The PPE18 protein of Mycobacterium tuberculosis inhibits NF-κB/rel - Mediated proinflammatory cytokine production by upregulating and phosphorylating suppressor of cytokine signaling 3 protein

Journal of Immunology

Volumn 186, Issue 9, 2011, Pages 5413-5424

  Nair, Shiny ^a   Pandey, Akhilesh Datt ^a   Mukhopadhyay, Sangita ^a  

^a CENTRE FOR DNA FINGERPRINTING AND DIAGNOSTICS   (India)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 2; PROTEIN P50; PROTEIN PPE18; SMALL INTERFERING RNA; SUPPRESSOR OF CYTOKINE SIGNALING 3; SYNAPTOTAGMIN I; TRANSCRIPTION FACTOR REL; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INHIBITION; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; MACROPHAGE; MOLECULAR MECHANICS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS INHIBITION; PROTEIN TARGETING; UPREGULATION;

ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; BLOTTING, WESTERN; CELL LINE; CELL SEPARATION; CYTOKINES; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FLOW CYTOMETRY; HUMANS; IMMUNOPRECIPITATION; INFLAMMATION; MACROPHAGES; MYCOBACTERIUM TUBERCULOSIS; NF-KAPPA B; PHOSPHORYLATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TRANSCRIPTION FACTOR RELA; TRANSFECTION; TUBERCULOSIS; UP-REGULATION;

EID: 79955545573     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1000773     Document Type: Article

References (85)

1. Armstrong, J. A., and P. D. Hart. 1975. Phagosome-lysosome interactions in cultured macrophages infected with virulent tubercle bacilli. Reversal of the usual nonfusion pattern and observations on bacterial survival. J. Exp. Med. 142: 1-16.
2. Flynn, J. L., and J. Chan. 2001. Immunology of tuberculosis. Annu. Rev. Immunol. 19: 93-129.
3. Orme, I. M., and A. M. Cooper. 1999. Cytokine/chemokine cascades in immunity to tuberculosis. Immunol. Today 20: 307-312.
4. van Crevel, R., T. H. Ottenhoff, and J. W. van der Meer. 2002. Innate immunity to Mycobacterium tuberculosis. Clin. Microbiol. Rev. 15: 294-309.
5. Ottenhoff, T. H., F. A. Verreck, E. G. Lichtenauer-Kaligis, M. A. Hoeve, O. Sanal, and J. T. van Dissel. 2002. Genetics, cytokines and human infectious disease: lessons from weakly pathogenic mycobacteria and salmonellae. Nat. Genet. 32: 97-105.
6. Senaldi, G., S. Yin, C. L. Shaklee, P. F. Piguet, T. W. Mak, and T. R. Ulich. 1996. Corynebacterium parvum- and Mycobacterium bovis bacillus Calmette-Guerin-induced granuloma formation is inhibited in TNF receptor I (TNF-RI) knockout mice and by treatment with soluble TNF-RI. J. Immunol. 157: 5022-5026.
7. Roach, D. R., A. G. Bean, C. Demangel, M. P. France, H. Briscoe, and W. J. Britton. 2002. TNF regulates chemokine induction essential for cell recruitment, granuloma formation, and clearance of mycobacterial infection. J. Immunol. 168: 4620-4627.
8. Giacomini, E., E. Iona, L. Ferroni, M. Miettinen, L. Fattorini, G. Orefici, I. Julkunen, and E. M. Coccia. 2001. Infection of human macrophages and dendritic cells with Mycobacterium tuberculosis induces a differential cytokine gene expression that modulates T cell response. J. Immunol. 166: 7033-7041.
9. Nau, G. J., J. F. Richmond, A. Schlesinger, E. G. Jennings, E. S. Lander, and R. A. Young. 2002. Human macrophage activation programs induced by bacterial pathogens. Proc. Natl. Acad. Sci. USA 99: 1503-1508.
10. Koul, A., T. Herget, B. Klebl, and A. Ullrich. 2004. Interplay between mycobacteria and host signalling pathways. Nat. Rev. Microbiol. 2: 189-202.
11. Beltan, E., L. Horgen, and N. Rastogi. 2000. Secretion of cytokines by human macrophages upon infection by pathogenic and non-pathogenic mycobacteria. Microb. Pathog. 28: 313-318.
12. Falcone, V., E. B. Bassey, A. Toniolo, P. G. Conaldi, and F. M. Collins. 1994. Differential release of tumor necrosis factor-alpha from murine peritoneal macrophages stimulated with virulent and avirulent species of mycobacteria. FEMS Immunol. Med. Microbiol. 8: 225-232.
13. Stauffer, F., E. P. Petrow, H. Burgmann, W. Graninger, and A. Georgopoulos. 1994. Release of TNF α and IL6 from human monocytes infected with Mycobacterium kansasii: a comparison to Mycobacterium avium. Infection 22: 326-329.
14. Fattorini, L., Y. Xiao, B. Li, C. Santoro, F. Ippoliti, and G. Orefici. 1994. Induction of IL-1 β, IL-6, TNF-α, GM-CSF and G-CSF in human macrophages by smooth transparent and smooth opaque colonial variants of Mycobacterium avium. J. Med. Microbiol. 40: 129-133.
15. Cole, S. T., R. Brosch, J. Parkhill, T. Garnier, C. Churcher, D. Harris, S. V. Gordon, K. Eiglmeier, S. Gas, C. E. Barry, III, et al. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393: 537-544. (Pubitemid 28319235)
16. Gey van Pittius, N. C., S. L. Sampson, H. Lee, Y. Kim, P. D. van Helden, and R. M. Warren. 2006. Evolution and expansion of the Mycobacterium tuberculosis PE and PPE multigene families and their association with the duplication of the ESAT-6 (esx) gene cluster regions. BMC Evol. Biol. 6: 95.
17. Voskuil, M. I., D. Schnappinger, R. Rutherford, Y. Liu, and G. K. Schoolnik. 2004. Regulation of the Mycobacterium tuberculosis PE/PPE genes. Tuberculosis (Edinb.) 84: 256-262.
18. Brennan, M. J., and G. Delogu. 2002. The PE multigene family: a 'molecular mantra' for mycobacteria. Trends Microbiol. 10: 246-249.
19. Choudhary, R. K., S. Mukhopadhyay, P. Chakhaiyar, N. Sharma, K. J. Murthy, V. M. Katoch, and S. E. Hasnain. 2003. PPE antigen Rv2430c of Mycobacterium tuberculosis induces a strong B-cell response. Infect. Immun. 71: 6338-6343.
20. Khan, N., K. Alam, S. Nair, V. L. Valluri, K. J. Murthy, and S. Mukhopadhyay. 2008. Association of strong immune responses to PPE protein Rv1168c with active tuberculosis. Clin. Vaccine Immunol. 15: 974-980.
21. Ramakrishnan, L., N. A. Federspiel, and S. Falkow. 2000. Granuloma-specific expression of Mycobacterium virulence proteins from the glycine-rich PE-PGRS family. Science 288: 1436-1439. (Pubitemid 30366332)
22. Li, Y., E. Miltner, M. Wu, M. Petrofsky, and L. E. Bermudez. 2005. A Mycobacterium avium PPE gene is associated with the ability of the bacterium to grow in macrophages and virulence in mice. Cell. Microbiol. 7: 539-548.
23. Basu, S., S. K. Pathak, A. Banerjee, S. Pathak, A. Bhattacharyya, Z. Yang, S. Talarico, M. Kundu, and J. Basu. 2007. Execution of macrophage apoptosis by PE-PGRS33 of Mycobacterium tuberculosis is mediated by Toll-like receptor 2-dependent release of tumor necrosis factor-a. J. Biol. Chem. 282: 1039-1050.
24. Nair, S., P. A. Ramaswamy, S. Ghosh, D. C. Joshi, N. Pathak, I. Siddiqui, P. Sharma, S. E. Hasnain, S. C. Mande, and S. Mukhopadhyay. 2009. The PPE18 of Mycobacterium tuberculosis interacts with TLR2 and activates IL-10 induction in macrophage. J. Immunol. 183: 6269-6281.
25. Narayana, Y., and K. N. Balaji. 2008. NOTCH1 up-regulation and signaling involved in Mycobacterium bovis BCG-induced SOCS3 expression in macrophages. J. Biol. Chem. 283: 12501-12511.
26. Berlato, C., M. A. Cassatella, I. Kinjyo, L. Gatto, A. Yoshimura, and F. Bazzoni. 2002. Involvement of suppressor of cytokine signaling-3 as a mediator of the inhibitory effects of IL-10 on lipopolysaccharide-induced macrophage activation. J. Immunol. 168: 6404-6411. (Pubitemid 34620065)
27. Qasimi, P., A. Ming-Lum, A. Ghanipour, C. J. Ong, M. E. Cox, J. Ihle, N. Cacalano, A. Yoshimura, and A. L. Mui. 2006. Divergent mechanisms utilized by SOCS3 to mediate interleukin-10 inhibition of tumor necrosis factor a and nitric oxide production by macrophages. J. Biol. Chem. 281: 6316-6324.
28. Yokota, S., N. Yokosawa, T. Okabayashi, T. Suzutani, S. Miura, K. Jimbow, and N. Fujii. 2004. Induction of suppressor of cytokine signaling-3 by herpes simplex virus type 1 contributes to inhibition of the interferon signaling pathway. J. Virol. 78: 6282-6286. (Pubitemid 38715926)
29. Takatori, H., H. Nakajima, K. Hirose, S. Kagami, T. Tamachi, A. Suto, K. Suzuki, Y. Saito, and I. Iwamoto. 2005. Indispensable role of Stat5a in Stat6-independent Th2 cell differentiation and allergic airway inflammation. J. Immunol. 174: 3734-3740. (Pubitemid 40354085)
30. Manca, C., L. Tsenova, S. Freeman, A. K. Barczak, M. Tovey, P. J. Murray, C. Barry, and G. Kaplan. 2005. Hypervirulent M. tuberculosis W/Beijing strains upregulate type I IFNs and increase expression of negative regulators of the Jak-Stat pathway. J. Interferon Cytokine Res. 25: 694-701. (Pubitemid 43010524)
31. Imai, K., T. Kurita-Ochiai, and K. Ochiai. 2003. Mycobacterium bovis bacillus Calmette-Guérin infection promotes SOCS induction and inhibits IFN-γ-stimulated JAK/STAT signaling in J774 macrophages. FEMS Immunol. Med. Microbiol. 39: 173-180.
32. Vázquez, N., T. Greenwell-Wild, S. Rekka, J. M. Orenstein, and S. M. Wahl. 2006. Mycobacterium avium-induced SOCS contributes to resistance to IFNγ-mediated mycobactericidal activity in human macrophages. J. Leukoc. Biol. 80: 1136-1144.
33. Liu, X., Y. Zhang, Y. Yu, X. Yang, and X. Cao. 2008. SOCS3 promotes TLR4 response in macrophages by feedback inhibiting TGF-β1/Smad3 signaling. Mol. Immunol. 45: 1405-1413.
34. Frobøse, H., S. G. Rønn, P. E. Heding, H. Mendoza, P. Cohen, T. Mandrup-Poulsen, and N. Billestrup. 2006. Suppressor of cytokine Signaling-3 inhibits interleukin-1 signaling by targeting the TRAF-6/TAK1 complex. Mol. Endocrinol. 20: 1587-1596.
35. Seki, Y., H. Inoue, N. Nagata, K. Hayashi, S. Fukuyama, K. Matsumoto, O. Komine, S. Hamano, K. Himeno, K. Inagaki-Ohara, et al. 2003. SOCS-3 regulates onset and maintenance of T(H)2-mediated allergic responses. Nat. Med. 9: 1047-1054.
36. Li, Y., N. Chu, A. Rostami, and G. X. Zhang. 2006. Dendritic cells transduced with SOCS-3 exhibit a tolerogenic/DC2 phenotype that directs type 2 Th cell differentiation in vitro and in vivo. J. Immunol. 177: 1679-1688.
37. Song, M. M., and K. Shuai. 1998. The suppressor of cytokine signaling (SOCS) 1 and SOCS3 but not SOCS2 proteins inhibit interferon-mediated antiviral and antiproliferative activities. J. Biol. Chem. 273: 35056-35062.
38. Karlsen, A. E., S. G. Rønn, K. Lindberg, J. Johannesen, E. D. Galsgaard, F. Pociot, J. H. Nielsen, T. Mandrup-Poulsen, J. Nerup, and N. Billestrup. 2001. Suppressor of cytokine signaling 3 (SOCS-3) protects β -cells against interleukin-1β - and interferon-γ -mediated toxicity. Proc. Natl. Acad. Sci. USA 98: 12191-12196.
39. Jo, D., D. Liu, S. Yao, R. D. Collins, and J. Hawiger. 2005. Intracellular protein therapy with SOCS3 inhibits inflammation and apoptosis. Nat. Med. 11: 892-898.
40. Gao, H., and P. A. Ward. 2007. STAT3 and suppressor of cytokine signaling 3: potential targets in lung inflammatory responses. Expert Opin. Ther. Targets 11: 869-880.
41. Khan, N., S. Ghousunnissa, S. M. Jegadeeswaran, D. Thiagarajan, S. E. Hasnain, and S. Mukhopadhyay. 2007. Anti-B7-1/B7-2 antibody elicits innate-effector responses in macrophages through NF-kappaB-dependent pathway. Int. Immunol. 19: 477-486.
42. Alam, K., S. Ghousunnissa, S. Nair, V. L. Valluri, and S. Mukhopadhyay. 2010. Glutathione-redox balance regulates c-rel-driven IL-12 production in macrophages: possible implications in antituberculosis immunotherapy. J. Immunol. 184: 2918-2929.
43. Mukhopadhyay, S., M. Mohanty, A. Mangla, A. George, V. Bal, S. Rath, and B. Ravindran. 2002. Macrophage effector functions controlled by Bruton's tyrosine kinase are more crucial than the cytokine balance of T cell responses for microfilarial clearance. J. Immunol. 168: 2914-2921. (Pubitemid 34211671)
44. Ding, Y., D. Chen, A. Tarcsafalvi, R. Su, L. Qin, and J. S. Bromberg. 2003. Suppressor of cytokine signaling 1 inhibits IL-10-mediated immune responses. J. Immunol. 170: 1383-1391.
45. Krutzik, P. O., and G. P. Nolan. 2003. Intracellular phospho-protein staining techniques for flow cytometry: monitoring single cell signaling events. Cytometry A 55: 61-70.
46. Khan, N., S. S. Rahim, C. S. Boddupalli, S. Ghousunnissa, S. Padma, N. Pathak, D. Thiagarajan, S. E. Hasnain, and S. Mukhopadhyay. 2006. Hydrogen peroxide inhibits IL-12 p40 induction in macrophages by inhibiting c-rel translocation to the nucleus through activation of calmodulin protein. Blood 107: 1513-1520. (Pubitemid 43242389)
47. Rahim, S. S., N. Khan, C. S. Boddupalli, S. E. Hasnain, and S. Mukhopadhyay. 2005. Interleukin-10 (IL-10) mediated suppression of IL-12 production in RAW 264.7 cells also involves c-rel transcription factor. Immunology 114: 313-321. (Pubitemid 40314804)
48. Baldwin, A. S., Jr. 1996. The NF-κ B and I k B proteins: new discoveries and insights. Annu. Rev. Immunol. 14: 649-683.
49. Ghosh, S., M. J. May, and E. B. Kopp. 1998. NF-κ B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16: 225-260.
50. Murphy, T. L., M. G. Cleveland, P. Kulesza, J. Magram, and K. M. Murphy. 1995. Regulation of interleukin 12 p40 expression through an NF-kappa B halfsite. Mol. Cell. Biol. 15: 5258-5267.
51. Sanjabi, S., A. Hoffmann, H. C. Liou, D. Baltimore, and S. T. Smale. 2000. Selective requirement for c-Rel during IL-12 P40 gene induction in macrophages. Proc. Natl. Acad. Sci. USA 97: 12705-12710.
52. Ziegler-Heitbrock, H. W., T. Sternsdorf, J. Liese, B. Belohradsky, C. Weber, A. Wedel, R. Schreck, P. Bäuerle, and M. Ströbel. 1993. Pyrrolidine dithiocarbamate inhibits NF-κ B mobilization and TNF production in human monocytes. J. Immunol. 151: 6986-6993. (Pubitemid 24001073)
53. Ma, X., J. M. Chow, G. Gri, G. Carra, F. Gerosa, S. F. Wolf, R. Dzialo, and G. Trinchieri. 1996. The interleukin 12 p40 gene promoter is primed by interferon γ in monocytic cells. J. Exp. Med. 183: 147-157.
54. Takasuka, N., K. Matsuura, S. Yamamoto, and K. S. Akagawa. 1995. Suppression of TNF-α mRNA expression in LPS-primed macrophages occurs at the level of nuclear factor-κ B activation, but not at the level of protein kinase C or CD14 expression. J. Immunol. 154: 4803-4812.
55. Beg, A. A., and A. S. Baldwin, Jr. 1993. The I κ B proteins: multifunctional regulators of Rel/NF-κ B transcription factors. Genes Dev. 7: 2064-2070.
56. May, M. J., and S. Ghosh. 1997. Rel/NF-κ B and I κ B proteins: an overview. Semin. Cancer Biol. 8: 63-73.
57. Karin, M., and Y. Ben-Neriah. 2000. Phosphorylation meets ubiquitination: the control of NF-[κ]B activity. Annu. Rev. Immunol. 18: 621-663.
58. Li, Z.W.,W. Chu, Y. Hu, M. Delhase, T. Deerinck, M. Ellisman, R. Johnson, and M. Karin. 1999. The IKKbeta subunit of IkappaB kinase (IKK) is essential for nuclear factor kappaB activation and prevention of apoptosis. J. Exp. Med. 189: 1839-1845.
59. Hoffmann, A., G. Natoli, and G. Ghosh. 2006. Transcriptional regulation via the NF-kappaB signaling module. Oncogene 25: 6706-6716. (Pubitemid 44657847)
60. Marine, J. C., C. McKay, D. Wang, D. J. Topham, E. Parganas, H. Nakajima, H. Pendeville, H. Yasukawa, A. Sasaki, A. Yoshimura, and J. N. Ihle. 1999. SOCS3 is essential in the regulation of fetal liver erythropoiesis. Cell 98: 617-627.
61. Dey, B. R., R. W. Furlanetto, and P. Nissley. 2000. Suppressor of cytokine signaling (SOCS)-3 protein interacts with the insulin-like growth factor-I receptor. Biochem. Biophys. Res. Commun. 278: 38-43.
62. Sitko, J. C., C. I. Guevara, and N. A. Cacalano. 2004. Tyrosine-phosphorylated SOCS3 interacts with the Nck and Crk-L adapter proteins and regulates Nck activation. J. Biol. Chem. 279: 37662-37669.
63. Cohney, S. J., D. Sanden, N. A. Cacalano, A. Yoshimura, A. Mui, T. S. Migone, and J. A. Johnston. 1999. SOCS-3 is tyrosine phosphorylated in response to interleukin-2 and suppresses STAT5 phosphorylation and lymphocyte proliferation. Mol. Cell. Biol. 19: 4980-4988.
64. Cacalano, N. A., D. Sanden, and J. A. Johnston. 2001. Tyrosine-phosphorylated SOCS-3 inhibits STAT activation but binds to p120 RasGAP and activates Ras. Nat. Cell Biol. 3: 460-465.
65. Bode, J. G., S. Ludwig, C. A. Freitas, F. Schaper, M. Ruhl, S. Melmed, P. C. Heinrich, and D. Häussinger. 2001. The MKK6/p38 mitogen-activated protein kinase pathway is capable of inducing SOCS3 gene expression and inhibits IL-6-induced transcription. Biol. Chem. 382: 1447-1453.
66. Ehlting, C., W. S. Lai, F. Schaper, E. D. Brenndörfer, R. J. Matthes, P. C. Heinrich, S. Ludwig, P. J. Blackshear, M. Gaestel, D. Häussinger, and J. G. Bode. 2007. Regulation of suppressor of cytokine signaling 3 (SOCS3) mRNA stability by TNF-α involves activation of the MKK6/p38MAPK/MK2 cascade. J. Immunol. 178: 2813-2826.
67. Caruso, R., C. Stolfi, M. Sarra, A. Rizzo, M. C. Fantini, F. Pallone, T. T. MacDonald, and G. Monteleone. 2009. Inhibition of monocyte-derived inflammatory cytokines by IL-25 occurs via p38 Map kinase-dependent induction of Socs-3. Blood 113: 3512-3519.
68. Sommer, U., C. Schmid, R. M. Sobota, U. Lehmann, N. J. Stevenson, J. A. Johnston, F. Schaper, P. C. Heinrich, and S. Haan. 2005. Mechanisms of SOCS3 phosphorylation upon interleukin-6 stimulation. Contributions of Srcand receptor-tyrosine kinases. J. Biol. Chem. 280: 31478-31488.
69. Blake, R. A., M. A. Broome, X. Liu, J. Wu, M. Gishizky, L. Sun, and S. A. Courtneidge. 2000. SU6656, a selective src family kinase inhibitor, used to probe growth factor signaling. Mol. Cell. Biol. 20: 9018-9027.
70. Hunter, T. 1987. A tail of two src's: mutatis mutandis. Cell 49: 1-4.
71. Shiratsuchi, H., and M. D. Basson. 2004. Extracellular pressure stimulates macrophage phagocytosis by inhibiting a pathway involving FAK and ERK. Am. J. Physiol. Cell Physiol. 286: C1358-C1366.
72. Johnsen, I. B., T. T. Nguyen, M. Ringdal, A. M. Tryggestad, O. Bakke, E. Lien, T. Espevik, and M. W. Anthonsen. 2006. Toll-like receptor 3 associates with c-Src tyrosine kinase on endosomes to initiate antiviral signaling. EMBO J. 25: 3335-3346.
73. Bain, J., L. Plater, M. Elliott, N. Shpiro, C. J. Hastie, H. McLauchlan, I. Klevernic, J. S. Arthur, D. R. Alessi, and P. Cohen. 2007. The selectivity of protein kinase inhibitors: a further update. Biochem. J. 408: 297-315.
74. Lang, R., A. L. Pauleau, E. Parganas, Y. Takahashi, J. Mages, J. N. Ihle, R. Rutschman, and P. J. Murray. 2003. SOCS3 regulates the plasticity of gp130 signaling. Nat. Immunol. 4: 546-550.
75. Qin, H., C. A. Wilson, K. L. Roberts, B. J. Baker, X. Zhao, and E. N. Benveniste. 2006. IL-10 inhibits lipopolysaccharide-induced CD40 gene expression through induction of suppressor of cytokine signaling-3. J. Immunol. 177: 7761-7771.
76. Dalpke, A., K. Heeg, H. Bartz, and A. Baetz. 2008. Regulation of innate immunity by suppressor of cytokine signaling (SOCS) proteins. Immunobiology 213: 225-235. (Pubitemid 351479858)
77. Dillon, D. C., M. R. Alderson, C. H. Day, D. M. Lewinsohn, R. Coler, T. Bement, A. Campos-Neto, Y. A. Skeiky, I. M. Orme, A. Roberts, et al. 1999. Molecular characterization and human T-cell responses to a member of a novel Mycobacterium tuberculosis mtb39 gene family. Infect. Immun. 67: 2941-2950.
78. Dennis, V. A., A. Jefferson, S. R. Singh, F. Ganapamo, and M. T. Philipp. 2006. Interleukin-10 anti-inflammatory response to Borrelia burgdorferi, the agent of Lyme disease: a possible role for suppressors of cytokine signaling 1 and 3. Infect. Immun. 74: 5780-5789.
79. Cassatella, M. A., S. Gasperini, C. Bovolenta, F. Calzetti, M. Vollebregt, P. Scapini, M. Marchi, R. Suzuki, A. Suzuki, and A. Yoshimura. 1999. Interleukin-10 (IL-10) selectively enhances CIS3/SOCS3 mRNA expression in human neutrophils: evidence for an IL-10-induced pathway that is independent of STAT protein activation. Blood 94: 2880-2889. (Pubitemid 29477317)
80. Mercurio, F., B. W. Murray, A. Shevchenko, B. L. Bennett, D. B. Young, J. W. Li, G. Pascual, A. Motiwala, H. Zhu, M. Mann, and A. M. Manning. 1999. IkappaB kinase (IKK)-associated protein 1, a common component of the heterogeneous IKK complex. Mol. Cell. Biol. 19: 1526-1538.
81. Mercurio, F., H. Zhu, B. W. Murray, A. Shevchenko, B. L. Bennett, J. Li, D. B. Young, M. Barbosa, M. Mann, A. Manning, and A. Rao. 1997. IKK-1 and IKK-2: cytokine-activated IkappaB kinases essential for NF-kappaB activation. Science 278: 860-866. (Pubitemid 27467923)
82. Yin, M. J., L. B. Christerson, Y. Yamamoto, Y. T. Kwak, S. Xu, F. Mercurio, M. Barbosa, M. H. Cobb, and R. B. Gaynor. 1998. HTLV-I Tax protein binds to MEKK1 to stimulate IkappaB kinase activity and NF-kappaB activation. Cell 93: 875-884.
83. Haan, S., P. Ferguson, U. Sommer, M. Hiremath, D. W. McVicar, P. C. Heinrich, J. A. Johnston, and N. A. Cacalano. 2003. Tyrosine phosphorylation disrupts elongin interaction and accelerates SOCS3 degradation. J. Biol. Chem. 278: 31972-31979.
84. Park, S. H., K. E. Kim, H. Y. Hwang, and T. Y. Kim. 2003. Regulatory effect of SOCS on NF-kappaB activity in murine monocytes/macrophages. DNA Cell Biol. 22: 131-139.
85. Peraldi, P., C. Filloux, B. Emanuelli, D. J. Hilton, and E. Van Obberghen. 2001. Insulin induces suppressor of cytokine signaling-3 tyrosine phosphorylation through janus-activated kinase. J. Biol. Chem. 276: 24614-24620.