Role of Btk in B cell development and signaling

Current Opinion in Immunology

Volumn 9, Issue 4, 1997, Pages 534-540

  Desiderio, Stephen ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LYMPHOCYTE RECEPTOR; PROTEIN TYROSINE KINASE;

B LYMPHOCYTE; HUMAN; IMMUNE DEFICIENCY; MOUSE; NONHUMAN; REVIEW; X CHROMOSOME LINKAGE;

EID: 0030840550     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0952-7915(97)80107-0     Document Type: Article

References (65)

1. Tsukada S, Saffran DC, Rawlings DJ, Parolini O, Allen RC, Klisak I, Sparkes RS, Kubagawa H, Mohandas T, Quan S, et al. Deficient expression of a B cell cytoplasmic tyrosine kinase in human X-linked agammaglobulinemia. Cell. 72:1993;279-290.
2. Vetrie D, Vorechovsky I, Sideras P, Holland J, Davies A, Flinter F, Hammarstrom L, Kinnon C, Levinsky R, Bobrow M, et al. The gene involved in X-linked agammaglobulinemia is a member of the src family of protein-tyrosine kinases. Nature. 361:1993;226-233.
3. Pearl E, Vogler LB, Okos AJ, Crist WM, Lawton AR, Cooper MD. B lymphocyte precursors in human bone marrow: an analysis of normal individuals and patients with antibody-deficiency states. J Immunol. 120:1978;1169-1175.
4. Rawlings DJ, Saffran DC, Tsukada S, Largaespada DA, Grimaldi JC, Cohen L, Mohr RN, Bazan JF, Howard M, Copland NG, et al. Mutation of the unique region of Bruton's tyrosine kinase in immunodeficient XID mice. Science. 261:1993;358-361.
5. Thomas JD, Sideras P, Smith CIE, Vorechovsky I, Chapman V, Paul WE. Colocalization of X-linked agammaglobulinemia and X-linked immunodeficiency genes. Science. 261:1993;355-358.
6. Scher I. The CBA/N mouse strain: an experimental model illustrating the influence of the X chromosome on immunity. Adv Immunol. 33:1982;1-71.
7. Hardy RR, Hayakawa K, Parks DR, Herzenberg LA. Demonstration of B-cell maturation in X-linked immunodeficient mice by simultaneous three color immunofluorescence. Nature. 306:1982;270-272.
8. Hayakawa K, Hardy RR, Herzenberg LA. Peritoneal Ly-1 B cells: genetic control, autoantibody production, increased light chain expression. Eur J Immunol. 16:1986;450-456.
9. Perlmutter RM, Nahm M, Stein KE, Slack J, Zitron I, Paul WE, Davie JM. Immunoglobulin subclass deficiency in mice with an X-linked B-lymphocyte defect. J Exp Med. 149:1979;993-998.
10. Siliciano J, Morrow TA, Desiderio SV. itk, a T-cell-specific tyrosine kinase gene inducible by interleukin 2. Proc Natl Acad Sci USA. 89:1992;11194-11198.
11. Heyeck SD, Berg IJ. Developmental regulation of a murine T-cell-specific tyrosine kinase gene, Tsk. Proc Natl Acad Sci USA. 90:1993;669-673.
12. Mano H, Mano K, Tang B, Koehler M, Yi T, Gilbert DJ, Jenkins NA, Copeland NG, Ihle JN. Expression of a novel form of Tec kinase in hematopoietic cells and mapping of the gene to chromosome 5 near Kit. Oncogene. 8:1993;417-424.
13. Tamagnone L, Lahtinen I, Mustonen T, Virtaneva K, Francis F, Muscatelli F, Alitalo R, Smith CI, Larsson C, Alitalo K. BMX, a novel nonreceptor tyrosine kinase gene of the BTK/ITK/TEC/TXK family located in chromosome Xp22.2. Oncogene. 9:1994;3683-3688.
14. Vihinen M, Nilsson L, Smith CIE. Tec homology (TH) adjacent to the PH domain. FEBS Lett. 350:1994;263-265.
15. Smith CIE, Notarangelo LD. Molecular basis for X-linked immunodeficiencies. Adv Genet. 35:1997;57-115.
16. Vihinen M, Iwata T, Kinnon C, Kwan S-P, Ochs HD, Vorechovsky I, Smith CIE. BTKbase, mutation database for X-linked agammaglobulinemia (XLA). Nucleic Acids Res. 24:1996;160-165.
17. DeWeers M, Mensink RGJ, Kraakman MEM, Schuurmann RKB, Hendricks RW. Mutation analysis of Bruton's tyrosine kinase gene in X-linked agammaglobulinemia: identification of a mutation which affects the same codon as is altered in immunodeficient xid mice. Hum Mol Genet. 3:1994;161-166.
18. Khan WN, Alt FW, Gerstein RM, Malynn BA, Larsson I, Rathbun G, Davidson L, Mueller S, Kantor AB, Herzenberg LA, et al. Defective B cell development and function in Btk-deficient mice. Immunity. 3:1995;283-299.
19. Kerner JD, Appleby MW, Mohr RN, Chien S, Rawlings DJ, Maliszewski CR, Witte ON, Perlmutter RM. Impaired expansion of mouse B cell progenitors lacking Btk. Immunity. 3:1995;301-312.
20. Hendriks RW, de Bruijn MFTR, Maas A, Dingjan GM, Karis A, Grosveld F. Inactivation of Btk by insertion of IacZ reveals defects in B cell development only past the pre-B cell stage. of special interest EMBO J. 15:1996;4862-4872 An elegant study of the competition in vivo between wild-type and Btk-null B lymphoid cells during their development in the bone marrow and in the periphery. Btk deficiency is associated with a selective disadvantage at two distinct steps in B cell development occurring after the pre-B stage.
21. Kawakami Y, Yao L, Miura T, Tsukada S, Witte ON, Kawakami T. Tyrosine phosphorylation and activation of Bruton tyrosine kinase upon FcεRI cross-linking. Mol Cell Biol. 14:1994;5108-5113.
22. Hasbold J, Klaus GGB. B cells from CBA/N mice do not proliferate following ligation of CD40. Eur J Immunol. 24:1994;152-157.
23. Goldstein MD, Debenedette MA, Hollenbaugh D, Watts TH. Induction of costimulatory molecules B7-1 and B7-2 in murine B cells: the CBA/N mouse reveals a role for Bruton's tyrosine kinase in CD40-mediated B7 induction. Mol Immunol. 33:1996;541-552.
24. Hitoshi Y, Sonoda E, Kikuchi Y, Yonehara S, Nakauchi H, Takatsu K. IL-5 receptor positive B cells, but not eosinophils, are functionally and numerically influenced in mice carrying the X-linked immune defect. Int Immunol. 5:1993;1183-1190.
25. Go NF, Castle BE, Barrett R, Kastelein R, Dang W, Mosmann TR, Moore KW, Howard M. Interleukin 10, a novel B cell stimulatory factor: unresponsivenes of X chromosome-linked immunodeficiency B cells. J Exp Med. 172:1990;1625-1631.
26. Santos-Argumedo L, Lund FE, Heath AW, Solvason N, Wu WW, Grimaldi JC, Parkhouse RME, Howard M. CD38 unresponsiveness of xid B cells implicates Bruton's tyrosine kinase (btk) as a regulator of CD38 induced signal transduction. Int Immunol. 7:1995;163-170.
27. Li T, Tsukada S, Satterthwaite A, Havlik MH, Park H, Takatsu K, Witte ON. Activation of Bruton's tyrosine kinase (BTK) by a point mutation in its pleckstrin homology (PH) domain. Immunity. 2:1995;451-460.
28. Saouaf S, Mahajan S, Rowley R, Kut S, Fargnoli J, Burkhardt A, Tsukada S, Witte O, Bolen J. Temporal differences in the activation of three classes of non-transmembrane protein tyrosine kinases following B-cell antigen receptor surface engagement. Proc Natl Acad Sci USA. 91:1994;9524-9528.
29. Rawlings DJ, Scharenberg AM, Park H, Wahl MI, Lin S, Kato RM, Fluckiger A-C, Witte ON, Kinet J-P. Activation of BTK by a phosphorylation mechanism initiated by SRC family kinases. of outstanding interest Science. 271:1996;822-825 This paper sets forth a mechanism by which Src-type kinases activate Btk and draws important parallels between this process and the activation, by displacement of an intramolecular inhibitory loop, of the insulin receptor kinase.
30. Mahajan S, Fargnoli J, Burkhardt AL, Kut SA, Saouaf SJ, Bolen JB. Src family protein tyrosine kinases induce autoactivation of Bruton's tyrosine kinase. Mol Cell Biol. 15:1995;5304-5311.
31. Park H, Wahl MI, Afar DEH, Turck CW, Rawlings DJ, Tam C, Scharenberg AM, Kinet J-P, Witte ON. Regulation of Btk function by a major autophosphorylation site within the SH3 domain. of special interest Immunity. 4:1996;515-525 The autophosphorylation site of Btk is mapped to a residue (Y223) within the SH3 domain, mutation of which enhances cell transformation by the Btk E41K mutant.
32. Hubbard SR, Wei L, Ellis L, Hendrickson WA. Crystal structure of the tyrosine kinase domain of the human insulin receptor. Nature. 372:1994;746-754.
33. Sicher F, Moarefi I, Kuriyan J. Crystal structure of the Src family tyrosine kinase Hck. of special interest Nature. 385:1997;602-609 See annotation [34].
34. Xu W, Harrison SC, Eck MJ. Three-dimensional structure of the tyrosine kinase c-Src. of special interest Nature. 385:1997;595-602 This paper, along with [33], presents structures of Src-type kinases in their entirety. In the enzymatically inactive forms examined here, inhibition of activity is achieved by the interaction of the catalytic domain with the SH3 and SH2 domains.
35. Andreotti AH, Bunnell SC, Feng S, Berg LJ, Schreiber SL. Regulatory intramolecular association in a tyrosine kinase of the Tec family. of special interest Nature. 385:1997;93-97 In this structural analysis of a fragment of Itk, the SH3 domain is shown to engage the proline-rich segment of the TH domain in cis, which has implications for the regulation of accessibility of these two regions of the protein.
36. Cheng G, Ye Z, Baltimore D. Binding of Bruton's tyrosine kinase to Fyn, Lyn, or Hck through a Src homology 3 domain-mediated interaction. Proc Natl Acad Sci USA. 91:1994;8152-8155.
37. Yang W, Malek SN, Desiderio S. A sequence motif conserved in Btk and related tyrosine kinases mediates SH3-dependent interactions in vitro and in vivo. J Biol Chem. 270:1995;20832-20840.
38. Cory GOC, Lovering RC, Hinshelwood S, MacCarthy-Morrogh L, Levinsky RJ, Kinnon C. The protein product of the c-cbl protooncogene is phosphorylated after B cell receptor stimulation and binds the SH3 domain of Bruton's tyrosine kinase. J Exp Med. 182:1995;611-615.
39. Bunnell SC, Henry PA, Kolluri R, Kirchhausen T, Rickles RJ, Berg LJ. Identification of Itk/Tsk Src homology 3 domain ligands. J Biol Chem. 271:1996;25646-25656.
40. Afar DEH, Park H, Howell BW, Rawlings DJ, Cooper J, Witte ON. Regulation of Btk by Src family tyrosine kinases. Mol Cell Biol. 16:1996;3465-3471.
41. Hibbs ML, Tarlinton DM, Armes J, Grail D, Hodgson G, Maglito R, Stacker SA, Dunn ARR. Multiple defects in the immune system of Lyn-deficient mice, culminating in autoimmune disease. Cell. 83:1995;301-311.
42. T in interleukin-5 receptor signaling. J Exp Med. 182:1995;811-820.
43. Mano H, Yamashita Y, Miyazato A, Miura Y, Ozawa K. Tec protein-tyrosine kinase is an effector molecule of Lyn protein-tyrosine kinase. FASEB J. 10:1996;637-642.
44. Gibson S, August A, Branch D, Dupont B, Mills GB. Functional LCK is required for optimal CD28-mediated activation of the TEC family tyrosine kinase EMT/ITK. J Biol Chem. 271:1996;7079-7083.
45. Lemmon MA, Ferguson KM, Schlessinger J. PH domains - diverse sequences with a common fold recruit signaling molecules to the cell surface. Cell. 85:1996;621-624.
46. Gaul U, Mardon G, Rubin GM. A putative Ras GTPase activating protein acts as a negative regulator of signaling by the sevenless receptor tyrosine kinase. Cell. 68:1992;1007-1019.
47. Maekawa M, Li S, Iwamatsu A, Morishita T, Yokota K, Imai Y, Kohsaka S, Nakamura S, Hattori S. A novel mammalian Ras GTPase-activating protein which has phospholipid-binding and Btk homology regions. Mol Cell Biol. 14:1994;6879-6885.
48. 4.
49. m. J Biol Chem. 271:1996;18838-18842.
50. Fukuda M, Kojima T, Kabayama H, Mikoshiba K. Mutation of the pleckstrin homology domain of Bruton's tyrosine kinase in immunodeficiency impaired inositol 1,3,4,5-tetrakisphosphate binding capacity. of special interest J Biol Chem. 271:1996;30303-30306 Demonstration of the specific binding of the Btk PH domain to inositol 1,3,4,5-tetrakisphosphate with an affinity of 10-100nM; impairment of binding by the introduction of the xid mutation (R28C), or XLA-associated mutations, into Btk was also shown.
51. Salim K, Bottomley MJ, Querfurth E, Zvelebil MJ, Gout I, Scaife R, Margolis RL, Gigg R, Edvard Smith CI, Driscoll PC, et al. Distinct specificity in the recognition of phosphoinositides by the pleckstrin homology domains of dynamin and Bruton's tyrosine kinase. of special interest EMBO J. 15:1996;6241-6250 This paper demonstrates the stereoselective, PH domain dependent activation of dynamin GTPase by phosphatidylinositol 4,5-bisphosphate; the authors also demonstrate a specific interaction between the Btk PH domain and phosphatidylinositol 3,4,5-trisphosphate.
52. Franke TF, Kaplan DR, Cantley LC, Toker A. Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-bisphosphate. of outstanding interest Science. 275:1997;665-668 This work establishes a paradigm for the PH domain dependent activation of a protein kinase by a phospholipid. Phosphatidylinositol 3,4-bisphosphate is shown to bind the PH domain of the serine/threonine kinase Akt, facilitating Akt dimerization and concomitantly increasing its enzyme activity.
53. Langhans-Rajasekaran SA, Wan Y, Huang X-Y. Activation of Tsk and Btk tyrosine kinases by G protein βγ subunits. Proc Natl Acad Sci USA. 92:1995;8601-8605.
54. Koch WJ, Inglese J, Stone WC, Lefkowitz RJ. The binding site for the βγ subunits of heterotrimetric G proteins on the β-adrenergic receptor kinase. J Biol Chem. 268:1993;8256-8260.
55. Yao L, Kawakami Y, Kawakami T. The pleckstrin homology domain of Bruton tyrosine kinase interacts with protein kinase C. Proc Natl Acad Sci USA. 91:1994;9175-9179.
56. Leitges M, Schmedt C, Guinamard R, Davoust J, Schaal S, Stabel S, Tarakhovsky A. Immunodeficiency in protein kinase Cβ-deficient mice. Science. 273:1996;788-791.
57. Takata M, Kurosaki T. A role for Bruton's tyrosine kinase in B cell antigen receptor-mediated activation of phospholipase C-γ2. of outstanding interest J Exp Med. 184:1996;31-40 An incisive study that uses gene ablation to locate Btk in a phospholipase-dependent signaling pathway emanating from the BCR.
58. ++ mobilization through distinct pathways. EMBO J. 13:1994;1341-1349.
59. Sidorenko SP, Law C-L, Klaus SJ, Chandran KA, Takata M, Kurosaki T, Clark EA. Protein kinase C μ (PKCμ) associates with the B cell antigen receptor complex and regulates lymphocyte signaling. Immunity. 5:1996;353-363.
60. Uckun FM, Waddick KG, Mahajan S, Jun X, Takata M, Bolen J, Kurosaki T. BTK as a mediator of radiation-induced apoptosis in DT-40 lymphoma B cells. of special interest Science. 273:1996;1096-1100 A convincing demonstration that Btk is essential for two distinct apoptotic responses in DT40 cells: one is induced by BCR cross-linking and is dependent on Syk and PLC-γ2, the other is induced by radiation and is independent of Syk or PLC-γ2.
61. Anderson JS, Teutsch M, Dong Z, Wortis HH. An essential role for tyrosine kinase in the regulation of Bruton's B-cell apoptosis. Proc Natl Acad Sci USA. 93:1996;10966-10971.
62. Woodland RT, Schmidt MR, Korsmeyer SJ, Gravel KA. Regulation of B cell survival in xid mice by the proto-oncogene bcl-2. J Immunol. 156:1996;2143-2154.
63. Kenny JJ, Fischer RT, Lustig A, Dintzis H, Katsumata M, Reed JC, Longo DL. bcl-2 alters the antigen-driven selection of B cells in μκ but not in μ-only xid transgenic mice. J Immunol. 157:1996;1054-1061.
64. Yang W-Y, Desiderio S. BAP-135, a target for Bruton's tyrosine kinase in response to B cell receptor engagement. of special interest Proc Natl Acad Sci USA. 94:1997;604-609 Identification of a candidate target for Btk in vivo. BAP-135, a substrate for Btk, is associated with Btk in B cells and is phosphorylated on tyrosine in response to BCR cross-linking.
65. Hyvonen M, Saraste M. Structure of the PH domain and Btk motif from Bruton's tyrosine kinase: molecular explanations for X-linked agammaglobulinaemia. EMBO J. 16:1997;3396-3404.