NF-κB signaling regulates functional expression of the MHC class I-related neonatal Fc receptor for IgG via intronic binding sequences

Journal of Immunology

Volumn 179, Issue 5, 2007, Pages 2999-3011

  Liu, Xindong ^a   Ye, Lilin ^a   Christianson, Gregory J ^b   Yang, Jun Qi ^c   Roopenian, Derry C ^b   Zhu, Xiaoping ^a  

^a UNIVERSITY OF MARYLAND   (United States)

^b JACKSON LABORATORY   (United States)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CPG OLIGODEOXYNUCLEOTIDE; FC RECEPTOR; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN G; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; LUCIFERASE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PROTEIN P50; SYNAPTOTAGMIN I; TUMOR NECROSIS FACTOR ALPHA; FC RECEPTOR, NEONATAL; HLA ANTIGEN CLASS 1; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CELL STIMULATION; CELL STRAIN CACO 2; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; INTRON; MONOCYTE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; REPORTER GENE; DRUG ANTAGONISM; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INTESTINE MUCOSA; METABOLISM; PROMOTER REGION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

BASE SEQUENCE; BINDING SITES; CACO-2 CELLS; GENE EXPRESSION; GENE EXPRESSION REGULATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNOGLOBULIN G; INTERLEUKIN-1BETA; INTESTINAL MUCOSA; INTRONS; LUCIFERASES; NF-KAPPA B; PROMOTER REGIONS (GENETICS); PROTEIN TRANSPORT; RECEPTORS, FC; RECEPTORS, IGG; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 38449100939     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.5.2999     Document Type: Article

References (54)

1. Ravetch, J. V., and S. Bolland. 2001. IgG Fc receptors. Annu. Rev. Immunol. 19: 275-290.
2. Nimmerjahn, F., P. Bruhns, K. Horiuchi, and J. V. Ravetch. 2005. FcγRIV: a novel FcR with distinct IgG subclass specificity. Immunity 23: 41-51.
3. Simister, N. E., and K. E. Mostov. 1989. An Fc receptor structurally related to MHC class I antigens Nature 337: 184-187.
4. Burmeister, W. P., A. H. Huber, and P. J. Bjorkman. 1994. Crystal structure of the complex of rat neonatal Fc receptor with Fc. Nature 372: 379-383.
5. Ghetie, V., and E. S. Ward. 2000. Multiple roles for the major histocompatibility complex class I- related receptor FcRn. Annu. Rev. Immunol. 18: 739-766.
6. Chaudhury, C., S. Mehnaz, J. M. Robinson, W. L. Hayton, D. K. Pearl, D. C. Roopenian, and C. L. Anderson. 2003. The major histocompatibility complex-related Fc receptor for IgG (FcRn) binds albumin and prolongs its lifespan. J. Exp. Med. 197: 315-322.
7. Brambell, F. W., W. A. Hemmings, and I. G. Morris. 1964. A theoretical model of γ-globulin catabolism. Nature 203: 1352-1354.
8. Roopenian, D. C., G. J. Christianson, T. J. Sproule, A. C. Brown, S. Akilesh, N. Jung, S. Petkova, L. Avanessian, E. Y. Choi, D. J. Shaffer, et al. 2003. The MHC class I-like IgG receptor controls perinatal IgG transport, IgG homeostasis, and fate of IgG-Fc-coupled drugs. J. Immunol. 170: 3528-3533.
9. Zhu, X., G. Meng, B. L. Dickinson, X. Li, E. Mizoguchi, L. Miao, Y. Wang, C. Robert, B. Wu, P. D. Smith, et al. 2001. MHC class I-related Fc receptor for IgG is functionally expressed in monocytes, intestinal macrophages, and dendritic cells. J. Immunol. 166: 3266-3276.
10. Petkova, S. B., S. Akilesh, T. J. Sproule, G. J. Christianson, H. Al Khabbaz, A. C. Brown, L. G. Presta, Y. G. Meng, and D. C. Roopenian. 2006. Enhanced half-life of genetically engineered human IgG1 antibodies in a humanized FcRn mouse model: potential application in humorally mediated autoimmune disease. Int. Immunol. 18: 1759-1769.
11. Akilesh. S., S. Petkova, T. J. Sproule, D. J. Shaffer, G. J. Christianson, and D. Roopenian. 2004. The MHC class I-like Fc receptor promotes humorally mediated autoimmune disease. J. Clin. Invest. 113: 1328-1333.
12. Li, N., M. Zhao, J. Hilario-Vargas, P. Prisayanh, S. Warren, L. A. Diaz, D. C. Roopenian, and Z. Liu. 2005. Complete FcRn dependence for intravenous Ig therapy in autoimmune skin blistering diseases. J. Clin. Invest. 115: 3440-3450.
13. Li, Q., and I. M. Verma. 2002. NF-κB regulation in the immune system. Nat. Rev. Immunol. 2: 725-734.
14. Hayden, M. S., and S. Ghosh. 2004. Signaling to NF-κB. Genes Dev. 18: 2195-2224.
15. Traenckner, E. B., H. L. Pahl, T. Henkel, K. N. Schmidt, S. Wilk, and P. A. Baeuerle. 1995. Phosphorylation of human IκBα on serines 32 and 36 controls IκBα proteolysis and NF-κB activation in response to diverse stimuli. EMBO J. 14: 2876-2883.
16. DiDonato, J., F. Mercurio, C. Rosette, J. Wu-Li, H. Suyang, S. Ghosh, and M. Karin. 1996. Mapping of the inducible IκB phosphorylation sites that signal its ubiquitination and degradation. Mol. Cell. Biol. 16: 1295-1304.
17. Karin, M., and Y. Ben-Neriah. 2000. Phosphorylation meets ubiquitination: the control of NF-κB activity. Annu. Rev. Immunol. 18: 621-663.
18. Mikulska, J. E., and N. E. Simister. 2000. Analysis of the promoter region of the human FcRn gene. Biochim. Biophys. Acta 1492: 180-184.
19. Zhu, X., J. Peng, R. Raychowdhury, A. Nakajima, W. I. Lencer, and R. S. Blumberg. 2002. The heavy chain of neonatal Fc receptor for IgG is sequestered in the endoplasmic reticulum by forming oligomers in the absence of β2m association. Biochem. J. 367: 703-714.
20. Zhu, X., J. Peng, D. Chen, X. Liu, L. Ye, H. Iijima, K. Kadavil, W. I. Lencer, and R. S. Blumberg. 2005. Calnexin and ERp57 facilitate the assembly of the neonatal Fc receptor for IgG with β2-microglobulin in the endoplasmic reticulum. J. Immunol. 175: 967-876.
21. Dekker, J., K. Rippe, M. Dekker, and N. Kleckner. 2002. Capturing chromosome conformation. Science 295: 1306-1311.
22. Eivazova, E. R., and T. M. Aune. 2004. Dynamic alterations in the conformation of the Ifng gene region during T helper cell differentiation. Proc. Natl. Acad. Sci. USA 101: 251-256.
23. Tolhuis, B., R. J. Palstra, E. Splinter, F. Grosveld, and W. de Laat. 2002. Looping and interaction between hypersensitive sites in the active β-globin locus. Mol. Cell. 10: 1453-1465.
24. Liu, Z., and W. T. Garrard. 2005. Long-range interactions between three transcriptional enhancers, active Vκ gene promoters, and a 3′ boundary sequence spanning 46 kilobases. Mol. Cell. Biol. 25: 3220-3231.
25. Dickinson, B. L., K. Badizadegan, Z. Wu, J. C. Ahouse, X. Zhu, N. E. Simister, R. S. Blumberg, and W. I. Lencer. 1999. Bidirectional FcRn-dependent IgG transport in a polarized human intestinal epithelial cell line. J. Clin. Invest. 104: 903-911.
26. Schjerven, H., P. Brandtzaeg, and F. E. Johansen. 2001. A novel NF-κB/Rel site in intron 1 cooperates with proximal promoter elements to mediate TNF-α-induced transcription of the human polymeric Ig receptor. J. Immunol. 167: 6412-6420.
27. Medzhitov, R. 2001. Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1: 135-145.
28. Hmama, Z., D. Nandan, L. Sly, K. L. Knutson, P. Herrera-Velit, and N. E. Reiner. 1999. 1α, 25-dihydroxyvitamin D3-induced myeloid cell differentiation is regulated by a vitamin D receptor-phosphatidylinositol 3-kinase signaling complex. J. Exp. Med. 190: 1583-1594.
29. Natarajan, K., S. Singh, T. R. Burke, D. Grunberger, and B. B. Aggarwal. 1996. Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-κB. Proc. Natl. Acad. Sci. USA 93: 9090-9095.
30. Guo, Z., G. H. Boekhoudt, and J. M. Boss. 2003. Role of the intronic enhancer in tumor necrosis factor-mediated induction of manganous superoxide dismutase. J. Biol. Chem. 278: 23570-23578.
31. Molinero, L. L., M. B. Fuertes, M. V. Girart, L. Fainboim, G. A. Rabinovich, M. A. Costas, and N. W. Zwirner. 2004. NF-κB regulates expression of the MHC class I-related chain A gene in activated T lymphocytes. J. Immunol. 173: 5583-5590.
32. Spilianakis, C. G., and R. A. Flavell. 2004. Long-range intrachromosomal interactions in the T helper type 2 cytokine locus. Nat. Immunol. 5: 1017-1027.
33. Elewaut, D., J. A. DiDonato, J. M. Kim, F. Truong, L. Eckmann, and M. F. Kagnoff. 1999. NF-κB is a central regulator of the intestinal epithelial cell innate immune response induced by infection with enteroinvasive bacteria. J. Immunol. 163: 1457-1466.
34. Israel, A., O. Le Bail, D. Hatat, J. Piette, M. Kieran, F. Logeat, D. Wallach, M. Fellous, and P. Kourilsky. 1989. TNF stimulates expression of mouse MHC class I genes by inducing an NF-κB-like enhancer binding activity which displaces constitutive factors. EMBO J. 8: 3793-3800.
35. Kvale, D., D. Lovhaug, L. M. Sollid, and P. Brandtzaeg. 1988. Tumor necrosis factor-α up-regulates expression of secretory component, the epithelial receptor for polymeric Ig. J. Immunol. 140: 3086-3089.
36. Covert, M. W., T. H. Leung, J. E. Gaston, and D. Baltimore. 2005. Achieving stability of lipopolysaccharide-induced NF-κB activation. Science 309: 1854-1857.
37. Lee, J. Y., N. A. Kim, A. Sanford, and K. E. Sullivan. 2003. Histone acetylation and chromatin conformation are regulated separately at the TNF-α promoter in monocytes and macrophages. J. Leukocyte Biol. 73: 862-871.
38. Gobin, S. J., P. Biesta, and P. J. van den Essen. 2003. Regulation of human β 2-microglobulin transactivation in hematopoietic cells. Blood 101: 3058-3064.
39. Martone, R., G. Euskirchen, P. Bertone, S. Hartman, T. E. Royce, N. M. Luscombe, J. L. Rinn, F. K. Nelson, P. Miller, M. Gerstein, et al. 2003. Distribution of NF-κB-binding sites across human chromosome 22. Proc. Natl. Acad. Sci. USA 100: 12247-12252.
40. Natoli, G., S. Saccani, D. Bosisio, and I. Marazzi. 2005. Interactions of NF-κB with chromatin: the art of being at the right place at the right time. Nat. Immunol. 6: 439-445.
41. Ge, B., O. Li, P. Wilder, A. Rizzino, and T. W. McKeithan. 2003. NF-κB regulates BCL3 transcription in T lymphocytes through an intronic enhancer. J. Immunol. 171: 4210-4218.
42. Leung, T. H., A. Hoffmann, and D. Baltimore. 2004. One nucleotide in a κB site can determine cofactor specificity for NF-κB dimers. Cell 118: 453-464.
43. Cha-Molstad, H., A. Agrawal, D. Zhang, D. Samols, and I. Kushner. 2000. The Rel family member P50 mediates cytokine-induced C-reactive protein expression by a novel mechanism. J. Immunol. 165: 4592-4597.
44. Ping, D., G. Boekhoudt, F. Zhang, A. Morris, S. Philipsen, S. T. Warren, and J. M. Boss. 2000. Sp1 binding is critical for promoter assembly and activation of the MCP-1 gene by tumor necrosis factor. J. Biol. Chem. 275: 1708-1714.
45. Boekhoudt, G. H., Z. Guo, G. W. Beresford, and J. M. Boss. 2003. Communication between NF-κB and Sp1 controls histone acetylation within the proximal promoter of the monocyte chemoattractant protein 1 gene. J. Immunol. 170: 4139-4147.
46. Stein, B., A. S. Baldwin, D. W. Ballard, W. C. Greene, P. Angel, and P. Herrlich. 1993. Cross-coupling of the NF-κB p65 and Fos/Jun transcription factors produces potentiated biological function. EMBO J. 12: 3879-3891.
47. Kunsch, C., R. K. Lang, C. A. Rosen, and M. F. Shannon. 1994. Synergistic transcriptional activation of the IL-8 gene by NF-κB p65 (RelA) and NF-IL-6. J. Immunol. 153: 153-164.
48. Tomaras, G. D., D. A. Foster, C. M. Burrer, and S. M. Taffet. 1999. ETS transcription factors regulate an enhancer activity in the third intron of TNF-α. J. Leukocyte Biol. 66: 183-193.
49. Kandil, E., M. Noguchi, T. Ishibashi, and M. Kasahara. 1995. Structural and phylogenetic analysis of the MHC class I-like Fc receptor gene. J. Immunol. 154: 5907-5918.
50. Jiang, L., J. Wang, R. S. Solorzano-Vargas, H. V. Tsai, E. M. Gutierrez, L. O. Ontiveros, P. R. Kiela, S. V. Wu, and M. G. Martin. 2004. Characterization of the rat intestinal Fc receptor (FcRn) promoter: transcriptional regulation of FcRn gene by the Sp family of transcription factors. Am. J. Physiol. 286: G922-G931.
51. Tiwari, B., and R. P. Junghans. 2005. Functional analysis of the mouse Fcgrt 5′ proximal promoter. Biochim. Biophys. Acta 1681: 88-98.
52. Svenungsson, E., G. Z. Fei, K. Jensen-Urstad, U. de Faire, A. Hamsten, and J. Frostegard. 2003. TNF-α: a link between hypertriglyceridaemia and inflammation in SLE patients with cardiovascular disease. Lupus 12: 454-461.
53. Sun, S. C., P. A. Ganchi, D. W. Ballard, and W. C. Greene. 1993. NF-κB controls expression of inhibitor IκBα: evidence for an inducible autoregulatory pathway. Science 259: 1912-1915.
54. Rugtveit, J., E. M. Nilsen, A. Bakka, H. Carlsen, P. Brandtzaeg, and H. Scott. 1997. Cytokine profiles differ in newly recruited and resident subsets of mucosal macrophages from inflammatory bowel disease. Gastroenterology 112: 1493-1505.