NFκB is an unexpected major mediator of interleukin-15 signaling in cerebral endothelia

Cellular Physiology and Biochemistry

Volumn 28, Issue 1, 2011, Pages 115-124

  Stone, Kirsten P ^a   Kastin, Abba J ^a   Pan, Weihong ^a  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

Author keywords

BBB; Cytokine receptors; Endothelial cells; IL 15; NF B; TNF

Indexed keywords

3 (4 METHYLPHENYLSULFONYL) 2 PROPENENITRILE; CAVEOLIN 1; CLAUDIN 2; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 15; INTERLEUKIN 15 RECEPTOR ALPHA; INTERLEUKIN 2 RECEPTOR GAMMA; LUCIFERASE; OCCLUDIN; PROTEIN ZO2; STAT3 PROTEIN; STAT5 PROTEIN; SYNAPTOTAGMIN I; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; VIMENTIN; CLAUDIN; CLDN2 PROTEIN, MOUSE; I KAPPA B KINASE; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; BRAIN CELL; ENDOTHELIUM CELL; ENZYME ACTIVITY; GENE CONTROL; HUMAN; HUMAN CELL; MICROVASCULATURE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION; ANIMAL; BLOOD BRAIN BARRIER; CELL CULTURE; CEREBELLUM; CYTOLOGY; DRUG ANTAGONISM; ENZYME ACTIVATION; GENETICS; METABOLISM; MOUSE MUTANT; PHOSPHORYLATION; TRANSCRIPTION INITIATION;

MUS;

ANIMALS; BLOOD-BRAIN BARRIER; CAVEOLIN 1; CELLS, CULTURED; CEREBELLUM; CLAUDINS; ENDOTHELIAL CELLS; ENZYME ACTIVATION; I-KAPPA B KINASE; INTERLEUKIN-15; INTERLEUKIN-15 RECEPTOR ALPHA SUBUNIT; MICE; MICE, KNOCKOUT; NF-KAPPA B; PHOSPHORYLATION; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RELA; TRANSCRIPTIONAL ACTIVATION; TUMOR NECROSIS FACTOR-ALPHA; VIMENTIN;

EID: 80051959842     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000331720     Document Type: Article

References (54)

1. Giri JG, Ahdieh M, Eisenman J, Shanebeck K, Grabstein K, Kumaki S, Namen A, Park LS, Cosman D, Anderson D: Utilization of the beta and gamma chains of the IL-receptor by the novel cytokine IL-15. EMBO J 1994;13:2822-2830. (Pubitemid 24191692)
2. Giri JG, Kumaki S, Ahdieh M, Friend DJ, Loomis A, Shanebeck K, DuBose R, Cosman D, Park LS, Anderson DM: Identification and cloning of a novel IL-binding protein that is structurally related to the alpha chain of the IL-2 receptor. EMBO J 1995;14:3654-3663.
3. Johnston JA, Bacon CM, Finbloom DS, Rees RC, Kaplan D, Shibuya K, Ortaldo JR, Gupta S, Chen YQ, Giri JD: Tyrosine phosphorylation and activation of STAT5, STAT3, and Janus kinases by interleukins 2 and 15. Proc Natl Acad Sci USA 1995;92:8705-8709.
4. de Jong JL, Farner NL, Widmer MB, Giri JG, Sondel PM: Interaction of IL-15 with the shared IL-2 receptor beta and gamma c subunits. The IL-15/beta/gamma c receptor-ligand complex is less stable than the IL-2/beta/gamma c receptorligand complex. J Immunol 1996;156:1339-1348.
5. Nielsen M, Nordahl M, Svejgaard A, Odum N: Interleukin 2 and 15 activate Stat3alpha in human T lymphocytes. Cytokine 1998;10:735-738. (Pubitemid 28495224)
6. de Totero D, Meazza R, Capaia M, Fabbi M, Azzarone B, Balleari E, Gobbi M, Cutrona G, Ferrarini M, Ferrini S: The opposite effects of IL-15 and IL-21 on CLL B cells correlate with differential activation of the JAK/STAT and ERK1/2 pathways. Blood 2008;111:517-524.
7. Pan W, Yu C, Hsuchou H, Khan RS, Kastin AJ: Cerebral microvascular IL15 is a novel mediator of TNF action. J Neurochem 2009;111:819-827.
8. Pan W, Wu X, Kastin AJ, Zhang Y, Hsuchou H, Halberg H, Chatu F, Khan RS, Robert B, Kastin AJ: Potential protective role of IL15Ra during inflammation. J Mol Neurosci 2010;43:412-423.
9. Wu X, Pan W, He Y, Hsuchou H, Kastin AJ: Cerebral interleukin-15 shows upregulation and beneficial effects in experimental autoimmune encephalomyelitis. J Neuroimmunol 2010;223:65-72.
10. Sun SC, Ganchi PA, Beraud C, Ballard DW, Greene WC: Autoregulation of the NF-kappa B transactivator RelA (p65) by multiple cytoplasmic inhibitors containing ankyrin motifs. Proc Natl Acad Sci USA 1994;91:1346-1350.
11. Dempsey PW, Doyle SE, He JQ, Cheng G: The signaling adaptors and pathways activated by TNF superfamily. Cytokine Growth Factor Rev 2003;14:193-209. (Pubitemid 36693141)
12. Yu C, Argyropoulos G, Zhang Y, Kastin AJ, Hsuchou H, Pan W: Neuroinflammation activates Mdr1b efflux transport through NFkappaB: promoter analysis in BBB endothelia. Cell Physiol Biochem 2008;22:745-756.
13. Zhang Y, Wu X, He Y, Kastin AJ, Hsuchou H, Rosenblum CI, Pan W: Melanocortin potentiates leptin-induced STAT3 signaling via MAPK pathway. J Neurochem 2009;110:390-399.
14. Stone KP, Kastin AJ, Hsuchou H, Yu C, Pan W: Rapid endocytosis of interleukin-15 by cerebral endothelia. J Neurochem 2011;116:544-553.
15. Yu C, Kastin AJ, Ding Y, Pan W: Gamma glutamyl transpeptidase is a dynamic indicator of endothelial response to stroke. Exp Neurol 2007;203:116-122. (Pubitemid 44821169)
16. Pereno R, Giron-Michel J, Gaggero A, Cazes E, Meazza R, Monetti M, Monaco E, Mishal Z, Jasmin C, Indiveri F, Ferrini S, Azzarone B: IL-15/IL-15Ralpha intracellular trafficking in human melanoma cells and signal transduction through the IL-15Ralpha. Oncogene 2000;19:5153-5162.
17. Wang CY, Mayo MW, Korneluk RG, Goeddel DV, Baldwin AS: NF-kappaB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 1998;281:1680-1683.
18. Tiruppathi C, Shimizu J, Miyawaki-Shimizu K, Vogel SM, Bair AM, Minshall RD, Predescu D, Malik AB: Role of NFkappaB-dependent caveolin-1 expression in the mechanism of increased endothelial permeability induced by lipopolysaccharide. J Biol Chem 2008;283:4210-4218.
19. Yamamoto T, Kojima T, Murata M, Takano K, Go M, Chiba H, Sawada N: IL-1beta regulates expression of Cx32, occludin, and claudin-2 of rat hepatocytes via distinct signal transduction pathways. Exp Cell Res 2004;299:427-441. (Pubitemid 39179809)
20. Lilienbaum A, Paulin D: Activation of the human vimentin gene by the Tax human T-cell leukemia virus. I. Mechanisms of regulation by the NFkappa B transcription factor. J Biol Chem 1993;268:2180-2188. (Pubitemid 23033631)
21. Pereno R, Gaggero A, Scudeletti M, Lanza L, Meazza R, Mishal Z, Jasmin C, Indiveri F, Ferrini S, Azzarone B: IL-15/IL-15R alpha intracellular trafficking in human cells and protection from apoptosis. Ann N Y Acad Sci 1999;876:236-245. (Pubitemid 29352131)
22. Giron-Michel J, Caignard A, Fogli M, Brouty-Boye D, Briard D, van Dijk M, Meazza R, Ferrini S, Lebousse-Kerdiles C, Clay D, Bompais H, Chouaib S, Peault B, Azzarone B: Differential STAT3, STAT5, and NF-kappaB activation in human hematopoietic progenitors by endogenous interleukin-15: implications in the expression of functional molecules. Blood 2003;102:109-117. (Pubitemid 36759643)
23. Pilette C, Detry B, Guisset A, Gabriels J, Sibille Y: Induction of interleukin-10 expression through Fcalpha receptor in human monocytes and monocytederived dendritic cells: role of p38 MAPKinase. Immunol Cell Biol 2010;88:486-493.
24. Romashkova JA, Makarov SS: NFkappaB is a target of AKT in antiapoptotic PDGF signalling. Nature 1999;401:86-90.
25. Madrid LV, Mayo MW, Reuther JY, Baldwin AS: Akt stimulates the transactivation potential of the RelA/p65 Subunit of NF-kappa B through utilization of the Ikappa B kinase and activation of the mitogen-activated protein kinase p38. J Biol Chem 2001;276:18934-18940.
26. Nyga R, Pecquet C, Harir N, Gu H, Dhennin-Duthille I, Regnier A, Gouilleux-Gruart V, Lassoued K, Gouilleux F: Activated STAT5 proteins induce activation of the PI 3-kinase/Akt and Ras/MAPK pathways via the Gab2 scaffolding adapter. Biochem J 2005;390:359-366. (Pubitemid 41192263)
27. Gu H, Maeda H, Moon JJ, Lord JD, Yoakim M, Nelson BH, Neel BG: New role for Shc in activation of the phosphatidylinositol 3-kinase/Akt pathway. Mol Cell Biol 2000;20:7109-7120.
28. Gomez-Nicola D, Valle-Argos B, Nieto-Sampedro M: Blockade of IL-15 activity inhibits microglial activation through the NFkappaB, p38, and ERK1/2 pathways, reducing cytokine and chemokine release. Glia 2010;58:264-276.
29. Kempe S, Kestler H, Lasar A, Wirth T: NF-kappaB controls the global proinflammatory response in endothelial cells: evidence for the regulation of a pro-atherogenic program. Nucleic Acids Res 2005;33:5308-5319. (Pubitemid 41487834)
30. Bulfone-Paus S, Ungureanu D, Pohl T, Lindner G, Paus R, Ruckert R, Krause H, Kunzendorf U: Interleukin-15 protects from lethal apoptosis in vivo. Nat Med 1997;3:1124-1128. (Pubitemid 27444454)
31. Malamut G, El Machhour R, Montcuquet N, Martin-Lanneree S, Dusanter-Fourt I, Verkarre V, Mention JJ, Rahmi G, Kiyono H, Butz EA, Brousse N, Cellier C, Cerf-Bensussan N, Meresse B: IL-15 triggers an antiapoptotic pathway in human intraepithelial lymphocytes that is a potential new target in celiac diseaseassociated inflammation and lymphomagenesis. J Clin Invest 2010;120:2131-2143.
32. Obermeier F, Hausmann M, Kellermeier S, Kiessling S, Strauch UG, Duitman E, Bulfone-Paus S, Herfarth H, Bock J, Dunger N, Stoeck M, Scholmerich J, Falk W, Rogler G: IL-15 protects intestinal epithelial cells. Eur J Immunol 2006;36:2691-2699. (Pubitemid 44608453)
33. Hodge DL, Yang J, Buschman MD, Schaughency PM, Dang H, Bere W, Yang Y, Savan R, Subleski JJ, Yin XM, Loughran TP, Young HA: Interleukin-15 enhances proteasomal degradation of bid in normal lymphocytes: implications for large granular lymphocyte leukemias. Cancer Res 2009;69:3986-3994.
34. Huang Z, Ha GK, Petitto JM: IL-15 and IL-15R alpha gene deletion: effects on T lymphocyte trafficking and the microglial and neuronal responses to facial nerve axotomy. Neurosci Lett 2007;417:160-164. (Pubitemid 46551351)
35. Hoontrakoon R, Chu HW, Gardai SJ, Wenzel SE, McDonald P, Fadok VA, Henson PM, Bratton DL: Interleukin-15 inhibits spontaneous apoptosis in human eosinophils via autocrine production of granulocyte macrophagecolony stimulating factor and nuclear factor-kappaB activation. Am J Respir Cell Mol Biol 2002;26:404-412. (Pubitemid 34253924)
36. Yeh WC, Shahinian A, Speiser D, Kraunus J, Billia F, Wakeham A, de la Pompa JL, Ferrick D, Hum B, Iscove N, Ohashi P, Rothe M, Goeddel DV, Mak TW: Early lethality, functional NF-kappaB activation, and increased sensitivity to TNF-induced cell death in TRAF2-deficient mice. Immunity 1997;7:715-725. (Pubitemid 28156638)
37. Natoli G, Costanzo A, Guido F, Moretti F, Bernardo A, Burgio VL, Agresti C, Levrero M: Nuclear factor kBindependent cytoprotective pathways originating at tumor necrosis factor receptor-associated factor 2. J Biol Chem 1998;273:31262-31272. (Pubitemid 28533142)
38. McDonald PP, Russo MP, Ferrini S, Cassatella MA: Interleukin-15 (IL-15) induces NF-kappaB activation and IL-8 production in human neutrophils. Blood 1998;92:4828-4835. (Pubitemid 29005886)
39. Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ: Structure and function of the blood-brain barrier. Neurobiol Dis 2010;37:13-25.
40. Abbott NJ, Ronnback L, Hansson E: Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 2006;7:41-53. (Pubitemid 41828930)
41. Minshall RD, Malik AB: Transport across the endothelium: regulation of endothelial permeability. Handb Exp Pharmacol 2006;176:107-144.
42. Pan W, Kastin AJ: Tumor necrosis factor and stroke: role of the blood-brain barrier. Prog Neurobiol 2007;83:363-374. (Pubitemid 350116341)
43. Song L, Ge S, Pachter JS: Caveolin-1 regulates expression of junctionassociated proteins in brain microvascular endothelial cells. Blood 2007;109:1515-1523. (Pubitemid 46239584)
44. Amasheh M, Fromm A, Krug SM, Amasheh S, Andres S, Zeitz M, Fromm M, Schulzke JD: TNFalpha-induced and berberine-antagonized tight junction barrier impairment via tyrosine kinase, Akt and NFkappaB signaling. J Cell Sci 2010;123:4145-4155.
45. Mendez MG, Kojima S, Goldman RD: Vimentin induces changes in cell shape, motility, and adhesion during the epithelial to mesenchymal transition. FASEB J 2010;24:1838-1851.
46. Schoumacher M, Goldman RD, Louvard D, Vignjevic DM: Actin, microtubules, and vimentin intermediate filaments cooperate for elongation of invadopodia. J Cell Biol 2010;189:541-556.
47. Nishiyama R, Sakaguchi T, Kinugasa T, Gu X, MacDermott RP, Podolsky DK, Reinecker HC: Interleukin-2 receptor beta subunit-dependent and-independent regulation of intestinal epithelial tight junctions. J Biol Chem 2001;276:35571-35580.
48. Wang L, Lim EJ, Toborek M, Hennig B: The role of fatty acids and caveolin-1 in tumor necrosis factor alpha-induced endothelial cell activation. Metabolism 2008;57:1328-1339.
49. Silwedel C, Forster C: Differential susceptibility of cerebral and cerebellar murine brain microvascular endothelial cells to loss of barrier properties in response to inflammatory stimuli. J Neuroimmunol 2006;179:37-45. (Pubitemid 44441594)
50. Yu C, Kastin AJ, Pan W: Cell-type specific response to hypoxia in relation to differential cytokine receptor expression. Abstract of the Society for Neurosci 2006;83:14.
51. Fasler-Kan E, Suenderhauf C, Barteneva N, Poller B, Gygax D, Huwyler J: Cytokine signaling in the human brain capillary endothelial cell line hCMEC/D3. Brain Res 2010;1354:15-22.
52. Potokar M, Kreft M, Li L, Daniel AJ, Pangrsic T, Chowdhury HH, Pekny M, Zorec R: Cytoskeleton and vesicle mobility in astrocytes. Traffic 2007;8:12-20. (Pubitemid 44921879)
53. Haseloff RF, Krause E, Bigl M, Mikoteit K, Stanimirovic D, Blasig IE: Differential protein expression in brain capillary endothelial cells induced by hypoxia and posthypoxic reoxygenation. Proteomics 2006;6:1803-1809.
54. Deli MA, Descamps L, Dehouck MP, Cecchelli R, Joo F, Abraham CS, Torpier G: Exposure of tumor necrosis factoralpha to luminal membrane of bovine brain capillary endothelial cells cocultured with astrocytes induces a delayed increase of permeability and cytoplasmic stress fiber formation of actin. J Neurosci Res 1995;41:717-726.