Pubitemid 350273633)
118. Brezis M, Rosen S. Hypoxia of the renal medulla-its implications for disease. N Engl J Med. 1995; 332(10):647-655.
119. DuBose TD Jr, Alpern R. Renal Tubular Acidosis. 8th ed. New York, New York, USA: McGraw-Hill; 2001.
120. Brown D, Breton S. Mitochondria-rich, proton-secreting epithelial cells. J Exp Biol. 1996; 199(pt 11):2345-2358. (Pubitemid 27040248) Kidney Diseases Kidney Diseases