Hepcidin as a major component of renal antibacterial defenses against uropathogenic Escherichia coli

Journal of the American Society of Nephrology

Volumn 27, Issue 3, 2016, Pages 835-846

  Houamel, Dounia ^a,b,c   Ducrot, Nicolas ^a,b,c   Lefebvre, Thibaud ^a,b,c,d   Daher, Raed ^a,b,c   Moulouel, Boualem ^a,b,c   Sari, Marie Agnes ^e   Letteron, Philippe ^a,b   Lyoumi, Said ^a,b,c   Millot, Sarah ^a,b,c   Tourret, Jerome ^b,f   Bouvet, Odile ^b,f   Vaulont, Sophie ^f,g   Vandewalle, Alain ^a,b   Denamur, Erick ^b,f   Puy, Hervé ^a,b,c,d   Beaumont, Carole ^a,b,c   Gouya, Laurent ^a,b,c,d   Karim, Zoubida ^a,b,c  

^a CENTRE DE RECHERCHE SUR L INFLAMMATION   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c GREX   (France)

^d HÔPITAL LOUIS MOURIER   (France)

^e CNRS   (France)

^f UNIVERSITÉ PARIS DIDEROT   (France)

^g INSTITUT COCHIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HEPCIDIN; IRON; SMAD PROTEIN; ANTIINFECTIVE AGENT; CYTOKINE; MESSENGER RNA; STAT3 PROTEIN; STAT3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL LOAD; BACTERIAL STRAIN; BACTERIOSTASIS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EXPERIMENTAL INFECTION; FEMALE; HOST RESISTANCE; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; KIDNEY CELL; KIDNEY MEDULLA; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; URINARY TRACT INFECTION; URINE PH; UROPATHOGENIC ESCHERICHIA COLI; ANIMAL; BACTERIAL COUNT; CBA MOUSE; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; GENETICS; METABOLISM; MICROBIOLOGY; NEPHRITIS; NEUTROPHIL; PATHOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; ANTI-INFECTIVE AGENTS; BACTERIAL LOAD; CELLS, CULTURED; COLONY COUNT, MICROBIAL; CYTOKINES; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FEMALE; HEPCIDINS; IRON; KIDNEY MEDULLA; MICE; MICE, INBRED CBA; MICE, KNOCKOUT; NEPHRITIS; NEUTROPHILS; PHOSPHORYLATION; RNA, MESSENGER; SIGNAL TRANSDUCTION; SMAD PROTEINS; STAT3 TRANSCRIPTION FACTOR; URINARY TRACT INFECTIONS;

EID: 84959923301     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2014101035     Document Type: Article

References (49)

1. Kaper JB, Nataro JP, Mobley HL: Pathogenic Escherichia coli. Nat Rev Microbiol 2: 123-140, 2004
2. Totsika M, Moriel DG, Idris A, Rogers BA, Wurpel DJ, Phan MD, Paterson DL, Schembri MA: Uropathogenic Escherichia coli mediated urinary tract infection. Curr Drug Targets 13: 1386-1399, 2012
3. Foxman B: Urinary tract infection syndromes: occurrence, recurrence, bacteriology, risk factors, and disease burden. Infect Dis Clin North Am 28: 1-13, 2014
4. Foxman B, Brown P: Epidemiology of urinary tract infections: transmission and risk factors, incidence, and costs. Infect Dis Clin North Am 17: 227-241, 2003
5. Snyder JA,HaugenBJ, Buckles EL, LockatellCV, Johnson DE,Donnenberg MS, Welch RA, Mobley HL: Transcriptome of uropathogenic Escherichia coli during urinary tract infection. Infect Immun 72: 6373-6381, 2004
6. Chu BC, Garcia-Herrero A, Johanson TH, Krewulak KD, Lau CK, Peacock RS, Slavinskaya Z, Vogel HJ: Siderophore uptake in bacteria and the battle for iron with the host; a bird's eye view. Biometals 23: 601-611, 2010
7. Moulouel B, Houamel D, Delaby C, Tchernitchko D, Vaulont S, Letteron P, Thibaudeau O, Puy H, Gouya L, Beaumont C, Karim Z: Hepcidin regulates intrarenal iron handling at the distal nephron. Kidney Int 84: 756-766, 2013
8. Krause A, Neitz S,Mägert HJ, Schulz A, ForssmannWG, Schulz-Knappe P, Adermann K: LEAP-1, a novel highly disulfide-bonded human peptide, exhibits antimicrobial activity. FEBS Lett 480: 147-150, 2000
9. Park CH, Valore EV, Waring AJ, Ganz T: Hepcidin, a urinary antimicrobial peptide synthesized in the liver. JBiol Chem276: 7806-7810, 2001
10. NicolasG, BennounM, Devaux I, Beaumont C,Grandchamp B, Kahn A, Vaulont S: Lack of hepcidin gene expression and severe tissue iron overload in upstream stimulatory factor 2 (USF2) knockout mice. Proc Natl Acad Sci U S A 98: 8780-8785, 2001
11. Pigeon C, Ilyin G, Courselaud B, Leroyer P, Turlin B, Brissot P, Loréal O: A new mouse liver-specific gene, encoDing a protein homologous to human antimicrobial peptide hepcidin, is overexpressed during iron overload. J Biol Chem 276: 7811-7819, 2001
12. Nemeth E, Tuttle MS, Powelson J, Vaughn MB, Donovan A, Ward DM, Ganz T, Kaplan J: Hepcidin regulates cellular iron efflux by binDing to ferroportin and inducing its internalization. Science 306: 2090-2093, 2004
13. Delaby C, Pilard N, Gonçalves AS, Beaumont C, Canonne-Hergaux F: Presence of the iron exporter ferroportin at the plasma membrane of macrophages is enhanced by iron loaDing and down-regulated by hepcidin. Blood 106: 3979-3984, 2005
14. Yamaji S, Sharp P, Ramesh B, Srai SK: Inhibition of iron transport across human intestinal epithelial cells by hepcidin. Blood 104: 2178-2180, 2004
15. Mena NP, Esparza A, Tapia V, Valdés P, Núñez MT: Hepcidin inhibits apical iron uptake in intestinal cells. Am J Physiol Gastrointest Liver Physiol 294: G192-G198, 2008
16. Chaston T, Chung B,MascarenhasM,Marks J, Patel B, Srai SK, Sharp P: Evidence for differential effects of hepcidin in macrophages and intestinal epithelial cells. Gut 57: 374-382, 2008
17. Brasse-LagnelC,Karim Z, Letteron P, Bekri S,BadoA,BeaumontC: Intestinal DMT1 cotransporter is down-regulated by hepcidin via proteasome internalization and degradation. Gastroenterology 140: 1261-1271, e1, 2011
18. Babitt JL, Huang FW, Wrighting DM, Xia Y, Sidis Y, Samad TA, Campagna JA, Chung RT, Schneyer AL,Woolf CJ, AndrewsNC, Lin HY: Bone morphogenetic protein signaling by hemojuvelin regulates hepcidin expression. Nat Genet 38: 531-539, 2006
19. Wang RH, Li C, Xu X, Zheng Y, Xiao C, Zerfas P, Cooperman S, Eckhaus M, Rouault T, Mishra L, Deng CX: A role of SMAD4 in iron metabolism through the positive regulation of hepcidin expression. Cell Metab 2: 399-409, 2005
20. Silvestri L, Guillem F, Pagani A, Nai A, Oudin C, Silva M, Toutain F, Kannengiesser C, Beaumont C, Camaschella C, Grandchamp B: Molecular mechanisms of the defective hepcidin inhibition in TMPRSS6 mutations associatedwith iron-refractory iron deficiency anemia. Blood 113: 5605-5608, 2009
21. Ganz T, Nemeth E: Iron sequestration and anemia of inflammation. Semin Hematol 46: 387-393, 2009
22. NicolasG,ChauvetC, Viatte L, Danan JL, Bigard X, Devaux I, Beaumont C, Kahn A, Vaulont S: The gene encoDing the iron regulatory peptide hepcidin is regulated by anemia, hypoxia, and inflammation. J Clin Invest 110: 1037-1044, 2002
23. Nemeth E, Rivera S,Gabayan V, Keller C, Taudorf S, Pedersen BK,Ganz T: IL-6 mediates hypoferremia of inflammation by inducing the synthesis of the iron regulatory hormone hepcidin. J Clin Invest 113: 1271-1276, 2004
24. Besson-Fournier C, Latour C, Kautz L, Bertrand J, Ganz T, Roth MP, Coppin H: Induction of activin B by inflammatory stimuli up-regulates expression of the iron-regulatory peptide hepcidin through Smad1/5/8 signaling. Blood 120: 431-439, 2012
25. Peyssonnaux C, Zinkernagel AS, Datta V, Lauth X, Johnson RS, Nizet V: TLR4-dependent hepcidin expression by myeloid cells in response to bacterial pathogens. Blood 107: 3727-3732, 2006
26. Frazier MD, Mamo LB, Ghio AJ, Turi JL: Hepcidin expression in human airway epithelial cells is regulated by interferon-g. Respir Res 12: 100, 2011
27. Gnana-Prakasam JP, Martin PM, Mysona BA, Roon P, Smith SB, Ganapathy V: Hepcidin expression in mouse retina and its regulation via lipopolysaccharide/Toll-like receptor-4 pathway independent of Hfe. Biochem J 411: 79-88, 2008
28. Schwarz P, Kübler JA, Strnad P, Müller K, Barth TF, Gerloff A, Feick P, Peyssonnaux C, Vaulont S, Adler G, Kulaksiz H: Hepcidin is localised in gastric parietal cells, regulates acid secretion and is induced by Helicobacter pylori infection. Gut 61: 193-201, 2012
29. Kulaksiz H, Theilig F, Bachmann S, Gehrke SG, Rost D, Janetzko A, Cetin Y, Stremmel W: The iron-regulatory peptide hormone hepcidin: expression and cellular localization in the mammalian kidney. J Endocrinol 184: 361-370, 2005
30. Chassin C, Tourneur E, BensM, Vandewalle A: A role for collecting duct epithelial cells in renal antibacterial defences. CellMicrobiol 13: 1107-1113, 2011
31. Paragas N, Kulkarni R, Werth M, Schmidt-OttKM, ForsterC,Deng R, Zhang Q, SingerE, KloseAD, Shen TH, Francis KP,Ray S, Vijayakumar S, Seward S, Bovino ME, Xu K, Takabe Y, Amaral FE, Mohan S,Wax R, Corbin K, Sanna-Cherchi S, Mori K, Johnson L, Nickolas T, D'Agati V, Lin CS, Qiu A, Al-Awqati Q, Ratner AJ, Barasch J: a-Intercalated cells defend the urinary system from bacterial infection. J Clin Invest 124: 2963-2976, 2014
32. Karim Z, Attmane-Elakeb A, Sibella V, BicharaM: Acid pH increases the stability of BSC1/NKCC2 mRNA in the medullary thick ascenDing limb. J Am Soc Nephrol 14: 2229-2236, 2003
33. Karim Z, Szutkowska M, Vernimmen C, Bichara M: Recent concepts concerning the renal handling of NH3/NH4+. J Nephrol 19[Suppl 9]: S27-S32, 2006
34. Attmane-Elakeb A, Mount DB, Sibella V, Vernimmen C, Hebert SC, Bichara M: Stimulation by in vivo and in vitro metabolic acidosis of expression of rBSC-1, the Na+-K+(NH4+)-2Cl-cotransporter of the rat medullary thick ascenDing limb. J Biol Chem273: 33681-33691, 1998
35. Bobulescu IA, Moe OW: Na+/H+ exchangers in renal regulation of acid-base balance. Semin Nephrol 26: 334-344, 2006
36. Singh PK, Shiha MJ, Kumar A: Antibacterial responses of retinal Müller glia: production of antimicrobial peptides, oxidative burst and phagocytosis. J Neuroinflammation 11: 33, 2014
37. Thomson MJ, Pritchard DM, Boxall SA, Abuderman AA, Williams JM, Varro A, Crabtree JE: Gastric Helicobacter infection induces iron deficiency in the INS-GAS mouse. PLoS ONE 7: e50194, 2012
38. Muotiala A, Helander IM, Pyhälä L, Kosunen TU, Moran AP: Low biological activity of Helicobacter pylori lipopolysaccharide. Infect Immun 60: 1714-1716, 1992
39. Gaddy JA, Radin JN, Loh JT, Zhang F, Washington MK, Peek RM Jr, Algood HM, Cover TL: High dietary salt intake exacerbates Helicobacter pylori-induced gastric carcinogenesis. Infect Immun 81: 2258-2267, 2013
40. PoliM, Asperti M, Naggi A, Campostrini N, Girelli D, Corbella M, Benzi M, Besson-Fournier C, Coppin H, Maccarinelli F, Finazzi D, Arosio P: Glycol-split nonanticoagulant heparins are inhibitors of hepcidin expression in vitro and in vivo. Blood 123: 1564-1573, 2014
41. PoliM,GirelliD, CampostriniN,Maccarinelli F, FinazziD, Luscieti S,Nai A, Arosio P: Heparin: a potent inhibitor of hepcidin expression in vitro and in vivo. Blood 117: 997-1004, 2011
42. Vann WF, Schmidt MA, Jann B, Jann K: The structure of the capsular polysaccharide (K5 antigen) of urinary-tract-infective Escherichia coli 010:K5:H4. A polymer similar to desulfo-heparin. Eur J Biochem 116: 359-364, 1981
43. Schmidt MA, Jann K: Structure of the 2-keto-3-deoxy-D-manno-octonicacid-containing capsular polysaccharide (K12 antigen) of the urinarytract-infective Escherichia coli O4:K12:H-. Eur J Biochem 131: 509-517, 1983
44. Benesova K, Vujic Spasic M, Schaefer SM, Stolte J, Baehr-Ivacevic T, Waldow K, Zhou Z, Klingmueller U, Benes V, Mall MA, Muckenthaler MU: Hfe deficiency impairs pulmonary neutrophil recruitment in response to inflammation. PLoS ONE 7: e39363, 2012
45. Nairz M, Schleicher U, Schroll A, Sonnweber T, Theurl I, Ludwiczek S, TalaszH, Brandacher G,Moser PL,MuckenthalerMU, Fang FC, Bogdan C, Weiss G: Nitric oxide-mediated regulation of ferroportin-1 controls macrophage iron homeostasis and immune function in Salmonella infection. J ExpMed 210: 855-873, 2013
46. Nairz M, Fritsche G, CrouchML, Barton HC, Fang FC, Weiss G: Slc11a1 limits intracellular growth of Salmonella enterica sv. Typhimurium by promoting macrophage immune effector functions and impairing bacterial iron acquisition. Cell Microbiol 11: 1365-1381, 2009
47. Labat F, Pradillon O, Garry L, Peuchmaur M, Fantin B, Denamur E: Mutator phenotype confers advantage in Escherichia coli chronic urinary tract infection pathogenesis. FEMS Immunol Med Microbiol 44: 317-321, 2005
48. Li H, Rose MJ, Tran L, Zhang J, Miranda LP, James CA, Sasu BJ: Development of amethod for the sensitive and quantitative determination of hepcidin in human serum using LC-MS/MS. J Pharmacol Toxicol Methods 59: 171-180, 2009
49. Khemtemourian L, Desbenoit N, Mahesh P, Chatterjee S, Deschemin JC, Vaulont S, Tomas A, Sari MA, Artaud I: Synthesis and biological activity of mouse hepcidin peptide analogs containing three disulfide bridges: manual and microwave-assisted solid-phase peptide synthesis. Protein Pept Lett 19: 219-227, 2012