Cyclosporine A suppresses immunoglobulin G biosynthesis via inhibition of cyclophilin B in murine hybridomas and B cells

International Immunopharmacology

Volumn 12, Issue 1, 2012, Pages 42-49

  Lee, Jisun ^a   Choi, Tae Gyu ^a   Ha, Joohun ^a   Kim, Sung Soo ^a  

^a Kyung Hee University Hospital   (South Korea)

Author keywords

Cyclophilin B; Cyclosporine A; ER stress; ERAD pathway; Immunoglobulin G

Indexed keywords

CHAPERONE; CYCLOPHILIN B; CYCLOSPORIN A; IMMUNOGLOBULIN G; MULTIPROTEIN COMPLEX; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CHEMICAL BOND; CONTROLLED STUDY; DISEASE MARKER; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HYBRIDOMA; IMMUNOGLOBULIN PRODUCTION; IMMUNOPRECIPITATION; IMMUNOSUPPRESSIVE TREATMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN SYNTHESIS; QUALITY CONTROL;

ANIMALS; B-LYMPHOCYTES; CELL LINE; CYCLOPHILINS; CYCLOSPORINE; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; GLUTATHIONE TRANSFERASE; HEAT-SHOCK PROTEINS; HYBRIDOMAS; HYDROGEN PEROXIDE; IMMUNOGLOBULIN G; IMMUNOSUPPRESSIVE AGENTS; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; PROTEIN FOLDING; RNA, MESSENGER; TRANSCRIPTION FACTORS;

EID: 84856105458     PISSN: 15675769     EISSN: 18781705     Source Type: Journal    
DOI: 10.1016/j.intimp.2011.10.007     Document Type: Article

References (64)

1. J.M. Woof, and D.R. Burton Human antibody-Fc receptor interactions illuminated by crystal structures Nat Rev Immunol 4 2004 89 99 (Pubitemid 38209203)
2. R. Huber, J. Deisenhofer, P.M. Colman, M. Matsushima, and W. Palm Crystallographic structure studies of an IgG molecule and an Fc fragment Nature 264 1976 415 420
3. S.M. Hurtley, and A. Helenius Protein oligomerization in the endoplasmic reticulum Annu Rev Cell Biol 5 1989 277 307 (Pubitemid 19286686)
4. M.J. Gething, and J. Sambrook Protein folding in the cell Nature 355 1992 33 45
5. A.M. Fra, C. Fagioli, D. Finazzi, R. Sitia, and C.M. Alberini Quality control of ER synthesized proteins: an exposed thiol group as a three-way switch mediating assembly, retention and degradation EMBO J 12 1993 4755 4761 (Pubitemid 23330281)
6. R.D. Klausner, and R. Sitia Protein degradation in the endoplasmic reticulum Cell 62 1990 611 614
7. R.E. Handschumacher, M.W. Harding, J. Rice, R.J. Drugge, and D.W. Speicher Cyclophilin: a specific cytosolic binding protein for cyclosporin A Science 226 1984 544 547 (Pubitemid 14018525)
8. G. Spik, B. Haendler, O. Delmas, C. Mariller, M. Chamoux, and P. Maes A novel secreted cyclophilin-like protein (SCYLP) J Biol Chem 266 1991 10735 10738 (Pubitemid 21906865)
9. E.R. Price, L.D. Zydowsky, M.J. Jin, C.H. Baker, F.D. McKeon, and C.T. Walsh Human cyclophilin B: a second cyclophilin gene encodes a peptidyl-prolyl isomerase with a signal sequence Proc Natl Acad Sci U S A 88 1991 1903 1907 (Pubitemid 21916335)
10. J. Fanghanel, and G. Fischer Insights into the catalytic mechanism of peptidyl prolyl cis/trans isomerases. Front Biosci J Virtual Library 9 2004 3453 3478
11. M.A. Rycyzyn, S.C. Reilly, K. O'Malley, and C.V. Clevenger Role of cyclophilin B in prolactin signal transduction and nuclear retrotranslocation Mol Endocrinol 14 2000 1175 1186 (Pubitemid 32260479)
12. J. Heitman, and B.R. Cullen Cyclophilin B escorts the hepatitis C virus RNA polymerase: a viral achilles heel? Mol Cell 19 2005 145 146 (Pubitemid 41019662)
13. K. Watashi, N. Ishii, M. Hijikata, D. Inoue, T. Murata, and Y. Miyanari Cyclophilin B is a functional regulator of hepatitis C virus RNA polymerase Mol Cell 19 2005 111 122 (Pubitemid 40884662)
14. F. Fang, A.J. Flegler, P. Du, S. Lin, and C.V. Clevenger Expression of cyclophilin B is associated with malignant progression and regulation of genes implicated in the pathogenesis of breast cancer Am J Pathol 174 2009 297 308
15. F. Fang, J. Zheng, T.L. Galbaugh, A.A. Fiorillo, E.E. Hjort, and X. Zeng Cyclophilin B as a co-regulator of prolactin-induced gene expression and function in breast cancer cells J Mol Endocrinol 44 2010 319 329
16. F. Allain, A. Denys, and G. Spik Cyclophilin B mediates cyclosporin A incorporation in human blood T-lymphocytes through the specific binding of complexed drug to the cell surface Biochem J 317 Pt 2 1996 565 570 (Pubitemid 26253996)
17. J.L. Kofron, P. Kuzmic, V. Kishore, E. Colon-Bonilla, and D.H. Rich Determination of kinetic constants for peptidyl prolyl cis-trans isomerases by an improved spectrophotometric assay Biochemistry 30 1991 6127 6134
18. C.S. Hemenway, and J. Heitman Calcineurin. Structure, function, and inhibition Cell Biochem Biophys 30 1999 115 151
19. N.A. Clipstone, and G.R. Crabtree Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation Nature 357 1992 695 697
20. D.B. Durand, J.P. Shaw, M.R. Bush, R.E. Replogle, R. Belagaje, and G.R. Crabtree Characterization of antigen receptor response elements within the interleukin-2 enhancer Mol Cell Biol 8 1988 1715 1724
21. K.M. Latinis, L.A. Norian, S.L. Eliason, and G.A. Koretzky Two NFAT transcription factor binding sites participate in the regulation of CD95 (Fas) ligand expression in activated human T cells J Biol Chem 272 1997 31427 31434 (Pubitemid 28013280)
22. P.G. McCaffrey, A.E. Goldfeld, and A. Rao The role of NFATp in cyclosporin A-sensitive tumor necrosis factor-alpha gene transcription J Biol Chem 269 1994 30445 30450 (Pubitemid 24376523)
23. S.J. Szabo, J.S. Gold, T.L. Murphy, and K.M. Murphy Identification of cis-acting regulatory elements controlling interleukin-4 gene expression in T cells: roles for NF-Y and NF-ATc Mol Cell Biol 13 1993 4793 4805 (Pubitemid 23220385)
24. C. Stevens, N. Lempert, and B.M. Freed The effects of immunosuppressive agents on in vitro production of human immunoglobulins Transplantation 51 1991 1240 1244
25. T. Paavonen, and P. Hayry Effect of cyclosporin A on T-dependent and T-independent immunoglobulin synthesis in vitro Nature 287 1980 542 544 (Pubitemid 11232852)
26. R.L. O'Brien, P. Marrack, U. Storb, and J.W. Kappler B cells expressing Ig transgenes respond to a T-dependent antigen only in the presence of Ia-compatible T cells J Immunol 141 1988 3335 3341
27. A. Rahemtulla, W.P. Fung-Leung, M.W. Schilham, T.M. Kundig, S.R. Sambhara, and A. Narendran Normal development and function of CD8 + cells but markedly decreased helper cell activity in mice lacking CD4 Nature 353 1991 180 184 (Pubitemid 21912486)
28. M.J. Grusby, R.S. Johnson, V.E. Papaioannou, and L.H. Glimcher Depletion of CD4 + T cells in major histocompatibility complex class II-deficient mice Science 253 1991 1417 1420 (Pubitemid 21917295)
29. D.J. Steele, T.M. Laufer, S.T. Smiley, Y. Ando, M.J. Grusby, and L.H. Glimcher Two levels of help for B cell alloantibody production J Exp Med 183 1996 699 703 (Pubitemid 26059527)
30. I.C. MacLennan Germinal centers Annu Rev Immunol 12 1994 117 139 (Pubitemid 24140411)
31. S. Heidt, D.L. Roelen, C. Eijsink, M. Eikmans, C. van Kooten, and F.H. Claas Calcineurin inhibitors affect B cell antibody responses indirectly by interfering with T cell help Clin Exp Immunol 159 2010 199 207
32. K.J. Choi, Y.J. Piao, M.J. Lim, J.H. Kim, J. Ha, and W. Choe Overexpressed cyclophilin A in cancer cells renders resistance to hypoxia- and cisplatin-induced cell death Cancer Res 67 2007 3654 3662 (Pubitemid 46762150)
33. M.A. Rycyzyn, and C.V. Clevenger The intranuclear prolactin/cyclophilin B complex as a transcriptional inducer Proc Natl Acad Sci U S A 99 2002 6790 6795 (Pubitemid 34526210)
34. D.A. Rubinson, C.P. Dillon, A.V. Kwiatkowski, C. Sievers, L. Yang, and J. Kopinja A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference Nat Genet 33 2003 401 406 (Pubitemid 36278858)
35. A.A. Mamchak, and P.D. Hodgkin Absence of lipopolysaccharide high-dose paralysis in B-cell responses: implications for the one-signal theory Immunol Cell Biol 78 2000 133 141 (Pubitemid 30220108)
36. A.J. Robe, J.A. Kirby, D.E. Jones, and J.M. Palmer A key role for autoreactive B cells in the breakdown of T-cell tolerance to pyruvate dehydrogenase complex in the mouse Hepatology 41 2005 1106 1112 (Pubitemid 40593918)
37. J. Liu, J.D. Farmer Jr. , W.S. Lane, J. Friedman, I. Weissman, and S.L. Schreiber Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes Cell 66 1991 807 815 (Pubitemid 121001714)
38. E.R. Price, M. Jin, D. Lim, S. Pati, C.T. Walsh, and F.D. McKeon Cyclophilin B trafficking through the secretory pathway is altered by binding of cyclosporin A Proc Natl Acad Sci U S A 91 1994 3931 3935 (Pubitemid 24139546)
39. P. Fearon, A.A. Lonsdale-Eccles, O.K. Ross, C. Todd, A. Sinha, and F. Allain Keratinocyte Secretion of Cyclophilin B via the Constitutive Pathway Is Regulated through Its Cyclosporin-Binding Site J Invest Dermatol 131 2011 1085 1094
40. K. Kokame, K.L. Agarwala, H. Kato, and T. Miyata Herp, a new ubiquitin-like membrane protein induced by endoplasmic reticulum stress J Biol Chem 275 2000 32846 32853
41. A. Schulze, S. Standera, E. Buerger, M. Kikkert, S. van Voorden, and E. Wiertz The ubiquitin-domain protein HERP forms a complex with components of the endoplasmic reticulum associated degradation pathway J Mol Biol 354 2005 1021 1027 (Pubitemid 41698912)
42. Y. Okuda-Shimizu, and L.M. Hendershot Characterization of an ERAD pathway for nonglycosylated BiP substrates, which require Herp Mol Cell 28 2007 544 554 (Pubitemid 350137789)
43. D. Ron, and P. Walter Signal integration in the endoplasmic reticulum unfolded protein response Nat Rev Mol Cell Biol 8 2007 519 529 (Pubitemid 46985379)
44. C. Hammond, and A. Helenius Quality control in the secretory pathway: retention of a misfolded viral membrane glycoprotein involves cycling between the ER, intermediate compartment, and Golgi apparatus J Cell Biol 126 1994 41 52 (Pubitemid 24214927)
45. L. Meunier, Y.K. Usherwood, K.T. Chung, and L.M. Hendershot A subset of chaperones and folding enzymes form multiprotein complexes in endoplasmic reticulum to bind nascent proteins Mol Biol Cell 13 2002 4456 4469 (Pubitemid 35471198)
46. J. Zhang, and H. Herscovitz Nascent lipidated apolipoprotein B is transported to the Golgi as an incompletely folded intermediate as probed by its association with network of endoplasmic reticulum molecular chaperones, GRP94, ERp72, BiP, calreticulin, and cyclophilin B J Biol Chem 278 2003 7459 7468 (Pubitemid 36800752)
47. R.Y. Hampton ER-associated degradation in protein quality control and cellular regulation Curr Opin Cell Biol 14 2002 476 482 (Pubitemid 35279108)
48. B.N. Lilley, and H.L. Ploegh Multiprotein complexes that link dislocation, ubiquitination, and extraction of misfolded proteins from the endoplasmic reticulum membrane Proc Natl Acad Sci U S A 102 2005 14296 14301 (Pubitemid 41429692)
49. H. Lilie, R. Rudolph, and J. Buchner Association of antibody chains at different stages of folding: prolyl isomerization occurs after formation of quaternary structure J Mol Biol 248 1995 190 201
50. M.J. Thies, J. Mayer, J.G. Augustine, C.A. Frederick, H. Lilie, and J. Buchner Folding and association of the antibody domain CH3: prolyl isomerization preceeds dimerization J Mol Biol 293 1999 67 79 (Pubitemid 29494870)
51. M.J. Feige, S. Groscurth, M. Marcinowski, Y. Shimizu, H. Kessler, and L.M. Hendershot An unfolded CH1 domain controls the assembly and secretion of IgG antibodies Mol Cell 34 2009 569 579
52. N. Pallet, N. Bouvier, A. Bendjallabah, M. Rabant, J.P. Flinois, and A. Hertig Cyclosporine-induced endoplasmic reticulum stress triggers tubular phenotypic changes and death Am J Transplant 8 2008 2283 2296
53. N. Bouvier, J.P. Flinois, J. Gilleron, F.L. Sauvage, C. Legendre, and P. Beaune Cyclosporine triggers endoplasmic reticulum stress in endothelial cells: a role for endothelial phenotypic changes and death Am J Physiol Renal Physiol 296 2009 F160 F169
54. F. Hong, J. Lee, J.W. Song, S.J. Lee, H. Ahn, and J.J. Cho Cyclosporin A blocks muscle differentiation by inducing oxidative stress and inhibiting the peptidyl-prolyl-cis-trans isomerase activity of cyclophilin A: cyclophilin A protects myoblasts from cyclosporin A-induced cytotoxicity FASEB J 16 2002 1633 1635
55. S. Lopez-Ongil, O. Hernandez-Perera, J. Navarro-Antolin, G. Perez de Lema, M. Rodriguez-Puyol, and S. Lamas Role of reactive oxygen species in the signalling cascade of cyclosporine A-mediated up-regulation of eNOS in vascular endothelial cells Br J Pharmacol 124 1998 447 454 (Pubitemid 28254499)
56. H.W. Chen, C.T. Chien, S.L. Yu, Y.T. Lee, and W.J. Chen Cyclosporine A regulate oxidative stress-induced apoptosis in cardiomyocytes: mechanisms via ROS generation, iNOS and Hsp70 Br J Pharmacol 137 2002 771 781
57. S. Nadanaka, T. Okada, H. Yoshida, and K. Mori Role of disulfide bridges formed in the luminal domain of ATF6 in sensing endoplasmic reticulum stress Mol Cell Biol 27 2007 1027 1043 (Pubitemid 46174565)
58. P.I. Merksamer, A. Trusina, and F.R. Papa Real-time redox measurements during endoplasmic reticulum stress reveal interlinked protein folding functions Cell 135 2008 933 947
59. C.M. Haynes, E.A. Titus, and A.A. Cooper Degradation of misfolded proteins prevents ER-derived oxidative stress and cell death Mol Cell 15 2004 767 776 (Pubitemid 39194906)
60. C.X. Santos, L.Y. Tanaka, J. Wosniak, and F.R. Laurindo Mechanisms and implications of reactive oxygen species generation during the unfolded protein response: roles of endoplasmic reticulum oxidoreductases, mitochondrial electron transport, and NADPH oxidase Antioxid Redox Signal 11 2009 2409 2427
61. J.D. Malhotra, H. Miao, K. Zhang, A. Wolfson, S. Pennathur, and S.W. Pipe Antioxidants reduce endoplasmic reticulum stress and improve protein secretion Proc Natl Acad Sci U S A 105 2008 18525 18530
62. J. Kim, T.G. Choi, Y. Ding, Y. Kim, K.S. Ha, and K.H. Lee Overexpressed cyclophilin B suppresses apoptosis associated with ROS and Ca2 + homeostasis after ER stress J Cell Sci 121 2008 3636 3648
63. Y. Oh, E.Y. Kim, Y. Kim, J. Jin, B.K. Jin, and G.H. Jahng Neuroprotective effects of overexpressed cyclophilin B against Abeta-induced neurotoxicity in PC12 cells Free Radic Biol Med 51 2011 905 920
64. T. Horibe, C. Yosho, S. Okada, M. Tsukamoto, H. Nagai, and Y. Hagiwara The chaperone activity of protein disulfide isomerase is affected by cyclophilin B and cyclosporin A in vitro J Biochem 132 2002 401 407