Hematopoietic stem cell-independent hematopoiesis: emergence of erythroid, megakaryocyte, and myeloid potential in the mammalian embryo

FEBS Letters

Volumn 590, Issue 22, 2016, Pages 3965-3974

  Palis, James ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

erythro myeloid progenitor; erythroid; hematopoiesis; macrophage; megakaryocyte; primitive; yolk sac

Indexed keywords

ERYTHROPOIETIN; ERYTHROPOIETIN RECEPTOR;

ADULT STEADY STATE HEMATOPOIESIS; BONE MARROW CELL; CELL EXPANSION; CELL MATURATION; DEFINITIVE ERYTHROPOIESIS; EMBRYO; EMBRYO SURVIVAL; EMBRYONIC ORGAN; EMBRYONIC STRUCTURES; ENGRAFTMENT; ERYTHROBLAST; ERYTHROID CELL; ERYTHROMYELOID PROGENITOR; ERYTHROPOIESIS; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC STEM CELL INDEPENDENT HEMATOPOIESIS; HOMEOSTASIS; HUMAN; KUPFFER CELL; LANGERHANS CELL; LUNG ALVEOLUS MACROPHAGE; MACROPHAGE; MEGAKARYOCYTE; MICROGLIA; MOLECULAR DYNAMICS; NONHUMAN; ONTOGENY; PRIMITIVE ERYTHROPOIESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; STEM CELL; STRESS HEMATOPOIESIS; SURVIVAL; YOLK SAC; ANIMAL; CYTOLOGY; GENETICS; MAMMALIAN EMBRYO; MOUSE;

ANIMALS; EMBRYO, MAMMALIAN; ERYTHROID CELLS; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HUMANS; MEGAKARYOCYTES; MICE; MYELOID CELLS;

EID: 84995962590     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1002/1873-3468.12459     Document Type: Review

References (79)

1. Yoder M (2004) Blood cell progenitors: insights into the properties of stem cells. Anat Rec A Discov Mol Cell Evol Biol 267, 66–74.
2. Sawai CM, Babovic S, Upadhaya S, Knapp DJ, Lavin Y, Lau CM, Goloborodko A, Feng J, Fujisaki J, Ding L et al. (2016) Hematopoietic stem cells are the major source of multilineage hematopoiesis in adult animals. Immunity 45, 597–609.
3. Muller AM, Medvinsky A, Strouboulis J, Grosveld F and Dzierzak E (1994) Development of hematopoietic stem cell activity in the mouse embryo. Immunity 1, 291–301.
4. de Bruijn MFTR, Speck NA, Peeters MCE and Dzierzak E (2000) Definitive hematopoietic stem cells first develop within the major arterial regions of the mouse embryo. EMBO J 19, 2465–2474.
5. de Bruijn MF, Ma X, Robin C, Ottersbach K, Sanchez MJ and Dzierzak E (2002) Hematopoietic stem cells localize to the endothelial cell layer in the midgestation mouse aorta. Immunity 16, 673–683.
6. Maximow AA (1909) Untersuchungen uber blut und bindegewebe 1. Die fruhesten entwicklungsstadien der blut- und binde- gewebszellan bein saugetierembryo, bis zum anfang der blutbilding unden leber. Arch Mikroskop Anat 73, 444–561.
7. Ferkowicz MJ and Yoder MC (2005) Blood island formation: longstanding observations and modern interpretations. Exp Hematol 33, 1041–1047.
8. Wong PM, Chung SW, Reicheld SM and Chui DH (1986) Hemoglobin switching during murine embryonic development: evidence for two populations of embryonic erythropoietic progenitor cells. Blood 67, 716–721.
9. Palis J, Kennedy M, Robertson S, Wall C and Keller G (1999) Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse embryo. Development 126, 5073–5084.
10. Ji RP, Phoon CKL, Aristizábal O, McGrath KE, Palis J and Turnbull DH (2003) Onset of cardiac function during early mouse embryogenesis coincides with entry of primitive erythroblasts into the embryo proper. Circ Res 92, 133–135.
11. McGrath KE, Koniski AD, Malik J and Palis J (2003) Circulation is established in a step-wise pattern in the mammalian embryo. Blood 101, 1669–1676.
12. Kingsley PD, Malik J, Emerson RL, Bushnell TP, McGrath KE, Bloedorn LA, Bulger M and Palis J (2006) “Maturational” globin switching in primary primitive erythroid cells. Blood 107, 1665–1672.
13. Kingsley PD, Malik J, Fantauzzo KA and Palis J (2004) Yolk sac-derived primitive erythroblasts enucleate during mammalian embryogenesis. Blood 104, 19–25.
14. Fraser ST, Isern J and Baron M (2007) Maturation and enucleation of primitive erythroblasts during mouse embryogenesis is accompanied by changes in cell-surface antigen expression. Blood 109, 343–352.
15. McGann JK, Silver L, Liesveld J and Palis J (1997) Erythropoietin-receptor expression and function during the initiation of murine yolk sac erythropoiesis. Exp Hematol 25, 1149–1157.
16. Kimura T, Sonoda Y, Iwai N, Satoh M, Yamaguchi-Tsukio M, Izui T, Suda M, Sasaki K and Nakano T (2000) Proliferation and cell death of embryonic primitive erythrocytes. Exp Hematol 28, 635–641.
17. Suzuki N, Hirano I, Pan X, Minegishi N and Yamamoto M (2013) Erythropoietin production in neuroepithelial and neural crest cells during primitive erythropoiesis. Nat Commun 4, 2902.
18. Wu H, Liu X, Jaenisch R and Lodish HF (1995) Generation of committed erythroid BFU-E and CFU-E progenitors does not require erythropoietin or the erythropoietin receptor. Cell 83, 59–67.
19. Lin C-S, Lim S-K, D'Agati V and Constantini F (1996) Differential effects of an erythropoietin receptor gene disruption on primitive and definitive erythropoiesis. Genes Dev 10, 154–164.
20. Malik J, Kim AR, Tyre KA, Cherukuri AR and Palis J (2013) Erythropoietin critically regulates murine and human primitive erythroblast survival and terminal maturation. Haematologica 98, 1778–1787.
21. Shivdasani RA, Mayer EL and Orkin SH (1995) Absence of blood formation in mice lacking T-cell leukemia oncoprotein tal-1/SCL. Nature 373, 432–434.
22. Scialdone A, Tanaka Y, Jawaid W, Moignard V, Wilson NK, McCaulay IC, Marioni JC, Gottgens B. (2016) Resolving early mesoderm diversification through single-cell expression profiling. Nature 535, 289–293.
23. Tsang AP, Fujiwara Y, Hom DB and Orkin SH (1998) Failure of megakaryopoiesis and arrested erythropoiesis in mice lacking the GATA-1 transcriptional cofactor FOG. Genes Dev 15, 1176–1188.
24. Fujiwara Y, Browne CP, Cunniff K, Goff SC and Orkin SH (1996) Arrested development of embryonic red cell precursors in mouse embryos lacking transcription factor GATA-1. Proc Natl Acad Sci USA 93, 12355–12358.
25. Warren AJ, Colledge WH, Carlton MB, Evans MJ, Smith AJ and Rabbitts TH (1994) The oncogenic cysteine-rich LIM domain protein is essential for erythroid development. Cell 78, 45–57.
26. Mukhopadhyay M, Teufel A, Yamashita T, Agulnick AD, Chen L, Downs KM, Schindler A, Grinberg A, Huang SP, Dorward D et al. (2003) Functional ablation of the mouse Ldb1 gene results in severe patterning defects during gastrulation. Development 130, 495–505.
27. Drissen R, von Lindern M, Kolbus A, Driegen S, Steinlein P, Beug H, Grosveld F and Philipsen S et al. (2005) The erythroid phenotype of EKLF-null mice: defects in hemoglobin metabolism and membrane stability. Mol Cell Biol 25, 5205–5214.
28. Hodge D, Coghill E, Keys J, Maguire T, Hartmann B, McDowall A, Weiss M, Grimmond S and Perkins A (2006) A global role for EKLF in definitive and primitive erythropoiesis. Blood 107, 3359–3370.
29. Yokomizo T, Hasegawa K, Ishitobi H, Osato M, Ema M, Ito Y, Yamamoto and Takahashi S (2008) Runx1 is involved in primitive erythropoiesis in the mouse. Blood 111, 4075–4080.
30. Basu P, Morris PE, Haar JL, Wani MA, Lingrel JB, Gaensler KM and Lloyd JA (2005) KLF2 is essential for primitive erythropoiesis and regulates the human and murine embryonic beta-like globin genes in vivo. Blood 106, 2566–2571.
31. Vinjamur DS, Wade KJ, Mohamad SF, Haar JL, Sawyer ST and Lloyd JA (2014) Krüppel-like transcription factors KLF1 and KLF2 have unique and coordinate roles in regulating embryonic erythroid precursor maturation. Haematologica 99, 1565–1573.
32. McGrath KE, Frame JM, Fromm GJ, Koniski AD, Kingsley PD, Little J, Bulger M and Palis J (2011) A transient definitive erythroid lineage with unique regulation of the beta-globin locus in the mammalian embryo. Blood 117, 4600–4608.
33. Lux CT, Yoshimoto M, McGrath K, Conway SJ, Palis J and Yoder MC (2008) All primitive and definitive hematopoietic progenitor cells emerging before E10 in the mouse embryo are products of the yolk sac. Blood 111, 3434–3438.
34. Mucenski ML, McLain K, Kier AB, Swerdlow SH, Schreiner CM, Miller TA, Pietryga DW, Scott WJ Jr and Potter SS (1991) A functional c-myb gene is required for noMmal murine fetal hepatic hematopoiesis. Cell 65, 677–689.
35. Yi Z, Cohen-Barak O, Hagiwara N, Kingsley PD, Fuch D, Erickson D, Epner E, Palis J and Brilliant M (2006) Sox6 directly silences epsilon globin expression in definitive erythropoiesis. PLoS Genet 2, e14.
36. Dumitriu B, Patrick MR, Petschek JP, Cherukuri S, Klingmuller U, Fox PL and Lefebvre V (2006) Sox6 cell-autonomously stimulates erythroid cell survival, proliferation, and terminal maturation and is thereby an important enhancer of definitive erythropoiesis during mouse development. Blood 108, 1198–1207.
37. Sankaran VG, Xu J, Ragoczy T, Ippolito GC, Walkley CR, Maika SD, Fujiwara Y, Ito M, Groudine M, Bender MA et al. (2009) Developmental and species-divergent globin switching are driven by BCL11A. Nature 460, 1093–1097.
38. Xu MJ, Matsuoka S, Yang FC, Ebihara Y, Manabe A, Tanaka R, Eguchi M, Asano S, Nakahata T and Tsuji K (2001) Evidence for the presence of murine primitive megakaryocytopoiesis in the early yolk sac. Blood 97, 2016–2022.
39. Tober J, Koniski A, McGrath KE, Vemishetti R, Emerson R, de Mesy-Bentley KK, Waugh R and Palis J (2007) The megakaryocyte lineage originates from hemangioblast precursors and is an integral component both of primitive and definitive hematopoiesis. Blood 109, 1433–1441.
40. Potts KS, Sargeant TJ, Markham JF, Shi W, Biben C, Josefsson EC, Whitehead LW, Rogers KL, Liakhovitskaia A, Smyth A et al. (2014) A lineage of diploid platelet-forming cells precedes polyploid megakaryocyte formation in the mouse embryo. Blood 124, 2725–2729.
41. Xie X, Chan RJ, Johnson SA, Starr M, McCarthy J, Kapur R and Yoder MC (2003) Thrombopoietin promotes mixed lineage and megakaryocytic colony-forming cell growth but inhibits primitive and definitive erythropoiesis in cells isolated from early murine yolk sacs. Blood 101, 1329–1335.
42. Gurney AL, Carver-Moore K, de Sauvage FJ and Moore MW (1994) Thrombocytopenia in c-mpl-deficient mice. Science 265, 1445–1447.
43. Potts KS, Sargeant TJ, Dawson CA, Josefsson EC, Hilton DJ, Alexander WS and Taoudi S (2015) Mouse prenatal platelet-forming lineages share a core transcriptional program but divergent dependence on MPL. Blood 126, 807–816.
44. De Cuyper IM, Meinders M, van de Vijver E, de Korte D, Porcelijn L, de Haas M, Eble JA, Seeger K, Rutella S, Pagliara D et al. (2013) A novel flow cytometry-based platelet aggregation assay. Blood 121, e70–e80.
45. Bertozzi CC, Schmaier AA, Mericko P, Hess PR, Zou Z, Chen M, Chen CY, Xu B, Lu MM, Zhou D et al. (2010) Platelets regulate lymphatic vascular development through CLEC-2-SLP-76 signaling. Blood 116, 661–670.
46. Carramolino L, Fuentes J, Garcia-Andres C, Azcoitia V, Riethmacher D and Torres M (2010) Platelets play an essential role in separating the blood and lymphatic vasculatures during embryonic angiogenesis. Circ Res 106, 1197–1201.
47. Moore MA and Metcalf D (1970) Ontogeny of the haematopoietic system: yolk sac origin of in vivo and in vitro colony forming cells in the developing embryo. Br J Haematol 18, 279–296.
48. Palis J, Chan RJ, Koniski A, Patel R, Starr M and Yoder MC (2001) Spatial and temporal emergence of high proliferative potential hematopoietic precursors during murine embryogenesis. Proc Natl Acad Sci USA 98, 4528–4533.
49. Bradley TR and Hodgson GS (1979) Detection of primitive macrophage progenitor cells in mouse bone marrow. Blood 54, 1446–1450.
50. McGrath KE, Frame JM, Fegan KM, Bowen JR, Conway SJ, Catherman SC, Kingsley PD, Koniski AD and Palis J (2015) Distinct sources of hematopoietic progenitors emerge before HSC and provide functional blood cells in the mammalian embryo. Cell Rep 11, 1892–1904.
51. Takahashi K, Yamamura F and Naito M (1989) Differentiation, maturation, and proliferation of macrophages in the mouse yolk sac: a light-microscopic, enzyme-cytochemical, immunohistochemical, and ultrastructural study. J Leukoc Biol 45, 87–96.
52. Morris L, Graham CF and Gordon S (1991) Macrophages in haemopoietic and other tissues of the developing mouse detected by the monoclonal antibody F4/80. Development 112, 517–526.
53. Hume DA, Monkley SJ and Wainwright BJ (1995) Detection of c-fms protooncogene in early mouse embryos by whole mount in situ hybridization indicates roles for macrophages in tissue remodelling. Br J Haematol 90, 939–942.
54. Naito M, Yamamura F, Nishikawa S and Takahashi K (1989) Development, differentiation, and maturation of fetal mouse yolk sac macrophages in cultures. J Leukoc Biol 46, 1–10.
55. Gautier EL, Shay T, Miller J, Greter M, Jakubzick C, Ivanov S, Helft J, Chow A, Elpek KG, Gordonov S et al. (2012) Gene expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat Immunol 13, 1118–1128.
56. Gosselin D, Link VM, Romanoski CE, Fonseca GJ, Eichenfield DZ, Spann NJ, Stender JD, Chun HB, Garner H, Geissmann F et al. (2014) Environment drives selection and function of enhancers controlling tissue-specific macrophage identities. Cell 159, 1327–1340.
57. Mass E, Ballesteros I, Farlik M, Halbritter F, Günther P, Crozet L, Jacome-Galarza CE, Handler K, Klughammer J, Kobayashi Y et al. (2016) Specification of tissue-resident macrophages during organogenesis. Science 9, 353. pii: aaf4238.
58. Soucie EL, Weng Z, Geirsdóttir L, Molawi K, Maurizio J, Fenouil R, Mossadegh-Keller N, Gimenez G, VanHille L, Beniazza M et al. (2016) Lineage-specific enhancers activate self-renewal genes in macrophages and embryonic stem cells. Science 351, aad5510.
59. McGrath KE, Frame JM and Palis J (2015) Early hematopoiesis and macrophage development. Semin Immunol 7, 379–387.
60. Paluru P, Hudock KM, Cheng X, Mills JA, Ying L, Galvao AM, Lu L, Tiyaboonchai A, Sim X, Sullivan SK et al. (2014) The negative impact of Wnt signaling on megakaryocyte and primitive erythroid progenitors derived from human embryonic stem cells. Stem Cell Res 12, 441–451.
61. Ferkowicz MJ, Starr M, Xie X, Li W, Johnson SA, Shelley WC, Morrison PR and Yoder MC (2003) CD41 expression defines the onset of primitive and definitive hematopoiesis in the murine embryo. Development 130, 4393–4403.
62. Mikkola HKA, Fujiwara Y, Schlaeger TM, Traver D and Orkin SH (2003) Expression of CD41 marks the initiation of definitive hematopoiesis in the mouse embryo. Blood 101, 508–516.
63. Bertrand JY, Jalil A, Klaine M, Jung S, Cumano A and Godin I (2005) Three pathways to mature macrophages in the early yolk sac. Blood 106, 3004–3011.
64. Chen MJ, Li Y, De Obaldia ME, Yang Q, Yzaguirre AD, Yamada-Inagawa T, Vink CS, Bhandoola A, Dzierzak E and Speck NA (2011) Erythroid/myeloid progenitors and hematopoietic stem cells originate from distinct populations of endothelial cells. Cell Stem Cell 9, 541–552.
65. Choi K, Kennedy M, Kazarov A, Papadimitriou JC and Keller G (1998) A common precursor for hematopoietic and endothelial cells. Development 125, 725–732.
66. Huber TL, Kouskoff V, Fehling HJ, Palis J and Keller G (2004) Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature 432, 625–630.
67. Ueno H and Weissman IL (2006) Clonal analysis of mouse development reveals a polyclonal origin for yolk sac blood islands. Dev Cell 11, 519–533.
68. Padrón-Barthe L, Temiño S, Villa del Campo C, Carramolino L, Isern J and Torres M (2014) Clonal analysis identifies hemogenic endothelium as the source of the blood-endothelial common lineage in the mouse embryo. Blood 124, 2523–2532.
69. Li W, Ferkowicz MJ, Johnson SA, Shelley WC and Yoder MC (2005) Endothelial cells in the early murine yolk sac give rise to CD41-expressing hematopoietic cells. Stem Cells Dev 14, 44–54.
70. Frame JM, Fegan KH, Conway S, McGrath KE and Palis J (2015) Definitive hematopoiesis in the yolk sac emerges from Wnt-responsive hemogenic endothelium independently of circulation and arterio-venous identity. Stem Cells 34, 431–434.
71. Okuda T, van Deursen J, Hiebert SW, Grosveld G and Downing JR (1996) AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell 84, 321–330.
72. Hadland BK, Huppert SS, Kanungo J, Xue Y, Jiang R, Gridley T, Conlon RA, Cheng AM, Kopan R and Longmore GD (2004) A requirement for Notch1 distinguishes 2 phases of definitive hematopoiesis during development. Blood 104, 3097–3105.
73. Keller G, Kennedy M, Papayannopoulou T and Wiles MV (1993) Hematopoietic commitment during embryonic stem cell differentiation in culture. Mol Cell Biol 13, 473–486.
74. Fujimoto TT, Kohata S, Suzuki H, Miyazaki H and Fujimura K (2003) Production of functional platelets by differentiated embryonic stem (ES) cells in vitro. Blood 102, 4044–4051.
75. Kennedy Kennedy M, D'Souza SL, Lynch-Kattman M, Schwantz S and Keller G (2007) Development of the hemangioblast defines the onset of hematopoiesis in human ES cell differentiation cultures. Blood 109, 2679–2687.
76. Zambidis ET, Peault B, Park TS, Bunz F and Civin CI (2005) Hematopoietic differentiation of human embryonic stem cells progresses through sequential hematoendothelial, primitive, and definitive stages resembling human yolk sac development. Blood 106, 860–870.
77. Klimchenko O, Mori M, Distefano A, Langlois T, Larbret F, Lecluse Y, Feraud O, Vainchenker W, Norol F and Debili N (2009) A common bipotent progenitor generates the erythroid and megakaryocyte lineages in embryonic stem cell-derived primitive hematopoiesis. Blood 114, 1506–1517.
78. North TE, Goessling W, Peeters M, Li P, Ceol C, Lord AM, Weber GJ, Harris J, Cutting CC, Huang P et al. (2009) Hematopoietic stem cell development is dependent on blood flow. Cell 137, 736–748.
79. Li Y, Esain V, Teng L, Xu J, Kwan W, Frost IM, Yzaguirre AD, Cai X, Cortes M, Maijenburg MW et al. (2014) Inflammatory signaling regulates embryonic hematopoietic stem and progenitor cell production. Genes Dev 28, 2597–2612.