Lipocalin 2: Novel component of proinflammatory signaling in Alzheimer's disease

FASEB Journal

Volumn 26, Issue 7, 2012, Pages 2811-2823

  Naudé, Petrus J W ^a,b   Nyakas, Csaba ^c,d   Eiden, Lee E ^e   Ait Ali, Djida ^e   Van Der Heide, Ragna ^a   Engelborghs, Sebastiaan ^f,g   Luiten, Paul G M ^a,b   De Deyn, Peter P ^b,f,g   Den Boer, Johan A ^b   Eisel, Ulrich L M ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c SEMMELWEIS UNIVERSITY   (Hungary)

^d INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^e NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^f ZiekenhuisNetwerk Antwerpen   (Belgium)

^g UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

Mild cognitive impairment; Neurodegeneration; TNF

Indexed keywords

AMYLOID BETA PROTEIN; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR 2;

AGED; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AUTOPSY; BRAIN CELL; BRAIN CORTEX; BRAIN TISSUE; CEREBROSPINAL FLUID; CONTROLLED STUDY; EMBRYO; FEMALE; GENE SILENCING; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MICROGLIA; MILD COGNITIVE IMPAIRMENT; MOUSE; NERVE CELL CULTURE; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION;

ACUTE-PHASE PROTEINS; AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BASE SEQUENCE; BRAIN; CASE-CONTROL STUDIES; CELLS, CULTURED; FEMALE; GENE EXPRESSION; GLUTAMIC ACID; HUMANS; INFLAMMATION MEDIATORS; LIPOCALINS; MALE; MICE; MILD COGNITIVE IMPAIRMENT; MODELS, NEUROLOGICAL; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE II; RNA, MESSENGER; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

MURINAE;

EID: 84863211375     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-202457     Document Type: Article

References (58)

1. Nelson, P. T., Braak, H., and Markesbery, W. R. (2009) Neuropathology and cognitive impairment in Alzheimer disease: a complex but coherent relationship. J. Neuropathol. Exp. Neurol. 68, 1-14
2. Small, G. W., Kepe, V., Ercoli, L. M., Siddarth, P., Bookheimer, S. Y., Miller, K. J., Lavretsky, H., Burggren, A. C., Cole, G. M., Vinters, H. V., Thompson, P. M., Huang, S.-C., Satyamurthy, N., Phelps, M. E., and Barrio, J. R. (2006) PET of brain amyloid and tau in mild cognitive impairment. N. Engl. J. Med. 355, 2652-2663 (Pubitemid 44969124)
3. Lee, Y. J., Han, S. B., Nam, S. Y., Oh, K. W., and Hong, J. T. (2010) Inflammation and Alzheimer's disease. Arch. Pharm. Res. 33, 1539-1556
4. Eikelenboom, P., Veerhuis, R., Scheper, W., Rozemuller, A. J., van Gool, W. A., and Hoozemans, J. J. (2006) The significance of neuroinflammation in understanding Alzheimer's disease. J. Neural Transm. 113, 1685-1695 (Pubitemid 44657664)
5. Rosenberg, P. B. (2005) Clinical aspects of inflammation in Alzheimer's disease. Int. Rev. Psychiatry 17, 503-514
6. Rao, J. S., Rapoport, S. I., and Kim, H. W. (2011) Altered neuroinflammatory, arachidonic acid cascade and synaptic markers in postmortem Alzheimer's disease brain. Transl. Psychiatry 1, e31
7. Zhao, M., Cribbs, D. H., Anderson, A. J., Cummings, B. J., Su, J. H., Wasserman, A. J., and Cotman, C. W. (2003) The induction of the TNFα death domain signaling pathway in Alzheimer's disease brain. Neurochem. Res. 28, 307-318 (Pubitemid 36207354)
8. Wajant, H., Pfizenmaier, K., and Scheurich, P. (2003) Tumor necrosis factor signaling. Cell Death Differ. 10, 45-65 (Pubitemid 36511832)
9. Fontaine, V., Mohand-Said, S., Hanoteau, N., Fuchs, C., Pfizenmaier, K., and Eisel, U. (2002) Neurodegenerative and neuro-protective effects of tumor necrosis factor (TNF) in retinal ischemia: opposite roles of TNF receptor 1 and TNF receptor 2. J. Neurosci. 22, 216RC
10. Chakrabarty, P., Herring, A., Ceballos-Diaz, C., Das, P., and Golde, T. E. (2011) Hippocampal expression of murine TNFαresults in attenuation of amyloid deposition in vivo. Mol. Neurodegener. 6, 16
11. Montgomery, S. L., Mastrangelo, M. A., Habib, D., Narrow, W. C., Knowlden, S. A., Wright, T. W., and Bowers, W. J. (2011) Ablation of TNF-RI/RII expression in Alzheimer's disease mice leads to an unexpected enhancement of pathology: implications for chronic Pan-TNF-α suppressive therapeutic strategies in the brain. Am. J. Pathol. 179, 2053-2070
12. He, P., Zhong, Z., Lindholm, K., Berning, L., Lee, W., Lemere, C., Staufenbiel, M., Li, R., and Shen, Y. (2007) Deletion of tumor necrosis factor death receptor inhibits amyloid β generation and prevents learning and memory deficits in Alzheimer's mice. J. Cell Biol. 178, 829-841 (Pubitemid 47347367)
13. Nijholt, I. M., Granic, I., Luiten, P. G., and Eisel, U. L. (2011) TNFR2-target for therapeutics against neurodegenerative diseases? Adv. Exp. Med. Biol. 691, 567-573
14. Kjeldsen, L., Johnsen, A. H., Sengelov, H., and Borregaard, N. (1993) Isolation and primary structure of NGAL, a novel protein associated with human neutrophil gelatinase. J. Biol. Chem. 268, 10425-10432 (Pubitemid 23150227)
15. Liu, Q., and Nilsen-Hamilton, M. (1995) Identification of a new acute phase protein. J. Biol. Chem. 270, 22565-22570
16. Wu, Z.-L., Ciallella, J. R., Flood, D. G., O'Kane, T. M., Bozyczko-Coyne, D., and Savage, M. J. (2006) Comparative analysis of cortical gene expression in mouse models of Alzheimer's disease. Neurobiol. Aging 27, 377-386 (Pubitemid 43185323)
17. Mucha, M., Skrzypiec, A. E., Schiavon, E., Attwood, B. K., Kucerova, E., and Pawlak, R. (2011) Lipocalin-2 controls neuronal excitability and anxiety by regulating dendritic spine formation and maturation. Proc. Natl. Acad. Sci. U. S. A. 108, 18436-18441
18. Hvidberg, V., Jacobsen, C., Strong, R. K., Cowland, J. B., Moestrup, S. K., and Borregaard, N. (2005) The endocytic receptor megalin binds the iron transporting neutrophil-gelatinase-associated lipocalin with high affinity and mediates its cellular uptake. FEBS Lett. 579, 773-777
19. Devireddy, L. R., Gazin, C., Zhu, X., and Green, M. R. (2005) A cell-surface receptor for lipocalin 24p3 selectively mediates apoptosis and iron uptake. Cell 123, 1293-1305 (Pubitemid 41821786)
20. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408 (Pubitemid 34164012)
21. Granic, I., Masman, M. F., Kees Mulder, C., Nijholt, I. M., Naude, P. J., de Haan, A., Borbely, E., Penke, B., Luiten, P. G., and Eisel, U. L. (2010) LPYFDa neutralizes amyloid-β-induced memory impairment and toxicity. J. Alzheimers Dis. 19, 991-1005
22. Cheng, X., Yang, L., He, P., Li, R., and Shen, Y. (2010) Differential activation of tumor necrosis factor receptors distinguishes between brains from Alzheimer's disease and nondemented patients. J. Alzheimers Dis. 19, 621-630
23. Egan, B. S., Lane, K. B., and Shepherd, V. L. (1999) PU.1 and USF are required for macrophage-specific mannose receptor promoter activity. J. Biol. Chem. 274, 9098-9107 (Pubitemid 29164717)
24. Joo, M., Hahn, Y. S., Kwon, M., Sadikot, R. T., Blackwell, T. S., and Christman, J. W. (2005) Hepatitis C virus core protein suppresses NF-κB activation and cyclooxygenase-2 expression by direct interaction with IκB kinase β. J. Virol. 79, 7648-7657 (Pubitemid 40756798)
25. Conductier, G., Blondeau, N., Guyon, A., Nahon, J. L., and Rovere, C. (2010) The role of monocyte chemoattractant protein MCP1/CCL2 in neuroinflammatory diseases. J. Neuroimmunol. 224, 93-100
26. Renner, N. A., Ivey, N. S., Redmann, R. K., Lackner, A. A., and MacLean, A. G. (2011) MCP-3/CCL7 production by astrocytes: implications for SIV neuroinvasion and AIDS encephalitis. J. Neurovirol. 17, 146-152
27. Haroutunian, V., Purohit, D. P., Perl, D. P., Marin, D., Khan, K., Lantz, M., Davis, K. L., and Mohs, R. C. (1999) Neurofibrillary tangles in nondemented elderly subjects and mild Alzheimer disease. Arch. Neurol. 56, 713-718 (Pubitemid 29266472)
28. Haroutunian, V., Perl, D. P., Purohit, D. P., Marin, D., Khan, K., Lantz, M., Davis, K. L., and Mohs, R. C. (1998) Regional distribution of neuritic plaques in the nondemented elderly and subjects with very mild Alzheimer disease. Arch. Neurol. 55, 1185-1191 (Pubitemid 28427489)
29. Braak, H., and Braak, E. (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 82, 239-259
30. Laakso, M. P., Frisoni, G. B., K̈onönen, M., Mikkonen, M., Beltramello, A., Geroldi, C., Bianchetti, A., Trabucchi, M., Soininen, H., and Aronen, H. J. (2000) Hippocampus and entorhinal cortex in frontotemporal dementia and Alzheimer's disease: a morphometric MRI study. Biol. Psychiatry 47, 1056-1063 (Pubitemid 30336214)
31. Marchetti, L., Klein, M., Schlett, K., Pfizenmaier, K., and Eisel, U. L. (2004) Tumor necrosis factor (TNF)-mediated neuroprotection against glutamate-induced excitotoxicity is enhanced by N-methyl-d-aspartate receptor activation. Essential role of a TNF receptor 2-mediated phosphatidylinositol 3-kinase-dependent NF-κB pathway. J. Biol. Chem. 279, 32869-32881 (Pubitemid 39014747)
32. Jin, D., Zhang, Y., and Chen, X. (2011) Lipocalin 2 deficiency inhibits cell proliferation, autophagy, and mitochondrial biogenesis in mouse embryonic cells. Mol. Cell. Biochem. 351, 165-172
33. Guo, H., Jin, D., Zhang, Y., Wright, W., Bazuine, M., Brockman, D. A., Bernlohr, D. A., and Chen, X. (2010) Lipocalin-2 deficiency impairs thermogenesis and potentiates diet-induced insulin resistance in mice. Diabetes 59, 1376-1385
34. Kim, S., Domon-Dell, C., Kang, J., Chung, D. H., Freund, J.-N., and Evers, B. M. (2004) Down-regulation of the tumor suppressor PTEN by the tumor necrosis factor-α/nuclear factor-κB (NF-κB)-inducing kinase/NF-κB pathway is linked to a default IκB-α autoregulatory loop. J. Biol. Chem. 279, 4285-4291 (Pubitemid 38199016)
35. Shi, H., Gu, Y., Yang, J., Xu, L., Mi, W., and Yu, W. (2008) Lipocalin 2 promotes lung metastasis of murine breast cancer cells. J. Exp. Clin. Cancer Res. 27, 83
36. Mak, L. H., Vilar, R., and Woscholski, R. (2010) Characterisation of the PTEN inhibitor VO-OHpic. J. Chem. Biol. 3, 157-163
37. Patel, J. R., and Brewer, G. J. (2008) Age-related differences in NFκB translocation and Bcl-2/Bax ratio caused by TNFα and Aβ42 promote survival in middle-age neurons and death in old neurons. Exp. Neurol. 213, 93-100
38. Grell, M., Douni, E., Wajant, H., Lohden, M., Clauss, M., Maxeiner, B., Georgopoulos, S., Lesslauer, W., Kollias, G., Pfizenmaier, K., and Scheurich, P. (1995) The transmembrane form of tumor necrosis factor is the prime activating ligand of the 80 kDa tumor necrosis factor receptor. Cell 83, 793-802
39. Grell, M., Wajant, H., Zimmermann, G., and Scheurich, P. (1998) The type 1 receptor (CD120a) is the high-affinity receptor for soluble tumor necrosis factor. Proc. Natl. Acad. Sci. U. S. A. 95, 570-575 (Pubitemid 28083784)
40. Lee, S., Lee, J., Kim, S., Park, J. Y., Lee, W. H., Mori, K., Kim, S. H., Kim, I. K., and Suk, K. (2007) A dual role of lipocalin 2 in the apoptosis and deramification of activated microglia. J. Immunol. 179, 3231-3241
41. Lee, S., Park, J. Y., Lee, W. H., Kim, H., Park, H. C., Mori, K., and Suk, K. (2009) Lipocalin-2 is an autocrine mediator of reactive astrocytosis. J. Neurosci. 29, 234-249
42. Chopra, K., Misra, S., and Kuhad, A. (2011) Neurobiological aspects of Alzheimer's disease. Expert Opin. Ther. Targets 15, 535-555
43. Bolignano, D., Della Torre, A., Lacquaniti, A., Costantino, G., Fries, W., and Buemi, M. (2010) Neutrophil gelatinase-associated lipocalin levels in patients with Crohn disease undergoing treatment with infliximab. J. Investig. Med. 58, 569-571
44. Viel, J. J., McManus, D. Q., Smith, S. S., and Brewer, G. J. (2001) Age- and concentration-dependent neuroprotection and toxicity by TNF in cortical neurons from β-amyloid. J. Neurosci. Res. 64, 454-465 (Pubitemid 32521765)
45. Fernandes, A., Barateiro, A., Falcão, A. S., Silva, S. L.-A., Vaz, A. R., Brito, M. A., Marques Silva, R. F., and Brites, D. (2011) Astrocyte reactivity to unconjugated bilirubin requires TNF-αand IL-1β receptor signaling pathways. Glia 59, 14-25
46. Veroni, C., Gabriele, L., Canini, I., Castiello, L., Coccia, E., Remoli, M. E., Columba-Cabezas, S., Aricò, E., Aloisi, F., and Agresti, C. (2010) Activation of TNF receptor 2 in microglia promotes induction of anti-inflammatory pathways. Mol. Cell. Neurosci. 45, 234-244
47. Choi, J., Lee, H.-W., and Suk, K. (2011) Increased plasma levels of lipocalin 2 in mild cognitive impairment. J. Neurol. Sci. 305, 28-33
48. Marques, F., Rodrigues, A. J., Sousa, J. C., Coppola, G., Geschwind, D. H., Sousa, N., Correia-Neves, M., and Palha, J. A. (2008) Lipocalin 2 is a choroid plexus acute-phase protein. J. Cereb. Blood Flow Metab. 28, 450-455 (Pubitemid 351304271)
49. Serot, J. M., Bene, M. C., and Faure, G. C. (2003) Choroid plexus, aging of the brain, and Alzheimer's disease. Front. Biosci. 8, s515-521
50. Alvira-Botero, X., and Carro, E. M. (2010) Clearance of amyloidbeta peptide across the choroid plexus in Alzheimer's disease. Curr. Aging Sci. 3, 219-229
51. Prvulovic, D., and Hampel, H. (2011) Amyloid β (Aβ) and phospho-tau (p-tau) as diagnostic biomarkers in Alzheimer's disease. Clin. Chem. Lab. Med. 49, 367-374
52. Zlokovic, B. V., Martel, C. L., Matsubara, E., McComb, J. G., Zheng, G., McCluskey, R. T., Frangione, B., and Ghiso, J. (1996) Glycoprotein 330/megalin: probable role in receptor-mediated transport of apolipoprotein J alone and in a complex with Alzheimer disease amyloid β at the blood-brain and bloodcerebrospinal fluid barriers. Proc. Natl. Acad. Sci. U. S. A. 93, 4229-4234
53. Hammad, S. M., Ranganathan, S., Loukinova, E., Twal, W. O., and Argraves, W. S. (1997) Interaction of apolipoprotein J-amyloid β-peptide complex with low density lipoprotein receptorrelated protein-2/megalin. J. Biol. Chem. 272, 18644-18649
54. Wang, X., Pal, R., Chen, X. W., Kumar, K. N., Kim, O. J., and Michaelis, E. K. (2007) Genome-wide transcriptome profiling of region-specific vulnerability to oxidative stress in the hippocampus. Genomics 90, 201-212 (Pubitemid 47030800)
55. Miharada, K., Hiroyama, T., Sudo, K., Danjo, I., Nagasawa, T., and Nakamura, Y. (2008) Lipocalin 2-mediated growth suppression is evident in human erythroid and monocyte/macrophage lineage cells. J. Cell. Physiol. 215, 526-537 (Pubitemid 351468965)
56. O'Connor, L., Strasser, A., O'Reilly, L. A., Hausmann, G., Adams, J. M., Cory, S., and Huang, D. C. S. (1998) Bim: a novel member of the Bcl-2 family that promotes apoptosis. EMBO J. 17, 384-395 (Pubitemid 28045479)
57. Li, P. T., Lee, Y. C., Elangovan, N., and Chu, S. T. (2007) Mouse 24p3 protein has an effect on L929 cell viability. Int. J. Biol. Sci. 3, 100-107 (Pubitemid 46238639)
58. Rathore, K. I., Berard, J. L., Redensek, A., Chierzi, S., Lopez-Vales, R., Santos, M., Akira, S., and David, S. (2011) Lipocalin 2 plays an immunomodulatory role and has detrimental effects after spinal cord injury. J. Neurosci. 31, 13412-13419