Cytoskeletal protein 4.1R negatively regulates T-cell activation by inhibiting the phosphorylation of LAT

Blood

Volumn 113, Issue 24, 2009, Pages 6128-6137

  Kang, Qiaozhen ^a   Yu, Yu ^a   Pei, Xinhong ^a   Hughes, Richard ^a   Heck, Susanne ^a   Zhang, Xihui ^a   Guo, Xinhua ^a   Halverson, Gregory ^a   Mohandas, Narla ^a   An, Xiuli ^a,b  

^a NEW YORK BLOOD CENTER   (United States)

^b PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSKELETON PROTEIN; ERYTHROCYTE BAND 4.1 PROTEIN; GAMMA INTERFERON; INTERLEUKIN 2; LAT PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE C GAMMA1; PROTEIN KINASE B; PROTEIN KINASE ZAP 70; T LYMPHOCYTE ANTIGEN; T LYMPHOCYTE RECEPTOR; 4.1R PROTEIN, MOUSE; LAT PROTEIN, MOUSE; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHOPROTEIN; PLASMA PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; ZAP70 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ERYTHROCYTE; HUMORAL IMMUNITY; IMMUNIZATION; IMMUNOMODULATION; IMMUNOREGULATION; INTERFERON PRODUCTION; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RECEPTOR UPREGULATION; REGULATORY MECHANISM; T LYMPHOCYTE ACTIVATION; ANIMAL; C57BL MOUSE; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; IMMUNOBLOTTING; IMMUNOLOGY; IMMUNOPRECIPITATION; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE MUTANT; PHOSPHORYLATION; PHYSIOLOGY; SURFACE PLASMON RESONANCE; T LYMPHOCYTE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BLOOD PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOBLOTTING; IMMUNOPRECIPITATION; INTERFERON-GAMMA; INTERLEUKIN-2; LYMPHOCYTE ACTIVATION; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHOPROTEINS; PHOSPHORYLATION; SURFACE PLASMON RESONANCE; T-LYMPHOCYTES; ZAP-70 PROTEIN-TYROSINE KINASE;

EID: 67650351935     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-10-182329     Document Type: Article

References (54)

1. Cemerski S, Shaw A. Immune synapses in T-cell activation. Curr Opin Immunol. 2006;18:298-304.
2. Iwashima M, Irving BA, van Oers NS, Chan AC, Weiss A. Sequential interactions of the TCR with two distinct cytoplasmic tyrosine kinases. Science. 1994;263:1136-1139. (Pubitemid 24105959)
3. Chan AC, Shaw AS. Regulation of antigen receptor signal transduction by protein tyrosine kinases. Curr Opin Immunol. 1996;8:394-401. (Pubitemid 26229662)
4. Williams BL, Schreiber KL, Zhang W, et al. Genetic evidence for differential coupling of Syk family kinases to the T-cell receptor: reconstitution studies in a ZAP-70-deficient Jurkat T-cell line. Mol Cell Biol. 1998;18:1388-1399. (Pubitemid 28100903)
5. Zhang W, Sloan-Lancaster J, Kitchen J, Trible RP, Samelson LE. LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell. 1998;92:83-92. (Pubitemid 28053300)
6. Samelson LE. Signal transduction mediated by the T cell antigen receptor: the role of adapter proteins. Annu Rev Immunol. 2002;20:371-394. (Pubitemid 34293429)
7. Gilliland LK, Schieven GL, Norris NA, Kanner SB, Aruffo A, Ledbetter JA. Lymphocyte lineage-restricted tyrosine-phosphorylated proteins that bind PLC gamma 1 SH2 domains. J Biol Chem. 1992;267:13610-13616.
8. Buday L, Egan SE, Rodriguez Viciana P, Cantrell DA, Downward J. A complex of Grb2 adaptor protein, Sos exchange factor, and a 36-kDa membrane-bound tyrosine phosphoprotein is implicated in ras activation in T cells. J Biol Chem. 1994;269:9019-9023. (Pubitemid 24209221)
9. Sieh M, Batzer A, Schlessinger J, Weiss A. GRB2 and phospholipase C-gamma 1 associate with a 36- to 38-kilodalton phosphotyrosine protein after T-cell receptor stimulation. Mol Cell Biol. 1994;14: 4435-4442. (Pubitemid 2104754)
10. Fukazawa T, Reedquist KA, Panchamoorthy G, et al. T cell activation-dependent association between the p85 subunit of the phosphatidylinositol 3-kinase and Grb2/phospholipase C-gamma 1-binding phosphotyrosyl protein pp36/38. J Biol Chem. 1995;270:20177-20182.
11. Conboy J, Kan YW, Shohet SB, Mohandas N. Molecular cloning of protein 4.1, a major structural element of the human erythrocyte membrane skeleton. Proc Natl Acad Sci U S A. 1986; 83:9512-9516. (Pubitemid 17223390)
12. Parra M, Gascard P, Walensky LD, et al. Molecular and functional characterization of protein 4.1B, a novel member of the protein 4.1 family with high level, focal expression in brain. J Biol Chem. 2000;275:3247-3255. (Pubitemid 30083025)
13. Parra M, Gascard P, Walensky LD, Snyder SH, Mohandas N, Conboy JG. Cloning and characterization of 4.1G (EPB41L2), a new member of the skeletal protein 4.1 (EPB41) gene family. Genomics. 1998;49:298-306. (Pubitemid 28240697)
14. Walensky LD, Blackshaw S, Liao D, et al. A novel neuron-enriched homolog of the erythrocyte membrane cytoskeletal protein 4.1. J Neurosci. 1999;19:6457-6467. (Pubitemid 29347445)
15. Chishti AH, Kim AC, Marfatia SM, et al. The FERM domain: a unique module involved in the linkage of cytoplasmic proteins to the membrane. Trends Biochem Sci. 1998;23:281-282.
16. Pearson MA, Reczek D, Bretscher A, Karplus PA. Structure of the ERM protein moesin reveals the FERM domain fold masked by an extended actin binding tail domain. Cell. 2000;101:259-270.
17. Han BG, Nunomura W, Takakuwa Y, Mohandas N, Jap BK. Protein 4.1R core domain structure and insights into regulation of cytoskeletal organization. Nat Struct Biol. 2000;7:871-875. (Pubitemid 30786105)
18. Marfatia SM, Lue RA, Branton D, Chishti AH. In vitro binding studies suggest a membrane-associated complex between erythroid p55, protein 4.1, and glycophorin C. J Biol Chem. 1994;269: 8631-8634.
19. Pasternack GR, Anderson RA, Leto TL, Marchesi VT. Interactions between protein 4.1 and band 3. An alternative binding site for an element of the membrane skeleton. J Biol Chem. 1985;260: 3676-3683.
20. Nunomura W, Takakuwa Y, Tokimitsu R, Krauss SW, Kawashima M, Mohandas N. Regulation of CD44-protein 4.1 interaction by Ca2+ and calmodulin. Implications for modulation of CD44-ankyrin interaction. J Biol Chem. 1997;272: 30322-30328.
21. Yonemura S, Hirao M, Doi Y, Takahashi N, Kondo T, Tsukita S. Ezrin/radixin/moesin (ERM) proteins bind to a positively charged amino acid cluster in the juxta-membrane cytoplasmic domain of CD44, CD43, and ICAM-2. J Cell Biol. 1998;140: 885-895. (Pubitemid 28141226)
22. Tsukita S, Yonemura S. ERM proteins: head-to-tail regulation of actin-plasma membrane interaction. Trends Biochem Sci. 1997;22:53-58. (Pubitemid 27076806)
23. Manno S, Takakuwa Y, Mohandas N. Modulation of erythrocyte membrane mechanical function by protein 4.1 phosphorylation. J Biol Chem. 2005; 280:7581-7587. (Pubitemid 40349650)
24. An X, Zhang X, Debnath G, Baines AJ, Mohandas N. Phosphatidylinositol-4, 5-biphosphate (PIP2) differentially regulates the interaction of human erythrocyte protein 4.1 (4.1R) with membrane proteins. Biochemistry. 2006;45:5725-5732.
25. Saotome I, Curto M, McClatchey AI. Ezrin is essential for epithelial organization and villus morphogenesis in the developing intestine. Dev Cell. 2004;6:855-864. (Pubitemid 38745419)
26. Kitajiri S, Fukumoto K, Hata M, et al. Radixin deficiency causes deafness associated with progressive degeneration of cochlear stereocilia. J Cell Biol. 2004;166:559-570. (Pubitemid 39097175)
27. Kikuchi S, Hata M, Fukumoto K, et al. Radixin deficiency causes conjugated hyperbilirubinemia with loss of Mrp2 from bile canalicular membranes. Nat Genet. 2002;31:320-325. (Pubitemid 34887601)
28. Roumier A, Olivo-Marin JC, Arpin M, et al. The membrane-microfilament linker ezrin is involved in the formation of the immunological synapse and in T cell activation. Immunity. 2001;15:715-728. (Pubitemid 34008500)
29. Delon J, Kaibuchi K, Germain RN. Exclusion of CD43 from the immunological synapse is mediated by phosphorylation-regulated relocation of the cytoskeletal adaptor moesin. Immunity. 2001; 15:691-701. (Pubitemid 34008498)
30. Faure S, Salazar-Fontana LI, Semichon M, et al. ERM proteins regulate cytoskeleton relaxation promoting T cell-APC conjugation. Nat Immunol. 2004;5:272-279. (Pubitemid 38332124)
31. Shi ZT, Afzal V, Coller B, et al. Protein 4.1R-deficient mice are viable but have erythroid membrane skeleton abnormalities. J Clin Invest. 1999; 103:331-340. (Pubitemid 29069982)
32. Kang Q, Wang T, Zhang H, Mohandas N, An X. A Golgi-associated protein 4.1B variant required for assimilation of proteins in the membrane. J Cell Sci. 2009;122:1091-1099.
33. Huse M, Lillemeier BF, Kuhns MS, Chen DS, Davis MM. T cells use two directionally distinct pathways for cytokine secretion. Nat Immunol. 2006;7:247-255.
34. Perkins SJ. Protein volumes and hydration effects. The calculations of partial specific volumes, neutron scattering matchpoints and 280-nm absorption coefficients for proteins and glycoproteins from amino acid sequences. Eur J Biochem. 1986;157:169-180.
35. Pei X, An X, Guo X, Tarnawski M, Coppel R, Mohandas N. Structural and functional studies of interaction between Plasmodium falciparum knob-associated histidine-rich protein (KAHRP) and erythrocyte spectrin. J Biol Chem. 2005;280: 31166-31171.
36. Tang TK, Leto TL, Correas I, Alonso MA, Marchesi VT, Benz EJ, Jr. Selective expression of an erythroid-specific isoform of protein 4.1. Proc Natl Acad Sci U S A. 1988;85:3713-3717.
37. Luque CM, Lallena MJ, Perez-Ferreiro CM, et al. The N-terminal 209-aa domain of high molecular-weight 4.1R isoforms abrogates 4.1R targeting to the nucleus. Proc Natl Acad Sci U S A. 1999;96: 14925-14930.
38. Lyons AB, Parish CR. Determination of lymphocyte division by flow cytometry. J Immunol Methods. 1994;171:131-137. (Pubitemid 24140219)
39. Zhang W, Trible RP, Zhu M, Liu SK, McGlade CJ, Samelson LE. Association of Grb2, Gads, and phospholipase C-gamma 1 with phosphorylated LAT tyrosine residues. Effect of LAT tyrosine mutations on T cell antigen receptor-mediated signaling. J Biol Chem. 2000;275:23355-23361. (Pubitemid 30646238)
40. Songyang Z, Shoelson SE, Chaudhuri M, et al. SH2 domains recognize specific phosphopeptide sequences. Cell. 1993;72:767-778. (Pubitemid 23093884)
41. Sun CX, Robb VA, Gutmann DH. Protein 4.1 tumor suppressors: getting a FERM grip on growth regulation. J Cell Sci. 2002;115:3991-4000.
42. Ralston KJ, Hird SL, Zhang X, et al. The LFA-1-associated molecule PTA-1 (CD226) on T cells forms a dynamic molecular complex with protein 4.1G and human discs large. J Biol Chem. 2004; 279:33816-33828.
43. Tran YK, Bogler O, Gorse KM, Wieland I, Green MR, Newsham IF. A novel member of the NF2/ERM/4.1 superfamily with growth suppressing properties in lung cancer. Cancer Res. 1999;59: 35-43. (Pubitemid 29062951)
44. Gutmann DH, Donahoe J, Perry A, et al. Loss of DAL-1, a protein 4.1-related tumor suppressor, is an important early event in the pathogenesis of meningiomas. Hum Mol Genet. 2000;9:1495-1500. (Pubitemid 30386704)
45. Robb VA, Li W, Gascard P, Perry A, Mohandas N, Gutmann DH. Identification of a third Protein 4.1 tumor suppressor, Protein 4.1R, in meningioma pathogenesis. Neurobiol Dis. 2003;13:191-202. (Pubitemid 36937202)
46. Cavanna T, Pokorna E, Vesely P, Gray C, Zicha D. Evidence for protein 4.1B acting as a metastasis suppressor. J Cell Sci. 2007;120:606-616. (Pubitemid 46437895)
47. Wong SY, Haack H, Kissil JL, et al. Protein 4.1B suppresses prostate cancer progression and metastasis. Proc Natl Acad Sci U S A. 2007;104: 12784-12789. (Pubitemid 47255232)
48. Ohtani K, Sakamoto H, Rutherford T, Chen Z, Satoh K, Naftolin F. Ezrin, a membrane-cytoskeletal linking protein, is involved in the process of invasion of endometrial cancer cells. Cancer Lett. 1999;147:31-38.
49. Khanna C, Wan X, Bose S, et al. The membrane-cytoskeleton linker ezrin is necessary for osteosarcoma metastasis. Nat Med. 2004;10:182-186. (Pubitemid 38524889)
50. Ling E, Danilov YN, Cohen CM. Modulation of red cell band 4.1 function by cAMP-dependent kinase and protein kinase C phosphorylation. J Biol Chem. 1988;263:2209-2216. (Pubitemid 18060275)
51. Subrahmanyam G, Bertics PJ, Anderson RA. Phosphorylation of protein 4.1 on tyrosine-418 modulates its function in vitro. Proc Natl Acad Sci U S A. 1991;88:5222-5226. (Pubitemid 21914716)
52. Nunomura W, Takakuwa Y, Parra M, Conboy JG, Mohandas N. Ca(2+)-dependent and Ca(2+)-independent calmodulin binding sites in erythrocyte protein 4.1. Implications for regulation of protein 4.1 interactions with transmembrane proteins. J Biol Chem. 2000;275:6360-6367.
53. An XL, Takakuwa Y, Manno S, Han BG, Gascard P, Mohandas N. Structural and functional characterization of protein 4.1R-phosphatidylserine interaction: potential role in 4.1R sorting within cells. J Biol Chem. 2001;276:35778-35785.
54. Allenspach EJ, Cullinan P, Tong J, et al. ERM-dependent movement of CD43 defines a novel protein complex distal to the immunological synapse. Immunity. 2001;15:739-750. (Pubitemid 34008502)