Plasma neutrophil gelatinase-associated lipocalin is primarily related to inflammation during sepsis: A translational approach

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Otto, Gordon P ^a   Hurtado Oliveros, Jorge ^a   Chung, Ha Yeun ^a   Knoll, Kristin ^a   Neumann, Thomas ^a   Müller, Hans J ^b   Herbsleb, Marco ^b   Kohl, Matthias ^c   Busch, Martin ^a   Sossdorf, Maik ^a   Claus, Ralf A ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^c FURTWANGEN UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CREATININE; INTERLEUKIN 10; INTERLEUKIN 6; INTERLEUKIN 8; LACTATE DEHYDROGENASE; LIPOCALIN; LIPOPOLYSACCHARIDE; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; ACUTE PHASE PROTEIN; BIOLOGICAL MARKER; LCN2 PROTEIN, HUMAN; LCN2 PROTEIN, MOUSE; ONCOPROTEIN;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANKYLOSING SPONDYLITIS; ARTICLE; CELL DAMAGE; CHRONIC INFLAMMATION; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; EXERCISE; FEMALE; HUMAN; IN VITRO STUDY; KIDNEY FUNCTION; KIDNEY INJURY; MALE; MIDDLE AGED; MOUSE; NONHUMAN; OBSERVATIONAL STUDY; PROTEIN BLOOD LEVEL; PSORIATIC ARTHRITIS; RHEUMATOID ARTHRITIS; SEPSIS; SEPTIC SHOCK; SURVIVAL RATE; ANIMAL; BLOOD; C57BL MOUSE; GLOMERULUS FILTRATION RATE; INFLAMMATION; INJURIES; KAPLAN MEIER METHOD; KIDNEY; METABOLISM; PATHOPHYSIOLOGY; RANDOMIZATION; RHEUMATIC DISEASE; TRANSLATIONAL RESEARCH;

MUS;

ACUTE-PHASE PROTEINS; ADULT; AGED; ANIMALS; BIOMARKERS; EXERCISE; FEMALE; GLOMERULAR FILTRATION RATE; HUMANS; INFLAMMATION; INTERLEUKIN-10; INTERLEUKIN-6; KAPLAN-MEIER ESTIMATE; KIDNEY; LIPOCALIN-2; LIPOCALINS; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; MIDDLE AGED; ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS; RANDOM ALLOCATION; RHEUMATIC DISEASES; SEPSIS; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84928914681     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0124429     Document Type: Article

References (49)

1. Chertow GM, Burdick E, Honour M, Bonventre JV, Bates DW (2005) Acute kidney injury, mortality, length of stay, and costs in hospitalized patients. J Am Soc Nephrol 16: 3365-3370. PMID: 16177006
2. Clerico A, Galli C, Fortunato A, Ronco C (2012) Neutrophil gelatinase-associated lipocalin (NGAL) as biomarker of acute kidney injury: a review of the laboratory characteristics and clinical evidences. Clin Chem Lab Med 50: 1505-1517. doi: 10.1515/cclm-2011-0814 PMID: 22962216
3. de Geus HR, Bakker J, Lesaffre EM, le Noble JL (2011) Neutrophil gelatinase-associated lipocalin at ICU admission predicts for acute kidney injury in adult patients. Am J Respir Crit Care Med 183: 907-914. doi: 10.1164/rccm.200908-1214OC PMID: 20935115
4. Kjeldsen L, Cowland JB, Borregaard N (2000) Human neutrophil gelatinase-associated lipocalin and homologous proteins in rat and mouse. Biochim Biophys Acta 1482: 272-283. PMID: 11058768
5. Cowland JB, Borregaard N (1997) Molecular characterization and pattern of tissue expression of the gene for neutrophil gelatinase-associated lipocalin from humans. Genomics 45: 17-23. PMID: 9339356
6. Mishra J, Ma Q, Prada A, Mitsnefes M, Zahedi K, et al. (2003) Identification of neutrophil gelatinase-associated lipocalin as a novel early urinary biomarker for ischemic renal injury. J Am Soc Nephrol 14: 2534-2543. PMID: 14514731
7. Kjeldsen L, Bainton DF, Sengelov H, Borregaard N (1994) Identification of neutrophil gelatinase-associated lipocalin as a novel matrix protein of specific granules in human neutrophils. Blood 83: 799-807. PMID: 8298140
8. Bao G, Clifton M, Hoette TM, Mori K, Deng SX, et al. (2010) Iron traffics in circulation bound to a siderocalin (Ngal)-catechol complex. Nat Chem Biol 6: 602-609. doi: 10.1038/nchembio.402 PMID: 20581821
9. Li JY, Ram G, Gast K, Chen X, Barasch K, et al. (2004) Detection of intracellular iron by its regulatory effect. Am J Physiol Cell Physiol 287: C1547-1559. PMID: 15282194
10. Oikonomou KA, Kapsoritakis AN, Theodoridou C, Karangelis D, Germenis A, et al. (2012) Neutrophil gelatinase-associated lipocalin (NGAL) in inflammatory bowel disease: association with pathophysiology of inflammation, established markers, and disease activity. J Gastroenterol 47: 519-530. doi: 10.1007/s00535-011-0516-5 PMID: 22200942
11. Flo TH, Smith KD, Sato S, Rodriguez DJ, Holmes MA, et al. (2004) Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 432: 917-921. PMID: 15531878
12. Landro L, Damas JK, Flo TH, Heggelund L, Ueland T, et al. (2008) Decreased serum lipocalin-2 levels in human immunodeficiency virus-infected patients: increase during highly active anti-retroviral therapy. Clin Exp Immunol 152: 57-63. doi: 10.1111/j.1365-2249.2008.03592.x PMID: 18241231
13. Meheus LA, Fransen LM, Raymackers JG, Blockx HA, Van Beeumen JJ, et al. (1993) Identification by microsequencing of lipopolysaccharide-induced proteins secreted by mouse macrophages. J Immunol 151: 1535-1547. PMID: 8335946
14. Liu Q, Nilsen-Hamilton M (1995) Identification of a new acute phase protein. J Biol Chem 270: 22565-22570. PMID: 7545679
15. Otto GP, Busch M, Sossdorf M, Claus RA (2013) Impact of sepsis-associated cytokine storm on plasma NGAL during acute kidney injury in a model of polymicrobial sepsis. Crit Care 17: 419. doi: 10.1186/cc12540 PMID: 23514603
16. Han M, Li Y, Liu M, Cong B (2012) Renal neutrophil gelatinase associated lipocalin expression in lipopolysaccharide-induced acute kidney injury in the rat. BMC Nephrol 13: 25. doi: 10.1186/1471-2369-13-25 PMID: 22564340
17. Schmidt-Ott KM, Mori K, Li JY, Kalandadze A, Cohen DJ, et al. (2007) Dual action of neutrophil gelatinase-associated lipocalin. J Am Soc Nephrol 18: 407-413. PMID: 17229907
18. Haase M, Haase-Fielitz A, Bellomo R (2012) Is there a need to reassess what defines acute kidney injury? Am J Respir Crit Care Med 185: 343-344. PMID: 22298369
19. Darmon M, Gonzalez F, Vincent F (2011) Limits of neutrophil gelatinase-associated lipocalin at intensive care unit admission for prediction of acute kidney injury. Am J Respir Crit Care Med 184: 142-143; author reply 143. PMID: 21737595
20. Otto GP, Grunwald B, Geis C, Kothe S, Hurtado-Oliveros J, et al. (2015) Impact of Antibiotic Treatment Intensity on Long-Term Sepsis-Associated Kidney Injury in a Polymicrobial Peritoneal Contamination and Infection Model. Nephron.
21. Hotchkiss RS, Monneret G, Payen D (2013) Sepsis-induced immunosuppression: from cellular dysfunctions to immunotherapy. Nat Rev Immunol 13: 862-874. doi: 10.1038/nri3552 PMID: 24232462
22. Rittirsch D, Flierl MA, Ward PA (2008) Harmful molecular mechanisms in sepsis. Nat Rev Immunol 8: 776-787. doi: 10.1038/nri2402 PMID: 18802444
23. Mellor A, Boos C, Stacey M, Hooper T, Smith C, et al. (2013) Neutrophil gelatinase-associated lipocalin: its response to hypoxia and association with acute mountain sickness. Dis Markers 35: 537-542. doi: 10.1155/2013/601214 PMID: 24227892
24. de Geus HR, Betjes MG, Schaick R, Groeneveld JA (2013) Plasma NGAL similarly predicts acute kidney injury in sepsis and nonsepsis. Biomark Med 7: 415-421. doi: 10.2217/bmm.13.5 PMID: 23734805
25. Huang HL, Nie X, Cai B, Tang JT, He Y, et al. (2013) Procalcitonin levels predict acute kidney injury and prognosis in acute pancreatitis: a prospective study. PLoS One 8: e82250. doi: 10.1371/journal.pone.0082250 PMID: 24349237
26. Bihorac A, Baslanti TO, Cuenca AG, Hobson CE, Ang D, et al. (2013) Acute kidney injury is associated with early cytokine changes after trauma. J Trauma Acute Care Surg 74: 1005-1013. doi: 10.1097/TA.0b013e31828586ec PMID: 23511138
27. Wan L, Bellomo R, Di Giantomasso D, Ronco C (2003) The pathogenesis of septic acute renal failure. Curr Opin Crit Care 9: 496-502. PMID: 14639069
28. Langenberg C, Wan L, Egi M, May CN, Bellomo R (2007) Renal blood flow and function during recovery from experimental septic acute kidney injury. Intensive Care Med 33: 1614-1618. PMID: 17572879
29. Cunningham PN, Dyanov HM, Park P, Wang J, Newell KA et al. (2002) Acute renal failure in endotoxemia is caused by TNF acting directly on TNF receptor-1 in kidney. J Immunol 168: 5817-5823. PMID: 12023385
30. Baud L, Oudinet JP, Bens M, Noe L, Peraldi MN, et al. (1989) Production of tumor necrosis factor by rat mesangial cells in response to bacterial lipopolysaccharide. Kidney Int 35: 1111-1118. PMID: 2549293
31. Bagshaw SM, Bennett M, Haase M, Haase-Fielitz A, Egi M, et al. (2010) Plasma and urine neutrophil gelatinase-associated lipocalin in septic versus non-septic acute kidney injury in critical illness. Intensive Care Med 36: 452-461. doi: 10.1007/s00134-009-1724-9 PMID: 19956924
32. Katagiri D, Doi K, Matsubara T, Negishi K, Hamasaki Y, et al. (2013) New biomarker panel of plasma neutrophil gelatinase-associated lipocalin and endotoxin activity assay for detecting sepsis in acute kidney injury. J Crit Care 28: 564-570. doi: 10.1016/j.jcrc.2013.01.009 PMID: 23499422
33. Bellmann-Weiler R, Schroll A, Engl S, Nairz M, Talasz H, et al. (2013) Neutrophil gelatinase-associated lipocalin and interleukin-10 regulate intramacrophage Chlamydia pneumoniae replication by modulating intracellular iron homeostasis. Immunobiology 218: 969-978. doi: 10.1016/j.imbio.2012.11.004 PMID: 23317919
34. Esposito BP, Breuer W, Sirankapracha P, Pootrakul P, Hershko C et al. (2003) Labile plasma iron in iron overload: redox activity and susceptibility to chelation. Blood 102: 2670-2677. PMID: 12805056
35. Tilg H, Ulmer H, Kaser A, Weiss G (2002) Role of IL-10 for induction of anemia during inflammation. J Immunol 169: 2204-2209. PMID: 12165551
36. Saraiva M, O'Garra A (2010) The regulation of IL-10 production by immune cells. Nat Rev Immunol 10: 170-181. doi: 10.1038/nri2711 PMID: 20154735
37. Nairz M, Theurl I, Schroll A, Theurl M, Fritsche G, et al. (2009) Absence of functional Hfe protects mice from invasive Salmonella enterica serovar Typhimurium infection via induction of lipocalin-2. Blood 114: 3642-3651. doi: 10.1182/blood-2009-05-223354 PMID: 19700664
38. Berger T, Togawa A, Duncan GS, Elia AJ, You-Ten A, et al. (2006) Lipocalin 2-deficient mice exhibit increased sensitivity to Escherichia coli infection but not to ischemia-reperfusion injury. Proc Natl Acad Sci U S A 103: 1834-1839. PMID: 16446425
39. Eller K, Schroll A, Banas M, Kirsch AH, Huber JM, et al. (2013) Lipocalin-2 expressed in innate immune cells is an endogenous inhibitor of inflammation in murine nephrotoxic serum nephritis. PLoS One 8: e67693. doi: 10.1371/journal.pone.0067693 PMID: 23861783
40. Roudkenar MH, Halabian R, Bahmani P, Roushandeh AM, Kuwahara Y et al. (2011) Neutrophil gelatinase-associated lipocalin: a new antioxidant that exerts its cytoprotective effect independent on Heme Oxygenase-1. Free Radic Res 45: 810-819. doi: 10.3109/10715762.2011.581279 PMID: 21545264
41. Mishra J, Mori K, Ma Q, Kelly C, Yang J, et al. (2004) Amelioration of ischemic acute renal injury by neutrophil gelatinase-associated lipocalin. J Am Soc Nephrol 15: 3073-3082. PMID: 15579510
42. Mori K, Lee HT, Rapoport D, Drexler IR, Foster K, et al. (2005) Endocytic delivery of lipocalin-siderophore-iron complex rescues the kidney from ischemia-reperfusion injury. J Clin Invest 115: 610-621. PMID: 15711640
43. Cowland JB, Muta T, Borregaard N (2006) IL-1beta-specific up-regulation of neutrophil gelatinase-associated lipocalin is controlled by IkappaB-zeta. J Immunol 176: 5559-5566. PMID: 16622025
44. Cowland JB, Sorensen OE, Sehested M, Borregaard N (2003) Neutrophil gelatinase-associated lipocalin is up-regulated in human epithelial cells by IL-1 beta, but not by TNF-alpha. J Immunol 171: 6630-6639. PMID: 14662866
45. Arena A, Stassi G, Iannello D, Gazzara D, Calapai M, et al. (2010) Both IL-1beta and TNF-alpha regulate NGAL expression in polymorphonuclear granulocytes of chronic hemodialysis patients. Mediators Inflamm 2010: 613937. doi: 10.1155/2010/613937 PMID: 21403867
46. Eichacker PQ, Parent C, Kalil A, Esposito C, Cui X, et al. (2002) Risk and the efficacy of antiinflammatory agents: retrospective and confirmatory studies of sepsis. Am J Respir Crit Care Med 166: 1197-1205. PMID: 12403688
47. Levy MM, Fink MP, Marshall JC, Abraham E, Angus D, et al. (2003) 2001 SCCM/ESICM/ACCP/ATS/SIS International Sepsis Definitions Conference. Crit Care Med 31: 1250-1256. PMID: 12682500
48. Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF 3rd, et al. (2009) A new equation to estimate glomerular filtration rate. Ann Intern Med 150: 604-612. PMID: 19414839
49. Otto GP, Neugebauer S, Claus RA, Sossdorf M (2012) Arginine metabolism is markedly impaired in polymicrobial infected mice. Crit Care 16: 412. doi: 10.1186/cc11205 PMID: 22390776