Thymoquinone-induced Neu4 sialidase activates NFκB in macrophage cells and pro-inflammatory cytokines in vivo

Glycoconjugate Journal

Volumn 27, Issue 6, 2010, Pages 583-600

  Finlay, Trisha M ^a,d   Abdulkhalek, Samar ^a   Gilmour, Alanna ^a   Guzzo, Christina ^a   Jayanth, Preethi ^a   Amith, Schammim Ray ^a,e   Gee, Katrina ^a   Beyaert, Rudi ^b,c   Szewczuk, Myron R ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c GHENT UNIVERSITY   (Belgium)

^d UNIVERSITY OF CALGARY   (Canada)

^e UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Cell signaling; Cellular sialidase; Cytokines; Neu4 sialidase; NF B; Receptor activation; Thymoquinone; TOLL like receptor 4

Indexed keywords

CARBOXYPEPTIDASE C; CD14 ANTIGEN; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; DNA; G PROTEIN COUPLED RECEPTOR; GAMMA INTERFERON; GELATINASE B; ILOMASTAT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELOID DIFFERENTIATION FACTOR 88; OSELTAMIVIR; PERTUSSIS TOXIN; PROTEIN MD 2; SIALIDASE; THYMOQUINONE; TOLL LIKE RECEPTOR 4; TRIGGERING RECEPTOR EXPRESSED ON MYELOID CELLS 1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BLACK CUMIN; CELL NUCLEUS; CELL STIMULATION; CELL SURFACE; COMPLEX FORMATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DNA BINDING; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; FLOW CYTOMETRY; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; INHIBITION KINETICS; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; SPECTROFLUOROMETRY; WESTERN BLOTTING;

ANIMALS; BENZOQUINONES; BONE MARROW CELLS; CELLS, CULTURED; CYTOKINES; DIPEPTIDES; ENZYME ACTIVATION; ENZYME INDUCTION; HUMANS; INFLAMMATION MEDIATORS; LYMPHOCYTE ANTIGEN 96; MACROPHAGES; MATRIX METALLOPROTEINASE 9; MICE; MYELOID DIFFERENTIATION FACTOR 88; NEURAMINIDASE; NF-KAPPA B; OSELTAMIVIR; PERTUSSIS TOXIN; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN TRANSPORT; RECEPTORS, G-PROTEIN-COUPLED; TIME FACTORS; TOLL-LIKE RECEPTOR 4;

MUS; NIGELLA SATIVA;

EID: 77957569156     PISSN: 02820080     EISSN: 15734986     Source Type: Journal    
DOI: 10.1007/s10719-010-9302-5     Document Type: Article

References (38)

1. SR Amith P Jayanth S Franchuk S Siddiqui V Seyrantepe K Gee S Basta R Beyaert AV Pshezhetsky MR Szewczuk 2009 Dependence of pathogen molecule-induced Toll-like receptor activation and cell function on Neu1 sialidase Glycoconj. J. 26 1197 1212 1:CAS:528:DC%2BD1MXhsFGrsb7L 10.1007/s10719-009-9239-8 19430901
2. SR Amith P Jayanth S Franchuk T Finlay V Seyrantepe R Beyaert AV Pshezhetsky MR Szewczuk 2010 Neu1 desialylation of sialyl alpha-2, 3-linked beta-galactosyl residues of TOLL-like receptor 4 is essential for receptor activation and cellular signaling Cell. Signal. 22 314 324 1:CAS:528: DC%2BD1MXhsV2lu7jJ 10.1016/j.cellsig.2009.09.038 19796680
3. TM Finlay P Jayanth SR Amith A Glimour C Guzzo K Gee R Beyaert MR Szewczuk 2010 Thymoquinone from nutraceutical black cumin oil activates Neu4 sialidase in live macrophage, dendritic, and normal and type I sialidosis human fibroblast cells via GPCR Gαi proteins and matrix metalloproteinase-9 Glycoconj. J. 27 3 329 348 1:CAS:528:DC%2BC3cXktVaisbs%3D 10.1007/s10719-010- 9281-6 20213245
4. OM Fischer S Hart A Ullrich 2006 Dissecting the epidermal growth factor receptor signal transactivation pathway Methods Mol. Biol. 327 85 97 1:CAS:528:DC%2BD28Xhs1ajtb8%3D 16780214
5. M-H Lee G Murphy 2004 Matrix metalloproteinases at a glance J. Cell Sci. 117 4015 4016 1:CAS:528:DC%2BD2cXotlGrsbk%3D 10.1242/jcs.01223 15316076 (Pubitemid 39328289)
6. SM Le Gall R Auger C Dreux P Mauduit 2003 Regulated cell surface Pro-EGF ectodomain shedding is a zinc metalloprotease-dependent process J. Biol. Chem. 278 45255 45268 10.1074/jbc.M307745200 12947092 (Pubitemid 37432660)
7. S Murasawa Y Mori Y Nozawa N Gotoh M Shibuya H Masaki K Maruyama Y Tsutsumi Y Moriguchi Y Shibazaki Y Tanaka T Iwasaka M Inada H Matsubara 1998 Angiotensin II type 1 receptor-induced extracellular signal-regulated protein kinase activation is mediated by Ca2+/calmodulin-dependent transactivation of epidermal growth factor receptor Circ. Res. 82 1338 1348 1:CAS:528: DyaK1cXktFCgt7w%3D 9648731
8. M Gooz P Gooz LM Luttrell JR Raymond 2006 5-HT2A receptor induces ERK phosphorylation and proliferation through ADAM-17 Tumor Necrosis Factor-{alpha}-Converting Enzyme (TACE) activation and Heparin-bound Epidermal Growth Factor-like Growth Factor (HB-EGF) shedding in mesangial cells J. Biol. Chem. 281 21004 21012 10.1074/jbc.M512096200 16737974 (Pubitemid 44115441)
9. N Prenzel E Zwick H Daub M Leserer R Abraham C Wallasch A Ullrich 1999 EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF Nature 402 884 888 1:CAS:528: DC%2BD3cXitFSltQ%3D%3D 10622253
10. M Kovacsovics-Bankowski KL Rock 1994 Presentation of exogenous antigens by macrophages: analysis of major histocompatibility complex class I and II presentation and regulation by cytokines Eur. J. Immunol. 24 2421 2428 1:CAS:528:DyaK2cXmt1yht7k%3D 10.1002/eji.1830241024 7925570 (Pubitemid 24303087)
11. W Ma W Lim K Gee S Aucoin D Nandan M Kozlowski F Diaz-Mitoma A Kumar 2001 The p38 mitogen-activated kinase pathway regulates the human interleukin-10 promoter via the activation of Sp1 transcription factor in lipopolysaccharide- stimulated human macrophages J. Biol. Chem. 276 13664 13674 1:CAS:528: DC%2BD3MXjt12ktLk%3D 11278848
12. V Seyrantepe M Canuel S Carpentier K Landry S Durand F Liang J Zeng A Caqueret RA Gravel S Marchesini C Zwingmann J Michaud CR Morales T Levade AV Pshezhetsky 2008 Mice deficient in Neu4 sialidase exhibit abnormal ganglioside catabolism and lysosomal storage Hum. Mol. Genet. 17 1556 1568 1:CAS:528:DC%2BD1cXmvFSrtbk%3D 10.1093/hmg/ddn043 18270209 (Pubitemid 351737160)
13. V Seyrantepe A Hinek J Peng M Fedjaev S Ernest Y Kadota M Canuel K Itoh CR Morales J Lavoie J Tremblay AV Pshezhetsky 2008 Enzymatic activity of lysosomal carboxypeptidase (cathepsin) A is required for proper elastic fiber formation and inactivation of endothelin-1 Circulation 117 1973 1981 1:CAS:528:DC%2BD1cXktl2gsbg%3D 10.1161/CIRCULATIONAHA.107.733212 18391110 (Pubitemid 351543473)
14. A Alatery S Basta 2008 An efficient culture method for generating large quantities of mature mouse splenic macrophages J. Immunol. Methods 338 47 57 1:CAS:528:DC%2BD1cXhtFWlsLrJ 10.1016/j.jim.2008.07.009 18675819
15. V Seyrantepe K Landry S Trudel JA Hassan CR Morales AV Pshezhetsky 2004 Neu4, a novel human lysosomal lumen sialidase, confers normal phenotype to sialidosis and galactosialidosis cells J. Biol. Chem. 279 37021 37029 1:CAS:528:DC%2BD2cXmvFCmt7Y%3D 10.1074/jbc.M404531200 15213228 (Pubitemid 39129052)
16. KJ Ladner MA Caligiuri DC Guttridge 2003 Tumor necrosis factor-regulated biphasic activation of NF-kappa B is required for cytokine-induced loss of skeletal muscle gene products J. Biol. Chem. 278 2294 2303 1:CAS:528: DC%2BD3sXksFahsQ%3D%3D 10.1074/jbc.M207129200 12431991 (Pubitemid 36801299)
17. M Karin Y Ben-Neriah 2000 Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity Annu. Rev. Immunol. 18 621 663 1:CAS:528:DC%2BD3cXjs1Gmtro%3D 10.1146/annurev.immunol.18.1.621 10837071 (Pubitemid 30365393)
18. SC Sun PA Ganchi DW Ballard WC Greene 1993 NF-kappa B controls expression of inhibitor I kappa B alpha: evidence for an inducible autoregulatory pathway Science 259 1912 1915 1:CAS:528:DyaK3sXitFWhuro%3D 10.1126/science.8096091 8096091
19. ML Scott T Fujita HC Liou GP Nolan D Baltimore 1993 The p65 subunit of NF-kappa B regulates I kappa B by two distinct mechanisms Genes Dev. 7 1266 1276 1:CAS:528:DyaK3sXlsFyjtrk%3D 10.1101/gad.7.7a.1266 8319912
20. S Miyamoto PJ Chiao IM Verma 1994 Enhanced I kappa B alpha degradation is responsible for constitutive NF-kappa B activity in mature murine B-cell lines Mol. Cell. Biol. 14 3276 3282 1:CAS:528:DyaK2cXktVantbo%3D 8164680
21. PJ Chiao S Miyamoto IM Verma 1994 Autoregulation of I kappa B alpha activity Proc. Natl. Acad. Sci. U. S. A. 91 28 32 1:CAS:528:DyaK2cXpvVWhsg%3D%3D 10.1073/pnas.91.1.28 8278379 (Pubitemid 24018636)
22. F Arenzana-Seisdedos J Thompson MS Rodriguez F Bachelerie D Thomas RT Hay 1995 Inducible nuclear expression of newly synthesized I kappa B alpha negatively regulates DNA-binding and transcriptional activities of NF-kappa B Mol. Cell. Biol. 15 2689 2696 1:STN:280:DyaK2M3lsl2msg%3D%3D 7739549
23. C Johnson D Van Antwerp TJ Hope 1999 An N-terminal nuclear export signal is required for the nucleocytoplasmic shuttling of IkappaBalpha EMBO J. 18 6682 6693 1:CAS:528:DC%2BD3cXhslOqtA%3D%3D 10.1093/emboj/18.23.6682 10581242
24. A Bigi L Morosi C Pozzi M Forcella G Tettamanti B Venerando E Monti P Fusi 2010 Human sialidase NEU4 long and short are extrinsic proteins bound to outer mitochondrial membrane and the endoplasmic reticulum, respectively Glycobiology 20 148 157 1:CAS:528:DC%2BC3cXhtFyltA%3D%3D 10.1093/glycob/cwp156 19797320
25. T Hasegawa N Sugeno A Takeda M Matsuzaki-Kobayashi A Kikuchi K Furukawa T Miyagi Y Itoyama 2007 Role of Neu4L sialidase and its substrate ganglioside GD3 in neuronal apoptosis induced by catechol metabolites FEBS Lett 581 406 412 1:CAS:528:DC%2BD2sXhtVKnurs%3D 10.1016/j.febslet.2006.12.046 17234188 (Pubitemid 46149610)
26. P Jayanth SR Amith K Gee MR Szewczuk 2010 Neu1 sialidase and matrix metalloproteinase-9 cross-talk is essential for neurotrophin activation of Trk receptors and cellular signaling Cell. Signal. 22 1193 1205 1:CAS:528: DC%2BC3cXmtlyntbo%3D 10.1016/j.cellsig.2010.03.011 20347965
27. M El Gazzar R El Mezayen JC Marecki MR Nicolls A Canastar SC Dreskin 2006 Anti-inflammatory effect of thymoquinone in a mouse model of allergic lung inflammation Int. Immunopharmacol. 6 1135 1142 1:CAS:528:DC%2BD28XkvVyhtLg%3D 10.1016/j.intimp.2006.02.004 16714217 (Pubitemid 43728167)
28. MA El Gazzar R El Mezayen MR Nicolls SC Dreskin 2007 Thymoquinone attenuates proinflammatory responses in lipopolysaccharide-activated mast cells by modulating NF-kappaB nuclear transactivation Biochim. Biophys. Acta 1770 556 564 1:CAS:528:DC%2BD2sXit1Ggs7c%3D 17292554
29. M El Gazzar R El Mezayen MR Nicolls JC Marecki SC Dreskin 2006 Downregulation of leukotriene biosynthesis by thymoquinone attenuates airway inflammation in a mouse model of allergic asthma Biochim. Biophys. Acta 1760 1088 1095 1:CAS:528:DC%2BD28XlvF2htrg%3D 16624488 (Pubitemid 43867923)
30. R El Mezayen M El Gazzar MR Nicolls JC Marecki SC Dreskin H Nomiyama 2006 Effect of thymoquinone on cyclooxygenase expression and prostaglandin production in a mouse model of allergic airway inflammation Immunol Lett 106 72 81 1:CAS:528:DC%2BD28XntlCktL0%3D 10.1016/j.imlet.2006.04.012 16762422 (Pubitemid 44093055)
31. I Tekeoglu A Dogan L Ediz M Budancamanak A Demirel 2007 Effects of thymoquinone (volatile oil of black cumin) on rheumatoid arthritis in rat models Phytother. Res. 21 895 897 1:CAS:528:DC%2BD2sXhtFKgurbN 10.1002/ptr.2143 17562570 (Pubitemid 47401862)
32. C Gabay C Lamacchia G Palmer 2010 IL-1 pathways in inflammation and human diseases Nat. Rev. Rheumatol. 6 232 241 1:CAS:528:DC%2BC3cXktVCqtr0%3D 10.1038/nrrheum.2010.4 20177398
33. C Lamacchia G Palmer CA Seemayer D Talabot-Ayer C Gabay 2010 Enhanced Th1 and Th17 responses and arthritis severity in mice with a deficiency of myeloid cell-specific interleukin-1 receptor antagonist Arthritis Rheum. 62 452 462 1:CAS:528:DC%2BC3cXhtFGnu7%2FL 20112392
34. A Molto A Olive 2010 Anti-IL-1 molecules: new comers and new indications Jt. Bone Spine 77 102 107 1:CAS:528:DC%2BC3cXptVajtb0%3D 10.1016/j.jbspin.2009. 10.011
35. BA Fox MM Stephens 2010 Treatment of knee osteoarthritis with Orthokine-derived autologous conditioned serum Expert Rev. Clin. Immunol. 6 335 345 1:CAS:528:DC%2BC3cXlsFOgsLo%3D 20441419
36. V Volarevic A Al-Qahtani N Arsenijevic S Pajovic ML Lukic 2010 Interleukin-1 receptor antagonist (IL-1Ra) and IL-1Ra producing mesenchymal stem cells as modulators of diabetogenesis Autoimmunity 43 255 263 1:CAS:528:DC%2BC3cXlvFOit7s%3D 10.3109/08916930903305641 19845478
37. B Vicenova V Vopalensky L Burysek M Pospisek 2009 Emerging role of interleukin-1 in cardiovascular diseases Physiol. Res. 58 481 498 1:CAS:528:DC%2BD1MXhtlGgu7jK 19093736
38. G Lavi E Voronov CA Dinarello RN Apte S Cohen 2007 Sustained delivery of IL-1 Ra from biodegradable microspheres reduces the number of murine B16 melanoma lung metastases J. Control. Release 123 123 130 1:CAS:528: DC%2BD2sXhtFyku7bK 10.1016/j.jconrel.2007.07.015 17900737 (Pubitemid 47562137)