Mice with disrupted type I protein kinase A anchoring in T cells resist retrovirus-induced immunodeficiency

Journal of Immunology

Volumn 186, Issue 9, 2011, Pages 5119-5130

  Mosenden, Randi ^a,b   Singh, Pratibha ^c   Cornez, Isabelle ^a,b   Heglind, Mikael ^d   Ruppelt, Anja ^a   Moutschen, Michel ^c   Enerbäck, Sven ^d   Rahmouni, Souad ^c   Taskén, Kjetil ^a,b  

^a UNIVERSITY OF OSLO   (Norway)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c UNIVERSITY OF LIÈGE   (Belgium)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE 1; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; EZRIN; HYBRID PROTEIN; INTERLEUKIN 2; PROGRAMMED DEATH 1 LIGAND 1; PROSTAGLANDIN E2; PROTEIN KINASE LCK; PROTEIN TYROSINE KINASE; T LYMPHOCYTE RECEPTOR;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISEASE COURSE; ENZYME ACTIVATION; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE DEFICIENCY; IMMUNOMODULATION; LIPID RAFT; LYMPHOCYTE FUNCTION; MOUSE; NONHUMAN; OPEN READING FRAME; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; RETROVIRUS; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TRANSGENIC MOUSE; VIRUS LOAD;

A KINASE ANCHOR PROTEINS; ANIMALS; BLOTTING, WESTERN; CELL SEPARATION; CYTOSKELETAL PROTEINS; DISEASE MODELS, ANIMAL; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MURINE ACQUIRED IMMUNODEFICIENCY SYNDROME; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TRANSFECTION;

EID: 79955541351     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100003     Document Type: Article

References (64)

1. Vang, T., K. M. Torgersen, V. Sundvold, M. Saxena, F. O. Levy, B. S. Skålhegg, V. Hansson, T. Mustelin, and K. Taskén. 2001. Activation of the COOH-terminal Src kinase (Csk) by cAMP-dependent protein kinase inhibits signaling through the T cell receptor. J. Exp. Med. 193: 497-507.
2. Schillace, R. V., S. F. Andrews, S. G. Galligan, K. A. Burton, H. J. Starks, H. G. Bouwer, G. S. McKnight, M. P. Davey, and D. W. Carr. 2005. The role of protein kinase A anchoring via the RII alpha regulatory subunit in the murine immune system. J. Immunol. 174: 6847-6853.
3. Skålhegg, B. S., B. F. Landmark, S. O. Døskeland, V. Hansson, T. Lea, and T. Jahnsen. 1992. Cyclic AMP-dependent protein kinase type I mediates the inhibitory effects of 3′,5′-cyclic adenosine monophosphate on cell replication in human T lymphocytes. J. Biol. Chem. 267: 15707-15714.
4. Skålhegg, B. S., K. Taskén, V. Hansson, H. S. Huitfeldt, T. Jahnsen, and T. Lea. 1994. Location of cAMP-dependent protein kinase type I with the TCR-CD3 complex. Science 263: 84-87. (Pubitemid 24076260)
5. Brdicka, T., D. Pavlistová, A. Leo, E. Bruyns, V. Korínek, P. Angelisová, J. Scherer, A. Shevchenko, I. Hilgert, J. Cerný, et al. 2000. Phosphoprotein associated with glycosphingolipid-enriched microdomains (PAG), a novel ubiquitously expressed transmembrane adaptor protein, binds the protein tyrosine kinase csk and is involved in regulation of T cell activation. J. Exp. Med. 191:1591-1604.
6. Kawabuchi, M., Y. Satomi, T. Takao, Y. Shimonishi, S. Nada, K. Nagai, A. Tarakhovsky, and M. Okada. 2000. Transmembrane phosphoprotein Cbp regulates the activities of Src-family tyrosine kinases. Nature 404: 999-1003. (Pubitemid 30243594)
7. Chow, L. M., M. Fournel, D. Davidson, and A. Veillette. 1993. Negative regulation of T-cell receptor signalling by tyrosine protein kinase p50csk. Nature 365: 156-160. (Pubitemid 23282060)
8. Okada, M., S. Nada, Y. Yamanashi, T. Yamamoto, and H. Nakagawa. 1991. CSK: a protein-tyrosine kinase involved in regulation of src family kinases. J. Biol. Chem. 266: 24249-24252.
9. Ruppelt, A., R. Mosenden, M. Grönholm, E. M. Aandahl, D. Tobin, C. R. Carlson, H. Abrahamsen, F. W. Herberg, O. Carpén, and K. Taskén. 2007. Inhibition of T cell activation by cyclic adenosine 5′-monophosphate requires lipid raft targeting of protein kinase A type I by the A-kinase anchoring protein ezrin. J. Immunol. 179: 5159-5168.
10. Brdicková, N., T. Brdicka, L. Andera, J. Spicka, P. Angelisová, S. L. Milgram, and V. Horejsí. 2001. Interaction between two adapter proteins, PAG and EBP50: a possible link between membrane rafts and actin cytoskeleton. FEBS Lett. 507:133-136. (Pubitemid 33001529)
11. Itoh, K., M. Sakakibara, S. Yamasaki, A. Takeuchi, H. Arase, M. Miyazaki, N. Nakajima, M. Okada, and T. Saito. 2002. Cutting edge: negative regulation of immune synapse formation by anchoring lipid raft to cytoskeleton through Cbp-EBP50-ERM assembly. J. Immunol. 168: 541-544. (Pubitemid 34049551)
12. Stokka, A. J., R. Mosenden, A. Ruppelt, B. Lygren, and K. Taskén. 2010. The adaptor protein EBP50 is important for localization of the protein kinase A-Ezrin complex in T-cells and the immunomodulating effect of cAMP. Biochem. J. 425:381-388.
13. Algrain, M., O. Turunen, A. Vaheri, D. Louvard, and M. Arpin. 1993. Ezrin contains cytoskeleton and membrane binding domains accounting for its proposed role as a membrane-cytoskeletal linker. J. Cell Biol. 120: 129-139.
14. Aziz, D. C., Z. Hanna, and P. Jolicoeur. 1989. Severe immunodeficiency disease induced by a defective murine leukaemia virus. Nature 338: 505-508. (Pubitemid 19107992)
15. Chattopadhyay, S. K., D. N. Sengupta, T. N. Fredrickson, H. C. Morse, III, and J.W. Hartley. 1991. Characteristics and contributions of defective, ecotropic, and mink cell focus-inducing viruses involved in a retrovirus-induced immunodeficiency syndrome of mice. J. Virol. 65: 4232-4241.
16. Rahmouni, S., E. M. Aandahl, M. Trebak, J. Boniver, K. Taskén, and M. Moutschen. 2001. Increased cAMP levels and protein kinase (PKA) type I activation in CD4+ T cells and B cells contribute to retrovirus-induced immunodeficiency of mice (MAIDS): a useful in vivo model for drug testing. FASEB J. 15: 1466-1468.
17. Rahmouni, S., E. M. Aandahl, B. Nayjib, M. Zeddou, S. Giannini, M. Verlaet, R. Greimers, J. Boniver, K. Taskén, and M. Moutschen. 2004. Cyclo-oxygenase type 2-dependent prostaglandin E2 secretion is involved in retrovirus-induced T-cell dysfunction in mice. Biochem. J. 384: 469-476. (Pubitemid 40018960)
18. Aandahl, E. M., P. Aukrust, B. S. Skålhegg, F. Müller, S. S. Frøland, V. Hansson, and K. Taskén. 1998. Protein kinase A type I antagonist restores immune responses of T cells from HIV-infected patients. FASEB J. 12: 855-862. (Pubitemid 28294675)
19. Carlson, C. R., B. Lygren, T. Berge, N. Hoshi, W. Wong, K. Taskén, and J. D. Scott. 2006. Delineation of type I protein kinase A-selective signaling events using an RI anchoring disruptor. J. Biol. Chem. 281: 21535-21545.
20. Jarnaess, E., A. Ruppelt, A. J. Stokka, B. Lygren, J. D. Scott, and K. Taskén. 2008. Dual specificity A-kinase anchoring proteins (AKAPs) contain an additional binding region that enhances targeting of protein kinase A type I. J. Biol. Chem. 283: 33708-33718.
21. Kozak, M. 1986. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 44: 283-292. (Pubitemid 16048214)
22. Brinster, R. L., J. M. Allen, R. R. Behringer, R. E. Gelinas, and R. D. Palmiter. 1988. Introns increase transcriptional efficiency in transgenic mice. Proc. Natl. Acad. Sci. USA 85: 836-840.
23. Palmiter, R. D., E. P. Sandgren, M. R. Avarbock, D. D. Allen, and R. L. Brinster. 1991. Heterologous introns can enhance expression of transgenes in mice. Proc. Natl. Acad. Sci. USA 88: 478-482.
24. Wildin, R. S., A. M. Garvin, S. Pawar, D. B. Lewis, K. M. Abraham, K. A. Forbush, S. F. Ziegler, J. M. Allen, and R. M. Perlmutter. 1991. Developmental regulation of lck gene expression in T lymphocytes. J. Exp. Med. 173: 383-393.
25. Wildin, R. S., H. U. Wang, K. A. Forbush, and R. M. Perlmutter. 1995. Functional dissection of the murine lck distal promoter. J. Immunol. 155: 1286-1295.
26. Brinster, R. L., H. Y. Chen, M. E. Trumbauer, M. K. Yagle, and R. D. Palmiter. 1985. Factors affecting the efficiency of introducing foreign DNA into mice by microinjecting eggs. Proc. Natl. Acad. Sci. USA 82: 4438-4442.
27. Gordon, J. W., G. A. Scangos, D. J. Plotkin, J. A. Barbosa, and F. H. Ruddle. 1980. Genetic transformation of mouse embryos by microinjection of purified DNA. Proc. Natl. Acad. Sci. USA 77: 7380-7384.
28. Jaenisch, R. 1988. Transgenic animals. Science 240: 1468-1474.
29. Clipstone, N. A., and G. R. Crabtree. 1992. Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation. Nature 357: 695-697.
30. Taskén, K., K. B. Andersson, B. S. Skålhegg, K. A. Taskén, V. Hansson, T. Jahnsen, and H. K. Blomhoff. 1993. Reciprocal regulation of mRNA and protein for subunits of cAMP-dependent protein kinase (RI alpha and C alpha) by cAMP in a neoplastic B cell line (Reh). J. Biol. Chem. 268: 23483-23489.
31. Carr, D. W., R. E. Stofko-Hahn, I. D. Fraser, S. M. Bishop, T. S. Acott, R. G. Brennan, and J. D. Scott. 1991. Interaction of the regulatory subunit (RII) of cAMP-dependent protein kinase with RII-anchoring proteins occurs through an amphipathic helix binding motif. J. Biol. Chem. 266: 14188-14192.
32. Durgerian, S., and S. S. Taylor. 1989. The consequences of introducing an autophosphorylation site into the type I regulatory subunit of cAMP-dependent protein kinase. J. Biol. Chem. 264: 9807-9813.
33. Hausken, Z. E., V. M. Coghlan, and J. D. Scott. 1998. Overlay, ligand blotting, and band-shift techniques to study kinase anchoring. Methods Mol. Biol. 88: 47-64.
34. Lygren, B., K. Taskén, and C. R. Carlson. 2005. A fast and sensitive method for isolation of detergent-resistant membranes from T cells. J. Immunol. Methods 305: 199-205. (Pubitemid 41416714)
35. Haas, M., and T. Reshef. 1980. Non-thymic malignant lymphomas induced in C57BL/6 mice by cloned dualtropic viruses isolated from hematopoietic stromal cell lines. Eur. J. Cancer 16: 909-917. (Pubitemid 10090027)
36. Zhang, W., R. P. Trible, and L. E. Samelson. 1998. LAT palmitoylation: its essential role in membrane microdomain targeting and tyrosine phosphorylation during T cell activation. Immunity 9: 239-246.
37. Perlmutter, R. M., J. D. Marth, D. B. Lewis, R. Peet, S. F. Ziegler, and C. B. Wilson. 1988. Structure and expression of lck transcripts in human lymphoid cells. J. Cell. Biochem. 38: 117-126.
38. Zhang, D. J., Q. Wang, J. Wei, G. Baimukanova, F. Buchholz, A. F. Stewart, X. Mao, and N. Killeen. 2005. Selective expression of the Cre recombinase in late-stage thymocytes using the distal promoter of the Lck gene. J. Immunol. 174: 6725-6731. (Pubitemid 40705634)
39. Witczak, O., B. S. Skålhegg, G. Keryer, M. Bornens, K. Taskén, T. Jahnsen, and S. Orstavik. 1999. Cloning and characterization of a cDNA encoding an A-kinase anchoring protein located in the centrosome, AKAP450. EMBO J. 18: 1858-1868. (Pubitemid 29158529)
40. Abrahamsen, H., G. Baillie, J. Ngai, T. Vang, K. Nika, A. Ruppelt, T. Mustelin, M. Zaccolo, M. Houslay, and K. Taskén. 2004. TCR- and CD28-mediated recruitment of phosphodiesterase 4 to lipid rafts potentiates TCR signaling. J. Immunol. 173: 4847-4858. (Pubitemid 39387765)
41. Lovatt, M., A. Filby, V. Parravicini, G. Werlen, E. Palmer, and R. Zamoyska. 2006. Lck regulates the threshold of activation in primary T cells, while both Lck and Fyn contribute to the magnitude of the extracellular signal-related kinase response. Mol. Cell. Biol. 26: 8655-8665.
42. Holmes, K. L., H. C. Morse, III, M. Makino, R. R. Hardy, and K. Hayakawa. 1990. A unique subset of normal murine CD4+ T cells lacking Thy-1 is expanded in a murine retrovirus-induced immunodeficiency syndrome, MAIDS. Eur. J. Immunol. 20: 2783-2787.
43. Moutschen, M. P., S. Colombi, M. Deprez, F. Van Wijk, C. Hotermans, M. T. Martin, R. Greimers, and J. Boniver. 1994. Population dynamics of CD4+ T cells lacking Thy-1 in murine retrovirus-induced immunodeficiency syndrome (MAIDS). Scand. J. Immunol. 39: 216-224. (Pubitemid 24253204)
44. de Leval, L., S. Colombi, S. Debrus, M. A. Demoitié, R. Greimers, P. Linsley, M. Moutschen, and J. Boniver. 1998. CD28-B7 costimulatory blockade by CTLA4Ig delays the development of retrovirus-induced murine AIDS. J. Virol. 72: 5285-5290. (Pubitemid 28215716)
45. Williams, R. O. 2002. Cutting edge: A-kinase anchor proteins are involved in maintaining resting T cells in an inactive state. J. Immunol. 168: 5392-5396. (Pubitemid 34556114)
46. Mosenden, R., and K. Taskén. 2011. Cyclic AMP-mediated immune regulation-Overview of mechanisms of action in T cells. Cell Signal. 23: 1009-1016.
47. Torheim, E. A., E. Jarnaess, B. Lygren, and K. Taskén. 2009. Design of proteolytically stable RI-anchoring disruptor peptidomimetics for in vivo studies of anchored type I protein kinase A-mediated signalling. Biochem. J. 424: 69-78.
48. Kandel, E. S., and N. Hay. 1999. The regulation and activities of the multifunctional serine/threonine kinase Akt/PKB. Exp. Cell Res. 253: 210-229.
49. Stern, J. B., and K. A. Smith. 1986. Interleukin-2 induction of T-cell G1 progression and c-myb expression. Science 233: 203-206.
50. Betz, M., and B. S. Fox. 1991. Prostaglandin E2 inhibits production of Th1 lymphokines but not of Th2 lymphokines. J. Immunol. 146: 108-113.
51. Haraguchi, S., R. A. Good, and N. K. Day. 1995. Immunosuppressive retroviral peptides: cAMP and cytokine patterns. Immunol. Today 16: 595-603.
52. Hilkens, C. M., A. Snijders, F. G. Snijdewint, E. A. Wierenga, and M. L. Kapsenberg. 1996. Modulation of T-cell cytokine secretion by accessory cell-derived products. Eur. Respir. J. Suppl. 22: 90s-94s.
53. Snijdewint, F. G., P. Kaliñski, E. A. Wierenga, J. D. Bos, and M. L. Kapsenberg. 1993. Prostaglandin E2 differentially modulates cytokine secretion profiles of human T helper lymphocytes. J. Immunol. 150: 5321-5329.
54. Mahic, M., S. Yaqub, C. C. Johansson, K. Taskén, and E. M. Aandahl. 2006. FOXP3+CD4+CD25+ adaptive regulatory T cells express cyclooxygenase-2 and suppress effector T cells by a prostaglandin E2-dependent mechanism. J. Immunol. 177: 246-254.
55. Deaglio, S., K. M. Dwyer, W. Gao, D. Friedman, A. Usheva, A. Erat, J. F. Chen, K. Enjyoji, J. Linden, M. Oukka, et al. 2007. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J. Exp. Med. 204: 1257-1265.
56. Kobie, J. J., P. R. Shah, L. Yang, J. A. Rebhahn, D. J. Fowell, and T. R. Mosmann. 2006. T regulatory and primed uncommitted CD4 T cells express CD73, which suppresses effector CD4 T cells by converting 59-adenosine monophosphate to adenosine. J. Immunol. 177: 6780-6786.
57. Bopp, T., C. Becker, M. Klein, S. Klein-Hessling, A. Palmetshofer, E. Serfling, V. Heib, M. Becker, J. Kubach, S. Schmitt, et al. 2007. Cyclic adenosine monophosphate is a key component of regulatory T cell-mediated suppression. J. Exp. Med. 204: 1303-1310.
58. Aukrust, P., E. M. Aandahl, B. S. Skålhegg, I. Nordøy, V. Hansson, K. Taskén, S. S. Frøland, and F. Müller. 1999. Increased activation of protein kinase A type I contributes to the T cell deficiency in common variable immunodeficiency. J. Immunol. 162: 1178-1185. (Pubitemid 29035451)
59. Mayrand, S. M., P. A. Healy, B. E. Torbett, and W. R. Green. 2000. Anti-Gag cytolytic T lymphocytes specific for an alternative translational reading frame-derived epitope and resistance versus susceptibility to retrovirus-induced murine AIDS in F(1) mice. Virology 272: 438-449.
60. Rabbi, M. F., L. al-Harthi, M. Saifuddin, and K. A. Roebuck. 1998. The cAMP-dependent protein kinase A and protein kinase C-beta pathways synergistically interact to activate HIV-1 transcription in latently infected cells of monocyte/macrophage lineage. Virology 245: 257-269.
61. Amella, C. A., B. Sherry, D. H. Shepp, and H. Schmidtmayerova. 2005. Macrophage inflammatory protein 1alpha inhibits postentry steps of human immunodeficiency virus type 1 infection via suppression of intracellular cyclic AMP. J. Virol. 79: 5625-5631. (Pubitemid 40548231)
62. Cartier, C., B. Hemonnot, B. Gay, M. Bardy, C. Sanchiz, C. Devaux, and L. Briant. 2003. Active cAMP-dependent protein kinase incorporated within highly purified HIV-1 particles is required for viral infectivity and interacts with viral capsid protein. J. Biol. Chem. 278: 35211-35219.
63. Barnitz, R. A., F. Wan, V. Tripuraneni, D. L. Bolton, and M. J. Lenardo. 2010. Protein kinase A phosphorylation activates Vpr-induced cell cycle arrest during human immunodeficiency virus type 1 infection. J. Virol. 84: 6410-6424.
64. Li, P. L., T. Wang, K. A. Buckley, A. L. Chenine, S. Popov, and R. M. Ruprecht. 2005. Phosphorylation of HIV Nef by cAMP-dependent protein kinase. Virology 331: 367-374.