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Science 286 (5446): 1949-1954

Copyright © 1999 by the American Association for the Advancement of Science

Requirement for B Cell Linker Protein (BLNK) in B Cell Development

Rajita Pappu, 12 Alec M. Cheng, 123 Bin Li, 124 Qian Gong, 124 Chris Chiu, 12 Nancy Griffin, 124 Mike White, 13 Barry P. Sleckman, 13 Andrew C. Chan 1234*

Linker proteins function as molecular scaffolds to localize enzymes with substrates. In B cells, B cell linker protein (BLNK) links the B cell receptor (BCR)-activated Syk kinase to the phosphoinositide and mitogen-activated kinase pathways. To examine the in vivo role of BLNK, mice deficient in BLNK were generated. B cell development in BLNK-/- mice was blocked at the transition from B220+CD43+ progenitor B to B220+CD43- precursor B cells. Only a small percentage of immunoglobulin M++ (IgM++), but not mature IgMloIgDhi, B cells were detected in the periphery. Hence, BLNK is an essential component of BCR signaling pathways and is required to promote B cell development.

1 Center for Immunology;
2 Division of Rheumatology, Department of Medicine;
3 Department of Pathology;
4 Howard Hughes Medical Institute, Washington University School of Medicine, St. Louis, MO 63110, USA.
*   To whom correspondence should be addressed. E-mail: achan{at}

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Mol. Cell. Biol. 32, 4462-4471
   Abstract »    Full Text »    PDF »
Critical role of the IgM Fc receptor in IgM homeostasis, B-cell survival, and humoral immune responses.
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PNAS 109, E2699-E2706
   Abstract »    Full Text »    PDF »
Regulation of B Cell Linker Protein Transcription by PU.1 and Spi-B in Murine B Cell Acute Lymphoblastic Leukemia.
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J. Immunol. 189, 3347-3354
   Abstract »    Full Text »    PDF »
Agammaglobulinemia and absent B lineage cells in a patient lacking the p85{alpha} subunit of PI3K.
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J. Exp. Med. 209, 463-470
   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
The B-cell antigen receptor signals through a preformed transducer module of SLP65 and CIN85.
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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Science Signaling 3, ra60
   Abstract »    Full Text »    PDF »
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SLP-76 Couples Syk to the Osteoclast Cytoskeleton.
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BLNK Binds Active H-Ras to Promote B Cell Receptor-mediated Capping and ERK Activation.
Y. Imamura, A. Oda, T. Katahira, K. Bundo, K. A. Pike, M. J. H. Ratcliffe, and D. Kitamura (2009)
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Identification of differential gene expression during porcine conceptus rapid trophoblastic elongation and attachment to uterine luminal epithelium.
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   Abstract »    Full Text »    PDF »
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Int. Immunol. 20, 1417-1426
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J. Immunol. 178, 2336-2343
   Abstract »    Full Text »    PDF »
B Cell Receptor Signaling Down-Regulates Forkhead Box Transcription Factor Class O 1 mRNA Expression via Phosphatidylinositol 3-Kinase and Bruton's Tyrosine Kinase.
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J. Immunol. 178, 740-747
   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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A. Grabbe and J. Wienands (2006)
Blood 108, 3761-3768
   Abstract »    Full Text »    PDF »
BASH-novel PKC-Raf-1 pathway of pre-BCR signaling induces {kappa} gene rearrangement.
M. Yamamoto, K. Hayashi, T. Nojima, Y. Matsuzaki, Y. Kawano, H. Karasuyama, R. Goitsuka, and D. Kitamura (2006)
Blood 108, 2703-2711
   Abstract »    Full Text »    PDF »
Dual function for the adaptor MIST in IFN-{gamma} production by NK and CD4+NKT cells regulated by the Src kinase Fgr.
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Blood 107, 3647-3655
   Abstract »    Full Text »    PDF »
Phospholipase C{gamma}2 Dosage Is Critical for B Cell Development in the Absence of Adaptor Protein BLNK.
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J. Immunol. 176, 4690-4698
   Abstract »    Full Text »    PDF »
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T. Katahira, Y. Imamura, and D. Kitamura (2006)
Int. Immunol. 18, 545-553
   Abstract »    Full Text »    PDF »
Distinct Roles of Phosphoinositide-3 Kinase and Phospholipase C{gamma}2 in B-Cell Receptor-Mediated Signal Transduction.
X. Dai, Y. Chen, J. Schuman, Z. Hua, J. W. Adamson, R. Wen, and D. Wang (2006)
Mol. Cell. Biol. 26, 88-99
   Abstract »    Full Text »    PDF »
B Cell Receptor (BCR) Cross-Talk: CD40 Engagement Creates an Alternate Pathway for BCR Signaling That Activates I{kappa}B Kinase/I{kappa}B{alpha}/NF-{kappa}B without the Need for PI3K and Phospholipase C{gamma}.
T. Mizuno and T. L. Rothstein (2005)
J. Immunol. 174, 6062-6070
   Abstract »    Full Text »    PDF »
The Adaptor Protein HSH2 Attenuates Apoptosis in Response to Ligation of the B Cell Antigen Receptor Complex on the B Lymphoma Cell Line, WEHI-231.
B. R. Herrin, A. L. Groeger, and L. B. Justement (2005)
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   Abstract »    Full Text »    PDF »
Tumor suppressor function of Bruton tyrosine kinase is independent of its catalytic activity.
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Blood 105, 259-265
   Abstract »    Full Text »    PDF »
Impaired Receptor Editing in the Primary B Cell Repertoire of BASH-Deficient Mice.
K. Hayashi, T. Nojima, R. Goitsuka, and D. Kitamura (2004)
J. Immunol. 173, 5980-5988
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R. Wen, Y. Chen, J. Schuman, G. Fu, S. Yang, W. Zhang, D. K. Newman, and D. Wang (2004)
EMBO J. 23, 4007-4017
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BASH-deficient mice: limited primary repertoire and antibody formation, but sufficient affinity maturation and memory B cell generation, in anti-NP response.
M. Yamamoto, T. Nojima, K. Hayashi, R. Goitsuka, K. Furukawa, T. Azuma, and D. Kitamura (2004)
Int. Immunol. 16, 1161-1171
   Abstract »    Full Text »    PDF »
Immune Functions in Mice Lacking Clnk, an SLP-76-Related Adaptor Expressed in a Subset of Immune Cells.
O. Utting, B. J. Sedgmen, T. H. Watts, X. Shi, R. Rottapel, A. Iulianella, D. Lohnes, and A. Veillette (2004)
Mol. Cell. Biol. 24, 6067-6075
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Identification and Characterization of a Novel BASH N Terminus-associated Protein, BNAS2.
Y. Imamura, T. Katahira, and D. Kitamura (2004)
J. Biol. Chem. 279, 26425-26432
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Enhanced T Cell Proliferation in Mice Lacking the p85{beta} Subunit of Phosphoinositide 3-Kinase.
J. A. Deane, M. J. Trifilo, C. M. Yballe, S. Choi, T. E. Lane, and D. A. Fruman (2004)
J. Immunol. 172, 6615-6625
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Pax-5 Is Essential for {kappa} Sterile Transcription during Ig{kappa} Chain Gene Rearrangement.
H. Sato, F. Saito-Ohara, J. Inazawa, and A. Kudo (2004)
J. Immunol. 172, 4858-4865
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The Importance of Three Membrane-distal Tyrosines in the Adaptor Protein NTAL/LAB.
S. Koonpaew, E. Janssen, M. Zhu, and W. Zhang (2004)
J. Biol. Chem. 279, 11229-11235
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Increased Numbers of B-1 Cells and Enhanced Responses against TI-2 Antigen in Mice Lacking APS, an Adaptor Molecule Containing PH and SH2 Domains.
M. Iseki, C. Kubo, S.-M. Kwon, A. Yamaguchi, Y. Kataoka, N. Yoshida, K. Takatsu, and S. Takaki (2004)
Mol. Cell. Biol. 24, 2243-2250
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Macrophage activation and Fc{gamma} receptor-mediated signaling do not require expression of the SLP-76 and SLP-65 adaptors.
K. E. Nichols, K. Haines, P. S. Myung, S. Newbrough, E. Myers, H. Jumaa, D. J. Shedlock, H. Shen, and G. A. Koretzky (2004)
J. Leukoc. Biol. 75, 541-552
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J. Mestas and C. C. W. Hughes (2004)
J. Immunol. 172, 2731-2738
   Abstract »    Full Text »    PDF »
Analysis of Gene Expression and Ig Transcription in PU.1/Spi-B-Deficient Progenitor B Cell Lines.
B. L. Schweitzer and R. P. DeKoter (2004)
J. Immunol. 172, 144-154
   Abstract »    Full Text »    PDF »
Mimicry of Pre-B Cell Receptor Signaling by Activation of the Tyrosine Kinase Blk.
T. Tretter, A. E. Ross, D. I. Dordai, and S. Desiderio (2003)
J. Exp. Med. 198, 1863-1873
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Phospholipase C{gamma}2 Provides Survival Signals via Bcl2 and A1 in Different Subpopulations of B Cells.
R. Wen, Y. Chen, L. Xue, J. Schuman, S. Yang, S. W. Morris, and D. Wang (2003)
J. Biol. Chem. 278, 43654-43662
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B Cell Receptor-Mediated Syk-Independent Activation of Phosphatidylinositol 3-Kinase, Ras, and Mitogen-Activated Protein Kinase Pathways.
T. Yokozeki, K. Adler, D. Lankar, and C. Bonnerot (2003)
J. Immunol. 171, 1328-1335
   Abstract »    Full Text »    PDF »
Bruton's Tyrosine Kinase Cooperates with the B Cell Linker Protein SLP-65 as a Tumor Suppressor in Pre-B Cells.
R. Kersseboom, S. Middendorp, G. M. Dingjan, K. Dahlenborg, M. Reth, H. Jumaa, and R. W. Hendriks (2003)
J. Exp. Med. 198, 91-98
   Abstract »    Full Text »    PDF »
Haploinsufficiency of B cell linker protein enhances B cell signaling defects in mice expressing a limiting dosage of Bruton's tyrosine kinase.
L. R. Whyburn, K. E. Halcomb, C. M. Contreras, R. Pappu, O. N. Witte, A. C. Chan, and A. B. Satterthwaite (2003)
Int. Immunol. 15, 383-392
   Abstract »    Full Text »    PDF »
Essential, Nonredundant Role for the Phosphoinositide 3-Kinase p110{delta} in Signaling by the B-Cell Receptor Complex.
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Mol. Cell. Biol. 22, 8580-8591
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BLNK: molecular scaffolding through 'cis'-mediated organization of signaling proteins.
C. W. Chiu, M. Dalton, M. Ishiai, T. Kurosaki, and A. C. Chan (2002)
EMBO J. 21, 6461-6472
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Regulation of Signaling in B Cells through the Phosphorylation of Syk on Linker Region Tyrosines: A MECHANISM FOR NEGATIVE SIGNALING BY THE Lyn TYROSINE KINASE.
J. J. Hong, T. M. Yankee, M. L. Harrison, and R. L. Geahlen (2002)
J. Biol. Chem. 277, 31703-31714
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Delayed Cellular Maturation and Decreased Immunoglobulin {kappa} Light Chain Production In Immature B Lymphocytes Lacking B Cell Linker Protein.
S. Xu and K.-P. Lam (2002)
J. Exp. Med. 196, 197-206
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Src Homology Region 2 Domain-Containing Phosphatase 1 Positively Regulates B Cell Receptor-Induced Apoptosis by Modulating Association of B Cell Linker Protein with Nck and Activation of c-Jun NH2-Terminal Kinase.
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J. Immunol. 169, 778-786
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AP2 Adaptor Complex-Dependent Internalization of CD5: Differential Regulation in T and B Cells.
X. Lu, R. C. Axtell, J. F. Collawn, A. Gibson, L. B. Justement, and C. Raman (2002)
J. Immunol. 168, 5612-5620
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The Direct Recruitment of BLNK to Immunoglobulin {alpha} Couples the B-Cell Antigen Receptor to Distal Signaling Pathways.
S. Kabak, B. J. Skaggs, M. R. Gold, M. Affolter, K. L. West, M. S. Foster, K. Siemasko, A. C. Chan, R. Aebersold, and M. R. Clark (2002)
Mol. Cell. Biol. 22, 2524-2535
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Receptor-Facilitated Antigen Presentation Requires the Recruitment of B Cell Linker Protein to Ig{alpha}.
K. Siemasko, B. J. Skaggs, S. Kabak, E. Williamson, B. K. Brown, W. Song, and M. R. Clark (2002)
J. Immunol. 168, 2127-2138
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Essential Immunoregulatory Role for BCAP in B Cell Development and Function.
T. Yamazaki, K. Takeda, K. Gotoh, H. Takeshima, S. Akira, and T. Kurosaki (2002)
J. Exp. Med. 195, 535-545
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Fcgamma RIIB1/SHIP-mediated Inhibitory Signaling in B Cells Involves Lipid Rafts.
M. J. Aman, A.-C. Tosello-Trampont, and K. Ravichandran (2001)
J. Biol. Chem. 276, 46371-46378
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Ligand-independent Signaling Functions for the B Lymphocyte Antigen Receptor and Their Role in Positive Selection during B Lymphopoiesis.
G. Bannish, E. M. Fuentes-Panana, J. C. Cambier, W. S. Pear, and J. G. Monroe (2001)
J. Exp. Med. 194, 1583-1596
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S. J. Holland, X. C. Liao, M. K. Mendenhall, X. Zhou, J. Pardo, P. Chu, C. Spencer, A. Fu, N. Sheng, P. Yu, et al. (2001)
J. Exp. Med. 194, 1263-1276
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D. Watanabe, S. Hashimoto, M. Ishiai, M. Matsushita, Y. Baba, T. Kishimoto, T. Kurosaki, and S. Tsukada (2001)
J. Biol. Chem. 276, 38595-38601
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Synergistic Regulation of Immunoreceptor Signaling by SLP-76-Related Adaptor Clnk and Serine/Threonine Protein Kinase HPK-1.
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Mol. Cell. Biol. 21, 6102-6112
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B Cell Adaptor Containing Src Homology 2 Domain (Bash) Links B Cell Receptor Signaling to the Activation of Hematopoietic Progenitor Kinase 1.
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J. Exp. Med. 194, 529-540
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Epstein-Barr Virus Latent Membrane Protein 2a (Lmp2a) Employs the Slp-65 Signaling Module.
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J. Exp. Med. 194, 255-264
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Immune System Dysfunction and Autoimmune Disease in Mice Lacking Emk (Par-1) Protein Kinase.
J. B. Hurov, T. S. Stappenbeck, C. M. Zmasek, L. S. White, S. H. Ranganath, J. H. Russell, A. C. Chan, K. M. Murphy, and H. Piwnica-Worms (2001)
Mol. Cell. Biol. 21, 3206-3219
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I{kappa}b Kinase {alpha} Is Essential for Mature B Cell Development and Function.
T. Kaisho, K. Takeda, T. Tsujimura, T. Kawai, F. Nomura, N. Terada, and S. Akira (2001)
J. Exp. Med. 193, 417-426
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Cutting Edge Commentary: Origins of B-1 Cells.
H. H. Wortis and R. Berland (2001)
J. Immunol. 166, 2163-2166
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Cutting Edge: B Cell Linker Protein Is Dispensable for the Allelic Exclusion of Immunoglobulin Heavy Chain Locus But Required for the Persistence of CD5+ B Cells.
S. Xu, S.-C. Wong, and K.-P. Lam (2000)
J. Immunol. 165, 4153-4157
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Involvement of Lat, Gads, and Grb2 in Compartmentation of Slp-76 to the Plasma Membrane.
M. Ishiai, M. Kurosaki, K. Inabe, A. C. Chan, K. Sugamura, and T. Kurosaki (2000)
J. Exp. Med. 192, 847-856
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Cutting Edge: Essential Role of Phospholipase C-{gamma}2 in B Cell Development and Function.
A. Hashimoto, K. Takeda, M. Inaba, M. Sekimata, T. Kaisho, S. Ikehara, Y. Homma, S. Akira, and T. Kurosaki (2000)
J. Immunol. 165, 1738-1742
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Ras Mediates Effector Pathways Responsible for Pre-B Cell Survival, Which Is Essential for the Developmental Progression to the Late Pre-B Cell Stage.
H. Nagaoka, Y. Takahashi, R. Hayashi, T. Nakamura, K. Ishii, J. Matsuda, A. Ogura, Y. Shirakata, H. Karasuyama, T. Sudo, et al. (2000)
J. Exp. Med. 192, 171-182
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Fates of human B-cell precursors.
T. W. LeBien (2000)
Blood 96, 9-23
   Abstract »    Full Text »    PDF »
In vitro and in vivo macrophage function can occur independently of SLP-76.
P. S. Myung, J. L. Clements, D. W. White, Z. A. Malik, J. S. Cowdery, L.-A. H. Allen, J. T. Harty, D. J. Kusner, and G. A. Koretzky (2000)
Int. Immunol. 12, 887-897
   Abstract »    Full Text »    PDF »
The B cell-restricted adaptor BASH is required for normal development and antigen receptor-mediated activation of B cells.
K. Hayashi, R. Nittono, N. Okamoto, S. Tsuji, Y. Hara, R. Goitsuka, and D. Kitamura (2000)
PNAS 97, 2755-2760
   Abstract »    Full Text »    PDF »
B cell development and activation defects resulting in xid-like immunodeficiency in BLNK/SLP-65-deficient mice.
S. Xu, J. E.-L. Tan, E. P.-Y. Wong, A. Manickam, S. Ponniah, and K.-P. Lam (2000)
Int. Immunol. 12, 397-404
   Abstract »    Full Text »    PDF »
An Essential Role for BLNK in Human B Cell Development.
Y. Minegishi, J. Rohrer, E. Coustan-Smith, H. M. Lederman, R. Pappu, D. Campana, A. C. Chan, and M. E. Conley (1999)
Science 286, 1954-1957
   Abstract »    Full Text »
The Adaptor Protein BLNK Is Required for B Cell Antigen Receptor-induced Activation of Nuclear Factor-kappa B and Cell Cycle Entry and Survival of B Lymphocytes.
J. E.-L. Tan, S.-C. Wong, S. K.-E. Gan, S. Xu, and K.-P. Lam (2001)
J. Biol. Chem. 276, 20055-20063
   Abstract »    Full Text »    PDF »
SHP-1 Requires Inhibitory Co-receptors to Down-modulate B Cell Antigen Receptor-mediated Phosphorylation of Cellular Substrates.
T. Adachi, J. Wienands, C. Wakabayashi, H. Yakura, M. Reth, and T. Tsubata (2001)
J. Biol. Chem. 276, 26648-26655
   Abstract »    Full Text »    PDF »
MIST Functions through Distinct Domains in Immunoreceptor Signaling in the Presence and Absence of LAT.
R. Goitsuka, A. Tatsuno, M. Ishiai, T. Kurosaki, and D. Kitamura (2001)
J. Biol. Chem. 276, 36043-36050
   Abstract »    Full Text »    PDF »
Hematopoietic Progenitor Kinase 1 Associates Physically and Functionally with the Adaptor Proteins B Cell Linker Protein and SLP-76 in Lymphocytes.
K. Sauer, J. Liou, S. B. Singh, D. Yablonski, A. Weiss, and R. M. Perlmutter (2001)
J. Biol. Chem. 276, 45207-45216
   Abstract »    Full Text »    PDF »

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