Role of interleukin-7 in T-cell development from hematopoietic stem cells

Immunological Reviews

Volumn 165, Issue , 1998, Pages 13-28

  Akashi, Koichi ^a,b   Kondo, Motonari ^a   Weissman, Irving L ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN HEAVY CHAIN; INTERLEUKIN 7; INTERLEUKIN 7 RECEPTOR; PROTEIN BCL 2;

B LYMPHOCYTE DIFFERENTIATION; GENE REARRANGEMENT; HEMATOPOIETIC STEM CELL; LYMPHOCYTE DIFFERENTIATION; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; RECEPTOR UPREGULATION; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; THYMOCYTE;

EID: 0031757825     PISSN: 01052896     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-065X.1998.tb01226.x     Document Type: Review

References (137)

1. Morrison SJ, Weissman IL. The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity 1994;1:661-673.
2. Osawa M, Hanada K, Hamada H, Nakauchi H. Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 1996;273:242-245.
3. Spangrude GJ, Heimfeld S, Weissman IL. Purification and characterization of mouse hematopoietic stem cells. Science 1988;241:58-62.
4. Spangrude GJ, Scollay R. Differentiation of hematopoietic cells in irradiated mouse thymic lobes. J Immunol 1990;145:3661-3668.
5. Visser JWM, Gauman JGJ, Mulder AH, Eliason JF, de Leeuw AW. Isolation of murine pluripotent hemopoietic stem cells. J Exp Med 1984;59:1576-1590.
6. Andrews RG, Singer JW, Bernstein ID. Monoclonal antibody 12-8 recognizes a 115-kd molecule present on both unipotent and multipotent hematopoietic colony-forming cells and their precursors. Blood 1986;67:842-845.
7. Baum CM, Weissman IL, Tsukamoto AS, Buckle AM, Peault B. Isolation of a candidate human hematopoietic stem-cell population. Proc Natl Acad Sci USA 1992;89:2804-2808.
8. DiGiusto D, et al. Human fetal bone marrow early progenitors for T, B, and myeloid cells are found exclusively in the population expressing high levels of CD34. Blood 1994;84:421-432.
9. Strauss LC, Rowley SD, La Russa VF, Sharkis SJ, Stuart RK, Civin CI. Antigenic analysis of hematopoiesis. V. Characterization of My-10 antigen expression by normal lymphohematopoietic progenitor cells. Exp Hematol 1986;14:878-886.
10. Siminovitch L, McCulloch E, Till J. The distribution of colony-forming cells among spleen colonies. J Cell Comp Physiol 1963;62:327-336.
11. Namen AE, et al. Stimulation of B-cell progenitors by cloned murine interleukin-7. Nature 1988;333:571-573.
12. Peschon JJ, et al. Early lymphocyte expansion is severely impaired in interleukin 7 receptor-deficient mice. J Exp Med 1994;180:1955-1960.
13. Von Freeden-Jeffry U, Vieira P, Lucian LA, McNeil T, Burdach SE, Murray R. Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine. J Exp Med 1995;181:1519-1526.
14. Sudo T, et al. Expression and function of the interleukin 7 receptor in murine lymphocytes. Proc Natl Acad Sci USA 1993;90:9125-9129.
15. Akashi K, Kondo M, von Freeden-Jeffry U, Murray R, Weissman IL. Bcl-2 rescues T lymphopoiesis in interleukin-7 receptor-deficient mice. Cell 1997;89:1033-1041.
16. Corcoran AE, Riddell A, Krooshoop D, Venkitaraman AR. Impaired immunoglobulin gene rearrangement in mice lacking the IL-7 receptor. Nature 1998;391:904-907.
17. Murray R, Suda T, Wrighton N, Lee F, Zlotnik A. IL-7 is a growth and maintenance factor for mature and immature thymocyte subsets. Int Immunol 1989;1:526-531.
18. Goodwin RG, et al. Cloning of the human and murine interleukin-7 receptors: demonstration of a soluble form and homology to a new receptor superfamily. Cell 1990;60:941-951.
19. Noguchi M, et al. Interleukin-2 receptor gamma chain: a functional component of the interleukin-7 receptor. Science 1993;262:1877-1880.
20. Kondo M, et al. Functional participation of the IL-2 receptor gamma chain in IL-7 receptor complexes. Science 1994;263:1453-1454.
21. Takeshita T, et al. Cloning of the gamma chain of the human IL-2 receptor. Science 1992;257:379-382.
22. Kondo M, et al. Sharing of the interleukin-2 (IL-2) receptor gamma chain between receptors for IL-2 and IL-4. Science 1993;262:1874-1877.
23. Russell SM, et al. Interleukin-2 receptor gamma chain: a functional component of the interleukin-4 receptor. Science 1993;262:1880-1883.
24. Kimura Y, et al. Sharing of the IL-2 receptor gamma chain with the functional IL-9 receptor complex. Int Immunol 1995;7:115-120.
25. Giri JG, et al. Utilization of the beta and gamma chains of the IL-2 receptor by the novel cytokine IL-15. EMBO J 1994;13:2822-2830.
26. DiSanto JP, Rieux-Laucat F, Dautry-Varsat A, Fischer A, de Saint Basile G. Defective human interleukin 2 receptor gamma chain in an atypical X chromosome-linked severe combined immunodeficiency with peripheral T cells. Proc Natl Acad Sci USA 1994;91:9466-9470.
27. Cao X, et al. Defective lymphoid development in mice lacking expression of the common cytokine receptor gamma chain. Immunity 1995;2:223-238.
28. Ohbo K, et al. Modulation of hematopoiesis in mice with a truncated mutant of the interleukin-2 receptor gamma chain. Blood 1996;87:956-967.
29. Ogasawara K, et al. Requirement for IRF-1 in the microenvironment supporting development of natural killer cells [published erratum appears in Nature 1998;392:843]. Nature 1998;391:700-703.
30. Suzuki H, Duncan GS, Takimoto H, Mak TW. Abnormal development of intestinal intraepithelial lymphocytes and peripheral natural killer cells in mice lacking the IL-2 receptor beta chain. J Exp Med 1997;185:499-505.
31. Noguchi M, et al. Interleukin-2 receptor gamma chain mutation results in X-linked severe combined immunodeficiency in humans. Cell 1993;73:147-157.
32. Puck JM. et al. The interleukin-2 receptor gamma chain maps to Xq13.1 and is mutated in X-linked severe combined immunodeficiency, SCIDX1. Hum Mol Genet 1993;2:1099-1104.
33. Russell SM, et al. Interaction of IL-2R beta and gamma c chains with Jak1 and Jak3: implications for XSCID and XCID. Science 1994;266:1042-1045.
34. Miyazaki T, et al. Functional activation of Jak1 and Jak3 by selective association with IL-2 receptor subunits. Science 1994;266:1045-1047.
35. Asao H, et al. Interleukin 2-induced activation of JAK3: possible involvement in signal transduction for c-myc induction and cell proliferation. FEBS Lett 1994;351:201-206.
36. Park SY, et al. Developmental defects of lymphoid cells in Jak3 kinase-deficient mice. Immunity 1995;3:771-782.
37. Thomis DC, Gurniak CB, Tivol E, Sharpe AH, Berg LJ. Defects in B lymphocyte maturation and T lymphocyte activation in mice lacking Jak3. Science 1995;270:794-797.
38. Nosaka T, et al. Defective lymphoid development in mice lacking Jak3 [published erratum appears in Science 1996;271:17]. Science 1995;270:800-802.
39. Macchi P, et al. Mutations of Jak-3 gene in patients with autosomal severe combined immune deficiency (SCID). Nature 1995;377:65-68.
40. Russell SM, et al. Mutation of Jak3 in a patient with SCID: essential role of Jak3 in lymphoid development. Science 1995;270:797-800.
41. Smith LG, Weissman IL, Heimfeld S. Clonal analysis of hematopoietic stem-cell differentiation in vivo. Proc Natl Acad Sci USA 1991;88:2788-2792.
42. Bertoncello I, Hodgson GS, Bradley TR. Multiparameter analysis of transplantable hemopoietic stem cells: I. The separation and enrichment of stem cells homing to marrow and spleen on the basis of rhodamine-123 fluorescence. Exp Hematol 1985;13:999-1006.
43. Ploemacher RE, Brons RHC. Separation of CFU-S from primitive cells responsible for reconstitution of the bone marrow hemopoietic stem cell compartment following irradiation: evidence for a pre-CFU-S cells. Exp Hematol 1989;17:263-266.
44. Mulder AH, Visser JWM. Separation and functional analysis of bone marrow cells separated by rhodamine-123 fluorescence. Exp Hematol 1987;15:99-104.
45. Spangrude GJ, Brooks DM, Tumas DB. Long-term repopulation of irradiated mice with limiting numbers of purified hematopoietic stem cells: in vivo expansion of stem cell phenotype but not function. Blood 1995;85:1006-1016.
46. Ikuta K, Weissman IL. Evidence that hematopoietic stem cells express mouse c-kit but do not depend on steel factor for their generation. Proc Natl Acad Sci USA 1992;89:1502-1506.
47. Ogawa M, et al. Expression and function of c-kit in hemopoietic progenitor cells. J Exp Med 1991;174:63-71.
48. McKinstry WJ, Li CL, Rasko JE, Nicola NA, Johnson GR, Metcalf D. Cytokine receptor expression on hematopoietic stem and progenitor cells. Blood 1997;89:65-71.
49. Heimfeld S, Hudak S, Weissman I, Rennick D. The in vitro response of phenotypically defined mouse stem cells and myeloerythroid progenitors to single or multiple growth factors. Proc Natl Acad Sci USA 1991;88:9902-9906.
50. Sonoda Y, et al. Actions of human interleukin-4/B-cell stimulatory factor-1 on proliferation and differentiation of enriched hematopoietic progenitor cells in culture. Blood 1990;75:1615-1621.
51. Broxmeyer HE, et al. Synergistic effects of purified recombinant humin and murine B cell growth factor-1/IL-4 on colony formation in vitro by hematopoietic progenitor cells. Multiple actions. J Immunol 1988;141:3852-3862.
52. Kondo M, Weissman IL, Akashi K. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 1997;91:661-672.
53. Hardy RR, Carmack CE, Shinton SA, Kemp JD, Hayakawa K. Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow. J Exp Med 1991;173:1213-1225.
54. - triple-negative adult mouse thymocytes defined by CD44 and CD25 expression. J Immunol 1993;150:4244-4252.
55. Godfrey DI, Zlotnik A, Suda T. Phenotypic and functional characterization of c-kit expression during intrathymic T cell development. J Immunol 1992;149:2281-2285.
56. Wu L, Scollay R, Egerton M, Pearse M, Spangrude GJ, Shortman K. CD4 expressed on earliest T-lineage precursor cells in the adult murine thymus. Nature 1991;349:71-74.
57. Matsuzaki Y, et al. Characterization of c-kit positive intrathymic stem cells that are restricted to lymphoid differentiation. J Exp Med 1993;178:1283-1292.
58. Ardavin C, Wu L, Li C-L, Shortman K. Thymic dendritic cells and T cells develop simultaneously in the thymus from a common precursor population. Nature 1993;362:761-763.
59. Giblett ER, Anderson JE, Cohen F, Pollara B, Meuwissen HJ. Adenosine-deaminase deficiency in two patients with severely impaired cellular immunity. Lancet 1972;2:1067-1069.
60. Ochs HD, Yount JE, Giblett ER, Chen SH, Scott CR, Wedgwood RJ. Adenosine-deaminase deficiency and severe combined immunodeficiency syndrome. Lancet 1973;1:1393-1394.
61. Hirschhorn R. Adenosine deaminase deficiency. Immunodefic Rev 1990;2:175-198.
62. Lepault F, Ezine S, Gagnerault MC. T- and B-lymphocyte differentiation potentials of spleen colony-forming cells. Blood 1993;81:950-955.
63. Hirayama F, Shih JP. Awgulewitsch A, Warr GW, Clark SC, Ogawa M. Clonal proliferation of murine lymphohemopoietic progenitors in culture. Proc Natl Acad Sci USA 1992;89:5907-5911.
64. Hirayama F, Ogawa M. Negative regulation of early T lymphopoiesis by interleukin-3 and interleukin-1 alpha. Blood 1995;86:4527-4531.
65. Georgopoulos K, et al. The Ikaros gene is required for the development of all lymphoid lineages. Cell 1994;79:143-156.
66. Wu L, Antica M, Johnson GR, Scollay R, Shortman K. Developmental potential of the earliest precursor cells from the adult mouse thymus. J Exp Med 1991;174:1617-1627.
67. Ogawa M. Differentiation and proliferation of hematopietic stem cells. Blood 1993;81:2844-2853.
68. Suda J, Suda T, Ogawa M. Analysis of differentiation of mouse hemopoietic stem cells in culture by sequential replating of paired progenitors. Blood 1984;64:393-399.
69. Galy A, Travis M, Cen D, Chen B. Human T, B, natural killer, and dendritic cells arise from a common bone marrow progenitor cell subset. Immunity 1995;3:459-473.
70. Hakoda M, et al. Cloning of phenotypically different human lymphocytes originating from a single stem cell. J Exp Med 1989;169:1265-1276.
71. Antica M, Wu L, Shortman K, Scollay R. Thymic stem cells in mouse bone marrow. Blood 1994;84:111-117.
72. Spangrude GJ, Klein J, Heimfeld S, Aihara Y, Weissman IL. Two monoclonal antibodies identify thymic-repopulating cells in mouse bone marrow. J Immunol 1989;142:425-430.
73. Spangrude GJ, Aihara Y, Weissman IL, Klein J. The stem cell antigens Sca-1 and Sca-2 subdivide thymic and peripheral T lymphocytes into unique subsets. J Immunol 1988;141:3697-3707.
74. Aihara Y, Buhring H-J, Aihara M, Klein J. An attempt to produce pre-T cell hybridomas and to identify their antigens. Eur Immunol 1986;16:1391-1399.
75. Peault B, Khazaal I, Weissman IL. In vitro development of B cells and macrophages from early mouse fetal thymocytes. Eur J Immunol 1994;24:781-784.
76. Mori S, et al. Presence of B cell progenitors in the thymus. J Immunol 1997;158:4193-4199.
77. Barr RD, Fialkow PJ. Clonal origin of chronic myelocytic leukemia. N Engl J Med 1973;289:307-309.
78. Akashi K, et al. Simultaneous occurrence of myelomonocytic leukemia and multiple myeloma: involvement of common leukemic progenitors and their developmental abnormality of "lineage infidelity". J Cell Physiol 1991;148:446-456.
79. Akashi K, et al. T lymphoid/myeloid bilineal crisis in chronic myelogenous leukemia. Exp Hematol 1993;21:743-748.
80. Mirro J, et al. Clinical and laboratory characteristics of acute leukemia with the 4;11 translocation. Blood 1986;67:689-697.
81. Akashi K, et al. Acute 'bilineal-biphenotypic' leukaemia. Br J Haematol 1990;74:402-407.
82. Akashi K, et al. B-lymphoid/myeloid stem cell origin in Ph-positive acute leukemia with myeloid markers. Leuk Res 1993;17:549-555.
83. Fialkow PJ, Janssen JVY Bartram CR. Clonal remissions in acute nonlymphocytic leukemia: evidence for a multistep pathogenesis of the malignancy. Blood 1991;77:1415-1417.
84. Fialkow PJ, et al. Clonal development, stem-cell differentiation, and clinical remissions in acute nonlymphocytic leukemia. N Engl J Med 1987;317:468-473.
85. Jacobson RJ, Temple MJ, Singer JW, Raskind W, Powell J, Fialkow PJ. A clonal complete remission in a patient with acute nonlymphocytic leukemia originating in a multipotent stem cell. N Engl J Med 1984;310:1513-1517.
86. Klinken SP, Alexander WS, Adams JM. Hemopoietic lineage switch: v-raf oncogene converts Emu-myc transgenic B cells into macrophages. Cell 1988;53:857-867.
87. Cumano A, Paige CJ, Iscove NN, Brady G. Bipotential precursors of B cells and macrophages in murine fetal liver. Nature 1992;356:612-615.
88. Kawamoto H, Ohmura K, Katsura Y. Direct evidence for the commitment of hematopoietic stem cells to T, B and myeloid lineages in murine fetal liver. Int Immunol 1997;9:1011-1019.
89. Namen AE, et al. B cell precursor growth-promoting activity. Purification and characterization of a growth factor active on lymphocyte precursors. J Exp Med 1988;167:988-1002.
90. Karasuyama H, Rolink A, Melchers F. A complex of glycoproteins is associated with VpreB/lambda 5 surrogate light chain on the surface of mu heavy chain-negative early precursor B cell lines. J Exp Med 1993;178:469-478.
91. Karasuyama H, Rolink A, Shinkai Y, Young F, Alt FW, Melchers F. The expression of Vpre-B/lambda 5 surrogate light chain in early bone marrow precursor B cells of normal and B cell-deficient mutant mice. Cell 1994;77:133-143.
92. Groettrup M, et al. A novel disulfide-linked heterodimer on pre-T cells consists of the T cell receptor beta chain and a 33 kd glycoprotein. Cell 1993;75:283-294.
93. Rodewald HR, Ogawa M, Haller C, Waskow C, DiSanto JP. Pro-thymocyte expansion by c-kit and the common cytokine receptor gamma chain is essential for repertoire formation. Immunity 1997;6:265-272.
94. Muegge K, Vila MP, Durum SK. Interleukin-7: a cofactor for V(D)J rearrangement of the T cell receptor beta gene. Science 1993;261:93-95.
95. Oosterwegel MA, Haks MC, Jeffry U, Murray R, Kruisbeek AM. Induction of TCR gene rearrangements in uncommitted stem cells by a subset of IL-7 producing, MHC class-II-expressing thymic stromal cells. Immunity 1997;6:351-360.
96. Strasser A, Harris AW, Cory S. bcl-2 transgene inhibits T cell death and perturbs thymic self-censorship. Cell 1991;67:889-899.
97. Yang XF, Weber GF, Cantor H. A novel Bd-x isoform connected to the T cell receptor regulates apoptosis in T cells. Immunity 1997;7:629-639.
98. Nakayama K-I, Nakayama K, Dustin LB, Loh DY. T-B cell interaction inhibits spontaneous apoptosis of mature lymphocytes in Bd-2-deficient mice. Exp Med 1995;182:1101-1110.
99. Maki K, Sunaga S, Ikuta K. The V-J recombination of T cell receptor-gamma genes is blocked in interleukin-7 receptor-deficient mice. J Exp Med 1996;184:2423-2427.
100. Candeias S, Peschon JJ, Muegge K, Durum SK. Defective T-cell receptor gamma gene rearrangement in interleukin-7 receptor knockout mice. Immunol Lett 1997;57:9-14.
101. Corcoran AE, Smart FM, Cowling RJ, Crompton T, Owen MJ, Venkitaraman AR. The interleukin-7 receptor alpha chain transmits distinct signals for proliferation and differentiation during B lymphopoiesis. EMBO J 1996;15:1924-1932.
102. Domen J, Gandy KL, Weissman IL. Systemic overexpression of BCL-2 in the hematopoietic system protects transgenic mice from the consequences of lethal irradiation. Blood 1998;91:2272-2282.
103. Kondo M, Akashi K, Domen J, Sugamura K, Weissman IL. Bcl-2 rescues T lymphopoiesis, but not B or NK cell development, in common gamma chain-deficient mice. Immunity 1997;7:155-162.
104. Saint-Ruf C, Ungewiss K, Groettrup M, Bruno L, Fehling HJ, von Boehmer H. Analysis and expression of a cloned pre-T cell receptor gene. Science 1994;266:1208-1212.
105. + precursors. Proc Natl Acad Sci USA 1989;86:7542-7546.
106. Petrie HT, Livak F, Schatz DG, Strasser A, Crispe IN, Shortman K. Multiple rearrangements in T cell receptor alpha chain genes maximize the production of useful thymocytes. J Exp Med 1993;178:615-622.
107. + T cell selection in mice lacking invariant chain expression. J Exp Med 1993;177:1699-1712.
108. Viville S, et al. Mice lacking the MHC class II-associated invariant chain. Cell 1993;72:635-648.
109. + T cells in major histocompatibility complex class II-deficient mice. Science 1991;253:1417-1420.
110. Gosgrove D, et al. Mice lacking MHC class II molecules. Cell 1991;66:1051-1066.
111. + T cells. Science 1990;248:1227-1230.
112. + cytolytic T cells. Nature 1990;344:742-746.
113. Guidos CJ, Danska JS, Fathman CG, Weissman IL. T cell receptor-mediated negative selection of autoreactive T lymphocyte precursors occurs after commitment to the CD4 or CD8 lineages. J Exp Med 1990;172:835-846.
114. + maturation pathway in mouse thymic T cell development: lineages and selection. Immunity 1996;5:147-161.
115. Surh CD, Sprent J. T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature 1994;372:100-103.
116. +3(2+) thymocytes as post-selection intermediates leading to mature T cells. J Exp Med 1991;173:323-332.
117. Huesmann M, Scott B, Kisielow P, von Boehmer H. Kinetics and efficacy of positive selection in the thymus of normal and T cell receptor transgenic mice. Cell 1991;66:533-540.
118. Cheng AM, et al. The Syk and ZAP-70 SH2-containing tyrosine kinases are implicated in pre-T cell receptor signaling. Proc Natl Acad Sci USA 1997;94:9797-9801.
119. Fehling HJ, Krotkova A, Saint-Ruf C, von Boehmer H. Crucial role of the pre-T-cell receptor alpha gene in development of alpha beta but not gamma delta T cells. Nature 1995;375:795-798.
120. Rodewald HR, Kretzschmar K, Swat W, Takeda S. Intrathymically expressed c-kit ligand (stem cell factor) is a major factor driving expansion of very immature thymocytes in vivo. Immunity 1995;3:313-319.
121. Lucas B, Vasseur F, Penit C. Production, selection, and maturation of thymocytes with high surface density of TCR. J Immunol 1994;153:53-62.
122. Akashi K, Kondo M, Weissman IL. Two distinct pathways of positive selection for thymocytes. Proc Natl Acad Sci USA 1998;95:2486-2491.
123. Veis DJ, Sorenson CM, Shutter JR, Korsmeyer SJ. Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell 1993;75:229-240.
124. Nakayama K, et al. Disappearance of the lymphoid system in Bcl-2 homozygous mutant chimeric mice. Science 1993;261:1584-1588.
125. + stage during positive selection and promotes thymocyte differentiation at several control points. Immunity 1994;1:197-205.
126. + thymocytes is altered by overexpression of the BCL-2 protooncogene in the thymus. J Exp Med 1994;179:145-153.
127. Weissman IL. Developmental switches in the immune system. Cell 1994;76:207-218.
128. Vaux DL, Cory S, Adams JM. Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 1988;335:440-442.
129. 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 1993;74:823-832.
130. Mazel S, Burtrum D, Petrie HT. Regulation of cell division cycle progression by bcl-2 expression: a potential mechanism for inhibition of programmed cell death. J Exp Med 1996;183:2219-2226.
131. Strasser A, Harris AW, Corcoran LM, Cory S. Bcl-2 expression promotes B- but not T-lymphoid development in scid mice. Nature 1994;368:457-460.
132. Von Freeden-Jeffry U, Solvason N, Howard M, Murray R. The earliest T lineage-committed cells depend on IL-7 for Bcl-2 expression and normal cell cycle progression. Immunity 1997;7:147-154.
133. -/- mice. Cell 1997;89:1011-1019.
134. + thymocyte differentiation. Immunity 1996;5:461-177.
135. Robey E, et al. An activated form of Notch influences the choice between CD4 and CD8 T cell lineages. Cell 1996;87:483-192.
136. Boothby MR, Mora AL, Scherer DC, Brockman JA, Ballard DW. Perturbation of the T lymphocyte lineage in transgenic mice expressing a constitutive repressor of nuclear factor (NF)-κB. J Exp Med 1997;185:1897-1907.
137. Sharp LL, Schwarz DA, Bott CM, Marshall CJ, Hedrick SM. The influence of the MAPK pathway on T cell lineage commitment. Immunity 1997;7:609-618.