Top

Published in:

01-12-2008 | Review

The long road to the thymus: the generation, mobilization, and circulation of T-cell progenitors in mouse and man

Authors: Daniel A. Zlotoff, Benjamin A. Schwarz, Avinash Bhandoola

Published in: Seminars in Immunopathology | Issue 4/2008

Abstract

The majority of T cells develop in the thymus. T-cell progenitors in the thymus do not self-renew and so progenitor cells must be continuously imported from the blood into the thymus to maintain T-cell production. Recent work has shed light on both the identity of the cells that home to the thymus and the molecular mechanisms involved. This review will discuss the cells in the bone marrow and blood that are involved in early thymopoiesis in mouse and man. Understanding the pre-thymic steps in T-cell development may translate into new therapeutics, especially in the field of hematopoietic stem cell transplantation.

Morrison SJ, Uchida N, Weissman IL (1995) The biology of hematopoietic stem cells. Annu Rev Cell Dev Biol 11:35–71 doi:10.1146/annurev.cb.11.110195.000343 PubMed

Miller JF, Osoba D (1967) Current concepts of the immunological function of the thymus. Physiol Rev 47:437–520PubMed

Ladi E, Yin X, Chtanova T, Robey EA (2006) Thymic microenvironments for T cell differentiation and selection. Nat Immunol 7:338–343 doi:10.1038/ni1323 PubMed

Barthlott T, Keller MP, Krenger W, Hollander GA (2007) A short primer on early molecular and cellular events in thymus organogenesis and replacement. Swiss Med Wkly 137(Suppl 155):9S–13SPubMed

Jenkins M, Hanley MB, Moreno MB, Wieder E, McCune JM (1998) Human immunodeficiency virus-1 infection interrupts thymopoiesis and multilineage hematopoiesis in vivo. Blood 91:2672–2678PubMed

Teixeira L, Valdez H, McCune JM, Koup RA, Badley AD, Hellerstein MK, Napolitano LA, Douek DC, Mbisa G, Deeks S, Harris JM, Barbour JD, Gross BH, Francis IR, Halvorsen R, Asaad R, Lederman MM (2001) Poor CD4 T cell restoration after suppression of HIV-1 replication may reflect lower thymic function. AIDS 15:1749–1756 doi:10.1097/00002030-200109280-00002 PubMed

Maillard I, Schwarz BA, Sambandam A, Fang T, Shestova O, Xu L, Bhandoola A, Pear WS (2006) Notch-dependent T-lineage commitment occurs at extrathymic sites following bone marrow transplantation. Blood 107:3511–3519 doi:10.1182/blood-2005-08-3454 PubMed

Goronzy JJ, Weyand CM (2005) T cell development and receptor diversity during aging. Curr Opin Immunol 17:468–475PubMed

Mackall CL, Fleisher TA, Brown MR, Andrich MP, Chen CC, Feuerstein IM, Horowitz ME, Magrath IT, Shad AT, Steinberg SM et al (1995) Age, thymopoiesis, and CD4+ T-lymphocyte regeneration after intensive chemotherapy. N Engl J Med 332:143–149 doi:10.1056/NEJM199501193320303 PubMed

10.

Mackall CL, Fleisher TA, Brown MR, Magrath IT, Shad AT, Horowitz ME, Wexler LH, Adde MA, McClure LL, Gress RE (1994) Lymphocyte depletion during treatment with intensive chemotherapy for cancer. Blood 84:2221–2228PubMed

11.

Suda T, Arai F, Hirao A (2005) Hematopoietic stem cells and their niche. Trends Immunol 26:426–433 doi:10.1016/j.it.2005.06.006 PubMed

12.

Donskoy E, Goldschneider I (1992) Thymocytopoiesis is maintained by blood-borne precursors throughout postnatal life. A study in parabiotic mice. J Immunol 148:1604–1612PubMed

13.

Scollay R, Smith J, Stauffer V (1986) Dynamics of early T cells: prothymocyte migration and proliferation in the adult mouse thymus. Immunol Rev 91:129–157 doi:10.1111/j.1600-065X.1986.tb01487.x PubMed

14.

Goldschneider I, Komschlies KL, Greiner DL (1986) Studies of thymocytopoiesis in rats and mice. I. Kinetics of appearance of thymocytes using a direct intrathymic adoptive transfer assay for thymocyte precursors. J Exp Med 163:1–17 doi:10.1084/jem.163.1.1 PubMed

15.

Wallis VJ, Leuchars E, Chwalinski S, Davies AJ (1975) On the sparse seeding of bone marrow and thymus in radiation chimaeras. Transplantation 19:2–11 doi:10.1097/00007890-197501000-00002 PubMed

16.

Kadish JL, Basch RS (1976) Hematopoietic thymocyte precursors. I. Assay and kinetics of the appearance of progeny. J Exp Med 143:1082–1099 doi:10.1084/jem.143.5.1082 PubMed

17.

Spangrude GJ, Scollay R (1990) Differentiation of hematopoietic stem cells in irradiated mouse thymic lobes. Kinetics and phenotype of progeny. J Immunol 145:3661–3668PubMed

18.

Ceredig R, Bosco N, Rolink AG (2007) The B lineage potential of thymus settling progenitors is critically dependent on mouse age. Eur J Immunol 37:830–837 doi:10.1002/eji.200636728 PubMed

19.

Sambandam A, Maillard I, Zediak VP, Xu L, Gerstein RM, Aster JC, Pear WS, Bhandoola A (2005) Notch signaling controls the generation and differentiation of early T lineage progenitors. Nat Immunol 6:663–670 doi:10.1038/ni1216 PubMed

20.

Bell JJ, Bhandoola A (2008) The earliest thymic progenitors for T cells possess myeloid lineage potential. Nature 452:764–767 doi:10.1038/nature06840 PubMed

21.

Wada H, Masuda K, Satoh R, Kakugawa K, Ikawa T, Katsura Y, Kawamoto H (2008) Adult T-cell progenitors retain myeloid potential. Nature 452:768–772 doi:10.1038/nature06839 PubMed

22.

Benz C, Bleul CC (2005) A multipotent precursor in the thymus maps to the branching point of the T versus B lineage decision. J Exp Med 202:21–31 doi:10.1084/jem.20050146 PubMed

23.

Schwarz BA, Sambandam A, Maillard I, Harman BC, Love PE, Bhandoola A (2007) Selective thymus settling regulated by cytokine and chemokine receptors. J Immunol 178:2008–2017PubMed

24.

Lai AY, Kondo M (2007) Identification of a bone marrow precursor of the earliest thymocytes in adult mouse. Proc Natl Acad Sci U S A 104:6311–6316 doi:10.1073/pnas.0609608104 PubMed

25.

Scimone ML, Aifantis I, Apostolou I, von Boehmer H, von Andrian UH (2006) A multistep adhesion cascade for lymphoid progenitor cell homing to the thymus. Proc Natl Acad Sci U S A 103:7006–7011 doi:10.1073/pnas.0602024103 PubMed

26.

Uehara S, Grinberg A, Farber JM, Love PE (2002) A role for CCR9 in T lymphocyte development and migration. J Immunol 168:2811–2819PubMed

27.

Wurbel MA, Malissen B, Campbell JJ (2006) Complex regulation of CCR9 at multiple discrete stages of T cell development. Eur J Immunol 36:73–81 doi:10.1002/eji.200535203 PubMed

28.

Maillard I, Fang T, Pear WS (2005) Regulation of lymphoid development, differentiation, and function by the Notch pathway. Annu Rev Immunol 23:945–974 doi:10.1146/annurev.immunol.23.021704.115747 PubMed

29.

Schmitt TM, Zuniga-Pflucker JC (2002) Induction of T cell development from hematopoietic progenitor cells by delta-like-1 in vitro. Immunity 17:749–756 doi:10.1016/S1074-7613(02)00474-0 PubMed

30.

Spangrude GJ, Heimfeld S, Weissman IL (1988) Purification and characterization of mouse hematopoietic stem cells. Science 241:58–62 doi:10.1126/science.2898810 PubMed

31.

Huang X, Cho S, Spangrude GJ (2007) Hematopoietic stem cells: generation and self-renewal. Cell Death Differ 14:1851–1859 doi:10.1038/sj.cdd.4402225 PubMed

32.

Wagers AJ, Sherwood RI, Christensen JL, Weissman IL (2002) Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 297:2256–2259 doi:10.1126/science.1074807 PubMed

33.

Osawa M, Hanada K, Hamada H, Nakauchi H (1996) Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 273:242–245 doi:10.1126/science.273.5272.242 PubMed

34.

Ikuta K, Weissman IL (1992) Evidence that hematopoietic stem cells express mouse c-kit but do not depend on steel factor for their generation. Proc Natl Acad Sci U S A 89:1502–1506 doi:10.1073/pnas.89.4.1502 PubMed

35.

Li CL, Johnson GR (1995) Murine hematopoietic stem and progenitor cells: I. Enrichment and biologic characterization. Blood 85:1472–1479PubMed

36.

Adolfsson J, Borge OJ, Bryder D, Theilgaard-Monch K, Astrand-Grundstrom I, Sitnicka E, Sasaki Y, Jacobsen SE (2001) Upregulation of Flt3 expression within the bone marrow Lin(-)Sca1(+)c- kit(+) stem cell compartment is accompanied by loss of self-renewal capacity. Immunity 15:659–669 doi:10.1016/S1074-7613(01)00220-5 PubMed

37.

Christensen JL, Weissman IL (2001) Flk-2 is a marker in hematopoietic stem cell differentiation: a simple method to isolate long-term stem cells. Proc Natl Acad Sci U S A 98:14541–14546 doi:10.1073/pnas.261562798 PubMed

38.

Kiel MJ, Morrison SJ (2008) Uncertainty in the niches that maintain haematopoietic stem cells. Nat Rev Immunol 8:290–301 doi:10.1038/nri2279 PubMed

39.

Baum CM, Weissman IL, Tsukamoto AS, Buckle AM, Peault B (1992) Isolation of a candidate human hematopoietic stem-cell population. Proc Natl Acad Sci U S A 89:2804–2808 doi:10.1073/pnas.89.7.2804 PubMed

40.

Majeti R, Park CY, Weissman IL (2007) Identification of a hierarchy of multipotent hematopoietic progenitors in human cord blood. Cell Stem Cell 1:635–645 doi:10.1016/j.stem.2007.10.001 PubMed

41.

Kondo M, Wagers AJ, Manz MG, Prohaska SS, Scherer DC, Beilhack GF, Shizuru JA, Weissman IL (2003) Biology of hematopoietic stem cells and progenitors: implications for clinical application. Annu Rev Immunol 21:759–806 doi:10.1146/annurev.immunol.21.120601.141007 PubMed

42.

Herve P (2003) Donor-derived hematopoietic stem cells in organ transplantation: technical aspects and hurdles yet to be cleared. Transplantation 75:55S–57S doi:10.1097/01.TP.0000067954.60639.9C PubMed

43.

McKenzie JL, Takenaka K, Gan OI, Doedens M, Dick JE (2007) Low rhodamine 123 retention identifies long-term human hematopoietic stem cells within the Lin-CD34+CD38- population. Blood 109:543–545 doi:10.1182/blood-2006-06-030270 PubMed

44.

Sitnicka E, Buza-Vidas N, Larsson S, Nygren JM, Liuba K, Jacobsen SE (2003) Human CD34+ hematopoietic stem cells capable of multilineage engrafting NOD/SCID mice express flt3: distinct flt3 and c-kit expression and response patterns on mouse and candidate human hematopoietic stem cells. Blood 102:881–886 doi:10.1182/blood-2002-06-1694 PubMed

45.

Schofield R (1978) The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 4:7–25PubMed

46.

Lord BI, Testa NG, Hendry JH (1975) The relative spatial distributions of CFUs and CFUc in the normal mouse femur. Blood 46:65–72PubMed

47.

Nilsson SK, Johnston HM, Coverdale JA (2001) Spatial localization of transplanted hemopoietic stem cells: inferences for the localization of stem cell niches. Blood 97:2293–2299 doi:10.1182/blood.V97.8.2293 PubMed

48.

Zhang J, Niu C, Ye L, Huang H, He X, Tong WG, Ross J, Haug J, Johnson T, Feng JQ, Harris S, Wiedemann LM, Mishina Y, Li L (2003) Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425:836–841 doi:10.1038/nature02041 PubMed

49.

Calvi LM, Adams GB, Weibrecht KW, Weber JM, Olson DP, Knight MC, Martin RP, Schipani E, Divieti P, Bringhurst FR, Milner LA, Kronenberg HM, Scadden DT (2003) Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425:841–846 doi:10.1038/nature02040 PubMed

50.

Kiel MJ, He S, Ashkenazi R, Gentry SN, Teta M, Kushner JA, Jackson TL, Morrison SJ (2007) Haematopoietic stem cells do not asymmetrically segregate chromosomes or retain BrdU. Nature 449:238–242 doi:10.1038/nature06115 PubMed

51.

Kiel MJ, Radice GL, Morrison SJ (2007) Lack of evidence that hematopoietic stem cells depend on N-cadherin-mediated adhesion to osteoblasts for their maintenance. Cell Stem Cell 1:204–217 doi:10.1016/j.stem.2007.06.001 PubMed

52.

Arai F, Hirao A, Ohmura M, Sato H, Matsuoka S, Takubo K, Ito K, Koh GY, Suda T (2004) Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 118:149–161 doi:10.1016/j.cell.2004.07.004 PubMed

53.

Yoshihara H, Arai F, Hosokawa K, Hagiwara T, Takubo K, Nakamura Y, Gomei Y, Iwasaki H, Matsuoka S, Miyamoto K, Miyazaki H, Takahashi T, Suda T (2007) Thrombopoietin/MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell 1:685–697 doi:10.1016/j.stem.2007.10.020 PubMed

54.

Kimura S, Roberts AW, Metcalf D, Alexander WS (1998) Hematopoietic stem cell deficiencies in mice lacking c-Mpl, the receptor for thrombopoietin. Proc Natl Acad Sci U S A 95:1195–1200 doi:10.1073/pnas.95.3.1195 PubMed

55.

Xue Y, Gao X, Lindsell CE, Norton CR, Chang B, Hicks C, Gendron-Maguire M, Rand EB, Weinmaster G, Gridley T (1999) Embryonic lethality and vascular defects in mice lacking the Notch ligand Jagged1. Hum Mol Genet 8:723–730 doi:10.1093/hmg/8.5.723 PubMed

56.

Stier S, Cheng T, Dombkowski D, Carlesso N, Scadden DT (2002) Notch1 activation increases hematopoietic stem cell self-renewal in vivo and favors lymphoid over myeloid lineage outcome. Blood 99:2369–2378 doi:10.1182/blood.V99.7.2369 PubMed

57.

Mancini SJ, Mantei N, Dumortier A, Suter U, MacDonald HR, Radtke F (2005) Jagged1-dependent Notch signaling is dispensable for hematopoietic stem cell self-renewal and differentiation. Blood 105:2340–2342 doi:10.1182/blood-2004-08-3207 PubMed

58.

Maillard I, Koch U, Dumortier A, Shestova O, Xu L, Sai H, Pross SE, Aster JC, Bhandoola A, Radtke F, Pear WS (2008) Canonical notch signaling is dispensable for the maintenance of adult hematopoietic stem cells. Cell Stem Cell 2:356–366 doi:10.1016/j.stem.2008.02.011 PubMed

59.

Blank U, Karlsson G, Karlsson S (2008) Signaling pathways governing stem-cell fate. Blood 111:492–503 doi:10.1182/blood-2007-07-075168 PubMed

60.

Rebel VI, Miller CL, Eaves CJ, Lansdorp PM (1996) The repopulation potential of fetal liver hematopoietic stem cells in mice exceeds that of their liver adult bone marrow counterparts. Blood 87:3500–3507PubMed

61.

Adolfsson J, Mansson R, Buza-Vidas N, Hultquist A, Liuba K, Jensen CT, Bryder D, Yang L, Borge OJ, Thoren LA, Anderson K, Sitnicka E, Sasaki Y, Sigvardsson M, Jacobsen SE (2005) Identification of Flt3+ lympho-myeloid stem cells lacking erythro-megakaryocytic potential a revised road map for adult blood lineage commitment. Cell 121:295–306 doi:10.1016/j.cell.2005.02.013 PubMed

62.

Igarashi H, Gregory S, Yokota T, Sakaguchi N, Kincade P (2002) Transcription from the RAG1 locus marks the earliest lymphocyte progenitors in bone marrow. Immunity 17:117–130 doi:10.1016/S1074-7613(02)00366-7 PubMed

63.

Perry SS, Welner RS, Kouro T, Kincade PW, Sun XH (2006) Primitive lymphoid progenitors in bone marrow with T lineage reconstituting potential. J Immunol 177:2880–2887PubMed

64.

Kondo M, Weissman IL, Akashi K (1997) Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 91:661–672 doi:10.1016/S0092-8674(00)80453-5 PubMed

65.

Izon D, Rudd K, DeMuth W, Pear WS, Clendenin C, Lindsley RC, Allman D (2001) A common pathway for dendritic cell and early B cell development. J Immunol 167:1387–1392PubMed

66.

Rumfelt LL, Zhou Y, Rowley BM, Shinton SA, Hardy RR (2006) Lineage specification and plasticity in CD19- early B cell precursors. J Exp Med 203:675–687 doi:10.1084/jem.20052444 PubMed

67.

Lu M, Tayu R, Ikawa T, Masuda K, Matsumoto I, Mugishima H, Kawamoto H, Katsura Y (2005) The earliest thymic progenitors in adults are restricted to T, NK, and dendritic cell lineage and have a potential to form more diverse TCRbeta chains than fetal progenitors. J Immunol 175:5848–5856PubMed

68.

Sitnicka E, Bryder D, Theilgaard-Monch K, Buza-Vidas N, Adolfsson J, Jacobsen SE (2002) Key role of flt3 ligand in regulation of the common lymphoid progenitor but not in maintenance of the hematopoietic stem cell pool. Immunity 17:463–472 doi:10.1016/S1074-7613(02)00419-3 PubMed

69.

Karsunky H, Inlay MA, Serwold T, Bhattacharya D, Weissman IL (2008) Flk2+ common lymphoid progenitors possess equivalent differentiation potential for the B and T lineages. Blood 111:5562–5570 doi:10.1182/blood-2007-11-126219 PubMed

70.

Martin CH, Aifantis I, Scimone ML, Von Andrian UH, Reizis B, Von Boehmer H, Gounari F (2003) Efficient thymic immigration of B220(+) lymphoid-restricted bone marrow cells with T precursor potential. Nat Immunol 4:866–873 doi:10.1038/ni965 PubMed

71.

Radtke F, Wilson A, Stark G, Bauer M, van Meerwijk J, MacDonald HR, Aguet M (1999) Deficient T cell fate specification in mice with an induced inactivation of Notch1. Immunity 10:547–558 doi:10.1016/S1074-7613(00)80054-0 PubMed

72.

Tan JB, Visan I, Yuan JS, Guidos CJ (2005) Requirement for Notch1 signals at sequential early stages of intrathymic T cell development. Nat Immunol 6:671–679 doi:10.1038/ni1217 PubMed

73.

Guenechea G, Gan OI, Dorrell C, Dick JE (2001) Distinct classes of human stem cells that differ in proliferative and self-renewal potential. Nat Immunol 2:75–82 doi:10.1038/83199 PubMed

74.

Mazurier F, Gan OI, McKenzie JL, Doedens M, Dick JE (2004) Lentivector-mediated clonal tracking reveals intrinsic heterogeneity in the human hematopoietic stem cell compartment and culture-induced stem cell impairment. Blood 103:545–552 doi:10.1182/blood-2003-05-1558 PubMed

75.

McKenzie JL, Gan OI, Doedens M, Wang JC, Dick JE (2006) Individual stem cells with highly variable proliferation and self-renewal properties comprise the human hematopoietic stem cell compartment. Nat Immunol 7:1225–1233 doi:10.1038/ni1393 PubMed

76.

Galy A, Travis M, Cen D, Chen B (1995) Human T, B, natural killer, and dendritic cells arise from a common bone marrow progenitor cell subset. Immunity 3:459–473 doi:10.1016/1074-7613(95)90175-2 PubMed

77.

Ryan DH, Nuccie BL, Ritterman I, Liesveld JL, Abboud CN, Insel RA (1997) Expression of interleukin-7 receptor by lineage-negative human bone marrow progenitors with enhanced lymphoid proliferative potential and B-lineage differentiation capacity. Blood 89:929–940PubMed

78.

Manz MG, Miyamoto T, Akashi K, Weissman IL (2002) Prospective isolation of human clonogenic common myeloid progenitors. Proc Natl Acad Sci U S A 99:11872–11877 doi:10.1073/pnas.172384399 PubMed

79.

Hao QL, Zhu J, Price MA, Payne KJ, Barsky LW, Crooks GM (2001) Identification of a novel, human multilymphoid progenitor in cord blood. Blood 97:3683–3690 doi:10.1182/blood.V97.12.3683 PubMed

80.

Haddad R, Guardiola P, Izac B, Thibault C, Radich J, Delezoide AL, Baillou C, Lemoine FM, Gluckman JC, Pflumio F, Canque B (2004) Molecular characterization of early human T/NK and B-lymphoid progenitor cells in umbilical cord blood. Blood 104:3918–3926 doi:10.1182/blood-2004-05-1845 PubMed

81.

Haddad R, Guimiot F, Six E, Jourquin F, Setterblad N, Kahn E, Yagello M, Schiffer C, Andre-Schmutz I, Cavazzana-Calvo M, Gluckman JC, Delezoide AL, Pflumio F, Canque B (2006) Dynamics of thymus-colonizing cells during human development. Immunity 24:217–230 doi:10.1016/j.immuni.2006.01.008 PubMed

82.

Six EM, Bonhomme D, Monteiro M, Beldjord K, Jurkowska M, Cordier-Garcia C, Garrigue A, Dal Cortivo L, Rocha B, Fischer A, Cavazzana-Calvo M, Andre-Schmutz I (2007) A human postnatal lymphoid progenitor capable of circulating and seeding the thymus. J Exp Med 204:3085–3093 doi:10.1084/jem.20071003 PubMed

83.

Hao QL, George AA, Zhu J, Barsky L, Zielinska E, Wang X, Price M, Ge S, Crooks GM (2008) Human intrathymic lineage commitment is marked by differential CD7 expression: identification of CD7- lympho-myeloid thymic progenitors. Blood 111:1318–1326 doi:10.1182/blood-2007-08-106294 PubMed

84.

Goodman JW, Hodgson GS (1962) Evidence for stem cells in the peripheral blood of mice. Blood 19:702–714PubMed

85.

Dorie MJ, Maloney MA, Patt HM (1979) Turnover of circulating hematopoietic stem cells. Exp Hematol 7:483–489PubMed

86.

Wright DE, Wagers AJ, Gulati AP, Johnson FL, Weissman IL (2001) Physiological migration of hematopoietic stem and progenitor cells. Science 294:1933–1936 doi:10.1126/science.1064081 PubMed

87.

Papayannopoulou T (2004) Current mechanistic scenarios in hematopoietic stem/progenitor cell mobilization. Blood 103:1580–1585 doi:10.1182/blood-2003-05-1595 PubMed

88.

Schwarz BA, Bhandoola A (2006) Trafficking from the bone marrow to the thymus: a prerequisite for thymopoiesis. Immunol Rev 209:47–57 doi:10.1111/j.0105-2896.2006.00350.x PubMed

89.

Schwarz BA, Bhandoola A (2004) Circulating hematopoietic progenitors with T lineage potential. Nat Immunol 5:953–960 doi:10.1038/ni1101 PubMed

90.

Umland O, Mwangi WN, Anderson BM, Walker JC, Petrie HT (2007) The blood contains multiple distinct progenitor populations with clonogenic B and T lineage potential. J Immunol 178:4147–4152PubMed

91.

Barr RD, Whang-Peng J, Perry S (1975) Hemopoietic stem cells in human peripheral blood. Science 190:284–285 doi:10.1126/science.1179209 PubMed

92.

Cutler C, Antin JH (2001) Peripheral blood stem cells for allogeneic transplantation: a review. Stem Cells 19:108–117 doi:10.1634/stemcells.19-2-108 PubMed

93.

To LB, Haylock DN, Simmons PJ, Juttner CA (1997) The biology and clinical uses of blood stem cells. Blood 89:2233–2258PubMed

94.

Juttner CA, To LB, Haylock DN, Branford A, Kimber RJ (1985) Circulating autologous stem cells collected in very early remission from acute non-lymphoblastic leukaemia produce prompt but incomplete haemopoietic reconstitution after high dose melphalan or supralethal chemoradiotherapy. Br J Haematol 61:739–745 doi:10.1111/j.1365-2141.1985.tb02888.x PubMed

95.

Korbling M, Dorken B, Ho AD, Pezzutto A, Hunstein W, Fliedner TM (1986) Autologous transplantation of blood-derived hemopoietic stem cells after myeloablative therapy in a patient with Burkitt’s lymphoma. Blood 67:529–532PubMed

96.

Reiffers J, Bernard P, David B, Vezon G, Sarrat A, Marit G, Moulinier J, Broustet A (1986) Successful autologous transplantation with peripheral blood hemopoietic cells in a patient with acute leukemia. Exp Hematol 14:312–315PubMed

97.

Richman CM, Weiner RS, Yankee RA (1976) Increase in circulating stem cells following chemotherapy in man. Blood 47:1031–1039PubMed

98.

Shizuru JA, Negrin RS, Weissman IL (2005) Hematopoietic stem and progenitor cells: clinical and preclinical regeneration of the hematolymphoid system. Annu Rev Med 56:509–538 doi:10.1146/annurev.med.54.101601.152334 PubMed

99.

Wright DE, Bowman EP, Wagers AJ, Butcher EC, Weissman IL (2002) Hematopoietic stem cells are uniquely selective in their migratory response to chemokines. J Exp Med 195:1145–1154 doi:10.1084/jem.20011284 PubMed

100.

Nagasawa T, Hirota S, Tachibana K, Takakura N, Nishikawa S, Kitamura Y, Yoshida N, Kikutani H, Kishimoto T (1996) Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 382:635–638 doi:10.1038/382635a0 PubMed

101.

Tachibana K, Hirota S, Iizasa H, Yoshida H, Kawabata K, Kataoka Y, Kitamura Y, Matsushima K, Yoshida N, Nishikawa S, Kishimoto T, Nagasawa T (1998) The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 393:591–594 doi:10.1038/31261 PubMed

102.

Zou YR, Kottmann AH, Kuroda M, Taniuchi I, Littman DR (1998) Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393:595–599 doi:10.1038/31269 PubMed

103.

Ara T, Tokoyoda K, Sugiyama T, Egawa T, Kawabata K, Nagasawa T (2003) Long-term hematopoietic stem cells require stromal cell-derived factor-1 for colonizing bone marrow during ontogeny. Immunity 19:257–267 doi:10.1016/S1074-7613(03)00201-2 PubMed

104.

Kawabata K, Ujikawa M, Egawa T, Kawamoto H, Tachibana K, Iizasa H, Katsura Y, Kishimoto T, Nagasawa T (1999) A cell-autonomous requirement for CXCR4 in long-term lymphoid and myeloid reconstitution. Proc Natl Acad Sci U S A 96:5663–5667 doi:10.1073/pnas.96.10.5663 PubMed

105.

Ponomaryov T, Peled A, Petit I, Taichman RS, Habler L, Sandbank J, Arenzana-Seisdedos F, Magerus A, Caruz A, Fujii N, Nagler A, Lahav M, Szyper-Kravitz M, Zipori D, Lapidot T (2000) Induction of the chemokine stromal-derived factor-1 following DNA damage improves human stem cell function. J Clin Invest 106:1331–1339 doi:10.1172/JCI10329 PubMed

106.

Hattori K, Heissig B, Tashiro K, Honjo T, Tateno M, Shieh JH, Hackett NR, Quitoriano MS, Crystal RG, Rafii S, Moore MA (2001) Plasma elevation of stromal cell-derived factor-1 induces mobilization of mature and immature hematopoietic progenitor and stem cells. Blood 97:3354–3360 doi:10.1182/blood.V97.11.3354 PubMed

107.

Broxmeyer HE, Orschell CM, Clapp DW, Hangoc G, Cooper S, Plett PA, Liles WC, Li X, Graham-Evans B, Campbell TB, Calandra G, Bridger G, Dale DC, Srour EF (2005) Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD3100, a CXCR4 antagonist. J Exp Med 201:1307–1318 doi:10.1084/jem.20041385 PubMed

108.

Liles WC, Broxmeyer HE, Rodger E, Wood B, Hubel K, Cooper S, Hangoc G, Bridger GJ, Henson GW, Calandra G, Dale DC (2003) Mobilization of hematopoietic progenitor cells in healthy volunteers by AMD3100, a CXCR4 antagonist. Blood 102:2728–2730 doi:10.1182/blood-2003-02-0663 PubMed

109.

Fleming WH, Alpern EJ, Uchida N, Ikuta K, Weissman IL (1993) Steel factor influences the distribution and activity of muri ne hematopoietic stem cells in vivo. Proc Natl Acad Sci U S A 90:3760–3764 doi:10.1073/pnas.90.8.3760 PubMed

110.

Nakamura Y, Tajima F, Ishiga K, Yamazaki H, Oshimura M, Shiota G, Murawaki Y (2004) Soluble c-kit receptor mobilizes hematopoietic stem cells to peripheral blood in mice. Exp Hematol 32:390–396 doi:10.1016/j.exphem.2004.01.004 PubMed

111.

Papayannopoulou T, Priestley GV, Nakamoto B (1998) Anti-VLA4/VCAM-1-induced mobilization requires cooperative signaling through the kit/mkit ligand pathway. Blood 91:2231–2239PubMed

112.

Papayannopoulou T (1999) Hematopoietic stem/progenitor cell mobilization. A continuing quest for etiologic mechanisms. Ann N Y Acad Sci 872:187–197 discussion 197–9 doi:10.1111/j.1749-6632.1999.tb08464.x PubMed

113.

Morstyn G, Brown S, Gordon M, Crawford J, Demetri G, Rich W, McGuire B, Foote M, McNiece I (1994) Stem cell factor is a potent synergistic factor in hematopoiesis. Oncology 51:205–214PubMedCrossRef

114.

Nervi B, Link D, DiPersio J (2006) Cytokines and hematopoietic stem cell mobilization. J Cell Biochem 99:690–705 doi:10.1002/jcb.21043 PubMed

115.

Thomas J, Liu F, Link DC (2002) Mechanisms of mobilization of hematopoietic progenitors with granulocyte colony-stimulating factor. Curr Opin Hematol 9:183–189 doi:10.1097/00062752-200205000-00002 PubMed

116.

Liu F, Poursine-Laurent J, Link DC (2000) Expression of the G-CSF receptor on hematopoietic progenitor cells is not required for their mobilization by G-CSF. Blood 95:3025–3031PubMed

117.

Levesque JP, Hendy J, Takamatsu Y, Williams B, Winkler IG, Simmons PJ (2002) Mobilization by either cyclophosphamide or granulocyte colony-stimulating factor transforms the bone marrow into a highly proteolytic environment. Exp Hematol 30:440–449 doi:10.1016/S0301-472X(02)00788-9 PubMed

118.

Levesque JP, Takamatsu Y, Nilsson SK, Haylock DN, Simmons PJ (2001) Vascular cell adhesion molecule-1 (CD106) is cleaved by neutrophil proteases in the bone marrow following hematopoietic progenitor cell mobilization by granulocyte colony-stimulating factor. Blood 98:1289–1297 doi:10.1182/blood.V98.5.1289 PubMed

119.

Levesque JP, Hendy J, Takamatsu Y, Simmons PJ, Bendall LJ (2003) Disruption of the CXCR4/CXCL12 chemotactic interaction during hematopoietic stem cell mobilization induced by GCSF or cyclophosphamide. J Clin Invest 111:187–196PubMed

120.

Petit I, Szyper-Kravitz M, Nagler A, Lahav M, Peled A, Habler L, Ponomaryov T, Taichman RS, Arenzana-Seisdedos F, Fujii N, Sandbank J, Zipori D, Lapidot T (2002) G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat Immunol 3:687–694 doi:10.1038/ni813 PubMed

121.

Levesque JP, Hendy J, Winkler IG, Takamatsu Y, Simmons PJ (2003) Granulocyte colony-stimulating factor induces the release in the bone marrow of proteases that cleave c-KIT receptor (CD117) from the surface of hematopoietic progenitor cells. Exp Hematol 31:109–117 doi:10.1016/S0301-472X(02)01028-7 PubMed

122.

Heissig B, Hattori K, Dias S, Friedrich M, Ferris B, Hackett NR, Crystal RG, Besmer P, Lyden D, Moore MA, Werb Z, Rafii S (2002) Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 109:625–637 doi:10.1016/S0092-8674(02)00754-7 PubMed

123.

Mendez-Ferrer S, Lucas D, Battista M, Frenette PS (2008) Hematopoietic stem cell release is regulated by circadian oscillations. Nature 452:442–447 doi:10.1038/nature06685 PubMed

124.

Yamamoto Y, Yasumizu R, Amou Y, Watanabe N, Nishio N, Toki J, Fukuhara S, Ikehara S (1996) Characterization of peripheral blood stem cells in mice. Blood 88:445–454PubMed

125.

Harrison DE, Astle CM (1997) Short- and long-term multilineage repopulating hematopoietic stem cells in late fetal and newborn mice: models for human umbilical cord blood. Blood 90:174–181PubMed

126.

Rodewald HR, Kretzschmar K, Takeda S, Hohl C, Dessing M (1994) Identification of pro-thymocytes in murine fetal blood: T lineage commitment can precede thymus colonization. EMBO J 13:4229–4240PubMed

127.

Krueger A, von Boehmer H (2007) Identification of a T lineage-committed progenitor in adult blood. Immunity 26:105–116 doi:10.1016/j.immuni.2006.12.004 PubMed

128.

Kawamoto H, Ohmura K, Katsura Y (1997) Direct evidence for the commitment of hematopoietic stem cells to T, B and myeloid lineages in murine fetal liver. Int Immunol 9:1011–1019 doi:10.1093/intimm/9.7.1011 PubMed

129.

Kawamoto H, Ohmura K, Fujimoto S, Katsura Y (1999) Emergence of T cell progenitors without B cell or myeloid differentiation potential at the earliest stage of hematopoiesis in the murine fetal liver. J Immunol 162:2725–2731PubMed

130.

Dejbakhsh-Jones S, Garcia-Ojeda ME, Chatterjea-Matthes D, Zeng D, Strober S (2001) Clonable progenitors committed to the T lymphocyte lineage in the mouse bone marrow; use of an extrathymic pathway. Proc Natl Acad Sci U S A 98:7455–7460 doi:10.1073/pnas.131559798 PubMed

131.

von Andrian UH, Mempel TR (2003) Homing and cellular traffic in lymph nodes. Nat Rev Immunol 3:867–878 doi:10.1038/nri1222

132.

Foss DL, Donskoy E, Goldschneider I (2001) The importation of hematogenous precursors by the thymus is a gated phenomenon in normal adult mice. J Exp Med 193:365–374 doi:10.1084/jem.193.3.365 PubMed

133.

Donskoy E, Foss D, Goldschneider I (2003) Gated importation of prothymocytes by adult mouse thymus is coordinated with their periodic mobilization from bone marrow. J Immunol 171:3568–3575PubMed

134.

Rossi FM, Corbel SY, Merzaban JS, Carlow DA, Gossens K, Duenas J, So L, Yi L, Ziltener HJ (2005) Recruitment of adult thymic progenitors is regulated by P-selectin and its ligand PSGL-1. Nat Immunol 6:626–634 doi:10.1038/ni1203 PubMed

135.

Liu C, Saito F, Liu Z, Lei Y, Uehara S, Love P, Lipp M, Kondo S, Manley N, Takahama Y (2006) Coordination between CCR7- and CCR9-mediated chemokine signals in prevascular fetal thymus colonization. Blood 108:2531–2539 doi:10.1182/blood-2006-05-024190 PubMed

136.

Liu C, Ueno T, Kuse S, Saito F, Nitta T, Piali L, Nakano H, Kakiuchi T, Lipp M, Hollander GA, Takahama Y (2005) The role of CCL21 in recruitment of T-precursor cells to fetal thymi. Blood 105:31–39 doi:10.1182/blood-2004-04-1369 PubMed

137.

Zubkova I, Mostowski H, Zaitseva M (2005) Up-regulation of IL-7, stromal-derived factor-1 alpha, thymus-expressed chemokine, and secondary lymphoid tissue chemokine gene expression in the stromal cells in response to thymocyte depletion: implication for thymus reconstitution. J Immunol 175:2321–2330PubMed

138.

Kenins L, Gill JW, Boyd RL, Hollander GA, Wodnar-Filipowicz A (2008) Intrathymic expression of Flt3 ligand enhances thymic recovery after irradiation. J Exp Med 205:523–531 doi:10.1084/jem.20072065 PubMed

139.

Till JE, McCulloch EA (1961) Direct Measurement Of Radiation Sensitivity Of Normal Mouse Bone Marrow Cells. Radiat Res 14:213–222 doi:10.2307/3570892 PubMed

140.

Lancrin C, Schneider E, Lambolez F, Arcangeli ML, Garcia-Cordier C, Rocha B, Ezine S (2002) Major T cell progenitor activity in bone marrow-derived spleen colonies. J Exp Med 195:919–929 doi:10.1084/jem.20011475 PubMed

141.

Arcangeli ML, Lancrin C, Lambolez F, Cordier C, Schneider E, Rocha B, Ezine S (2005) Extrathymic hemopoietic progenitors committed to T cell differentiation in the adult mouse. J Immunol 174:1980–1988PubMed

142.

van den Brink MR, Alpdogan O, Boyd RL (2004) Strategies to enhance T-cell reconstitution in immunocompromised patients. Nat Rev Immunol 4:856–867 doi:10.1038/nri1484 PubMed

Title: The long road to the thymus: the generation, mobilization, and circulation of T-cell progenitors in mouse and man
Authors: Daniel A. Zlotoff
Benjamin A. Schwarz
Avinash Bhandoola
Publication date: 01-12-2008
Publisher: Springer-Verlag
Published in: Seminars in Immunopathology / Issue 4/2008
Print ISSN: 1863-2297
Electronic ISSN: 1863-2300
DOI: https://doi.org/10.1007/s00281-008-0133-4

ACC 2024 Congress Coverage

Heart Failure Video

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

The long road to the thymus: the generation, mobilization, and circulation of T-cell progenitors in mouse and man

Abstract

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2008

The immunopathology of thymic GVHD

Human intrathymic development: a selective approach

Lymphoid reconstitution following hematopoietic stem cell transplantation

Central tolerance: what have we learned from mice?

Strategies for reconstituting and boosting T cell-based immunity following haematopoietic stem cell transplantation: pre-clinical and clinical approaches

Adoptive precursor cell therapy to enhance immune reconstitution after hematopoietic stem cell transplantation in mouse and man

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page