• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of embojLink to Publisher's site
EMBO J. Apr 1, 1998; 17(7): 1973–1985.
PMCID: PMC1170543

Btk/Tec kinases regulate sustained increases in intracellular Ca2+ following B-cell receptor activation.

Abstract

Bruton's tyrosine kinase (Btk) is essential for B-lineage development and represents an emerging family of non-receptor tyrosine kinases implicated in signal transduction events initiated by a range of cell surface receptors. Increased dosage of Btk in normal B cells resulted in a striking enhancement of extracellular calcium influx following B-cell antigen receptor (BCR) cross-linking. Ectopic expression of Btk, or related Btk/Tec family kinases, restored deficient extracellular Ca2+ influx in a series of novel Btk-deficient human B-cell lines. Btk and phospholipase Cgamma (PLCgamma) co-expression resulted in tyrosine phosphorylation of PLCgamma and required the same Btk domains as those for Btk-dependent calcium influx. Receptor-dependent Btk activation led to enhanced peak inositol trisphosphate (IP3) generation and depletion of thapsigargin (Tg)-sensitive intracellular calcium stores. These results suggest that Btk maintains increased intracellular calcium levels by controlling a Tg-sensitive, IP3-gated calcium store(s) that regulates store-operated calcium entry. Overexpression of dominant-negative Syk dramatically reduced the initial phase calcium response, demonstrating that Btk/Tec and Syk family kinases may exert distinct effects on calcium signaling. Finally, co-cross-linking of the BCR and the inhibitory receptor, FcgammaRIIb1, completely abrogated Btk-dependent IP3 production and calcium store depletion. Together, these data demonstrate that Btk functions at a critical crossroads in the events controlling calcium signaling by regulating peak IP3 levels and calcium store depletion.

Full Text

The Full Text of this article is available as a PDF (666K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Afar DE, Park H, Howell BW, Rawlings DJ, Cooper J, Witte ON. Regulation of Btk by Src family tyrosine kinases. Mol Cell Biol. 1996 Jul;16(7):3465–3471. [PMC free article] [PubMed]
  • Sadighi Akha AA, Willmott NJ, Brickley K, Dolphin AC, Galione A, Hunt SV. Anti-Ig-induced calcium influx in rat B lymphocytes mediated by cGMP through a dihydropyridine-sensitive channel. J Biol Chem. 1996 Mar 29;271(13):7297–7300. [PubMed]
  • Benatar T, Carsetti R, Furlonger C, Kamalia N, Mak T, Paige CJ. Immunoglobulin-mediated signal transduction in B cells from CD45-deficient mice. J Exp Med. 1996 Jan 1;183(1):329–334. [PMC free article] [PubMed]
  • Berridge MJ. Inositol trisphosphate and calcium signalling. Nature. 1993 Jan 28;361(6410):315–325. [PubMed]
  • Bijsterbosch MK, Klaus GG. Crosslinking of surface immunoglobulin and Fc receptors on B lymphocytes inhibits stimulation of inositol phospholipid breakdown via the antigen receptors. J Exp Med. 1985 Dec 1;162(6):1825–1836. [PMC free article] [PubMed]
  • Bootman MD, Berridge MJ. The elemental principles of calcium signaling. Cell. 1995 Dec 1;83(5):675–678. [PubMed]
  • Braun J, Sha'afi RI, Unanue ER. Crosslinking by ligands to surface immunoglobulin triggers mobilization of intracellular 45Ca2+ in B lymphocytes. J Cell Biol. 1979 Sep;82(3):755–766. [PMC free article] [PubMed]
  • Brent LH, Gong Q, Ross JM, Wieland SJ. Mitogen-activated Ca++ channels in human B lymphocytes. J Cell Physiol. 1993 Jun;155(3):520–529. [PubMed]
  • Brown VK, Ogle EW, Burkhardt AL, Rowley RB, Bolen JB, Justement LB. Multiple components of the B cell antigen receptor complex associate with the protein tyrosine phosphatase, CD45. J Biol Chem. 1994 Jun 24;269(25):17238–17244. [PubMed]
  • Choquet D, Partiseti M, Amigorena S, Bonnerot C, Fridman WH, Korn H. Cross-linking of IgG receptors inhibits membrane immunoglobulin-stimulated calcium influx in B lymphocytes. J Cell Biol. 1993 Apr;121(2):355–363. [PMC free article] [PubMed]
  • Clapham DE. Calcium signaling. Cell. 1995 Jan 27;80(2):259–268. [PubMed]
  • Conley ME, Parolini O, Rohrer J, Campana D. X-linked agammaglobulinemia: new approaches to old questions based on the identification of the defective gene. Immunol Rev. 1994 Apr;138:5–21. [PubMed]
  • Daëron M, Latour S, Malbec O, Espinosa E, Pina P, Pasmans S, Fridman WH. The same tyrosine-based inhibition motif, in the intracytoplasmic domain of Fc gamma RIIB, regulates negatively BCR-, TCR-, and FcR-dependent cell activation. Immunity. 1995 Nov;3(5):635–646. [PubMed]
  • D'Ambrosio D, Hippen KL, Minskoff SA, Mellman I, Pani G, Siminovitch KA, Cambier JC. Recruitment and activation of PTP1C in negative regulation of antigen receptor signaling by Fc gamma RIIB1. Science. 1995 Apr 14;268(5208):293–297. [PubMed]
  • Diegel ML, Rankin BM, Bolen JB, Dubois PM, Kiener PA. Cross-linking of Fc gamma receptor to surface immunoglobulin on B cells provides an inhibitory signal that closes the plasma membrane calcium channel. J Biol Chem. 1994 Apr 15;269(15):11409–11416. [PubMed]
  • Dolmetsch RE, Lewis RS, Goodnow CC, Healy JI. Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature. 1997 Apr 24;386(6627):855–858. [PubMed]
  • Fanger CM, Hoth M, Crabtree GR, Lewis RS. Characterization of T cell mutants with defects in capacitative calcium entry: genetic evidence for the physiological roles of CRAC channels. J Cell Biol. 1995 Nov;131(3):655–667. [PMC free article] [PubMed]
  • Franke TF, Kaplan DR, Cantley LC, Toker A. Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-bisphosphate. Science. 1997 Jan 31;275(5300):665–668. [PubMed]
  • Fruehling S, Lee SK, Herrold R, Frech B, Laux G, Kremmer E, Grässer FA, Longnecker R. Identification of latent membrane protein 2A (LMP2A) domains essential for the LMP2A dominant-negative effect on B-lymphocyte surface immunoglobulin signal transduction. J Virol. 1996 Sep;70(9):6216–6226. [PMC free article] [PubMed]
  • 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. J Biol Chem. 1996 Nov 29;271(48):30303–30306. [PubMed]
  • Gamberucci A, Fulceri R, Tarroni P, Giunti R, Marcolongo P, Sorrentino V, Benedetti A. Calcium pools in Ehrlich carcinoma cells. A major, high affinity Ca2+ pool is sensitive to both inositol 1,4,5-trisphosphate and thapsigargin. Cell Calcium. 1995 Jun;17(6):431–441. [PubMed]
  • Gardner P. Calcium and T lymphocyte activation. Cell. 1989 Oct 6;59(1):15–20. [PubMed]
  • Gibson TJ, Hyvönen M, Musacchio A, Saraste M, Birney E. PH domain: the first anniversary. Trends Biochem Sci. 1994 Sep;19(9):349–353. [PubMed]
  • Gouy H, Cefai D, Christensen SB, Debré P, Bismuth G. Ca2+ influx in human T lymphocytes is induced independently of inositol phosphate production by mobilization of intracellular Ca2+ stores. A study with the Ca2+ endoplasmic reticulum-ATPase inhibitor thapsigargin. Eur J Immunol. 1990 Oct;20(10):2269–2275. [PubMed]
  • Healy JI, Dolmetsch RE, Timmerman LA, Cyster JG, Thomas ML, Crabtree GR, Lewis RS, Goodnow CC. Different nuclear signals are activated by the B cell receptor during positive versus negative signaling. Immunity. 1997 Apr;6(4):419–428. [PubMed]
  • Heyeck SD, Berg LJ. Developmental regulation of a murine T-cell-specific tyrosine kinase gene, Tsk. Proc Natl Acad Sci U S A. 1993 Jan 15;90(2):669–673. [PMC free article] [PubMed]
  • Hippen KL, Buhl AM, D'Ambrosio D, Nakamura K, Persin C, Cambier JC. Fc gammaRIIB1 inhibition of BCR-mediated phosphoinositide hydrolysis and Ca2+ mobilization is integrated by CD19 dephosphorylation. Immunity. 1997 Jul;7(1):49–58. [PubMed]
  • Hoth M, Penner R. Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature. 1992 Jan 23;355(6358):353–356. [PubMed]
  • Justement LB, Brown VK, Lin J. Regulation of B-cell activation by CD45: a question of mechanism. Immunol Today. 1994 Sep;15(9):399–406. [PubMed]
  • Khan AA, Steiner JP, Klein MG, Schneider MF, Snyder SH. IP3 receptor: localization to plasma membrane of T cells and cocapping with the T cell receptor. Science. 1992 Aug 7;257(5071):815–818. [PubMed]
  • Kiener PA, Lioubin MN, Rohrschneider LR, Ledbetter JA, Nadler SG, Diegel ML. Co-ligation of the antigen and Fc receptors gives rise to the selective modulation of intracellular signaling in B cells. Regulation of the association of phosphatidylinositol 3-kinase and inositol 5'-phosphatase with the antigen receptor complex. J Biol Chem. 1997 Feb 7;272(6):3838–3844. [PubMed]
  • Kolanus W, Romeo C, Seed B. T cell activation by clustered tyrosine kinases. Cell. 1993 Jul 16;74(1):171–183. [PubMed]
  • Kong GH, Bu JY, Kurosaki T, Shaw AS, Chan AC. Reconstitution of Syk function by the ZAP-70 protein tyrosine kinase. Immunity. 1995 May;2(5):485–492. [PubMed]
  • Langhans-Rajasekaran SA, Wan Y, Huang XY. Activation of Tsk and Btk tyrosine kinases by G protein beta gamma subunits. Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8601–8605. [PMC free article] [PubMed]
  • Lemmon MA, Ferguson KM, Schlessinger J. PH domains: diverse sequences with a common fold recruit signaling molecules to the cell surface. Cell. 1996 May 31;85(5):621–624. [PubMed]
  • Lewis RS, Cahalan MD. Potassium and calcium channels in lymphocytes. Annu Rev Immunol. 1995;13:623–653. [PubMed]
  • 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. 1995 May;2(5):451–460. [PubMed]
  • Li T, Rawlings DJ, Park H, Kato RM, Witte ON, Satterthwaite AB. Constitutive membrane association potentiates activation of Bruton tyrosine kinase. Oncogene. 1997 Sep 18;15(12):1375–1383. [PubMed]
  • Longnecker R, Miller CL, Tomkinson B, Miao XQ, Kieff E. Deletion of DNA encoding the first five transmembrane domains of Epstein-Barr virus latent membrane proteins 2A and 2B. J Virol. 1993 Aug;67(8):5068–5074. [PMC free article] [PubMed]
  • Lytton J, Westlin M, Hanley MR. Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca-ATPase family of calcium pumps. J Biol Chem. 1991 Sep 15;266(26):17067–17071. [PubMed]
  • 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. 1993 Feb;8(2):417–424. [PubMed]
  • Miller CL, Burkhardt AL, Lee JH, Stealey B, Longnecker R, Bolen JB, Kieff E. Integral membrane protein 2 of Epstein-Barr virus regulates reactivation from latency through dominant negative effects on protein-tyrosine kinases. Immunity. 1995 Feb;2(2):155–166. [PubMed]
  • Muta T, Kurosaki T, Misulovin Z, Sanchez M, Nussenzweig MC, Ravetch JV. A 13-amino-acid motif in the cytoplasmic domain of Fc gamma RIIB modulates B-cell receptor signalling. Nature. 1994 Mar 3;368(6466):70–73. [PubMed]
  • Noh DY, Shin SH, Rhee SG. Phosphoinositide-specific phospholipase C and mitogenic signaling. Biochim Biophys Acta. 1995 Dec 18;1242(2):99–113. [PubMed]
  • O'Keefe TL, Williams GT, Davies SL, Neuberger MS. Hyperresponsive B cells in CD22-deficient mice. Science. 1996 Nov 1;274(5288):798–801. [PubMed]
  • Ono M, Bolland S, Tempst P, Ravetch JV. Role of the inositol phosphatase SHIP in negative regulation of the immune system by the receptor Fc(gamma)RIIB. Nature. 1996 Sep 19;383(6597):263–266. [PubMed]
  • Ono M, Okada H, Bolland S, Yanagi S, Kurosaki T, Ravetch JV. Deletion of SHIP or SHP-1 reveals two distinct pathways for inhibitory signaling. Cell. 1997 Jul 25;90(2):293–301. [PubMed]
  • Parekh AB, Fleig A, Penner R. The store-operated calcium current I(CRAC): nonlinear activation by InsP3 and dissociation from calcium release. Cell. 1997 Jun 13;89(6):973–980. [PubMed]
  • Park H, Wahl MI, Afar DE, Turck CW, Rawlings DJ, Tam C, Scharenberg AM, Kinet JP, Witte ON. Regulation of Btk function by a major autophosphorylation site within the SH3 domain. Immunity. 1996 May;4(5):515–525. [PubMed]
  • Perlmutter RM, Levin SD, Appleby MW, Anderson SJ, Alberola-Ila J. Regulation of lymphocyte function by protein phosphorylation. Annu Rev Immunol. 1993;11:451–499. [PubMed]
  • Premack BA, Gardner P. Signal transduction by T-cell receptors: mobilization of Ca and regulation of Ca-dependent effector molecules. Am J Physiol. 1992 Dec;263(6 Pt 1):C1119–C1140. [PubMed]
  • Putney JW, Jr, Bird GS. The signal for capacitative calcium entry. Cell. 1993 Oct 22;75(2):199–201. [PubMed]
  • Qin S, Inazu T, Takata M, Kurosaki T, Homma Y, Yamamura H. Cooperation of tyrosine kinases p72syk and p53/56lyn regulates calcium mobilization in chicken B cell oxidant stress signaling. Eur J Biochem. 1996 Mar 1;236(2):443–449. [PubMed]
  • Rameh LE, Arvidsson A k, Carraway KL, 3rd, Couvillon AD, Rathbun G, Crompton A, VanRenterghem B, Czech MP, Ravichandran KS, Burakoff SJ, et al. A comparative analysis of the phosphoinositide binding specificity of pleckstrin homology domains. J Biol Chem. 1997 Aug 29;272(35):22059–22066. [PubMed]
  • Ransom JT, Harris LK, Cambier JC. Anti-Ig induces release of inositol 1,4,5-trisphosphate, which mediates mobilization of intracellular Ca++ stores in B lymphocytes. J Immunol. 1986 Jul 15;137(2):708–714. [PubMed]
  • Rawlings DJ, Witte ON. Bruton's tyrosine kinase is a key regulator in B-cell development. Immunol Rev. 1994 Apr;138:105–119. [PubMed]
  • Rawlings DJ, Witte ON. The Btk subfamily of cytoplasmic tyrosine kinases: structure, regulation and function. Semin Immunol. 1995 Aug;7(4):237–246. [PubMed]
  • Rawlings DJ, Saffran DC, Tsukada S, Largaespada DA, Grimaldi JC, Cohen L, Mohr RN, Bazan JF, Howard M, Copeland NG, et al. Mutation of unique region of Bruton's tyrosine kinase in immunodeficient XID mice. Science. 1993 Jul 16;261(5119):358–361. [PubMed]
  • Rawlings DJ, Scharenberg AM, Park H, Wahl MI, Lin S, Kato RM, Fluckiger AC, Witte ON, Kinet JP. Activation of BTK by a phosphorylation mechanism initiated by SRC family kinases. Science. 1996 Feb 9;271(5250):822–825. [PubMed]
  • Rigley KP, Harnett MM, Phillips RJ, Klaus GG. Analysis of signaling via surface immunoglobulin receptors on B cells from CBA/N mice. Eur J Immunol. 1989 Nov;19(11):2081–2086. [PubMed]
  • Rivera VM, Brugge JS. Clustering of Syk is sufficient to induce tyrosine phosphorylation and release of allergic mediators from rat basophilic leukemia cells. Mol Cell Biol. 1995 Mar;15(3):1582–1590. [PMC free article] [PubMed]
  • Salim K, Bottomley MJ, Querfurth E, Zvelebil MJ, Gout I, Scaife R, Margolis RL, Gigg R, 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. EMBO J. 1996 Nov 15;15(22):6241–6250. [PMC free article] [PubMed]
  • Saouaf SJ, Mahajan S, Rowley RB, Kut SA, Fargnoli J, Burkhardt AL, Tsukada S, Witte ON, Bolen JB. 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 U S A. 1994 Sep 27;91(20):9524–9528. [PMC free article] [PubMed]
  • Sato K, Mano H, Ariyama T, Inazawa J, Yazaki Y, Hirai H. Molecular cloning and analysis of the human Tec protein-tyrosine kinase. Leukemia. 1994 Oct;8(10):1663–1672. [PubMed]
  • Scharenberg AM, Kinet JP. The emerging field of receptor-mediated inhibitory signaling: SHP or SHIP? Cell. 1996 Dec 13;87(6):961–964. [PubMed]
  • Scharenberg AM, Lin S, Cuenod B, Yamamura H, Kinet JP. Reconstitution of interactions between tyrosine kinases and the high affinity IgE receptor which are controlled by receptor clustering. EMBO J. 1995 Jul 17;14(14):3385–3394. [PMC free article] [PubMed]
  • Scharenberg AM, El-Hillal O, Fruman DA, Beitz LO, Li Z, Lin S, Gout I, Cantley LC, Rawlings DJ, Kinet JP. Phosphatidylinositol-3,4,5-trisphosphate (PtdIns-3,4,5-P3)/Tec kinase-dependent calcium signaling pathway: a target for SHIP-mediated inhibitory signals. EMBO J. 1998 Apr 1;17(7):1961–1972. [PMC free article] [PubMed]
  • Serafini AT, Lewis RS, Clipstone NA, Bram RJ, Fanger C, Fiering S, Herzenberg LA, Crabtree GR. Isolation of mutant T lymphocytes with defects in capacitative calcium entry. Immunity. 1995 Aug;3(2):239–250. [PubMed]
  • Sideras P, Smith CI. Molecular and cellular aspects of X-linked agammaglobulinemia. Adv Immunol. 1995;59:135–223. [PubMed]
  • Siliciano JD, Morrow TA, Desiderio SV. itk, a T-cell-specific tyrosine kinase gene inducible by interleukin 2. Proc Natl Acad Sci U S A. 1992 Dec 1;89(23):11194–11198. [PMC free article] [PubMed]
  • Snyder FF, Jenuth JP, Mably ER, Mangat RK. Point mutations at the purine nucleoside phosphorylase locus impair thymocyte differentiation in the mouse. Proc Natl Acad Sci U S A. 1997 Mar 18;94(6):2522–2527. [PMC free article] [PubMed]
  • Sugawara H, Kurosaki M, Takata M, Kurosaki T. Genetic evidence for involvement of type 1, type 2 and type 3 inositol 1,4,5-trisphosphate receptors in signal transduction through the B-cell antigen receptor. EMBO J. 1997 Jun 2;16(11):3078–3088. [PMC free article] [PubMed]
  • Takata M, Kurosaki T. A role for Bruton's tyrosine kinase in B cell antigen receptor-mediated activation of phospholipase C-gamma 2. J Exp Med. 1996 Jul 1;184(1):31–40. [PMC free article] [PubMed]
  • Takata M, Sabe H, Hata A, Inazu T, Homma Y, Nukada T, Yamamura H, Kurosaki T. Tyrosine kinases Lyn and Syk regulate B cell receptor-coupled Ca2+ mobilization through distinct pathways. EMBO J. 1994 Mar 15;13(6):1341–1349. [PMC free article] [PubMed]
  • Takata M, Homma Y, Kurosaki T. Requirement of phospholipase C-gamma 2 activation in surface immunoglobulin M-induced B cell apoptosis. J Exp Med. 1995 Oct 1;182(4):907–914. [PMC free article] [PubMed]
  • Takemura H, Hughes AR, Thastrup O, Putney JW., Jr Activation of calcium entry by the tumor promoter thapsigargin in parotid acinar cells. Evidence that an intracellular calcium pool and not an inositol phosphate regulates calcium fluxes at the plasma membrane. J Biol Chem. 1989 Jul 25;264(21):12266–12271. [PubMed]
  • Takemura H, Ohshika H, Yokosawa N, Oguma K, Thastrup O. The thapsigargin-sensitive intracellular Ca2+ pool is more important in plasma membrane Ca2+ entry than the IP3-sensitive intracellular Ca2+ pool in neuronal cell lines. Biochem Biophys Res Commun. 1991 Nov 14;180(3):1518–1526. [PubMed]
  • Thastrup O, Dawson AP, Scharff O, Foder B, Cullen PJ, Drøbak BK, Bjerrum PJ, Christensen SB, Hanley MR. Thapsigargin, a novel molecular probe for studying intracellular calcium release and storage. Agents Actions. 1989 Apr;27(1-2):17–23. [PubMed]
  • Thomas JD, Sideras P, Smith CI, Vorechovský I, Chapman V, Paul WE. Colocalization of X-linked agammaglobulinemia and X-linked immunodeficiency genes. Science. 1993 Jul 16;261(5119):355–358. [PubMed]
  • 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. 1993 Jan 29;72(2):279–290. [PubMed]
  • Tsukada S, Simon MI, Witte ON, Katz A. Binding of beta gamma subunits of heterotrimeric G proteins to the PH domain of Bruton tyrosine kinase. Proc Natl Acad Sci U S A. 1994 Nov 8;91(23):11256–11260. [PMC free article] [PubMed]
  • Verma A, Hirsch DJ, Hanley MR, Thastrup O, Christensen SB, Snyder SH. Inositol trisphosphate and thapsigargin discriminate endoplasmic reticulum stores of calcium in rat brain. Biochem Biophys Res Commun. 1990 Oct 30;172(2):811–816. [PubMed]
  • Vetrie D, Vorechovský I, Sideras P, Holland J, Davies A, Flinter F, Hammarström L, Kinnon C, Levinsky R, Bobrow M, et al. The gene involved in X-linked agammaglobulinaemia is a member of the src family of protein-tyrosine kinases. Nature. 1993 Jan 21;361(6409):226–233. [PubMed]
  • Wacholtz MC, Cragoe EJ, Jr, Lipsky PE. A Na(+)-dependent Ca2+ exchanger generates the sustained increase in intracellular Ca2+ required for T cell activation. J Immunol. 1992 Sep 15;149(6):1912–1920. [PubMed]
  • Wacholtz MC, Cragoe EJ, Jr, Lipsky PE. Delineation of the role of a Na+/Ca2+ exchanger in regulating intracellular Ca2+ in T cells. Cell Immunol. 1993 Mar;147(1):95–109. [PubMed]
  • Weiss A, Littman DR. Signal transduction by lymphocyte antigen receptors. Cell. 1994 Jan 28;76(2):263–274. [PubMed]
  • Wicker LS, Scher I. X-linked immune deficiency (xid) of CBA/N mice. Curr Top Microbiol Immunol. 1986;124:87–101. [PubMed]
  • Wilson HA, Greenblatt D, Poenie M, Finkelman FD, Tsien RY. Crosslinkage of B lymphocyte surface immunoglobulin by anti-Ig or antigen induces prolonged oscillation of intracellular ionized calcium. J Exp Med. 1987 Aug 1;166(2):601–606. [PMC free article] [PubMed]
  • Yamada H, June CH, Finkelman F, Brunswick M, Ring MS, Lees A, Mond JJ. Persistent calcium elevation correlates with the induction of surface immunoglobulin-mediated B cell DNA synthesis. J Exp Med. 1993 Jun 1;177(6):1613–1621. [PMC free article] [PubMed]
  • Zacchetti D, Clementi E, Fasolato C, Lorenzon P, Zottini M, Grohovaz F, Fumagalli G, Pozzan T, Meldolesi J. Intracellular Ca2+ pools in PC12 cells. A unique, rapidly exchanging pool is sensitive to both inositol 1,4,5-trisphosphate and caffeine-ryanodine. J Biol Chem. 1991 Oct 25;266(30):20152–20158. [PubMed]
  • Zweifach A, Lewis RS. Mitogen-regulated Ca2+ current of T lymphocytes is activated by depletion of intracellular Ca2+ stores. Proc Natl Acad Sci U S A. 1993 Jul 1;90(13):6295–6299. [PMC free article] [PubMed]

Articles from The EMBO Journal are provided here courtesy of The European Molecular Biology Organization

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

  • Compound
    Compound
    PubChem Compound links
  • MedGen
    MedGen
    Related information in MedGen
  • PubMed
    PubMed
    PubMed citations for these articles
  • Substance
    Substance
    PubChem Substance links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...