Nature or nurture? Steady-state lymphocyte formation in adults does not recapitulate ontogeny

Immunological Reviews

Volumn 187, Issue , 2002, Pages 116-125

  Kincade, Paul W ^a   Owen, John J T ^a   Igarashi, Hideya ^a   Kouro, Taku ^a   Yokota, Takafumi ^a   Rossi, Maria Isabel D ^a  

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GLUCOCORTICOID; GREEN FLUORESCENT PROTEIN; INTERLEUKIN 7; INTERLEUKIN 7 RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; RAG1 PROTEIN; STEROID HORMONE;

B LYMPHOCYTE; BONE MARROW; BONE MARROW CELL; CELL FUNCTION; CELL LINEAGE; GENE EXPRESSION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; LYMPHOCYTE DIFFERENTIATION; LYMPHOPOIESIS; NONHUMAN; ONTOGENY; PHENOTYPE; PRIORITY JOURNAL; REVIEW; STEADY STATE; THYMUS;

ANIMALS; CELL LINEAGE; FETUS; HUMANS; LYMPHOCYTES; LYMPHOPOIESIS; STEM CELLS; STEROIDS; THYMUS GLAND;

EID: 0036749790     PISSN: 01052896     EISSN: None     Source Type: Journal    
DOI: 10.1034/j.1600-065X.2002.18710.x     Document Type: Review

References (81)

1. Maximow AA. Relation of blood cells to connective tissues and endothelium. Physiol Rev 1924;4;533-563.
2. Jaffredo T, Gautier R, Brajeul V, Dieterlen-Lievre F. Tracing the progeny of the aortic hemangioblast in the avian embryo. Dev Biol 2000;224:204-214.
3. Muller AM, Medvinsky A, Strouboulis J, Grosveld F, Dzierzak E. Development of hematopoietic stem cell activity in the mouse embryo. Immunity 1994;1:291-301.
4. Potocnik AJ, Brakebusch C, Fassler R. Fetal and adult hematopoietic stem cells require betal integrin function for colonizing fetal liver, spleen, and bone marrow. Immunity 2000;12:653-663.
5. Foss DL, Donskoy E, Goldschneider I. The importation of hematogenous precursors by the thymus is a gated phenomenon in normal adult mice. J Exp Med 2001;193:365-374.
6. Kawamoto H, Ikawa T, Ohmura K, Fujimoto S, Katsura Y. T cell progenitors emerge earlier than B cell progenitors in the murine fetal liver. Immunity 2000;12:441-450.
7. Katsura Y, Kawamoto H. Stepwise lineage restriction of progenitors in lympho-myelopoiesis. Int Rev Immunol 2001;20:1-20.
8. Kawamoto H, Ohmura K, Katsura Y. Presence of progenitors restricted to T, B, or myeloid lineage, but absence of multipotent stem cells, in the murine fetal thymus. J Immunol 1998;161:3799-3802.
9. Douagi I, Colucci F, Di Santo JP, Cumano A. Identification of the earliest prethymic bi-potent T/NK progenitor in murine fetal liver. Blood 2002;99:463-471.
10. Kondo M, Weissman IL, Akashi K. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 1997;91:661-672.
11. - cells, as well as macrophages. J Immunol 2001;166:6593-6601.
12. Radtke F, et al. Deficient T cell fate specification in mice with an induced inactivation of Notch1. Immunity 1999;10:547-558.
13. Wilson A, Ferrero I, MacDonald HR, Radtke F. Cutting edge: an essential role for Notch1 in the devdopment of both thymus-independent and -dependent T cells in the gut. J Immunol 2000;165:5397-5400.
14. Wilson A, MacDonald HR, Radtke F. Notch 1-deficient common lymphoid precursors adopt a B cell fate in the thymus. J Exp Med 2001;194:1003-1012.
15. Pui JC, et al. Notch1 expression in early lymphopoiesis influences B versus T lineage determination. Immunity 1999;11:299-308.
16. Crompton T, Outram SV, Buckland J, Owen MJ. Distinct roles of the interleukin-7 receptor alpha chain in fetal and adult thymocyte development revealed by analysis of interleukin-7 receptor alpha-deficient mice. Eur J Immunol 1998;28:1859-1866.
17. Arroyo AG, Yang JT, Rayburn H, Hynes RO. Differential requirements for alpha4 integrins during fetal and adult hematopoiesis. Cell 1996;85:997-1008.
18. Arroyo AG, et al. In vivo roles of integrins during leukocyte development and traffic: insights from the analysis of mice chimeric for alpha 5, alpha v, and alpha 4 integrins. J Immunol 2000;165:4667-4675.
19. Itoi M, Kawamoto H, Katsura Y, Amagai T. Two distract steps of immigration of hematopoietic progenitors into the early thymus anlage. Int Immunol 2001;13:1203-1211.
20. Wang JH, et al. Selective defects in the development of the fetal and adult lymphoid system in mice with an Ikaros null mutation. Immunity 1996;5:537-549.
21. Sano S, et al. Stat3 in thymic epithelial cells is essential for postnatal maintenance of thymic architecture and thymocyte survival. Immunity 2001;15:261-273.
22. Weissman IL, Heimfeld S, Spangrude G. Haemopoietic stem cell purification. Immunol Today 1989;10:184.
23. Morrison SJ, Weissman IL. The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity 1994;1:661-673.
24. Sugamura K, et al. The common gamma-chain for multiple cytokine receptors. Adv Immunol 1995;59:225-277.
25. Kouro T, Medina KL, Oritani K, Kincade PW. Characteristics of early murine B lymphocyte precursors and their direct sensitivity to negative regulators. Blood 2001;97:2708-2715.
26. Payne KJ, Medina KL, Kincade PW. Loss of c-kit accompanies B lineage commitment and acquisition of CD4SR in most murine B lymphocyte precursors. Blood 1999;94:713-723.
27. Spangrude GJ, Heimfeld S, Weissman IL. Purification and characterization of mouse hematopoietic stem cells. Science 1988;241:58-62.
28. Spangrude GJ, Scollay R. A simplified method for enrichment of mouse hematopoietic stem cells. Exp Hematol 1990;18:920-926.
29. Wiesmann A, et al. Expression of CD27 on murine hematopoietic stem and progenitor cells. Immunity 2000;12:193-199.
30. Adolfsson J, et al. Upregulation of Flt3 expression within the bone marrow Lin(-)Sca1(+)c-kit(+) stem cell compartment is accompanied by loss of self-renewal capacity. Immunity 2001;15:659-669.
31. Christensen JL, Weissman IL. Flk-2 is a marker in hematopoietic stem cell differentiation: a simple method to isolate long-term stem cells. Proc Natl Acad Sci USA 2001;98:14541-14546.
32. Medina KL, Garrett KP, Thompson LF, Rossi MID, Payne KJ, Kincade PW. Identification of very early lymphoid precursors in bone marrow and their regulation by estrogen. Nat Immunol 2001;2:718-724.
33. Igarasin H, Gregory SC, Yokota T, Sakaguchi N, Kincade PW. Transcription from the RAG1 locus marks the earliest lymphocyte progenitors in bone marrow. Immunity 2002;17:117-130.
34. Kouro T, Kumar V, Kincade PW. Relationship between early B and NK lineage lymphocyte precursors in bone marrow. Blood 2002;100: in press.
35. Osmond DG. B cell development in the bone marrow. Semin Immunol 1990;2:173-180.
36. Kincade PW, Lee G, Watanabe T, Sun L, Scheid MP. Antigens displayed on murine B lymphocyte precursors. J Immunol 1981;127:2262-2268.
37. Scheid MP, Landreth KS, Tung JS, Kincade PW. Preferential but nonexdusive expression of macromolecular antigens on B-lineage cells. Immunol Rev 1982;69:141-159.
38. Tudor K-SRS, Payne KJ, Yamashita Y, Kincade PW. Functional assessment of precursors from murine bone marrow suggests a sequence of early B-lineage differentiation events. Immunity 2000;12:335-345.
39. Lu LS et al. Identification of a germ-line pro-B cell subset that distinguishes the fetal/neonatal from the adult B cell development pathway. Proc Natl Acad Sci USA 2002;99:3007-3012.
40. + pro-B cells can give rise to dendritic cells in vitro. J Immunol 1998;161:5795-5799.
41. Izon D, et al. A common pathway for dendritic cell and early B cell development. J Immunol 2001;167:1387-1392.
42. Manz MG, et al. Dendritic cell development from common myeloid progenitors. Ann New York Acad Sci 2001;938:167-173.
43. Montecino-Rodriguez E, Leathers H, Dorshkind K. Bipotential B-macrophage progenitors are present in adult bone marrow. Nat Immunol 2001;2:83-88.
44. Kincade PW, et al. Lymphoid lineage cells in adult murine bone marrow diverge from those of other blood cells at an early, hormone-sensitive stage. Semin Immunol 2002;14:19-28.
45. Medina KL, Smithson GM, Kincade PW. Suppression of B lymphopoiesis during normal pregnancy. J Exp Med 1993;178:1507-1515.
46. Smithson G, Beamer WG, Shultz KL, Christianson SW, Shultz LD, Kincade PW. Increased B lymphopoiesis in genetically sex steroid-deficient hypogonadal (hpg) mice. J Exp Med 1994;180:717-720.
47. Smithson G, Couse JF, Lubahn DB, Korach KS, Kincade PW. The role of estrogen receptors and androgen receptors in sex steroid regulation of B lymphopoiesis. J Immunol 1998;161:27-34.
48. Smithson G, Medina K, Ponting I, Kincade PW. Estrogen suppresses stromal cell-dependent lymphopoiesis in culture. J Immunol 1995;155:3409-3417.
49. Medima KL, Kincade PW. Pregnancy-related steroids are potential negative regulators of B lymphopoiesis. Proc Natl Acad Sci USA 1994;91:5382-5386.
50. Medina KL, Strasser A, Kincade PW. Estrogen influences the differentiation, proliferation and survival of early B lineage precursors. Blood 2000;95:2059-2067.
51. Grimaldi CM, Michael DJ, Diamond B. Cutting edge: expansion and activation of a population of autoreactive marginal zone B cells in a model of estrogen-induced lupus. J Immunol 2001;167:1886-1890.
52. Igaraski H, Kouro T, Yokota T, Comp PC, Kincade PW. Age and stage dependency of estrogen receptor expression by lymphocyte precursors. Proc Natl Acad Sci USA 2001;98:15131-15136.
53. Landreth KS, Kincade PW, Lee G, Medlock ES. Phenotypic and functional characterization of murine B lymphocyte precursors isolated from fetal and adult tissues. J Immunol 1983;131:572-580.
54. Kincade PW, Landreth KS, Lee G. Apparent differences in B-lineage differentiation occurring in fetal and adult life. Ann NY Acad Sci 1982;399:296-303.
55. Kincade PW, Flaherty L, Lee G, Watanabe T, Michaelson J. Qa antigen expression on functional lymphoid, myeloid, and stem cells in adult mice. J Immunol 1980;124:2879-2885.
56. Hayakawa K, Tarlinton D, Hardy RR. Absence of MHC class II expression distinguishes fetal from adult B lymphopoiesis in mice. J Immunol 1994;152:4801-4807.
57. Lam K-P, Stall AM. Major histocompatibility complex class II expression distinguishes two distinct B cell developmental pathways during ontogeny. J Exp Med 1994;180:507-516.
58. Oltz EM, et al. A novel regulatory myosin light chain gene distinguishes pre-B cell subsets and is IL-7 inducible. EMBO J 1992;11:2759-2767.
59. Ogawa M. Changing phenotypes of hematopoietic stem cells. Exp Hematol 2002;30:3-6.
60. Jyonouchi H, Kincade PW. Precocious and enhanced functional maturation of B lineage cells in New Zealand Black mice during embryonic development. J Exp Med 1984;159:1277-1282.
61. Jyonouchi H, Kincade PW, Landreth KS, Lee G, Good RA, Gershwin ME. Age-dependent deficiency of B lymphocyte lineage precursors in NZB mice. J Exp Med 1982;155:1665-1678.
62. Merchant MS, Garvy BA, Riley RL. Autoantibodies inhibit interleukin-7-mediated proliferation and are associated with the age-dependent loss of pre-B cells in autoimmune New Zealand black mice. Blood 1996;87:3289-3296.
63. Carvalho TL, Mota-Santos T, Cumano A, Demengeot J, Vieira P. Arrested B lymphopoiesis and persistence of activated B cells in adult interleukin 7 (-/-) mice. J Exp Med 2001;194:1141-1150.
64. Hao Z, Rajewsky K. Homeostasis of peripheral B cells in the absence of B cell influx from the bone marrow. J Exp Med 2001;194:1151-1164.
65. Nutt SL, Thévenin C, Busslinger M. Essential functions of Pax-5 (BSAP) in pro-B cell development. Immunobiology 1997;198:227-235.
66. Ikuta K, et al. A developmental switch in thymic lymphocyte maturation potential occurs at the level of hematopoietic stem cells. Cell 1990;62:863-874.
67. Gilfillan S, Dierich A, LeMeur M, Benoist C, Mathis D. Mice lacking TdT: mature animals with an immature lymphocyte repertoire. Science 1993;261:1175-1178.
68. Martinez-Barnetche J, Madrid-Marina V, Flavell RA, Moreno J. Does CD40 ligation induce B cell negative selection? J Immunol 2002;168:1042-1049.
69. Born W, White J, Kappler J, Marrack P. Re-arrangement of IgH genes in normal thymocyte development. J Immunol 1988;140:3228-3232.
70. Takei F, et al. Ly49 and CD94/NKG2: developmentally regulated expression and evolution. Immunol Rev 2001;181:90-103.
71. Rossi MID et al. Relatively normal human lymphopoiesis but rapid turnover of newly formed B cell cells in transplanted nonobese diabetic/SCID mice. J Immunol 2001;167:3033-3042.
72. Nishihara M, et al. A combination of stem cell factor and granulocyte colony-stimulating factor enhances the growth of human progenitor B cells supported by murine stromal cell line MS-5. Eur J Immunol 1998;28:855-864.
73. Hao QL, Zhu J, Price MA, Payne KJ, Barsky LW, Crooks GM. Identification of a novel, human multilymphoid progenitor in cord blood. Blood 2001;97:3683-3690.
74. Rossi MID, et al. B lymphopoiesis is active throughout human life, but there are developmental age related changes. Blood 2002; in press.
75. Arakawa-Hoyt J, et al. The number and generative capacity of human B lymphocyte progenitors, measured in vitro and in vivo, is higher in umbilical cord blood than in adult or pediatric bone marrow. Bone Marrow Transplant 1999;24:1167-1176.
76. Nuñez C, et al. B cells are generated throughout life in humans. J Immunol 1996;156:866-872.
77. Pribyl JAR, Lebien TW. Interleukin 7 independent development of human B cells. Proc Natl Acad Sci USA 1996;93:10348-10353.
78. Chowdhury D, Sen R. Stepwise activation of the immunoglobulin mu heavy chain gene locus. EMBO J 2001;20:6394-6403.
79. Dzierzak E, Medvinsky A. Developmental origins of hematopoietic stem cells. In: Monroe JG, Rothenberg EV, eds. Molecular biology of B-cell and T-cell development. Totowa, NJ: Humana Press, 1998:3-25.
80. Jyonouchi H, Kincade PW, Good RA, Fernandes G. Reciprocal transfer of abnormalities in clonable B lymphocytes and myeloid progenitors between NZB and DBA/mice. J Immunol 1981;127:1232-1235.
81. Hardy RR, Hayakawa K. B cell development pathways. Annu Rev Immunol 2001;19:595-621.