Induction of PP2A Bβ, a regulator of IL-2 deprivation-induced T-cell apoptosis, is deficient in systemic lupus erythematosus

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 30, 2011, Pages 12443-12448

  Crispín, José C ^a   Apostolidis, Sokratis A ^a   Finnell, Melissa I ^a   Tsokos, George C ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 2; PHOSPHOPROTEIN PHOSPHATASE 2A; PHOSPHOPROTEIN PHOSPHATASE 2A B BETA; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; AUTOIMMUNE DISEASE; CELL DEATH; HUMAN; HUMAN CELL; IMMUNE RESPONSE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; REGULATORY MECHANISM; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; UPREGULATION;

ADULT; APOPTOSIS; CASE-CONTROL STUDIES; DOWN-REGULATION; FEMALE; HUMANS; INTERLEUKIN-2; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; NERVE TISSUE PROTEINS; PROTEIN PHOSPHATASE 2; RNA, MESSENGER; T-LYMPHOCYTES; UP-REGULATION; YOUNG ADULT;

EID: 79961088157     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1103915108     Document Type: Article

References (46)

1. Olsen JV, et al. (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127:635-648. (Pubitemid 44647421)
2. Shi Y (2009) Serine/threonine phosphatases: Mechanism through structure. Cell 139:468-484.
3. Janssens V, Longin S, Goris J (2008) PP2A holoenzyme assembly: In cauda venenum (the sting is in the tail). Trends Biochem Sci 33:113-121.
4. Janssens V, Goris J (2001) Protein phosphatase 2A: A highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem J 353:417-439. (Pubitemid 32158309)
5. Sontag E (2001) Protein phosphatase 2A: The Trojan Horse of cellular signaling. Cell Signal 13:7-16.
6. Janssens V, Goris J, Van Hoof C (2005) PP2A: The expected tumor suppressor. Curr Opin Genet Dev 15:34-41. (Pubitemid 40127629)
7. Tian Q, Wang J (2002) Role of serine/threonine protein phosphatase in Alzheimer's disease. Neurosignals 11:262-269. (Pubitemid 37494393)
8. Katsiari CG, Kyttaris VC, Juang YT, Tsokos GC (2005) Protein phosphatase 2A is a negative regulator of IL-2 production in patients with systemic lupus erythematosus. J Clin Invest 115:3193-3204. (Pubitemid 41567584)
9. Crispín JC, Kyttaris VC, Juang YT, Tsokos GC (2008) How signaling and gene transcription aberrations dictate the systemic lupus erythematosus T cell phenotype. Trends Immunol 29:110-115.
10. Dagda RK, et al. (2008) The spinocerebellar ataxia 12 gene product and protein phosphatase 2A regulatory subunit Bbeta2 antagonizes neuronal survival by promoting mitochondrial fission. J Biol Chem 283:36241-36248.
11. Cheng WT, et al. (2009) Oxidative stress promotes autophagic cell death in human neuroblastoma cells with ectopic transfer of mitochondrial PPP2R2B (Bbeta2). BMC Cell Biol 10:91.
12. Holmes SE, et al. (1999) Expansion of a novel CAG trinucleotide repeat in the 5′ region of PPP2R2B is associated with SCA12. Nat Genet 23:391-392.
13. Villarino AV, et al. (2007) Helper T cell IL-2 production is limited by negative feedback and STAT-dependent cytokine signals. J Exp Med 204:65-71. (Pubitemid 46148757)
14. Lenardo M, et al. (1999) Mature T lymphocyte apoptosis - immune regulation in a dynamic and unpredictable antigenic environment. Annu Rev Immunol 17:221-253. (Pubitemid 29241124)
15. Snow AL, et al. (2009) Restimulation-induced apoptosis of T cells is impaired in patients with X-linked lymphoproliferative disease caused by SAP deficiency. J Clin Invest 119:2976-2989.
16. Crispín JC, et al. (2010) Pathogenesis of human systemic lupus erythematosus: Recent advances. Trends Mol Med 16:47-57.
17. Xue C, Lan-Lan W, Bei C, Jie C, Wei-Hua F (2006) Abnormal Fas/FasL and caspase-3-mediated apoptotic signaling pathways of T lymphocyte subset in patients with systemic lupus erythematosus. Cell Immunol 239:121-128. (Pubitemid 44037544)
18. Gergely P, Jr., et al. (2002) Persistent mitochondrial hyperpolarization, increased reactive oxygen intermediate production, and cytoplasmic alkalinization characterize altered IL-10 signaling in patients with systemic lupus erythematosus. J Immunol 169:1092-1101.
19. Xu L, Zhang L, Yi Y, Kang HK, Datta SK (2004) Human lupus T cells resist inactivation and escape death by upregulating COX-2. Nat Med 10:411-415. (Pubitemid 38508521)
20. Snow AL, Pandiyan P, Zheng L, Krummey SM, Lenardo MJ (2010) The power and the promise of restimulation-induced cell death in human immune diseases. Immunol Rev 236:68-82.
21. Watanabe-Fukunaga R, Brannan CI, Copeland NG, Jenkins NA, Nagata S (1992) Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature 356:314-317.
22. Takahashi T, et al. (1994) Generalized lymphoproliferative disease in mice, caused by a point mutation in the Fas ligand. Cell 76:969-976. (Pubitemid 24106378)
23. Turbyville JC, Rao VK (2010) The autoimmune lymphoproliferative syndrome: A rare disorder providing clues about normal tolerance. Autoimmun Rev 9:488-493.
24. Cohen PL (2006) Apoptotic cell death and lupus. Springer Semin Immunopathol 28:145-152.
25. Datta SR, et al. (1997) Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91:231-241. (Pubitemid 27456390)
26. Zha J, Harada H, Yang E, Jockel J, Korsmeyer SJ (1996) Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X (L). Cell 87:619-628. (Pubitemid 26386936)
27. Scheid MP, Duronio V (1998) Dissociation of cytokine-induced phosphorylation of Bad and activation of PKB/akt: Involvement of MEK upstream of Bad phosphorylation. Proc Natl Acad Sci USA 95:7439-7444. (Pubitemid 28293271)
28. Pastorino JG, Tafani M, Farber JL (1999) Tumor necrosis factor induces phosphorylation and translocation of BAD through a phosphatidylinositide-3-OH kinase-dependent pathway. J Biol Chem 274:19411-19416.
29. Yang E, et al. (1995) Bad, a heterodimeric partner for Bcl-XL and Bcl-2, displaces Bax and promotes cell death. Cell 80:285-291.
30. Ayllón V, Martínez-A C, García A, Cayla X, Rebollo A (2000) Protein phosphatase 1alpha is a Ras-activated Bad phosphatase that regulates interleukin-2 deprivation-induced apoptosis. EMBO J 19:2237-2246. (Pubitemid 30259005)
31. Chiang CW, et al. (2001) Protein phosphatase 2A activates the proapoptotic function of BAD in interleukin-3-dependent lymphoid cells by a mechanism requiring 14-3-3 dissociation. Blood 97:1289-1297.
32. Chiang CW, et al. (2003) Protein phosphatase 2A dephosphorylation of phosphoserine 112 plays the gatekeeper role for BAD-mediated apoptosis. Mol Cell Biol 23:6350-6362.
33. Weller M, Malipiero U, Groscurth P, Fontana A (1995) T cell apoptosis induced by interleukin-2 deprivation or transforming growth factor-beta 2: Modulation by the phosphatase inhibitors okadaic acid and calyculin A. Exp Cell Res 221:395-403.
34. Martin M, et al. (2008) Protein phosphatase 2A controls the activity of histone deacetylase 7 during T cell apoptosis and angiogenesis. Proc Natl Acad Sci USA 105:4727-4732. (Pubitemid 351753814)
35. Ahmed NN, Grimes HL, Bellacosa A, Chan TO, Tsichlis PN (1997) Transduction of interleukin-2 antiapoptotic and proliferative signals via Akt protein kinase. Proc Natl Acad Sci USA 94:3627-3632. (Pubitemid 27180423)
36. Kim SW, Kim HJ, Chun YJ, Kim MY (2010) Ceramide produces apoptosis through induction of p27(kip1) by protein phosphatase 2A-dependent Akt dephosphorylation in PC-3 prostate cancer cells. J Toxicol Environ Health A 73:1465-1476.
37. Colotta F, Polentarutti N, Sironi M, Mantovani A (1992) Expression and involvement of c-fos and c-jun protooncogenes in programmed cell death induced by growth factor deprivation in lymphoid cell lines. J Biol Chem 267:18278-18283.
38. Devireddy LR, Green MR (2003) Transcriptional program of apoptosis induction following interleukin 2 deprivation: Identification of RC3, a calcium/calmodulin binding protein, as a novel proapoptotic factor. Mol Cell Biol 23:4532-4541. (Pubitemid 36734744)
39. Fleischer A, et al. (2007) Cascade of transcriptional induction and repression during IL-2 deprivation-induced apoptosis. Immunol Lett 112:9-29. (Pubitemid 47331685)
40. Kovacs B, Vassilopoulos D, Vogelgesang SA, Tsokos GC (1996) Defective CD3-mediated cell death in activated T cells from patients with systemic lupus erythematosus: Role of decreased intracellular TNF-alpha. Clin Immunol Immunopathol 81:293-302. (Pubitemid 26414559)
41. Fernandez D, Bonilla E, Mirza N, Niland B, Perl A (2006) Rapamycin reduces disease activity and normalizes T cell activation-induced calcium fluxing in patients with systemic lupus erythematosus. Arthritis Rheum 54:2983-2988. (Pubitemid 44497779)
42. Kyttaris VC, Juang YT, Tenbrock K, Weinstein A, Tsokos GC (2004) Cyclic adenosine 5′-monophosphate response element modulator is responsible for the decreased expression of c-fos and activator protein-1 binding in T cells from patients with systemic lupus erythematosus. J Immunol 173:3557-3563. (Pubitemid 39142067)
43. Juang YT, et al. (2008) PP2A dephosphorylates Elf-1 and determines the expression of CD3zeta and FcRgamma in human systemic lupus erythematosus T cells. J Immunol 181:3658-3664.
44. Juang YT, et al. (2011) Transcriptional activation of the cAMP-responsive modulator promoter in human T cells is regulated by protein phosphatase 2A-mediated dephosphorylation of SP-1 and reflects disease activity in patients with systemic lupus erythematosus. J Biol Chem 286:1795-1801.
45. Götz J, Probst A, Ehler E, Hemmings B, Kues W (1998) Delayed embryonic lethality in mice lacking protein phosphatase 2A catalytic subunit Calpha. Proc Natl Acad Sci USA 95:12370-12375. (Pubitemid 28483772)
46. Tan EM, et al. (1982) The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 25:1271-1277. (Pubitemid 13221242)