Signaling pathways activated in a unique mast cell line where interleukin-3 supports survival and stem cell factor is required for a proliferative response

Blood

Volumn 87, Issue 9, 1996, Pages 3655-3668

  O'Farrell, Anne Marie ^a   Ichihara, Masatoshi ^a   Mui, Alice L F ^a   Miyajima, Atsushi ^a  

^a MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 3; STEM CELL FACTOR;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; FEMALE; GENE EXPRESSION REGULATION; GROWTH STIMULATION; IMMUNOREGULATION; MAST CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIVISION; CELL LINE; CELL SURVIVAL; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; INTERLEUKIN-3; MAST CELLS; MICE; SIGNAL TRANSDUCTION; STEM CELL FACTOR;

EID: 0029988381     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood.v87.9.3655.bloodjournal8793655     Document Type: Article

References (99)

1. Galli SJ. New insights into "the riddle of the mast cells": Microenvironmental regulation of mast cell development and phenotypic heterogeneity. Lab Invest 62:5, 1990
2. Miller JS, Schwartz LB: Human mast cell proteases and mast cell heterogeneity. Curr Opin Immunol 1:637, 1989
3. Lee F, Yokota T, Otsuka T, Meyerson P, Villaret D, Coffman R, Mosmann T, Rennick D, Roehm N, Smith C, Zlotnik A, Arai K-i: Isolation and characterization of a mouse interleukin cDNA clone that expresses B-cell stimulatory factor 1 activities and T-cell- and mast-cell-stimulating activities. Proc Natl Acad Sci USA 83:2061, 1986
4. Thompson-Snipes L, Dhar V, Bond MW, Mosmann TR, Moore KW, Rennick DM: Interleukin 10: A novel stimulatory factor for mast cells and their progenitors. J Exp Med 173:507, 1991
5. Renauld JC, Goethals A, Houssiau F, Roost EV, Snick JV: Cloning and expression of a cDNA for the human homolog of mouse T cell and mast cell growth factor P40. Cytokine 2:9, 1990
6. Tsuji K, Zsebo KM, Ogawa M. Marine mast cell colony formation supported by IL-3, IL-4. and recombinant rat stem cell factor, ligand for c-kit. J Cell Physiol 148:362, 1991
7. Tsuji K, Zsebo KM, Ogawa M: Enhancement of murine blast cell colony formation in culture by recombinant rat stem cell factor, ligand for c-kit. Blood 78:1223, 1991
8. Zsebo KM, Williams DA, Geissler EN, Broudy VC, Martin FH, Atkins HL, Hsu RY, Birkett NC, Okino KH, Murdock DC, Jacobsen FW, Langley KE, Smith KA, Takeishi T, Cattanach BM, Gaill SJ, Suggs S: Stem cell factor is encoded at the Sl locus of the mouse and is the ligand for the c-kit tyrosine kinase receptor. Cell 63:213, 1990
9. Chabot B, Stephenson D, Chapman VM, Besmer P, Bernstein A. The proto-oncogene c-kit encoding a transmembrane tyrosine kinase receptor maps to the mouse W locus. Nature 335:88, 1988
10. d genotype, in Galli SJ, Austen KF (eds): Mast Cell and Basophil Differentiation and Function in Health and Disease. New York, NY, Raven, 1989
11. Nocka K, Buck J, Levi E, Besmer P: Candidate ligand for the c-kit transmembrane kinase receptor: KL, a fibroblast derived growth factor stimulates mast cells and erythroid progenitors. EMBO J 9:3287, 1990
12. Tsai M, Takeishi T, Thompson H, Langley KE, Zsebo KM, Metcalfe DD, Geissler EN, Galli SJ: Induction of mast cell proliferation, maturation, and heparin synthesis by the rat c-kit ligand, stem cell factor. Proc Natl Acad Sci USA 88:6382, 1991
13. Takagi M, Nakahata T, Kubo T, Shiohara M, Koike K, Miyajima A, Arai K, Nishikawa S, Zsebo KM, Komiyama A: Stimulation of mouse connective tissue-type mast cells by hemopoietic stem cell factor, a ligand for the c-kit receptor. J Immunol 148:3446, 1992
14. Bischoff SC, Dahinden CA: c-kit ligand: A unique potentiator of mediator release by human lung mast cells. J Exp Med 175:237, 1992
15. Nakajima K, Hirai K, Yamaguchi M, Takaishi T, Ohta K, Monta Y, Ito K: Stem cell factor has histamine releasing activity in rat connective tissue-type mast cells. Biochem Biophys Res Commun 183:1076, 1992
16. Wershil BK, Tsai M, Geissler EN, Zsebo KM, Galli SJ: The rat c-kit ligand, stem cell factor, induces c-kit receptor-dependent mouse mast cell activation in vivo. Evidence that signaling through the c-kit receptor can induce expression of cellular function. J Exp Med 175:245, 1992
17. Coleman JW, Holliday MR, Kimber I, Zsebo KM, Galli SJ: Regulation of mouse peritoneal mast cell secretory function by stem cell factor, IL-3 or IL-4. J Immunol 150:556, 1993
18. Dastych J, Metcalfe DD. Stem cell factor induces mast cell adhesion to fibronectin. J Immunol 152:213, 1994
19. Gurish MF, Ghildyal N, McNeil HP, Austen KF, Gillis S, Stevens RL: Differential expression of secretory granule proteases in mouse mast cells exposed to interleukin 3 and c-kit ligand. J Exp Med 175:1003, 1992
20. Haig DM, Huntley JF, MacKellar A, Newlands GF, Inglis L, Sangha R, Cohen D, Hapel A, Galli SJ, Miller HR: Effects of stem cell factor (kit-ligand) and interleukin-3 on the growth and serine proteinase expression of rat bone-marrow-derived or serosal mast cells. Blood 83:72, 1994
21. Haig DM, McMenamin C, Redmond J, Brown D, Young IG, Cohen SD, Hapel AJ: Rat IL-3 stimulates the growth of rat mucosal mast cells in culture. Immunology 65:205, 1988
22. Tsuji K, Nakahata T, Takagi M, Kobayashi T, Ishiguro A, Kikuchi T, Naganuma K, Koike K, Miyajima A, Arai K, Akabane T: Effects of interleukin-3 and interleukin-4 on the development of "connective tissue-type" mast cells: Interleukin-3 supports their survival and interleukin-4 triggers and supports their proliferation synergistically with interleukin-3. Blood 75:421, 1990
23. Tsuji K, Nakahata T, Takagi M, Kobayashi T, Ishiguro A, Kikuchi T, Naganuma K, Koike K, Miyajima A, Arai K, Akabane T: Synergistic action of phorbol ester and IL-3 in the induction of "connective tissue-type" mast cell proliferation. J Immunol 144:678, 1990
24. Tsai M, Shih LS, Newlands GF, Takeishi T, Langley KE, Zsebo KM, Miller HR, Geissler EN, Galli SJ: The rat c-kit ligand. stem cell factor, induces the development of connective tissue-type and mucosal mast cells in vivo. Analysis by anatomical distribution, histochemistry, and protease phenotype. J Exp Med 174:125, 1991
25. Rennick D, Hunte B, Holland G, Thompson-Snipes L: Cofactors are essential for stem cell factor-dependent growth and maturation of mast cell progenitors: Comparative effects of interleukin-3 (IL-3), IL-4, IL-10, and nbroblasts. Blood 85:57, 1995
26. Hara T, Miyajima A: Two distinct functional high affinity receptors for mouse IL-3. EMBO J 10:1875, 1992
27. O'Farrell A-M, Kinoshita T, Miyajima A: Haemopoietic growth factor receptors, in Whetton AD, Gordon J, Clark N (eds): Blood Cell Biochemistry, vol 7: Haemopoietic Cell Growth Factors. London, UK, Plenum, 1996 (in press)
28. Gorman DM, Itoh N, Kitamura T, Schreurs J, Yonehara S, Yahara I, Arai K, Miyajima A: Cloning and expression of a gene encoding an interleukin 3 receptor-like protein: Identification of another member of the cytokine receptor gene family. Proc Natl Acad Sci USA 87:5459, 1990
29. Morla AO, Schreurs J, Miyajima A, Wang JY: Hematopoietic growth factors activate the tyrosine phosphorylation of distinct sets of proteins in interleukin-3-dependent murine cell lines. Mol Cell Biol 8:2214, 1988
30. Sorensen P, Mui AL, Krystal G: Interleukin-3 stimulates the tyrosine phosphorylation of the 140-kilodalton interleukin-3 receptor. J Biol Chem 264:19253, 1989
31. Isfort RJ, Ihle JN Multiple hematopoietic growth factors signal through tyrosine phosphorylation. Growth Factors 2:213, 1990
32. Duronio V, Clark LI, Federsppiel B, Wieler JS, Schrader JW: Tyrosine phosphorylation of receptor beta subunits and common substrates in response to interleukin-3 and granulocyte-macrophage colony-stimulating factor. J Biol Chem 267:21856, 1992
33. Sakamaki K, Miyajima I, Kitamura T, Miyajima A: Critical cytoplasmic domains of the common beta subunit of the human GM-CSF, IL-3 and IL-5 receptors for growth signal transduction and tyrosine phosphorylation. EMBO J 11:3541, 1992
34. Sato N, Sakamaki K, Terada N, Arai K, Miyajima A: Signal transduction by the high-affinity GM-CSF receptor: Two distinct cytoplasmic regions of the common beta subunit responsible for different signaling. EMBO J 12:4181, 1993
35. Quelle FW, Sato N, Witthuhn BA, Inborn RC, Eder M, Miyajima A, Griffin JD, IhIe JN: Jak 2 associates with the beta c chain of the receptor for granulocyte-macrophage colony-stimulating factor, and its activation requires the membrane-proximal region. Mol Cell Biol 14:4335, 1994
36. Darnell JJ, Kerr IM, Stark GR: Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264:1415, 1994
37. Ihle JN, Witthuhn BA, Quelle FW, Yamamoto K, Thierfelder WE, Kreider B, Silvennoinen O: Signaling by the cytokine receptor superfamily: JAKs and STATs. Trends Biochem Sci 19:222, 1994
38. Rothman P, Kreider B, Azam M, Levy D, Wegenka U, Eilers A, Decker T, Horn F, Kashleva H, Ihle J, Schindler C: Cytokines and growth factors signal through tyrosine phosphorylation of a family of related transcription factors. Immunity 1:457, 1994
39. Mui AL, Wakao H, O'Farrell AM, Harada N, Miyajima A: Interleukin-3, granulocyte-macrophage colony-stimulating factor, and interleukin-5 transduce signals through two STATS homologs. EMBO J 14:1166, 1995
40. Mui AL, Wakao H, Harada N, O'Farrell AM, Miyajima A: Interleukin-3, granulocyte-macrophage colony-stimulating factor, and interleukin-5 transduce signals through two forms of STAT5. J Leuk Biol 57:799, 1995
41. Kinoshita T, Yokota T, Arai K, Miyajima A: Suppression of apoptotic death in hematopoietic cells by signalling through the IL-3/GM-CSF receptors. EMBO J 14:266, 1995
42. Nabel G, Galli SJ, Dvorak AM, Dvorak HF, Cantor H: Inducer T lymphocytes synthesize a factor that stimulates proliferation of cloned mast cells. Nature 291:332, 1981
43. Nagao K, Yokoro K, Aaronson SA: Continuous lines of basophil/mast cells derived from normal mouse bone marrow. Science 212:333, 1981
44. Razin E, Cordon CC, Good RA: Growth of a pure population of mouse mast cells in vitro with conditioned medium derived from concanavalin A-stimulated splenocytes. Proc Natl Acad Sci USA 78:2559, 1981
45. Schrader JW, Lewis SJ, Clark LI, Culvenor JG: The persisting (P) cell: Histamine content, regulation by a T cell-derived factor, origin from a bone marrow precursor, and relationship to mast cells. Proc Natl Acad Sci USA 78:323, 1981
46. Tertian G, Yung YP, Guy GD, Moore MA: Long-term in vitro culture of murine mast cells. I. Description of a growth factor-dependent culture technique. J Immunol 127:788, 1981
47. Otsu K, Nakano T, Kanakura Y, Asai H, Katz HR, Austen KF, Stevens RL, Galli SJ, Kitamura Y: Phenotypic changes of bone marrow-derived mast cells after intraperitoneal transfer into W/Wv mice that are genetically deficient in mast cells. J Exp Med 165:615, 1987
48. Ihle JN, Keller J, Oroszlan S, Henderson LE, Copeland TD, Fitch F, Prystowsky MB, Goldwasser E, Schrader JW, Palaszynski E, Dy M, Lebel B: Biologic properties of homogeneous interleukin 3. I. Demonstration of WEHI-3 growth factor activity, mast cell growth factor activity, p cell-stimulating factor activity, colony-stimulating factor activity, and histamine-producing cell-stimulating factor activity. J Immunol 131:282, 1983
49. Barrett KE, Pluznik DH, Metcalfe DD: Histamine release from the cultured mouse mast cell line PT18 in response to immunologic and nonimmunologic stimuli. Agents Actions 14:488, 1985
50. Miyajima A, Schreurs J, Otsu K, Kondo A, Arai K, Maeda S: Use of the silkworm, Bombyx mori, and an insect baculovirus vector for high-level expression and secretion of biologically active mouse interleukin-3. Gene 58:273, 1987
51. Kinoshita T, Yokota T, Arai K, Miyajima A: Regulation of Bcl-2 expression by oncogenic Ras protein in hematopoietic cells. Oncogene 10:2207, 1995
52. Hara T, Harada N, Mitsui H, Miura T, Ishizaka T, Miyajima A: Characterization of cell phenotype by a novel cDNA library subtraction system: Expression of CDS alpha in a mast cell-derived interleukin-4-dependent cell line. Blood 84:189, 1994
53. Reynolds DS, Stevens RL, Gurley DS, Lane WS, Austen KF, Serafin WE: Isolation and molecular cloning of mast cell carboxypeptidase A. A novel member of the carboxypeptidase gene family. J Biol Chem 264:20094, 1989
54. McNeil HP, Austen KF, Somerville LL, Gurish MF, Stevens RL: Molecular cloning of the mouse mast cell protease-5 gene. A novel secretory granule protease expressed early in the differentiation of serosal mast cells. J Biol Chem 266:20316, 1991
55. Huang RY, Blom T, Hellman L: Cloning and structural analysis of MMCP-1, MMCP-4 and MMCP-5, three mouse mast cell-specific serine proteases. Eur J Immunol 21:1611, 1991
56. Ghildyal N, McNeil HP, Gurish MF, Austen KF, Stevens RL: Transcriptional regulation of the mucosal mast cell-specific protease gene, MMCP-2, by interleukin 10 and interleukin 3. J Biol Chem 267:8473, 1992
57. Ichihara M, Hara T, Takagi M, Cho LC, Gorman DM, Miyajima A: Impaired interleukin-3 (IL-3) response of the AIJ mouse is caused by a branch point deletion in the IL-3 receptor alpha subunit gene. EMBO J 14:939, 1995
58. Ogorochi T, Hara T, Wang HM, Maruyama K, Miyajima A: Monoclonal antibodies specific for low-affinity interleukin-3 (IL-3) binding protein AIC2A: Evidence that AIC2A is a component of a high-affinity IL-3 receptor. Blood 79:895, 1992
59. Schreurs J, Arai K, Miyajima A: Evidence for a low-affinity interleukin-3 receptor. Growth Factors 2:221, 1990
60. Pritchard CA, Samuels M, Bosch E, McMahon M: Conditionally oncogenic forms of the A-Raf and B-Raf protein kinases display different biological and biochemical properties in NIH 3T3 cells. Mol Cell Biol 15:6430, 1995
61. Wakao H, Gouilleux F, Groner B: Mammary gland factor (MGF) is a novel family of the cytokine regulated transcription factor gene family and confers the prolactin response. EMBO J 13:2182, 1994
62. Mekori YA, Oh CK, Metcalfe DD: IL-3-dependent murine mast cells undergo apoptosis on removal of IL-3. Prevention of apoptosis by c-kit ligand. J Immunol 151:3775, 1993
63. Rennick D, Hunte B, Dang W, Thompson-Snipes L, Hudak S: Interleukin-10 promotes the growth of megakaryocyte, mast cell, and multilineage colonies: Analysis with committed progenitors and ThylloScal+ stem cells. Exp Hematol 22:136, 1994
64. Hendrie PC, Miyazama K, Yang Y-C, Langefeld CD, Broxmeyer HE: Mast cell growth factor (c-kit ligand) enhances cytokine stimulation of proliferation of the human factor-dependent cell line, MO7e. Exp Hematol 19:1031, 1991
65. Welham MJ, Duronio V, Sanghera JS, Pelech SL, Schrader JW: Multiple hemopoietic growth factors stimulate activation of mitogen-activated protein kinase family members. J Immunol 149:1683, 1992
66. McNiece IK, Langley KE, Zsebo KM: Recombinant human stem cell factor synergises with GM-CSF, G-CSF, IL-3 and epo to stimulate human progenitor cells of the myeloid and erythroid lineages. Exp Hematol 19:226, 1991
67. Heyworth CM, Whetton AD, Nicholls S, Zsebo K, Dexter TM: Stem cell factor directly stimulates the growth of enriched granulocyte-macrophage colony-forming cells and promotes the effects of other colony-stimulating factors. Blood 80:2230, 1992
68. Carroll MP, Clark LI, Rapp UR, May WS: Interleukin-3 and granulocyte-macrophage colony-stimulating factor mediate rapid phosphorylation and activation of cytosolic c-raf. J Biol Chem 265:19812, 1990
69. Duronio V, Welham MJ, Abraham S, Dryden P, Schrader JW: p21ras activation via hemopoietin receptors and c-kit requires tyrosine kinase activity but not tyrosine phosphorylation of p21ras GTPase-activating protein. Proc Natl Acad Sci USA 89:1587, 1992
70. Matsuguchi T, Salgia R, Hallek M, Eder M, Druker B, Ernst TJ, Griffin JD: She phosphorylation in myeloid cells is regulated by granulocyte macrophage colony-stimulating factor, interleukin-3, and steel factor and is constitutively increased by p21 OBCR/ABL. J Biol Chem 269:5016, 1994
71. Cutler RL, Lui L, Damen JE, Krystal G: Multiple cytokines induce the tyrosine phosphorylation of She and its association with Grb2 in hemopoietic cells. J Biol Chem 268:21463, 1993
72. Liu L, Damen JE, Cutler RL, Krystal G: Multiple cytokines stimulate the binding of a common 145-kilodalton protein to She at the Grb2 recognition site of She. Mol Cell Biol 14:6926, 1994
73. Conscience JF, Verrier B, Martin G: Interleukin-3-dependent expression of the c-myc and c-fos proto-oncogenes in hemopoietic cell lines. EMBO J 5:317, 1986
74. Askew DS, Ashmun RA, Simmons BC, Cleveland JL: Constitutive c-myc expression in an IL-3-dependent myeloid cell line suppresses cell cycle arrest and accelerates apoptosis. Oncogene 6:1915, 1991
75. Hume CR, Nocka KH, Sorrentino V, Lee JS, Fleissner E: Constitutive c-myc expression enhances the response of murine mast cells to IL-3, but does not eliminate their requirement for growth factors. Oncogene 2:223, 1988
76. Marcu KB, Bossone SA, Patel AJ: myc function and regulation. Annu Rev Biochem 61:809, 1992
77. Eilers M, Picard D, Yamamoto KR, Bishop MJ: Chimeras of myc oncoprotein and steroid receptors cause hormone-dependent transformation of cells. Nature 340:66, 1989
78. Hou J, Schindler U, Henzel WJ, Wong SC, McKnight SL: Identification and purification of human Stat proteins activated in response to interleukin-2. Immunity 2:321, 1995
79. Wakao H, Gouilleux F, Groner B: Mammary gland factor (MGF) is a novel member of the cytokine regulated transcription factor gene family and confers the prolactin response. EMBO J 14:854, 1995
80. Selten G, Cuypers HT, Berns A: Proviral activation of the putative oncogene Pim-1 in MuLV induced T-cell lymphomas. EMBO J 4:1793, 1985
81. Selten G, Cuypers HT, Boelens W, Robanus ME, Verbeek J, Domen J, Van BC, Berns A: The primary structure of the putative oncogene pim-1 shows extensive homology with protein kinases. Cell 46:603, 1986
82. Lilly M, Le T, Holland P, Hendrickson SL: Sustained expression of the pim-1 kinase is specifically induced in myeloid cells by cytokines whose receptors are structurally related. Oncogene 7:727, 1992
83. Miura O, Miura Y, Nakamura N, Quelle FW, Witthuhn BA, Ihle JN, Aoki N: Induction of tyrosine phosphorylation of Vav and expression of Pim-1 correlates with Jak 2-mediated growth signaling from the erythropoietin receptor. Blood 84:4135, 1994
84. Berns A: Tumorigenesis in transgenic mice: Identification and characterization of synergizing oncogenes J Cell Biochem 47:130, 1991
85. van Lohuizen M, Verbeek S, Scheijen B, Wientjens E, van der Gulden H, Berns A: Identification of cooperating oncogenes in E mu-myc transgenic mice by provirus tagging. Cell 65:737, 1991
86. Rottem M, Hull G, Metcalfe DD: Demonstration of differential effects of cytokines on mast cells derived from murine bone marrow and peripheral blood mononuclear cells. Exp Hematol 22:1147, 1994
87. Lantz CS, Huff TF: Differential responsiveness of purified mouse c-kit+ mast cells and their progenitors to IL-3 and stem cell factor. J Immunol 155:4024, 1995
88. Gurish MF, Ghildyal N, Arm J, Austen KF, Avraham S, Reynolds D, Stevens RL: Cytokine mRNA are preferentially increased relative to secretory granule protein mRNA in mouse bone marrow-derived mast cells that have undergone IgE-mediated activation and degranulation. J Immunol 146:1527, 1991
89. Fairbairn LJ, Cowling GJ, Reipert BM, Dexter TM: Suppression of apoptosis allows differentiation and development of a multipotent hemopoietic cell line in the absence of added growth factors. Cell 74:823, 1993
90. Stratford May W, Tyler G, Ito T, Armstrong DK, Qatsha KA, Davidson NA: Interleukin-3 and bryostatin mediate hyperphosphorylation of BCL2a in association with suppression of apoptosis. J Biol Chem 269:26865, 1994
91. Roussel MF, Cleveland JL, Shurtleff SA, Sherr CJ: Myc rescue of a mutant CSF-1 receptor impaired in mitogenic signalling Nature 353-361, 1991
92. Shibuya H, Yoneyama M, Ninomiya TJ, Matsumoto K, Taniguchi T: IL-2 and EGF receptors stimulate the hematopoietic cell cycle via different signaling pathways: Demonstration of a novel role for c-myc. Cell 70:57, 1992
93. Migone TS, Lin JX, Cereseto A, Mulloy JC, O'Shea JJ, Franchini G, Leonard WJ: Constitutively activated Jak-STAT pathway in T cells transformed with HTLV-I. Science 269:79, 1995
94. Mui AL-F, Wakao H, Kinoshita T, Kitamura T, Miyajima A: Suppression of interleukin-3 induced gene expression by a C-terminal truncated stat5: Role of stat5 in proliferation. EMBO J 1996 (in press)
95. Fujii H, Nakagawa Y, Schindler U, Kawahara A, Mori H, Gouilleux F, Groner B, Ihle JN, Minami Y, Miyazaki T, Taniguchi T: Activation of stat5 by interleukin-2 requires a carboxyl-terminal region of the interleukin-2 receptor-beta chain but is not essential for the proliferative signal transmission. Proc Natl Acad Sci USA 92:5482, 1995
96. Meeker TC, Nagarajan L, Rushdi A, Croce CM: Cloning and characterization of the human PIM-I gene: A putative oncogene related to the protein kinases. J Cell Biochem 35:105, 1987
97. Yip-Schneider MT, Horie M, Broxmeyer HE: Transcriptional induction of pim-1 protein-kinase gene-expression by interferon-gamma and posttranscriptional effects on costimulation with steel factor. Blood 85:3494, 1995
98. Moroy T, Grzeschiczek A, Petzold S, Hartmann KU: Expression of a Pim-1 transgene accelerates lymphoproliferation and inhibits apoptosis in 1pr/1pr mice. Proc Natl Acad Sci USA 90:10734, 1993
99. Domen J, van der Lugt NM, Laird PW, Saris CJ, Clarke AR, Hooper ML, Berns A: Impaired interleukin-3 response in Pim-1-deficient bone marrow-derived mast cells. Blood 82:1445, 1993