New Molecular Insights into Immune Cell Development

Literature Cited

1. 1.

   Weissman IL, Anderson DJ, Gage F 2001. Stem and progenitor cells: origins, phenotypes, lineage commitments, and transdifferentiations. Annu. Rev. Cell Dev. Biol. 17:387–403
   [Google Scholar]
2. 2.

   Höfer T, Busch K, Klapproth K, Rodewald HR 2016. Fate mapping and quantitation of hematopoiesis in vivo. Annu. Rev. Immunol. 34:449–478
   [Google Scholar]
3. 3.

   Akashi K, Traver D, Miyamoto T, Weissman IL 2000. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 404:193–97
   [Google Scholar]
4. 4.

   Kondo M, Weissman IL, Akashi K 1997. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 91:661–72Identification of a restricted lymphoid progenitor in bone marrow.
   [Google Scholar]
5. 5.

   Liu K, Nussenzweig MC 2010. Origin and development of dendritic cells. Immunol. Rev. 234:45–54
   [Google Scholar]
6. 6.

   Traver D, Akashi K, Manz M, Merad M, Miyamoto T et al. 2000. Development of CD8α-positive dendritic cells from a common myeloid progenitor. Science 290:2152–54
   [Google Scholar]
7. 7.

   Schlenner SM, Madan V, Busch K, Tietz A, Läufle C et al. 2010. Fate mapping reveals separate origins of T cells and myeloid lineages in the thymus. Immunity 32:426–36
   [Google Scholar]
8. 8.

   Miyamoto T, Iwasaki H, Reizis B, Ye M, Graf T et al. 2002. Myeloid or lymphoid promiscuity as a critical step in hematopoietic lineage commitment. Dev. Cell 3:137–47
   [Google Scholar]
9. 9.

   Adolfsson J, Borge OJ, Bryder D, Theilgaard-Mönch K, Astrand-Grundström I et al. 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 15:659–69
   [Google Scholar]
10. 10.

    Adolfsson J, Månsson R, Buza-Vidas N, Hultquist A, Liuba K et al. 2005. Identification of Flt3⁺ lympho-myeloid stem cells lacking erythro-megakaryocytic potential: a revised road map for adult blood lineage commitment. Cell 121:295–306Identification of a progenitor population primed for lymphoid gene expression.
    [Google Scholar]
11. 11.

    Månsson R, Hultquist A, Luc S, Yang L, Anderson K et al. 2007. Molecular evidence for hierarchical transcriptional lineage priming in fetal and adult stem cells and multipotent progenitors. Immunity 26:407–19Evidence for transcriptional lineage priming in hematopoietic progenitors.
    [Google Scholar]
12. 12.

    Rothenberg EV 2014. Transcriptional control of early T and B cell developmental choices. Annu. Rev. Immunol. 32:283–321
    [Google Scholar]
13. 13.

    Bain G, Robanus Maandag EC, te Riele HP, Feeney AJ, Sheehy A et al. 1997. Both E12 and E47 allow commitment to the B cell lineage. Immunity 6:145–54
    [Google Scholar]
14. 14.

    Lin H, Grosschedl R 1995. Failure of B-cell differentiation in mice lacking the transcription factor EBF. Nature 376:263–67
    [Google Scholar]
15. 15.

    Busslinger M 2004. Transcriptional control of early B cell development. Annu. Rev. Immunol. 22:55–79
    [Google Scholar]
16. 16.

    Koch U, Fiorini E, Benedito R, Besseyrias V, Schuster-Gossler K et al. 2008. Delta-like 4 is the essential, nonredundant ligand for Notch1 during thymic T cell lineage commitment. J. Exp. Med. 205:2515–23
    [Google Scholar]
17. 17.

    Rothenberg EV, Moore JE, Yui MA 2008. Launching the T-cell-lineage developmental programme. Nat. Rev. Immunol. 8:9–21
    [Google Scholar]
18. 18.

    De Obaldia ME, Bhandoola A 2015. Transcriptional regulation of innate and adaptive lymphocyte lineages. Annu. Rev. Immunol. 33:607–42
    [Google Scholar]
19. 19.

    Zook EC, Kee BL 2016. Development of innate lymphoid cells. Nat. Immunol. 17:775–82
    [Google Scholar]
20. 20.

    Rodewald HR, Ogawa M, Haller C, Waskow C, DiSanto JP 1997. Pro-thymocyte expansion by c-kit and the common cytokine receptors γ chain is essential for repertoire formation. Immunity 6:265–72
    [Google Scholar]
21. 21.

    Cumano A, Godin I 2007. Ontogeny of the hematopoietic system. Annu. Rev. Immunol. 25:745–85
    [Google Scholar]
22. 22.

    Bertrand JY, Jalil A, Klaine M, Jung S, Cumano A, Godin I 2005. Three pathways to mature macrophages in the early mouse yolk sac. Blood 106:3004–11
    [Google Scholar]
23. 23.

    Gomez Perdiguero E, Klapproth K, Schulz C, Busch K, Azzoni E et al. 2015. Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature 518:547–51
    [Google Scholar]
24. 24.

    Godin I, Cumano A 2002. The hare and the tortoise: an embryonic haematopoietic race. Nat. Rev. Immunol. 2:593–604
    [Google Scholar]
25. 25.

    Böiers C, Carrelha J, Lutteropp M, Luc S, Green JC et al. 2013. Lymphomyeloid contribution of an immune-restricted progenitor emerging prior to definitive hematopoietic stem cells. Cell Stem Cell 13:535–48
    [Google Scholar]
26. 26.

    Cumano A, Dieterlen-Lievre F, Godin I 1996. Lymphoid potential, probed before circulation in mouse, is restricted to caudal intraembryonic splanchnopleura. Cell 86:907–16
    [Google Scholar]
27. 27.

    Medvinsky A, Dzierzak E 1996. Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 86:897–906
    [Google Scholar]
28. 28.

    de Bruijn MF, Speck NA, Peeters MC, Dzierzak E 2000. Definitive hematopoietic stem cells first develop within the major arterial regions of the mouse embryo. EMBO J 19:2465–74
    [Google Scholar]
29. 29.

    Yoder MC, Hiatt K, Dutt P, Mukherjee P, Bodine DM, Orlic D 1997. Characterization of definitive lymphohematopoietic stem cells in the day 9 murine yolk sac. Immunity 7:335–44
    [Google Scholar]
30. 30.

    Gekas C, Dieterlen-Lièvre F, Orkin SH, Mikkola HK 2005. The placenta is a niche for hematopoietic stem cells. Dev. Cell 8:365–75
    [Google Scholar]
31. 31.

    Caprioli A, Minko K, Drevon C, Eichmann A, Dieterlen-Lièvre F, Jaffredo T 2001. Hemangioblast commitment in the avian allantois: cellular and molecular aspects. Dev. Biol. 238:64–78
    [Google Scholar]
32. 32.

    Bertrand JY, Giroux S, Golub R, Klaine M, Jalil A et al. 2005. Characterization of purified intraembryonic hematopoietic stem cells as a tool to define their site of origin. PNAS 102:134–39
    [Google Scholar]
33. 33.

    Taoudi S, Gonneau C, Moore K, Sheridan JM, Blackburn CC et al. 2008. Extensive hematopoietic stem cell generation in the AGM region via maturation of VE-cadherin⁺CD45⁺ pre-definitive HSCs. Cell Stem Cell 3:99–108
    [Google Scholar]
34. 34.

    Samokhvalov IM, Samokhvalova NI, Nishikawa S 2007. Cell tracing shows the contribution of the yolk sac to adult haematopoiesis. Nature 446:1056–61
    [Google Scholar]
35. 35.

    Cumano A, Ferraz JC, Klaine M, Di Santo JP, Godin I 2001. Intraembryonic, but not yolk sac hematopoietic precursors, isolated before circulation, provide long-term multilineage reconstitution. Immunity 15:477–85
    [Google Scholar]
36. 36.

    Kieusseian A, Brunet de la Grange P, Burlen-Defranoux O, Godin I, Cumano A 2012. Immature hematopoietic stem cells undergo maturation in the fetal liver. Development 139:3521–30
    [Google Scholar]
37. 37.

    Müller AM, Medvinsky A, Strouboulis J, Grosveld F, Dzierzak E 1994. Development of hematopoietic stem cell activity in the mouse embryo. Immunity 1:291–301
    [Google Scholar]
38. 38.

    Morrison SJ, Hemmati HD, Wandycz AM, Weissman IL 1995. The purification and characterization of fetal liver hematopoietic stem cells. PNAS 92:10302–6
    [Google Scholar]
39. 39.

    Passegué E, Wagers AJ, Giuriato S, Anderson WC, Weissman IL 2005. Global analysis of proliferation and cell cycle gene expression in the regulation of hematopoietic stem and progenitor cell fates. J. Exp. Med. 202:1599–611
    [Google Scholar]
40. 40.

    Wilson A, Laurenti E, Oser G, van der Wath RC, Blanco-Bose W et al. 2008. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 135:1118–29
    [Google Scholar]
41. 41.

    Jassinskaja M, Johansson E, Kristiansen TA, Åkerstrand H, Sjöholm K et al. 2017. Comprehensive proteomic characterization of ontogenic changes in hematopoietic stem and progenitor cells. Cell Rep 21:3285–97
    [Google Scholar]
42. 42.

    Igarashi H, Kouro T, Yokota T, Comp PC, Kincade PW 2001. Age and stage dependency of estrogen receptor expression by lymphocyte precursors. PNAS 98:15131–36
    [Google Scholar]
43. 43.

    Ikuta K, Kina T, MacNeil I, Uchida N, Peault B et al. 1990. A developmental switch in thymic lymphocyte maturation potential occurs at the level of hematopoietic stem cells. Cell 62:863–74
    [Google Scholar]
44. 44.

    Eberl G, Marmon S, Sunshine MJ, Rennert PD, Choi Y, Littman DR 2004. An essential function for the nuclear receptor RORγt in the generation of fetal lymphoid tissue inducer cells. Nat. Immunol. 5:64–73
    [Google Scholar]
45. 45.

    Haas JD, Ravens S, Düber S, Sandrock I, Oberdörfer L et al. 2012. Development of interleukin-17-producing γδ T cells is restricted to a functional embryonic wave. Immunity 37:48–59
    [Google Scholar]
46. 46.

    Hayakawa K, Hardy RR, Herzenberg LA, Herzenberg LA 1985. Progenitors for Ly-1 B cells are distinct from progenitors for other B cells. J. Exp. Med. 161:1554–68
    [Google Scholar]
47. 47.

    Herzenberg LA 2000. B-1 cells: the lineage question revisited. Immunol. Rev. 175:9–22
    [Google Scholar]
48. 48.

    Düber S, Hafner M, Krey M, Lienenklaus S, Roy B et al. 2009. Induction of B-cell development in adult mice reveals the ability of bone marrow to produce B-1a cells. Blood 114:4960–67
    [Google Scholar]
49. 49.

    Lam KP, Rajewsky K 1999. B cell antigen receptor specificity and surface density together determine B-1 versus B-2 cell development. J. Exp. Med. 190:471–77
    [Google Scholar]
50. 50.

    Kristiansen TA, Jaensson Gyllenbäck E, Zriwil A, Björklund T, Daniel JA et al. 2016. Cellular barcoding links B-1a B cell potential to a fetal hematopoietic stem cell state at the single-cell level. Immunity 45:346–57
    [Google Scholar]
51. 51.

    Montecino-Rodriguez E, Fice M, Casero D, Berent-Maoz B, Barber CL, Dorshkind K 2016. Distinct genetic networks orchestrate the emergence of specific waves of fetal and adult B-1 and B-2 development. Immunity 45:527–39
    [Google Scholar]
52. 52.

    Allison JP, Havran WL 1991. The immunobiology of T cells with invariant γδ antigen receptors. Annu. Rev. Immunol. 9:679–705
    [Google Scholar]
53. 53.

    Boyden LM, Lewis JM, Barbee SD, Bas A, Girardi M et al. 2008. Skint1, the prototype of a newly identified immunoglobulin superfamily gene cluster, positively selects epidermal γδ T cells. Nat. Genet. 40:656–62
    [Google Scholar]
54. 54.

    Di Marco Barros R, Roberts NA, Dart RJ, Vantourout P, Jandke A et al. 2016. Epithelia use butyrophilin-like molecules to shape organ-specific γδ T cell compartments. Cell 167:203–18.e17
    [Google Scholar]
55. 55.

    Turchinovich G, Hayday AC 2011. Skint-1 identifies a common molecular mechanism for the development of interferon-γ-secreting versus interleukin-17-secreting γδ T cells. Immunity 35:59–68
    [Google Scholar]
56. 56.

    Mebius RE, Miyamoto T, Christensen J, Domen J, Cupedo T et al. 2001. The fetal liver counterpart of adult common lymphoid progenitors gives rise to all lymphoid lineages, CD45⁺CD4⁺CD3⁻ cells, as well as macrophages. J. Immunol. 166:6593–601
    [Google Scholar]
57. 57.

    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 13:4229–40
    [Google Scholar]
58. 58.

    Carlyle JR, Zúñiga-Pflücker JC 1998. Requirement for the thymus in αβ T lymphocyte lineage commitment. Immunity 9:187–97
    [Google Scholar]
59. 59.

    Douagi I, Colucci F, Di Santo JP, Cumano A 2002. Identification of the earliest prethymic bipotent T/NK progenitor in murine fetal liver. Blood 99:463–71
    [Google Scholar]
60. 60.

    Kawamoto H, Ikawa T, Ohmura K, Fujimoto S, Katsura Y 2000. T cell progenitors emerge earlier than B cell progenitors in the murine fetal liver. Immunity 12:441–50
    [Google Scholar]
61. 61.

    Katsura Y 2002. Redefinition of lymphoid progenitors. Nat. Rev. Immunol. 2:127–32
    [Google Scholar]
62. 62.

    Schmitt TM, Zúñiga-Pflücker JC 2002. Induction of T cell development from hematopoietic progenitor cells by delta-like-1 in vitro. Immunity 17:749–56
    [Google Scholar]
63. 63.

    Masuda K, Kubagawa H, Ikawa T, Chen CC, Kakugawa K et al. 2005. Prethymic T-cell development defined by the expression of paired immunoglobulin-like receptors. EMBO J 24:4052–60A subset of fetal liver progenitors identified by a surface marker appears T cell committed.
    [Google Scholar]
64. 64.

    Mackarehtschian K, Hardin JD, Moore KA, Boast S, Goff SP, Lemischka IR 1995. Targeted disruption of the flk2/flt3 gene leads to deficiencies in primitive hematopoietic progenitors. Immunity 3:147–61
    [Google Scholar]
65. 65.

    Sitnicka E, Bryder D, Theilgaard-Mönch K, Buza-Vidas N, Adolfsson J, Jacobsen SEW 2002. Key role of flt3 ligand in regulation of the common lymphoid progenitor but not in maintenance of the hematopoietic stem cell pool. Immunity 17:463–72
    [Google Scholar]
66. 66.

    Noguchi M, Nakamura Y, Russell SM, Ziegler SF, Tsang M et al. 1993. Interleukin-2 receptor gamma chain: a functional component of the interleukin-7 receptor. Science 262:1877–80
    [Google Scholar]
67. 67.

    Turner AM, Lin NL, Issarachai S, Lyman SD, Broudy VC 1996. FLT3 receptor expression on the surface of normal and malignant human hematopoietic cells. Blood 88:3383–90
    [Google Scholar]
68. 68.

    Yokota T, Kouro T, Hirose J, Igarashi H, Garrett KP et al. 2003. Unique properties of fetal lymphoid progenitors identified according to RAG1 gene expression. Immunity 19:365–75
    [Google Scholar]
69. 69.

    Yokota T, Huang J, Tavian M, Nagai Y, Hirose J et al. 2006. Tracing the first waves of lymphopoiesis in mice. Development 133:2041–51
    [Google Scholar]
70. 70.

    Sawai CM, Babovic S, Upadhaya S, Knapp DJHF, Lavin Y et al. 2016. Hematopoietic stem cells are the major source of multilineage hematopoiesis in adult animals. Immunity 45:597–609
    [Google Scholar]
71. 71.

    Beaudin AE, Boyer SW, Perez-Cunningham J, Hernandez GE, Derderian SC et al. 2016. A transient developmental hematopoietic stem cell gives rise to innate-like B and T cells. Cell Stem Cell 19:768–83
    [Google Scholar]
72. 72.

    Mebius RE, Streeter PR, Michie S, Butcher EC, Weissman IL 1996. A developmental switch in lymphocyte homing receptor and endothelial vascular addressin expression regulates lymphocyte homing and permits CD4⁺ CD3⁻ cells to colonize lymph nodes. PNAS 93:11019–24
    [Google Scholar]
73. 73.

    Yoshida H, Honda K, Shinkura R, Adachi S, Nishikawa S et al. 1999. IL-7 receptor alpha⁺ CD3⁻ cells in the embryonic intestine induces the organizing center of Peyer's patches. Int. Immunol. 11:643–55
    [Google Scholar]
74. 74.

    Yoshida H, Kawamoto H, Santee SM, Hashi H, Honda K et al. 2001. Expression of α₄β₇ integrin defines a distinct pathway of lymphoid progenitors committed to T cells, fetal intestinal lymphotoxin producer, NK, and dendritic cells. J. Immunol. 167:2511–21
    [Google Scholar]
75. 75.

    Pereira de Sousa A, Berthault C, Granato A, Dias S, Ramond C et al. 2012. Inhibitors of DNA binding proteins restrict T cell potential by repressing Notch1 expression in Flt3-negative common lymphoid progenitors. J. Immunol. 189:3822–30
    [Google Scholar]
76. 76.

    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 111:5562–70
    [Google Scholar]
77. 77.

    Spits H, Artis D, Colonna M, Diefenbach A, Di Santo JP et al. 2013. Innate lymphoid cells—a proposal for uniform nomenclature. Nat. Rev. Immunol. 13:145–49
    [Google Scholar]
78. 78.

    Possot C, Schmutz S, Chea S, Boucontet L, Louise A et al. 2011. Notch signaling is necessary for adult, but not fetal, development of RORγt⁺ innate lymphoid cells. Nat. Immunol. 12:949–58Innate lymphoid cells derive from common lymphoid progenitors through a Notch-independent mechanism.
    [Google Scholar]
79. 79.

    Cherrier M, Sawa S, Eberl G 2012. Notch, Id2, and RORγt sequentially orchestrate the fetal development of lymphoid tissue inducer cells. J. Exp. Med. 209:729–40
    [Google Scholar]
80. 80.

    Klose CSN, Flach M, Möhle L, Rogell L, Hoyler T et al. 2014. Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell 157:340–56
    [Google Scholar]
81. 81.

    Constantinides MG, McDonald BD, Verhoef PA, Bendelac A 2014. A committed precursor to innate lymphoid cells. Nature 508:397–401
    [Google Scholar]
82. 82.

    Yokota Y, Mansouri A, Mori S, Sugawara S, Adachi S et al. 1999. Development of peripheral lymphoid organs and natural killer cells depends on the helix-loop-helix inhibitor Id2. Nature 397:702–6
    [Google Scholar]
83. 83.

    Yang Q, Li F, Harly C, Xing S, Ye L et al. 2015. TCF-1 upregulation identifies early innate lymphoid progenitors in the bone marrow. Nat. Immunol. 16:1044–50
    [Google Scholar]
84. 84.

    Mielke LA, Groom JR, Rankin LC, Seillet C, Masson F et al. 2013. TCF-1 controls ILC2 and NKp46⁺RORγt⁺ innate lymphocyte differentiation and protection in intestinal inflammation. J. Immunol. 191:4383–91
    [Google Scholar]
85. 85.

    Yagi R, Zhong C, Northrup DL, Yu F, Bouladoux N et al. 2014. The transcription factor GATA3 is critical for the development of all IL-7Rα-expressing innate lymphoid cells. Immunity 40:378–88
    [Google Scholar]
86. 86.

    Serafini N, Klein Wolterink RG, Satoh-Takayama N, Xu W, Vosshenrich CA et al. 2014. Gata3 drives development of RORγt⁺ group 3 innate lymphoid cells. J. Exp. Med. 211:199–208
    [Google Scholar]
87. 87.

    Aliahmad P, de la Torre B, Kaye J 2010. Shared dependence on the DNA-binding factor TOX for the development of lymphoid tissue-inducer cell and NK cell lineages. Nat. Immunol. 11:945–52
    [Google Scholar]
88. 88.

    Seillet C, Mielke LA, Amann-Zalcenstein DB, Su S, Gao J et al. 2016. Deciphering the innate lymphoid cell transcriptional program. Cell Rep 17:436–47
    [Google Scholar]
89. 89.

    Ishizuka IE, Chea S, Gudjonson H, Constantinides MG, Dinner AR et al. 2016. Single-cell analysis defines the divergence between the innate lymphoid cell lineage and lymphoid tissue-inducer cell lineage. Nat. Immunol. 17:269–76
    [Google Scholar]
90. 90.

    Chea S, Schmutz S, Berthault C, Perchet T, Petit M et al. 2016. Single-cell gene expression analyses reveal heterogeneous responsiveness of fetal innate lymphoid progenitors to Notch signaling. Cell Rep 14:1500–16
    [Google Scholar]
91. 91.

    Chea S, Perchet T, Petit M, Verrier T, Guy-Grand D et al. 2016. Notch signaling in group 3 innate lymphoid cells modulates their plasticity. Sci. Signal 9:ra45
    [Google Scholar]
92. 92.

    Bando JK, Liang HE, Locksley RM 2015. Identification and distribution of developing innate lymphoid cells in the fetal mouse intestine. Nat. Immunol. 16:153–60
    [Google Scholar]
93. 93.

    Cherrier DE, Serafini N, Di Santo JP 2018. Innate lymphoid cell development: a T cell perspective. Immunity 48:1091–103
    [Google Scholar]
94. 94.

    Lai AY, Kondo M 2008. T and B lymphocyte differentiation from hematopoietic stem cell. Semin. Immunol. 20:207–12
    [Google Scholar]
95. 95.

    Berthault C, Ramond C, Burlen-Defranoux O, Soubigou G, Chea S et al. 2017. Asynchronous lineage priming determines commitment to T cell and B cell lineages in fetal liver. Nat. Immunol. 18:1139–49Asynchronous B and T cell transcriptional priming determines lineage divergence in fetal liver.
    [Google Scholar]
96. 96.

    Lee DM, Schanberg LE, Fleenor DE, Seldin MF, Haynes BF, Kaufman RE 1996. The mouse CD7 gene: identification of a new element common to the human CD7 and mouse Thy-1 promoters. Immunogenetics 44:108–14
    [Google Scholar]
97. 97.

    Uehara S, Grinberg A, Farber JM, Love PE 2002. A role for CCR9 in T lymphocyte development and migration. J. Immunol. 168:2811–19
    [Google Scholar]
98. 98.

    Desanti GE, Jenkinson WE, Parnell SM, Boudil A, Gautreau-Rolland L et al. 2011. Clonal analysis reveals uniformity in the molecular profile and lineage potential of CCR9⁺ and CCR9⁻ thymus-settling progenitors. J. Immunol. 186:5227–35
    [Google Scholar]
99. 99.

    Ikawa T, Kawamoto H, Goldrath AW, Murre C 2006. E proteins and Notch signaling cooperate to promote T cell lineage specification and commitment. J. Exp. Med. 203:1329–42
    [Google Scholar]
100. 100.

     Carvalho TL, Mota-Santos T, Cumano A, Demengeot J, Vieira P 2001. Arrested B lymphopoiesis and persistence of activated B cells in adult interleukin 7^−/− mice. J. Exp. Med. 194:1141–50
     [Google Scholar]
101. 101.

     Vosshenrich CA, Cumano A, Müller W, Di Santo JP, Vieira P 2004. Pre-B cell receptor expression is necessary for thymic stromal lymphopoietin responsiveness in the bone marrow but not in the liver environment. PNAS 101:11070–75
     [Google Scholar]
102. 102.

     Sitnicka E, Brakebusch C, Martensson IL, Svensson M, Agace WW et al. 2003. Complementary signaling through flt3 and interleukin-7 receptor alpha is indispensable for fetal and adult B cell genesis. J. Exp. Med. 198:1495–506
     [Google Scholar]
103. 103.

     Rieger MA, Hoppe PS, Smejkal BM, Eitelhuber AC, Schroeder T 2009. Hematopoietic cytokines can instruct lineage choice. Science 325:217–18
     [Google Scholar]
104. 104.

     Dias S, Silva H Jr, Cumano A, Vieira P 2005. Interleukin-7 is necessary to maintain the B cell potential in common lymphoid progenitors. J. Exp. Med 201:971–79
     [Google Scholar]
105. 105.

     Kikuchi K, Lai AY, Hsu C-L, Kondo M 2005. IL-7 receptor signaling is necessary for stage transition in adult B cell development through up-regulation of EBF. J. Exp. Med. 201:1197–203
     [Google Scholar]
106. 106.

     Tsapogas P, Zandi S, Åhsberg J, Zetterblad J, Welinder E et al. 2011. IL-7 mediates Ebf-1-dependent lineage restriction in early lymphoid progenitors. Blood 118:1283–90
     [Google Scholar]
107. 107.

     Malin S, McManus S, Cobaleda C, Novatchkova M, Delogu A et al. 2010. Role of STAT5 in controlling cell survival and immunoglobulin gene recombination during pro-B cell development. Nat. Immunol. 11:171–79
     [Google Scholar]
108. 108.

     von Muenchow L, Alberti-Servera L, Klein F, Capoferri G, Finke D et al. 2016. Permissive roles of cytokines interleukin-7 and Flt3 ligand in mouse B-cell lineage commitment. PNAS 113:E8122–30
     [Google Scholar]
109. 109.

     Inlay MA, Bhattacharya D, Sahoo D, Serwold T, Seita J et al. 2009. Ly6d marks the earliest stage of B-cell specification and identifies the branchpoint between B-cell and T-cell development. Genes Dev 23:2376–81
     [Google Scholar]
110. 110.

     Mansson R, Zandi S, Welinder E, Tsapogas P, Sakaguchi N et al. 2010. Single-cell analysis of the common lymphoid progenitor compartment reveals functional and molecular heterogeneity. Blood 115:2601–9
     [Google Scholar]
111. 111.

     Ramond C, Berthault C, Burlen-Defranoux O, de Sousa AP, Guy-Grand D et al. 2014. Two waves of distinct hematopoietic progenitor cells colonize the fetal thymus. Nat. Immunol. 15:27–35In the mouse embryo the thymus is colonized by two different waves of hematopoietic progenitors.
     [Google Scholar]
112. 112.

     Porritt HE, Rumfelt LL, Tabrizifard S, Schmitt TM, Zúñiga-Pflücker JC, Petrie HT 2004. Heterogeneity among DN1 prothymocytes reveals multiple progenitors with different capacities to generate T cell and non-T cell lineages. Immunity 20:735–45
     [Google Scholar]
113. 113.

     Weber BN, Chi AW, Chavez A, Yashiro-Ohtani Y, Yang Q et al. 2011. A critical role for TCF-1 in T-lineage specification and differentiation. Nature 476:63–68
     [Google Scholar]
114. 114.

     Abramson J, Anderson G 2017. Thymic epithelial cells. Annu. Rev. Immunol. 35:85–118
     [Google Scholar]
115. 115.

     Luc S, Luis TC, Boukarabila H, Macaulay IC, Buza-Vidas N et al. 2012. The earliest thymic T cell progenitors sustain B cell and myeloid lineage potential. Nat. Immunol. 13:412–19Neonatal thymus–settling cells are multipotent lympho-myeloid-primed progenitors.
     [Google Scholar]
116. 116.

     Perry SS, Wang H, Pierce LJ, Yang AM, Tsai S, Spangrude GJ 2004. L-selectin defines a bone marrow analog to the thymic early T-lineage progenitor. Blood 103:2990–96
     [Google Scholar]
117. 117.

     Coltey M, Jotereau FV, Le Douarin NM 1987. Evidence for a cyclic renewal of lymphocyte precursor cells in the embryonic chick thymus. Cell Differ. 22:71–82
     [Google Scholar]
118. 118.

     Jotereau FV, Le Douarin NM 1982. Demonstration of a cyclic renewal of the lymphocyte precursor cells in the quail thymus during embryonic and perinatal life. J. Immunol. 129:1869–77
     [Google Scholar]
119. 119.

     Douagi I, Vieira P, Cumano A 2002. Lymphocyte commitment during embryonic development, in the mouse. Semin. Immunol. 14:361–69
     [Google Scholar]
120. 120.

     Bell JJ, Bhandoola A 2008. The earliest thymic progenitors for T cells possess myeloid lineage potential. Nature 452:764–67
     [Google Scholar]
121. 121.

     Wada H, Masuda K, Satoh R, Kakugawa K, Ikawa T et al. 2008. Adult T-cell progenitors retain myeloid potential. Nature 452:768–72
     [Google Scholar]
122. 122.

     Bhandoola A, von Boehmer H, Petrie HT, Zúñiga-Pflücker JC 2007. Commitment and developmental potential of extrathymic and intrathymic T cell precursors: plenty to choose from. Immunity 26:678–89
     [Google Scholar]
123. 123.

     Luis TC, Luc S, Mizukami T, Boukarabila H, Thongjuea S et al. 2016. Initial seeding of the embryonic thymus by immune-restricted lympho-myeloid progenitors. Nat. Immunol. 17:1424–35
     [Google Scholar]
124. 124.

     Ceredig R, Bosco N, Rolink AG 2007. The B lineage potential of thymus settling progenitors is critically dependent on mouse age. Eur. J. Immunol. 37:830–37
     [Google Scholar]
125. 125.

     Allman D, Sambandam A, Kim S, Miller JP, Pagan A et al. 2003. Thymopoiesis independent of common lymphoid progenitors. Nat. Immunol. 4:168–74
     [Google Scholar]
126. 126.

     Schwarz BA, Bhandoola A 2004. Circulating hematopoietic progenitors with T lineage potential. Nat. Immunol. 5:953–60
     [Google Scholar]
127. 127.

     Richie Ehrlich LI, Serwold T, Weissman IL 2011. In vitro assays misrepresent in vivo lineage potentials of murine lymphoid progenitors. Blood 117:2618–24
     [Google Scholar]
128. 128.

     Roberts NA, White AJ, Jenkinson WE, Turchinovich G, Nakamura K et al. 2012. Rank signaling links the development of invariant γδ T cell progenitors and Aire⁺ medullary epithelium. Immunity 36:427–37
     [Google Scholar]
129. 129.

     Nutt SL, Heavey B, Rolink AG, Busslinger M 1999. Commitment to the B-lymphoid lineage depends on the transcription factor Pax5. Nature 401:556–62
     [Google Scholar]
130. 130.

     Pereira P, Boucontet L, Cumano A 2012. Temporal predisposition to αβ and γδ T cell fates in the thymus. J. Immunol. 188:1600–8
     [Google Scholar]
131. 131.

     Hoppe PS, Schwarzfischer M, Loeffler D, Kokkaliaris KD, Hilsenbeck O et al. 2016. Early myeloid lineage choice is not initiated by random PU.1 to GATA1 protein ratios. Nature 535:299–302
     [Google Scholar]
132. 132.

     Teschendorff AE, Enver T 2017. Single-cell entropy for accurate estimation of differentiation potency from a cell's transcriptome. Nat. Commun. 8:15599
     [Google Scholar]
133. 133.

     Ferrell JE 2012. Bistability, bifurcations, and Waddington's epigenetic landscape. Curr. Biol. 22:R458–66
     [Google Scholar]