Pro-IL-16 is associated with MHC class II-mediated negative regulation of mouse resting B cell activation through MAP kinases, NF-κB and Skp2-dependent p27kip regulation

Scandinavian Journal of Immunology

Volumn 77, Issue 3, 2013, Pages 177-186

  Yang, H Y ^a   Kim, J ^b,c   Kim, S H ^a   Choe, C H ^a,b   Jang, Y S ^a  

^a Chonbuk National University   (South Korea)

^b Jeonju Bio Materials Institute   (South Korea)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 16; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN P27 KIP; S PHASE KINASE ASSOCIATED PROTEIN 2; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE ACTIVATION; CELL CYCLE REGULATION; CELL FUNCTION; CELL LINE; CELL MATURATION; CELL NUCLEUS; CELL PROLIFERATION; CONTROLLED STUDY; CYTOPLASM; GENE OVEREXPRESSION; GENE SILENCING; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; SIGNAL TRANSDUCTION; T CELL LYMPHOMA; T LYMPHOCYTE ACTIVATION;

ANIMALS; B-LYMPHOCYTES; BLOTTING, WESTERN; CELL LINE; CELL NUCLEUS; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P27; CYTOPLASM; HISTOCOMPATIBILITY ANTIGENS CLASS II; INTERLEUKIN-16; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICROSCOPY, CONFOCAL; MITOGEN-ACTIVATED PROTEIN KINASES; NF-KAPPA B; PROTEIN PRECURSORS; RNA INTERFERENCE; S-PHASE KINASE-ASSOCIATED PROTEINS; TANDEM MASS SPECTROMETRY;

EID: 84875590689     PISSN: 03009475     EISSN: 13653083     Source Type: Journal    
DOI: 10.1111/sji.12026     Document Type: Article

References (46)

1. Niederhuber JE, Frelinger JA, Dugan E, Coutinho A, Shreffler DC. Effects of anti-Ia serum on mitogenic responses. I. Inhibition of the proliferative response to B cell mitogen, LPS, by specific anti-Ia sera. J Immunol 1975;115:1672-6.
2. Forsgren S, Pobor G, Coutinho A, Pierres M. The role of I-A/E molecules in B lymphocyte activation. I. Inhibition of lipopolysaccharide-induced responses by monoclonal antibodies. J Immunol 1984;133:2104-10.
3. Clement LT, Tedder TF, Gartland GL. Antibodies reactive with class II antigens encoded for by the major histocompatibility complex inhibit human B cell activation. J Immunol 1986;136:2375-81.
4. Newell MK, VanderWall J, Beard KS, Freed JH. Ligation of major histocompatibility complex class II molecules mediates apoptotic cell death in resting B lymphocytes. Proc Natl Acad Sci USA 1993;90:10459-63.
5. Scholl PR, Geha RS. MHC class II signaling in B cell activation. Immunol Today 1994;15:418-22.
6. Kim J, Kim H-R, Lee J-C, Jang Y-S. Involvement of ERK, p38 MAP kinase, and PKC in MHC class II-mediated signal transduction in a resting B cell line. Biochem Biophys Res Commun 2002;291:139-45.
7. Al-Daccak R, Mooney N, Charron D. MHC class II signaling in antigen-presenting cells. Curr Opin Immunol 2004;16:108-13.
8. Bobbit KR, Justement LB. Regulation of MHC class II signal transduction by the B cell coreceptors CD19 and CD22. J Immunol 2000;165:5588-96.
9. Trede NS, Chatila T, Geha RS. Activator protein-1 (AP-1) is stimulated by microbial superantigens in human monocytic cells. Eur J Immunol 1993;23:2129-35.
10. Nashar TO, Drake JR. Dynamics of MHC class II-activating signals in murine resting B cells. J Immunol 2006;176:827-38.
11. Bishop GA. Requirements of class II-mediated B cell differentiation for class II cross-linking and cyclic AMP. J Immunol 1992;147:1107-14.
12. Haylett RS, Koch N, Rink L. MHC class II molecules activate NFAT and the ERK group of MAPK through distinct signaling pathways in B cells. Eur J Immunol 2009;39:1947-55.
13. Kissner TL, Ruthel G, Alam S, Ulrich RG, Fernandez S, Saikh KU. Activation of MyD88 signaling upon staphylococcal enterotoxin binding to MHC class II molecules. PLoS ONE 2011;6:e15985.
14. Nagy ZA, Mooney NA. A novel, alternative pathway of apoptosis triggered through class II major histocompatibility complex molecules. J Mol Med 2003;81:757-65.
15. Jin L, Stolpa JC, Young RM, Pugh-Bernard AE, Refaeli Y, Cambier JC. MHC class II structural requirements for the association with Igalpha/beta, and signaling of calcium mobilization and cell death. Immunol Lett 2008;116:184-94.
16. Yang H-Y, Kim J, Chung G-H, Lee J-C, Jang Y-S. Cross-linking of MHC class II molecules interferes with phorbol 12, 13-dibutyrate-induced differentiation of resting B cells by inhibiting Rac-associated ROS-dependent ERK/p38 MAP kinase pathways leading to NF-κB activation. Mol Immunol 2007;44:1577-86.
17. Yang H-Y, Kim J, Lee K-Y, Jang Y-S. Rac/ROS-related protein kinase C and phosphatidylinositol-3-kinase signaling are involved in a negative regulating cascade in B cell activation by antibody-mediated cross-linking of MHC class II molecules. Mol Immunol 2010;47:706-12.
18. Wilson KC, Cruikshank WW, Center DM, Zhang Y. Prointerleukin-16 contains a functional CcN motif that regulates nuclear localization. Biochemistry 2002;41:14306-12.
19. Center DM, Cruikshank WW, Zhang Y. Nuclear pro-IL-16 regulation of T cell proliferation: p27(KIP1)-dependent G0/G1 arrest mediated by inhibition of Skp2 transcription. J Immunol 2004;172:1654-60.
20. Kappler JW, Skidmore B, White J, Marrack P. Antigen-inducible, H-2-restricted, interleukin-2-producing T cell hybridomas. Lack of independent antigen and H-2 recognition. J Exp Med 1981;153:1198-214.
21. Park HJ, Kim J-Y, Jung KI, Kim TJ. Characterization of a novel gene in the extended MHC region of mouse, NG29/Cd320, a homolog of the human CD320. Immune Netw 2009;9:138-46.
22. Shin H-M, Cho W-D, Lee G-K et al. Characterization of monoclonal antibodies against human leukocyte common antigen (CD45). Immune Netw 2011;11:114-22.
23. Zhang Y, Center DM, Wu DM et al. Processing and activation of pro-interleukin-16 by caspase-3. J Biol Chem 1998;273:1144-9.
24. Zhang Y, Kornfeld H, Cruikshank WW, Kim S, Reardon CC, Center DM. Nuclear translocation of the N-terminal prodomain of interleukin-16. J Biol Chem 2001;276:1299-303.
25. Hara T, Kamura T, Nakayama K, Oshikawa K, Hatakeyama S. Degradation of p27(Kip1) at the G(0)-G(1) transition mediated by a Skp2-independent ubiquitination pathway. J Biol Chem 2001;276:48937-43.
26. Hershko DD. Oncogenic properties and prognostic implications of the ubiquitin ligase Skp2 in cancer. Cancer 2008;112:1415-24.
27. Spruck C, Strohmaier H, Watson M et al. A CDK-independent function of mammalian Cks1: targeting of SCF(Skp2) to the CDK inhibitor p27Kip1. Mol Cell 2001;7:639-50.
28. Kim J, Yang H-Y, Jang Y-S. A G protein-associated ERK pathway is involved in LPS-induced proliferation and a PTK-associated p38 MAPK pathway is involved in LPS-induced differentiation in resting B cells. Mol Immunol 2006;43:1232-42.
29. Setterblad N, Blancheteau V, Delaguillaumie A et al. Cognate MHC-TCR interaction leads to apoptosis of antigen-presenting cells. J Leukoc Biol 2004;75:1036-44.
30. Mooney NA, Grillot-Courvalin C, Hivroz C, Ju LY, Charron D. Early biochemical events after MHC class II-mediated signaling on human B lymphocytes. J Immunol 1990;145:2070-6.
31. Matsuoka T, Tabata H, Matsushita S. Monocytes are differentially activated through HLA-DR, -DQ, and -DP molecules via mitogen-activated protein kinases. J Immunol 2001;166:2202-8.
32. Angelisova P, Hilgert I, Horejsi V. Association of four antigens of the tetraspans family (CD37, CD53, TAPA-1, and R2/C33) with MHC class II glycoproteins. Immunogenetics 1994;39:249-56.
33. Rubinstein E, Le Naour F, Lagaudriere-Gesbert C, Billard M, Conjeaud H, Boucheix C. CD9, CD63, CD81, and CD82 are components of a surface tetraspan network connected to HLA-DR and VLA integrins. Eur J Immunol 1996;26:2657-65.
34. Léveillé C, Al-Daccak R, Mourad W. CD20 is physically and functionally coupled to MHC class II and CD40 on human B cell lines. Eur J Immunol 1999;29:65-74.
35. Artavanis-Tsakonas K, Kasperkovitz PV, Papa E et al. The tetraspanin CD82 is specifically recruited to fungal and bacterial phagosomes prior to acidification. Infect Immun 2011;79:1098-106.
36. Jin L, Waterman PM, Jonscher KR, Short CM, Reisdorph NA, Cambier JC. MPYS, a novel membrane tetraspanner, is associated with major histocompatibility complex class II and mediates transduction of apoptotic signals. Mol Cell Biol 2008;28:5014-26.
37. Wilson KC, Center DM, Cruikshank WW. The effect of interleukin-16 and its precursor on T lymphocyte activation and growth. Growth Factors 2004;22:97-104.
38. Kaser A, Dunzendorfer S, Offner FA et al. A role for IL-16 in the cross-talk between dendritic cells and T cells. J Immunol 1999;163:3232-8.
39. Sharma V, Sparks JL, Vail JD. Human B-cell lines constitutively express and secrete interleukin-16. Immunology 2000;99:266-71.
40. Wilson KC, Cattel DJ, Wan Z et al. Regulation of nuclear Prointerleukin-16 and p27(Kip1) in primary human T lymphocytes. Cell Immunol 2005;237:17-27.
41. Zhang Y, Tuzova M, Xiao ZX, Cruikshank WW, Center DM. Pro-IL-16 recruits histone deacetylase 3 to the Skp2 core promoter through interaction with transcription factor GABP. J Immunol 2008;180:402-8.
42. Fujihara SM, Nadler SG. Intranuclear targeted delivery of functional NF-κB by 70 kDa heat shock protein. EMBO J 1999;18:411-9.
43. Curiel-Lewandrowski C, Yamasaki H, Si CP et al. Loss of nuclear pro-IL-16 facilitates cell cycle progression in human cutaneous T cell lymphoma. J Clin Invest 2011;121:4838-49.
44. De Bie JJ, Jonker EH, Henricks PA et al. Exogenous interleukin-16 inhibits antigen-induced airway hyper-reactivity, eosinophilia and Th2-type cytokine production in mice. Clin Exp Allergy 2002;32:1651-8.
45. Little FF, de Bie J, van Oosterhout A, Kornfeld H, Center DM, Cruikshank WW. Immunomodulatory effect of interleukin-16 on allergic airway inflammation. Chest 2003;123:431S-2S.
46. Kim J, Kim H-R, Bae JL et al. Cross-linking of MHC class II molecules with anti-MHC class II antibody or epitope peptide prevents resting B lymphocyte differentiation by inhibiting NF-κB-dependent gene expression. Mol Cells 2001;12:67-76.