Lipocalin-2 deficiency attenuates neuroinflammation and brain injury after transient middle cerebral artery occlusion in mice

Journal of Cerebral Blood Flow and Metabolism

Volumn 34, Issue 8, 2014, Pages 1306-1314

  Jin, Myungwon ^a   Kim, Jong Heon ^a   Jang, Eunha ^a   Lee, Young Mi ^a   Soo Han, Hyung ^a   Woo, Dong Kyun ^b   Park, Dong Ho ^a   Kook, Hyun ^c   Suk, Kyoungho ^a  

^a Kyungpook National University School of Medicine   (South Korea)

^b Gyeongsang National University   (South Korea)

^c Chonnam National University Medical School   (South Korea)

Author keywords

astrocyte; blood brain barrier; ischemia reperfusion; lipocain 2; microglia; neuroinflammation

Indexed keywords

EVANS BLUE; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIAL PH; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BLOOD PRESSURE; BRAIN INFARCTION; BRAIN INJURY; BRAIN PERFUSION; CARBON DIOXIDE TENSION; CELL CULTURE; CELL DEATH; COCULTURE; COMPARATIVE STUDY; CONTROLLED STUDY; ELECTRIC RESISTANCE; ENDOTHELIUM CELL; HYPOXIC ISCHEMIC ENCEPHALOPATHY; IMMUNOFLUORESCENCE; LIPOCALIN 2 DEFICIENCY; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NERVE CELL; NERVOUS SYSTEM INFLAMMATION; NEUROTOXICITY; NONHUMAN; OXYGEN SATURATION; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSIENT ISCHEMIC ATTACK; WESTERN BLOTTING; WILD TYPE;

ACUTE-PHASE PROTEINS; ANIMALS; ASTROCYTES; CELL PROLIFERATION; CELL SURVIVAL; COCULTURE TECHNIQUES; CULTURE MEDIA; DISEASE MODELS, ANIMAL; INFARCTION, MIDDLE CEREBRAL ARTERY; ISCHEMIC ATTACK, TRANSIENT; LIPOCALINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUROGLIA; NEURONS; NEUTROPHIL INFILTRATION; ONCOGENE PROTEINS; REPERFUSION INJURY;

EID: 84905495037     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2014.83     Document Type: Article

References (41)

1. 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: 1033-1043.
2. Flower DR. The lipocalin protein family: structure and function. Biochem J 1996; 318(Pt 1): 1-14.
3. Kehrer JP. Lipocalin-2: pro- or anti-apoptotic? Cell Biol Toxicol 2010; 26: 83-89.
4. Yang J, Bielenberg DR, Rodig SJ, Doiron R, Clifton MC, Kung AL et al. Lipocalin 2 promotes breast cancer progression. Proc Natl Acad Sci USA 2009; 106: 3913-3918.
5. Bolignano D, Donato V, Coppolino G, Campo S, Buemi A, Lacquaniti A et al. Neutrophil gelatinase-associated lipocalin (NGAL) as a marker of kidney damage. Am J Kidney Dis 2008; 52: 595-605.
6. Flo TH, Smith KD, Sato S, Rodriguez DJ, Holmes MA, Strong RK et al. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 2004; 432: 917-921.
7. Devireddy LR, Gazin C, Zhu X, Green MR. A cell-surface receptor for lipocalin 24p3 selectively mediates apoptosis and iron uptake. Cell 2005; 123: 1293-1305.
8. Viau A, El Karoui K, Laouari D, Burtin M, Nguyen C, Mori K et al. Lipocalin 2 is essential for chronic kidney disease progression in mice and humans. J Clin Invest 2010; 120: 4065-4076.
9. Cruz DN, Gaiao S, Maisel A, Ronco C, Devarajan P. Neutrophil gelatinaseassociated lipocalin as a biomarker of cardiovascular disease: a systematic review. Clin Chem Lab Med 2012; 50: 1533-1545.
10. Yang J, Moses MA. Lipocalin 2: a multifaceted modulator of human cancer. Cell Cycle 2009; 8: 2347-2352.
11. Sunil VR, Patel KJ, Nilsen-Hamilton M, Heck DE, Laskin JD, Laskin DL. Acute endotoxemia is associated with upregulation of lipocalin 24p3/Lcn2 in lung and liver. Exp Mol Pathol 2007; 83: 177-187.
12. Lee S, Lee J, Kim S, Park JY, Lee WH, Mori K et al. A dual role of lipocalin 2 in the apoptosis and deramification of activated microglia. J Immunol 2007; 179: 3231-3241.
13. Lee S, Park JY, Lee WH, Kim H, Park HC, Mori K et al. Lipocalin-2 is an autocrine mediator of reactive astrocytosis. J Neurosci 2009; 29: 234-249.
14. Lee S, Kim JH, Seo JW, Han HS, Lee WH, Mori K et al. Lipocalin-2 Is a chemokine inducer in the central nervous system: role of chemokine ligand 10 (CXCL10) in lipocalin-2-induced cell migration. J Biol Chem 2011; 286: 43855-43870.
15. Bi F, Huang C, Tong J, Qiu G, Huang B, Wu Q et al. Reactive astrocytes secrete lcn2 to promote neuron death. Proc Natl Acad Sci USA 2013; 110: 4069-4074.
16. Lee S, Lee WH, Lee MS, Mori K, Suk K. Regulation by lipocalin-2 of neuronal cell death, migration, and morphology. J Neurosci Res 2012; 90: 540-550.
17. Ip JP, Nocon AL, Hofer MJ, Lim SL, Muller M, Campbell IL. Lipocalin 2 in the central nervous system host response to systemic lipopolysaccharide administration. J Neuroinflammation 2011; 8: 124.
18. Zamanian JL, Xu L, Foo LC, Nouri N, Zhou L, Giffard RG et al. Genomic analysis of reactive astrogliosis. J Neurosci 2012; 32: 6391-6410.
19. Berard JL, Zarruk JG, Arbour N, Prat A, Yong VW, Jacques FH et al. Lipocalin 2 is a novel immune mediator of experimental autoimmune encephalomyelitis pathogenesis and is modulated in multiple sclerosis. Glia 2012; 60: 1145-1159.
20. Dong M, Xi G, Keep RF, Hua Y. Role of iron in brain lipocalin 2 upregulation after intracerebral hemorrhage in rats. Brain Res 2013; 1505: 86-92.
21. Rathore KI, Berard JL, Redensek A, Chierzi S, Lopez-Vales R, Santos M et al. Lipocalin 2 plays an immunomodulatory role and has detrimental effects after spinal cord injury. J Neurosci 2011; 31: 13412-13419.
22. MacManus JP, Graber T, Luebbert C, Preston E, Rasquinha I, Smith B et al. Translation-state analysis of gene expression in mouse brain after focal ischemia. J Cereb Blood Flow Metab 2004; 24: 657-667.
23. Fernandez-Cadenas I, Rio-Espinola AD, Domingues-Montanari S, Mendioroz M, Fernandez-Morales J, Penalba A et al. Genes involved in hemorrhagic transformations that follow recombinant t-PA treatment in stroke patients. Pharmacogenomics 2013; 14: 495-504.
24. Chan CP, Jiang HL, Leung LY, Wan WM, Cheng NM, Ip WS et al. Multiple atherosclerosis- related biomarkers associated with short- and long-term mortality after stroke. Clin Biochem 2012; 45: 1308-1315.
25. Elkind MS. Inflammatory mechanisms of stroke. Stroke 2010; 41(10 Suppl): S3-S8.
26. Jin R, Yang G, Li G. Inflammatory mechanisms in ischemic stroke: role of inflammatory cells. J Leukoc Biol 2010; 87: 779-789.
27. Wang Q, Tang XN, Yenari MA. The inflammatory response in stroke. J Neuroimmunol 2007; 184: 53-68.
28. Nairz M, Theurl I, Schroll A, Theurl M, Fritsche G, Lindner E et al. Absence of functional Hfe protects mice from invasive Salmonella enterica serovar Typhimurium infection via induction of lipocalin-2. Blood 2009; 114: 3642-3651.
29. Han RQ, Ouyang YB, Xu L, Agrawal R, Patterson AJ, Giffard RG. Postischemic brain injury is attenuated in mice lacking the beta2-adrenergic receptor. Anesth Analg 2009; 108: 280-287.
30. Rice 3rd JE, Vannucci RC, Brierley JB. The influence of immaturity on hypoxicischemic brain damage in the rat. Ann Neurol 1981; 9: 131-141.
31. Bao Y, Qin L, Kim E, Bhosle S, Guo H, Febbraio M et al. CD36 is involved in astrocyte activation and astroglial scar formation. J Cereb Blood Flow Metab 2012; 32: 1567-1577.
32. Lee S, Jang E, Kim JH, Lee WH, Suk K. Lipocalin-type prostaglandin D2 synthase protein regulates glial cell migration and morphology through myristoylated alanine-rich C-kinase substrate: prostaglandin D2-independent effects. J Biol Chem 2012; 287: 9414-9428.
33. Ren X, Akiyoshi K, Dziennis S, Vandenbark AA, Herson PS, Hurn PD et al. Regulatory B cells limit CNS inflammation and neurologic deficits in murine experimental stroke. J Neurosci 2011; 31: 8556-8563.
34. Yenari MA, Xu L, Tang XN, Qiao Y, Giffard RG. Microglia potentiate damage to blood-brain barrier constituents: improvement by minocycline in vivo and in vitro. Stroke 2006; 37: 1087-1093.
35. Ock J, Han HS, Hong SH, Lee SY, Han YM, Kwon BM et al. Obovatol attenuates microglia-mediated neuroinflammation by modulating redox regulation. Br J Pharmacol 2010; 159: 1646-1662.
36. Faul F, Erdfelder E, Buchner A, Lang AG. Statistical power analyses using G*Power 3.1: tests for correlation and regression analyses. Behav Res Methods 2009; 41: 1149-1160.
37. Lo EH. A new penumbra: transitioning from injury into repair after stroke. Nat Med 2008; 14: 497-500.
38. Sandoval KE, Witt KA. Blood-brain barrier tight junction permeability and ischemic stroke. Neurobiol Dis 2008; 32: 200-219.
39. Abbott NJ, Ronnback L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 2006; 7: 41-53.
40. Mishra J, Ma Q, Prada A, Mitsnefes M, Zahedi K, Yang 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: 2534-2543.
41. Sickinger S, Maier H, Konig S, Vallant N, Kofler M, Schumpp P et al. Lipocalin-2 as mediator of chemokine expression and granulocyte infiltration during ischemia and reperfusion. Transpl Int 2013; 26: 761-769.