Boosting immune response with the invariant chain segments via association with non-peptide binding region of major histocompatibility complex class II molecules

BMC Immunology

Volumn 13, Issue , 2012, Pages

  Chen, Fangfang ^a   Meng, Fantao ^a   Pan, Ling ^a   Xu, Fazhi ^a   Liu, Xuelan ^a   Yu, Weiyi ^a  

^a ANHUI AGRICULTURAL UNIVERSITY   (China)

Author keywords

Antibody; Epitope; Hybrid; Li segments; Membrane co localization; MHC II

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; VIRUS FUSION PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY COMBINING SITE; ANTIBODY PRODUCTION; ARTICLE; CELL MEMBRANE; COMPLEX FORMATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; IMMUNE RESPONSE; IMMUNOPRECIPITATION; MOUSE; NON PEPTIDE BINDING REGION; NONHUMAN; WESTERN BLOTTING;

ANIMALS; ANTIBODY SPECIFICITY; ANTIGENS; ANTIGENS, DIFFERENTIATION, B-LYMPHOCYTE; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; COS CELLS; EPITOPES; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS II; IMMUNITY; IMMUNIZATION, SECONDARY; MICE; MICE, INBRED BALB C; PEPTIDES; PROTEIN BINDING; RECOMBINANT PROTEINS; TRANSFECTION;

EID: 84866640721     PISSN: None     EISSN: 14712172     Source Type: Journal    
DOI: 10.1186/1471-2172-13-55     Document Type: Article

References (51)

1. Strubin M, Berte C, Mach B. Alternative splicing and alternative initiation of translation explain the four forms of the Ia antigen-associated invariant chain. EMBO J 1986, 5:3483-3488. 1167384, 3104027.
2. Roche PA, Cresswell P. Invariant chain association with HLA-DR molecules inhibits immunogenic peptide binding. Nature 1990, 345:615-618. 10.1038/345615a0, 2190094.
3. Lindner R. Transient surface delivery of invariant chain-MHC II complexes via endosomes: a quantitative study. Traffic 2002, 3:133-146. 10.1034/j.1600-0854.2002.030206.x, 11929603.
4. Cella M, Sallusto F, Lanzavecchia A. Origin, maturation and antigen presenting function of dendritic cells. Curr Opin Immunol 1997, 9:10-16. 10.1016/S0952-7915(97)80153-7, 9039784.
5. Saudrais C, Spehner D, de la Salle H, Bohbot A, Cazenave JP, Goud B, Hanau D, Salamero J. Intracellular pathway for the generation of functional MHC class II peptide complexes in immature human dendritic cells. J Immunol 1998, 160:2597-2607.
6. Dugast M, Toussaint H, Dousset C, Benaroch P. AP2 clathrin adaptor complex, but not AP1, controls the access of the major histocompatibility complex (MHC) class II to endosomes. J Biol Chem 2005, 280:19656-19664. 10.1074/jbc.M501357200, 15749704.
7. McCormick PJ, Martina JA, Bonifacino JS. Involvement of clathrin and AP-2 in the trafficking of MHC class II molecules to antigen-processing compartments. Proc Natl Acad Sci USA 2005, 102:7910-7915. 10.1073/pnas.0502206102, 1138261, 15911768.
8. Schutze MP, Peterson PA, Jackson MR. An N-terminal double-arginine motif maintains type II membrane proteins in the endoplasmic reticulum. EMBO J 1994, 13:1696-1705. 395002, 8157008.
9. Stumptner P, Benaroch P. Interaction of MHC class II molecules with the invariant chain: role of the invariant chain (81-90) region. EMBO J 1997, 16:5807-5818. 10.1038/sj.emboj.7590555, 1170212, 9312039.
10. Romagnoli P, Germain RN. The CLIP region of invariant chain plays a critical role in regulating major histocompatibility complex class II folding, transport, and peptide occupancy. J Exp Med 1994, 180:1107-1113. 10.1084/jem.180.3.1107, 2191661, 8064228.
11. Hsing LC, Rudensky AY. The lysosomal cysteine proteases in MHC class II antigen presentation. Immunol Rev 2005, 207:229-241. 10.1111/j.0105-2896.2005.00310.x, 16181340.
12. Busch R, Rinderknecht CH, Roh S, Lee AW, Harding JJ, Burster T, Hornell TM, Mellins ED. Achieving stability through editing and chaperoning: regulation of MHC class II peptide binding and expression. Immunol Rev 2005, 207:242-260. 10.1111/j.0105-2896.2005.00306.x, 16181341.
13. Benaroch P, Yilla M, Raposo G, Ito K, Miwa K, Geuze HJ, Ploegh HL. How MHC class II molecules reach the endocytic pathway. EMBO J 1995, 14:37-49. 398050, 7530198.
14. Koch N, Lauer W, Habicht J, Dobberstein B. Primary structure of thegene for the murineIa antigen-associated invariant chains(Ii). An alternatively spliced exon encodes a cysteine-rich domain highly homologous to a repetitive sequence of thyroglobulin. EMBO J 1987, 6:1677-1683. 553541, 3038530.
15. Rudensky AY, Maric M, Eastman S, Shoemaker L, DeRoos PC, Blum JS. Intracellular assembly and transport of endogenous peptide-MHC class II complexes. Immunity 1994, 1:585-594. 10.1016/1074-7613(94)90048-5, 7600287.
16. Vogt AB, Stern LJ, Amshoff C, Dobberstein B, Hammerling BJ, Kropshofer H. Interference of distinct invariant chain regions with superantigen contact area and antigenic peptide binding groove of HLA-DR. J Immunol 1995, 155:4757-4765.
17. Ashman JB, Miller JJ. A role for the transmembrane domain in the trimerization of the MHC class II-associated invariant chain. Immunol 1999, 163:2704-2712.
18. Frauwirth K, Shastri N. Mutation of the invariant chain transmembrane region inhibits II degradation, prolongs association with MHC class II, and selectively disrupts antigen presentation. Cell Immunol 2001, 209:97-108. 10.1006/cimm.2001.1796, 11446742.
19. Dixon AM, Stanley BJ, Matthews EE, Dawson JP, Engelman DM. Invariant chain transmembrane domain trimerization: a step in MHC class II assembly. Biochemistry 2006, 45:5228-5234. 10.1021/bi052112e, 16618111.
20. Jasanoff A, Wagner G, Wiley DC. Structure of a trimeric domain of the MHC class II-associated chaperonin and targeting protein Ii. EMBO J 1998, 17:6812-6818. 10.1093/emboj/17.23.6812, 1171028, 9843486.
21. Kallinteris NL, Wu S, Lu X, Humphreys RE, von Hofe E, Xu M. Enhanced CD4+ T-cell response in DR4-transgenic mice to a hybrid peptide linking the Ii-Key segment of the invariant chain to the melanoma gp100(48-58) MHC class II epitope. J Immunother 2005, 28:352-358. 10.1097/01.cji.0000170362.45456.00, 16000953.
22. Zinckgraf JW, Sposato M, Zielinski V, Powell D, Treanor JJ, von Hofe E. Identification of HLA class II H5N1 hemagglutinin epitopes following subvirion influenza A (H5N1) vaccination. Vaccine 2009, 27:5393-5401. 10.1016/j.vaccine.2009.06.081, 19596415.
23. Xu M, Lu X, Sposato M, Zinckgraf JW, Wu S, von Hofe E. Ii-Key/HPV16 E7 hybrid peptide immunotherapy for HPV16+ cancers. Vaccine 2009, 27:4641-4647. 10.1016/j.vaccine.2009.05.054, 19520206.
24. Nagata T, Aoshi T, Suzuki M, Uchijima M, Kim YH, Yang Z, Koide Y. Induction of protective immunity to Listeria monocytogenes by immunization with plasmid DNA expressing a helper T-cell epitope that replaces the class II-associated invariant chain peptide of the invariant chain. Infect Immun 2002, 70:2676-2680. 10.1128/IAI.70.5.2676-2680.2002, 127905, 11953411.
25. Gao M, Wang HP, Wang YN, Zhou Y, Wang QL. HCV-NS3 Th1 minigene vaccine based on invariant chain CLIP genetic substitution enhances CD4(+) Th1 cell responses in vivo. Vaccine 2006, 24:5491-7. 10.1016/j.vaccine.2006.04.004, 16725235.
26. Adams S, Humphreys RE. Invariant chain peptides enhancing or inhibiting the presentation of antigenic peptides by major histocompatibility complex class II molecules. Eur J Immun 1995, 25:1693-1702.
27. Xu M, Lis J, Gulfo JV. MHC class II allosteric site drugs: New immunotherapeutics for malignant, infectious and autoimmune disease. Scan J Immunol 2001, 54:39-44.
28. Sotiriadou NN, Kallinteris NL, Gritzapis AD, Voutsas IF, Papamichail M, von Hofe E, Humphreys RE, Pavlis T, Perez SA, Baxevanis CN. Ii-Key/HER-2/neu(776-790) hybrid peptides induce more effective immunological responses over the native peptide in lymphocyte cultures from patients with HER-2/neu + tumors. Cancer Immunol Immunother 2007, 56:601-613. 10.1007/s00262-006-0213-z, 16960693.
29. Humphreys RE, Adams S, Koldzic G. Increasing the potentcy of MHC class II-presented epitopes by linking to Ii-Key peptide. Vaccine 2000, 18:2693-2697. 10.1016/S0264-410X(00)00067-0, 10781856.
30. Gillogly ME, Kallinteris NL, Xu M, Gulfo JV, Humphreys RE, Murray JL. Ii-Key/HER-2/neu MHC class-II antigenic epitope vaccine peptide for breast cancer. Cancer Immunol Immunother 2004, 53:490-496. 10.1007/s00262-003-0463-y, 14740174.
31. Rhyner C, Kündig T, Akdis CA, Crameri R. Targeting the MHC II presentation pathway in allergy vaccine development. Biochem Soc Trans 2007, 35:833-834. 10.1042/BST0350833, 17635159.
32. Gjertsson I, Laurie KL, Devitt J, Howe SJ, Thrasher AJ, Holmdahl R, Gustafsson K. Tolerance induction using lentiviral gene delivery delays onset and severity of collagen II arthritis. Mol Ther 2009, 17:632-640. 10.1038/mt.2009.299, 2835107, 19174762.
33. Dong L, Yu W, Xu F, Liu G. Cloning and identifying of mouse invariant chain gene and its identification in prokaryotic cells. J Anhui Agri Sci 2007, 35:7856-7857. Chines.
34. Xu F, Wu S, Yu W. Establishment of P815 cell line stably expressing Newcastle disease virus-F gene (NDV-F). J Agri Biotech 2009, 17:567-570. Chines.
35. Sadegh-Nasseri S, Germain RN. A role for peptide in determining MHC class II structure. Nature 1991, 353:167-170. 10.1038/353167a0, 1653903.
36. Sadegh-Nasseri S, Stern LJ, Wiley DC, Germain RN. MHC class II function preserved by lowaffinity peptide interactions preceding stable binding. Nature 1994, 370:647-650. 10.1038/370647a0, 8065450.
37. Sato AK, Zarutskie JA, Rushe MM, Lomakin A, Natarajan SK, Adegh-Nasseri SS. Determinants of the peptide-induced conformational change in the human class II major histocompatibility complex protein HLA-DR1. J Biol Chem 2000, 275:2165-2173. 10.1074/jbc.275.3.2165, 10636922.
38. Carven GJ, Stern LJ. Probing the ligand-induced conformational change in HLA-DR1 by selective chemical modification and mass spectrometric mapping. Biochemistry 2005, 44:13625-13637. 10.1021/bi050972p, 16229453.
39. Dornmair K, Rothenhausler B, McConnell HM. Structural intermediates in the reactions of antigenic peptides with MHC molecules. Cold Spring Harb Symp Quant Biol 1989, 54:409-416. 10.1101/SQB.1989.054.01.050, 2639762.
40. Witt SN, McConnell HM. Formation and dissociation of short-lived class II MHC-peptide complexes. Biochemistry 1994, 33:1861-1868. 10.1021/bi00173a032, 8110789.
41. Schmitt L, Boniface JJ, Davis MM, McConnell HM. Conformational isomers of a class II MHCpeptide complex in solution. J Mol Biol 1999, 286:207-218. 10.1006/jmbi.1998.2463, 9931260.
42. Natarajan SK, Assadi M, Sadegh-Nasser S. Stable peptide binding to MHC class II molecule is rapid and is determined by a receptive conformation shaped by prior association with low affinity peptides. J Immunol 1999, 162:4030-4036.
43. Rabinowitz JD, Vrljic M, Kasson PM, Liang MN, Busch R, Boniface JJ. Formation of a highly peptide-receptive state of class II MHC. Immunity 1998, 9:699-709. 10.1016/S1074-7613(00)80667-6, 9846491.
44. Germain RN, Hendrix LR. MHC class II structure, occupancy and surface expression determined by post-endoplasmic reticulum antigen binding. Nature 1991, 353:134-139. 10.1038/353134a0, 1891045.
45. Natarajan SK, Assadi M, Sadegh-Nasseri S. Stable peptide binding to MHC class II molecule is rapid and is determined by a receptive conformation shaped by prior association with low affinity peptides. J Immunol 1999, 162:4030-4036.
46. Huby RD, Dearman RJ, Kimber I. Intracellular phosphotyrosine induction by major histocompatibility complex class II requires co-aggregation with membrane rafts. J Biol Chem 1999, 274:22591-22596. 10.1074/jbc.274.32.22591, 10428838.
47. Karacsonyi C, Knorr R, Fulbier A, Lindner R. Association of major histocompatibility complex II with cholesterol- and sphingolipid-rich membranes precedes peptide loading. J Biol Chem 2004, 279:34818-34826. 10.1074/jbc.M404608200, 15184367.
48. Anderson HA, Hiltbold EM, Roche PA. Concentration of MHC class II molecules in lipid rafts facilitates antigen presentation. Nat Immunol 2000, 1:156-162. 10.1038/77842, 11248809.
49. Hiltbold EM, Poloso NJ, Roche PA. MHC class II-peptide complexes and APC lipid rafts accumulate at the immunological synapse. J Immunol 2003, 170:1329-1338.
50. Pond L, Watts C. Functional early endosomes are required for maturation of major histocompatibility complex class II molecules in human B lymphoblastoid cells. J Biol Chem 1999, 274:18049-18054. 10.1074/jbc.274.25.18049, 10364256.
51. Brachet V, Pehau-Arnaudet G, Desaymard C, Raposo G, Amigorena S. Early endosomes are required for major histocompatiblity complex class II transport to peptide-loading compartments. Mol Biol Cell 1999, 10:2891-2904. 25528, 10473634.