Early T-cell progenitors are the major granulocyte precursors in the adult mouse thymus

Blood

Volumn 121, Issue 1, 2013, Pages 64-71

  De Obaldia, Maria Elena ^a   Bell, J Jeremiah ^a   Bhandoola, Avinash ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 7 RECEPTOR ALPHA; RAG1 PROTEIN; TRANSCRIPTION FACTOR HES 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL AGGREGATION; CELL LINEAGE; CONTROLLED STUDY; EARLY THYMIC PROGENITOR; FEMALE; GENE TARGETING; GRANULOCYTE PRECURSOR; IN VIVO STUDY; LYMPHOCYTE SUBPOPULATION; MOUSE; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; THYMUS;

EID: 84872055615     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-08-451773     Document Type: Article

References (50)

1. 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(6304):71-74.
2. 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(6):1617-1627.
3. Ardavin C, Wu L, Li CL, Shortman K. Thymic dendritic cells and T cells develop simultaneously in the thymus from a common precursor population. Nature. 1993;362(6422):761-763.
4. Matsuzaki Y, Gyotoku J, Ogawa M, et al. Characterization of c-kit positive intrathymic stem cells that are restricted to lymphoid differentiation. J Exp Med. 1993;178(4):1283-1292.
5. Allman D, Sambandam A, Kim S, et al. Thymopoiesis independent of common lymphoid progenitors. Nat Immunol. 2003;4(2):168-174.
6. Benz C, Bleul CC. A multipotent precursor in the thymus maps to the branching point of the T versus B lineage decision. J Exp Med. 2005;202(1):21-31.
7. Balciunaite G, Ceredig R, Rolink AG. The earliest subpopulation of mouse thymocytes contains potent T, significant macrophage, and natural killer cell but no B-lymphocyte potential. Blood. 2005;105(5):1930-1936.
8. Sambandam A, Maillard I, Zediak VP, et al. Notch signaling controls the generation and differentiation of early T lineage progenitors. Nat Immunol. 2005;6(7):663-670.
9. Masuda K, Kubagawa H, Ikawa T, et al. Prethymic T-cell development defined by the expression of paired immunoglobulin-like receptors. EMBO J. 2005;24(23):4052-4060.
10. Bell JJ, Bhandoola A. The earliest thymic progenitors for T cells possess myeloid lineage potential. Nature. 2008;452(7188):764-767.
11. Wada H, Masuda K, Satoh R, et al. Adult T-cell progenitors retain myeloid potential. Nature. 2008;452(7188):768-772.
12. Schlenner SM, Madan V, Busch K, et al. Fate mapping reveals separate origins of T cells and myeloid lineages in the thymus. Immunity. 2010;32(3):426-436.
13. Luc S, Luis TC, Boukarabila H, et al. The earliest thymic T cell progenitors sustain B cell and myeloid lineage potential. Nat Immunol. 2012;13(4):412-419.
14. Radtke F, Ferrero I, Wilson A, Lees R, Aguet M, MacDonald HR. Notch1 deficiency dissociates the intrathymic development of dendritic cells and T cells. J Exp Med. 2000;191(7):1085-1094.
15. Feyerabend TB, Terszowski G, Tietz A, et al. Deletion of Notch1 converts pro-T cells to dendritic cells and promotes thymic B cells by cell-extrinsic and cell-intrinsic mechanisms. Immunity. 2009;30(1):67-79.
16. McCormack MP, Forster A, Drynan L, Pannell R, Rabbitts TH. The LMO2 T-cell oncogene is activated via chromosomal translocations or retroviral insertion during gene therapy but has no mandatory role in normal T-cell development. Mol Cell Biol. 2003;23(24):9003-9013.
17. Uehara S, Grinberg A, Farber JM, Love PE. A role for CCR9 in T lymphocyte development and migration. J Immunol. 2002;168(6):2811-2819.
18. Förster R, Schubel A, Breitfeld D, et al. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell. 1999;99(1):23-33.
19. Peschon JJ, Morrissey PJ, Grabstein KH, et al. Early lymphocyte expansion is severely impaired in interleukin 7 receptor-deficient mice. J Exp Med. 1994;180(5):1955-1960.
20. Zhang P, Iwasaki-Arai J, Iwasaki H, et al. Enhancement of hematopoietic stem cell repopulating capacity and self-renewal in the absence of the transcription factor C/EBP alpha. Immunity. 2004;21(6):853-863.
21. Donskoy E, Goldschneider I. Thymocytopoiesis is maintained by blood-borne precursors throughout postnatal life. A study in parabiotic mice. J Immunol. 1992;148(6):1604-1612.
22. Zhang DE, Zhang P, Wang ND, Hetherington CJ, Darlington GJ, Tenen DG. Absence of granulocyte colony-stimulating factor signaling and neutrophil development in CCAAT enhancer binding protein alpha-deficient mice. Proc Natl Acad Sci U SA. 1997;94(2):569-574.
23. Welner RS, Esplin BL, Garrett KP, et al. Asynchronous RAG-1 expression during B lymphopoiesis. J Immunol. 2009;183(12):7768-7777.
24. Lagasse E, Weissman IL. bcl-2 inhibits apoptosis of neutrophils but not their engulfment by macrophages. J Exp Med. 1994;179(3):1047-1052.
25. Zlotoff DA, Sambandam A, Logan TD, Bell JJ, Schwarz BA, Bhandoola A. CCR7 and CCR9 together recruit hematopoietic progenitors to the adult thymus. Blood. 2010;115(10):1897-1905.
26. Krueger A, Willenzon S, Lyszkiewicz M, Kremmer E, Forster R. CC chemokine receptor 7 and 9 double-deficient hematopoietic progenitors are severely impaired in seeding the adult thymus. Blood. 2010;115(10):1906-1912.
27. 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(4):1519-1526.
28. Noguchi M, Nakamura Y, Russell SM, et al. Interleukin-2 receptor gamma chain: a functional component of the interleukin-7 receptor. Science. 1993;262(5141):1877-1880.
29. Tomita K, Hattori M, Nakamura E, Nakanishi S, Minato N, Kageyama R. The bHLH gene Hes1 is essential for expansion of early T cell precursors. Genes Dev. 1999;13(9):1203-1210.
30. Jarriault S, Brou C, Logeat F, Schroeter EH, Kopan R, Israel A. Signalling downstream of activated mammalian Notch. Nature. 1995;377 (6547):355-358.
31. Nishimura M, Isaka F, Ishibashi M, et al. Structure, chromosomal locus, and promoter of mouse Hes2 gene, a homologue of Drosophila hairy and Enhancer of split. Genomics. 1998;49(1):69-75.
32. Wendorff AA, Koch U, Wunderlich FT, et al. Hes1 is a critical but context-dependent mediator of canonical Notch signaling in lymphocyte development and transformation. Immunity. 2010;33(5):671-684.
33. Walker F, Nicola NA, Metcalf D, Burgess AW. Hierarchical down-modulation of hemopoietic growth factor receptors. Cell. 1985;43(1):269-276.
34. Ceredig R, Rolink T. A positive look at double-negative thymocytes. Nat Rev Immunol. 2002;2(11):888-897.
35. Kawamata S, Du C, Li K, Lavau C. Overexpression of the Notch target genes Hes in vivo induces lymphoid and myeloid alterations. Oncogene. 2002;21(24):3855-3863.
36. Klinakis A, Lobry C, Abdel-Wahab O, et al. A novel tumour-suppressor function for the Notch pathway in myeloid leukaemia. Nature. 2011;473(7346):230-233.
37. Pui JC, Allman D, Xu L, et al. Notch1 expression in early lymphopoiesis influences B versus T lineage determination. Immunity. 1999;11(3):299-308.
38. Schmitt TM, Ciofani M, Petrie HT, Zuniga-Pflucker JC. Maintenance of T cell specification and differentiation requires recurrent notch receptor-ligand interactions. J Exp Med. 2004;200(4):469-479.
39. Yücel R, Karsunky H, Klein-Hitpass L, Moroy T. The transcriptional repressor Gfi1 affects development of early, uncommitted c-Kit+ T cell progenitors and CD4/CD8 lineage decision in the thymus. J Exp Med. 2003;197(7):831-844.
40. Hock H, Hamblen MJ, Rooke HM, et al. Intrinsic requirement for zinc finger transcription factor Gfi-1 in neutrophil differentiation. Immunity. 2003;18(1):109-120.
41. Traver D, Akashi K, Manz M, et al. Development of CD8alpha-positive dendritic cells from a common myeloid progenitor. Science. 2000;290(5499):2152- 2154.
42. Surh CD, Sprent J. T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature. 1994;372(6501):100-103.
43. Iyoda T, Nagata K, Akashi M, Kobayashi Y. Neutrophils accelerate macrophage-mediated digestion of apoptotic cells in vivo as well as in vitro. J Immunol. 2005;175(6):3475-3483.
44. Kim HJ, Alonzo ES, Dorothee G, Pollard JW, Sant'Angelo DB. Selective depletion of eosinophils or neutrophils in mice impacts the efficiency of apoptotic cell clearance in the thymus. PLoS One. 2010;5(7):e11439.
45. Ceredig R, Bosco N, Rolink AG. The B lineage potential of thymus settling progenitors is critically dependent on mouse age. Eur J Immunol. 2007;37(3):830-837.
46. Moore AJ, Sarmiento J, Mohtashami M, Braunstein M, Zuniga-Pflucker JC, Anderson MK. Transcriptional priming of intrathymic precursors for dendritic cell development. Development. 2012;139(2):373-384.
47. Donskoy E, Goldschneider I. Two developmentally distinct populations of dendritic cells inhabit the adult mouse thymus: demonstration by differential importation of hematogenous precursors under steady state conditions. J Immunol. 2003;170(7):3514-3521.
48. Li J, Park J, Foss D, Goldschneider I. Thymushoming peripheral dendritic cells constitute two of the three major subsets of dendritic cells in the steady-state thymus. J Exp Med. 2009;206(3):607-622.
49. Luche H, Ardouin L, Teo P, et al. The earliest intrathymic precursors of CD8alpha(+) thymic dendritic cells correspond to myeloid-type doublenegative 1c cells. Eur J Immunol. 2011;41(8):2165-2175.
50. Porritt HE, Rumfelt LL, Tabrizifard S, Schmitt TM, Zuniga-Pflucker JC, Petrie HT. Heterogeneity among DN1 prothymocytes reveals multiple progenitors with different capacities to generate T cell and non-T cell lineages. Immunity. 2004;20(6):735-745.