Activated microglia/macrophage whey acidic protein (AMWAP) inhibits NFΚB signaling and induces a neuroprotective phenotype in microglia

Journal of Neuroinflammation

Volumn 12, Issue 1, 2015, Pages

  Aslanidis, Alexander ^a   Karlstetter, Marcus ^a   Scholz, Rebecca ^a   Fauser, Sascha ^a   Neumann, Harald ^b   Fried, Cora ^a   Pietsch, Markus ^a   Langmann, Thomas ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

Activated microglia macrophage whey acidic protein (AMWAP); Microglia; Neurodegeneration; NF B; Photoreceptors

Indexed keywords

ACTIVATED MICROGLIA MACROPHAGE WHEY ACIDIC PROTEIN; CASPASE 3; CASPASE 7; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MARKER; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; NITRITE; PROTEASOME; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ACETYLLEUCYL-LEUCYL-NORLEUCINAL; ANTIBODY; ENZYME INHIBITOR; GM11428 PROTEIN, MOUSE; LEUPEPTIN; MESSENGER RNA; NERVE PROTEIN; NEUROPROTECTIVE AGENT;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOCYTOSIS; FILOPODIUM; MICROGLIA; NEUROPROTECTION; NONHUMAN; PARACRINE SIGNALING; PHAGOCYTOSIS; PHOTORECEPTOR; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UBIQUITINATION; ANIMAL; CELL PROLIFERATION; DRUG EFFECTS; HUMAN; IMMUNOLOGY; METABOLISM; MOUSE; PHOTORECEPTOR CELL; TRANSFORMED CELL LINE;

ANIMALS; ANTIBODIES; APOPTOSIS; CELL LINE, TRANSFORMED; CELL PROLIFERATION; ENZYME INHIBITORS; HUMANS; LEUPEPTINS; LIPOPOLYSACCHARIDES; MICE; MICROGLIA; NERVE TISSUE PROTEINS; NEUROPROTECTIVE AGENTS; NF-KAPPA B; NITRITES; PHAGOCYTOSIS; PHOTORECEPTOR CELLS; PROTEASOME ENDOPEPTIDASE COMPLEX; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 84928620390     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-015-0296-6     Document Type: Article

References (63)

1. Hanisch UK, Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci. 2007;10:1387-94.
2. Streit WJ. Microglia as neuroprotective, immunocompetent cells of the CNS. Glia. 2002;40:133-9.
3. Giulian D, Li J, Bartel S, Broker J, Li X, Kirkpatrick JB. Cell surface morphology identifies microglia as a distinct class of mononuclear phagocyte. J Neurosci. 1995;15:7712-26.
4. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, et al. ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci. 2005;8:752-8.
5. Nimmerjahn A, Kirchhoff F, Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science. 2005;308:1314-8.
6. Broderick C, Hoek RM, Forrester JV, Liversidge J, Sedgwick JD, Dick AD. Constitutive retinal CD200 expression regulates resident microglia and activation state of inflammatory cells during experimental autoimmune uveoretinitis. Am J Pathol. 2002;161:1669-77.
7. Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, Dijkstra IM, et al. Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci. 2006;9:917-24.
8. Heneka MT, Kummer MP, Latz E. Innate immune activation in neurodegenerative disease. Nat Rev Immunol. 2014;14:463-77.
9. Perry VH, Nicoll JA, Holmes C. Microglia in neurodegenerative disease. Nat Rev Neurol. 2010;6:193-201.
10. Orr CF, Rowe DB, Halliday GM. An inflammatory review of Parkinson's disease. Prog Neurobiol. 2002;68:325-40.
11. Raivich G, Banati R. Brain microglia and blood-derived macrophages: molecular profiles and functional roles in multiple sclerosis and animal models of autoimmune demyelinating disease. Brain Res Brain Res Rev. 2004;46:261-81.
12. Langmann T. Microglia activation in retinal degeneration. J Leukoc Biol. 2007;81:1345-51.
13. Karlstetter M, Scholz R, Rutar M, Wong WT, Provis JM, Langmann T. Retinal microglia: just bystander or target for therapy? Prog Retin Eye Res. 2015;45:30-57.
14. Karlstetter M, Walczak Y, Weigelt K, Ebert S, Van den Brulle J, Schwer H, et al. The novel activated microglia/macrophage WAP domain protein, AMWAP, acts as a counter-regulator of proinflammatory response. J Immunol. 2010;185:3379-90.
15. Karlstetter M, Sorusch N, Caramoy A, Dannhausen K, Aslanidis A, Fauser S, et al. Disruption of the retinitis pigmentosa 28 gene Fam161a in mice affects photoreceptor ciliary structure and leads to progressive retinal degeneration. Hum Mol Genet. 2014;23:5197-210.
16. Simpson KJ, Nicholas KR. The comparative biology of whey proteins. J Mammary Gland Biol Neoplasia. 2002;7:313-26.
17. Hennighausen LG, Sippel AE. Mouse whey acidic protein is a novel member of the family of 'four-disulfide core' proteins. Nucleic Acids Res. 1982;10:2677-84.
18. Scott A, Weldon S, Taggart CC. SLPI and elafin: multifunctional antiproteases of the WFDC family. Biochem Soc Trans. 2011;39:1437-40.
19. Bingle CD, Vyakarnam A. Novel innate immune functions of the whey acidic protein family. Trends Immunol. 2008;29:444-53.
20. Doumas S, Kolokotronis A, Stefanopoulos P. Anti-inflammatory and antimicrobial roles of secretory leukocyte protease inhibitor. Infect Immun. 2005;73:1271-4.
21. Lilo E, Wald-Altman S, Solmesky LJ, Ben Yaakov K, Gershoni-Emek N, Bulvik S, et al. Characterization of human sporadic ALS biomarkers in the familial ALS transgenic mSOD1(G93A) mouse model. Hum Mol Genet. 2013;22:4720-5.
22. Ghasemlou N, Bouhy D, Yang J, Lopez-Vales R, Haber M, Thuraisingam T, et al. Beneficial effects of secretory leukocyte protease inhibitor after spinal cord injury. Brain. 2010;133:126-38.
23. Hannila SS, Siddiq MM, Carmel JB, Hou J, Chaudhry N, Bradley PM, et al. Secretory leukocyte protease inhibitor reverses inhibition by CNS myelin, promotes regeneration in the optic nerve, and suppresses expression of the transforming growth factor-beta signaling protein Smad2. J Neurosci. 2013;33:5138-51.
24. Hannila SS. Secretory leukocyte protease inhibitor (SLPI): emerging roles in CNS trauma and repair. Neuroscientist. Published online before print August 12, 2014, doi:10.1177/1073858414546000.
25. Wulczyn FG, Krappmann D, Scheidereit C. The NF-kappa B/Rel and I kappa B gene families: mediators of immune response and inflammation. J Mol Med (Berl). 1996;74:749-69.
26. Mattson MP, Camandola S. NF-kappaB in neuronal plasticity and neurodegenerative disorders. J Clin Invest. 2001;107:247-54.
27. Krappmann D, Wulczyn FG, Scheidereit C. Different mechanisms control signal-induced degradation and basal turnover of the NF-kappaB inhibitor IkappaB alpha in vivo. EMBO J. 1996;15:6716-26.
28. Kohno H, Chen Y, Kevany BM, Pearlman E, Miyagi M, Maeda T, et al. Photoreceptor proteins initiate microglial activation via toll-like receptor 4 in retinal degeneration mediated by all-trans-retinal. J Biol Chem. 2013;288:15326-41.
29. Karin M, Ben-Neriah Y. Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu Rev Immunol. 2000;18:621-63.
30. Bhoj VG, Chen ZJ. Ubiquitylation in innate and adaptive immunity. Nature. 2009;458:430-7.
31. Taggart CC, Greene CM, McElvaney NG, O'Neill S. Secretory leucoprotease inhibitor prevents lipopolysaccharide-induced IkappaBalpha degradation without affecting phosphorylation or ubiquitination. J Biol Chem. 2002;277:33648-53.
32. Butler MW, Robertson I, Greene CM, O'Neill SJ, Taggart CC, McElvaney NG. Elafin prevents lipopolysaccharide-induced AP-1 and NF-kappaB activation via an effect on the ubiquitin-proteasome pathway. J Biol Chem. 2006;281:34730-5.
33. Dirscherl K, Karlstetter M, Ebert S, Kraus D, Hlawatsch J, Walczak Y, et al. Luteolin triggers global changes in the microglial transcriptome leading to a unique anti-inflammatory and neuroprotective phenotype. J Neuroinflammation. 2010;7:3.
34. Napoli I, Kierdorf K, Neumann H. Microglial precursors derived from mouse embryonic stem cells. Glia. 2009;57:1660-71.
35. Beutner C, Roy K, Linnartz B, Napoli I, Neumann H. Generation of microglial cells from mouse embryonic stem cells. Nat Protoc. 2010;5:1481-94.
36. Ebert S, Schoeberl T, Walczak Y, Stoecker K, Stempfl T, Moehle C, et al. Chondroitin sulfate disaccharide stimulates microglia to adopt a novel regulatory phenotype. J Leukoc Biol. 2008;84:736-40.
37. Beutner C, Linnartz-Gerlach B, Schmidt SV, Beyer M, Mallmann MR, Staratschek-Jox A, et al. Unique transcriptome signature of mouse microglia. Glia. 2013;61:1429-42.
38. O'Neill LA, Golenbock D, Bowie AG. The history of toll-like receptors - redefining innate immunity. Nat Rev Immunol. 2013;13:453-60.
39. Jin FY, Nathan C, Radzioch D, Ding A. Secretory leukocyte protease inhibitor: a macrophage product induced by and antagonistic to bacterial lipopolysaccharide. Cell. 1997;88:417-26.
40. Li Z, Moy A, Gomez SR, Franz AH, Lin-Cereghino J, Lin-Cereghino GP. An improved method for enhanced production and biological activity of human secretory leukocyte protease inhibitor (SLPI) in Pichia pastoris. Biochem Biophys Res Commun. 2010;402:519-24.
41. Li Z, Moy A, Sohal K, Dam C, Kuo P, Whittaker J, et al. Expression and characterization of recombinant human secretory leukocyte protease inhibitor (SLPI) protein from Pichia pastoris. Protein Expr Purif. 2009;67:175-81.
42. Honda K, Taniguchi T. IRFs: master regulators of signalling by toll-like receptors and cytosolic pattern-recognition receptors. Nat Rev Immunol. 2006;6:644-58.
43. Jin X, Kim SH, Jeon HM, Beck S, Sohn YW, Yin J, et al. Interferon regulatory factor 7 regulates glioma stem cells via interleukin-6 and Notch signalling. Brain. 2012;135:1055-69.
44. Kamijo R, Harada H, Matsuyama T, Bosland M, Gerecitano J, Shapiro D, et al. Requirement for transcription factor IRF-1 in NO synthase induction in macrophages. Science. 1994;263:1612-5.
45. Hamilton ST, Scott GM, Naing Z, Rawlinson WD. Human cytomegalovirus directly modulates expression of chemokine CCL2 (MCP-1) during viral replication. J Gen Virol. 2013;94:2495-503.
46. Vila-del Sol V, Punzon C, Fresno M. IFN-gamma-induced TNF-alpha expression is regulated by interferon regulatory factors 1 and 8 in mouse macrophages. J Immunol. 2008;181:4461-70.
47. Lee J, Hur J, Lee P, Kim JY, Cho N, Kim SY, et al. Dual role of inflammatory stimuli in activation-induced cell death of mouse microglial cells. Initiation of two separate apoptotic pathways via induction of interferon regulatory factor-1 and caspase-11. J Biol Chem. 2001;276:32956-65.
48. Greene CM, McElvaney NG, O'Neill SJ, Taggart CC. Secretory leucoprotease inhibitor impairs toll-like receptor 2- and 4-mediated responses in monocytic cells. Infect Immun. 2004;72:3684-7.
49. Viatour P, Merville MP, Bours V, Chariot A. Phosphorylation of NF-kappaB and IkappaB proteins: implications in cancer and inflammation. Trends Biochem Sci. 2005;30:43-52.
50. Jacobsen LC, Sorensen OE, Cowland JB, Borregaard N, Theilgaard-Monch K. The secretory leukocyte protease inhibitor (SLPI) and the secondary granule protein lactoferrin are synthesized in myelocytes, colocalize in subcellular fractions of neutrophils, and are coreleased by activated neutrophils. J Leukoc Biol. 2008;83:1155-64.
51. Taggart CC, Cryan SA, Weldon S, Gibbons A, Greene CM, Kelly E, et al. Secretory leucoprotease inhibitor binds to NF-kappaB binding sites in monocytes and inhibits p65 binding. J Exp Med. 2005;202:1659-68.
52. Gao Y, Lecker S, Post MJ, Hietaranta AJ, Li J, Volk R, et al. Inhibition of ubiquitin-proteasome pathway-mediated I kappa B alpha degradation by a naturally occurring antibacterial peptide. J Clin Invest. 2000;106:439-48.
53. Hiemstra PS, Maassen RJ, Stolk J, Heinzel-Wieland R, Steffens GJ, Dijkman JH. Antibacterial activity of antileukoprotease. Infect Immun. 1996;64:4520-4.
54. Ranganathan S, Simpson KJ, Shaw DC, Nicholas KR. The whey acidic protein family: a new signature motif and three-dimensional structure by comparative modeling. J Mol Graph Model. 1999;17:106-13.
55. Williams SE, Brown TI, Roghanian A, Sallenave JM. SLPI and elafin: one glove, many fingers. Clin Sci (Lond). 2006;110:21-35.
56. Yang J, Zhu J, Sun D, Ding A. Suppression of macrophage responses to bacterial lipopolysaccharide (LPS) by secretory leukocyte protease inhibitor (SLPI) is independent of its anti-protease function. Biochim Biophys Acta. 2005;1745:310-7.
57. Subramaniyam D, Hollander C, Westin U, Erjefalt J, Stevens T, Janciauskiene S. Secretory leukocyte protease inhibitor inhibits neutrophil apoptosis. Respirology. 2011;16:300-7.
58. Klimenkova O, Ellerbeck W, Klimiankou M, Unalan M, Kandabarau S, Gigina A, et al. A lack of secretory leukocyte protease inhibitor (SLPI) causes defects in granulocytic differentiation. Blood. 2014;123:1239-49.
59. Sierra A, Abiega O, Shahraz A, Neumann H. Janus-faced microglia: beneficial and detrimental consequences of microglial phagocytosis. Front Cell Neurosci. 2013;7:6.
60. Karlstetter M, Nothdurfter C, Aslanidis A, Moeller K, Horn F, Scholz R, et al. Translocator protein (18 kDa) (TSPO) is expressed in reactive retinal microglia and modulates microglial inflammation and phagocytosis. J Neuroinflammation. 2014;11:3.
61. Odaka C, Mizuochi T, Yang J, Ding A. Murine macrophages produce secretory leukocyte protease inhibitor during clearance of apoptotic cells: implications for resolution of the inflammatory response. J Immunol. 2003;171:1507-14.
62. Henriksen PA, Devitt A, Kotelevtsev Y, Sallenave JM. Gene delivery of the elastase inhibitor elafin protects macrophages from neutrophil elastase-mediated impairment of apoptotic cell recognition. FEBS Lett. 2004;574:80-4.
63. Mueller AM, Pedré X, Stempfl T, Kleiter I, Couillard-Despres S, Aigner L, et al. Novel role for SLPI in MOG-induced EAE revealed by spinal cord expression analysis. J Neuroinflammation. 2008;5:20.