Acceleration of mesoderm development and expansion of hematopoietic progenitors in differentiating ES cells by the mouse Mix-like homeodomain transcription factor

Blood

Volumn 107, Issue 8, 2006, Pages 3122-3130

  Willey, Stephen ^b   Ayuso Sacido, Angel ^b   Zhang, Hailan ^b   Fraser, Stuart T ^b   Sahr, Kenneth E ^b   Adlam, Matthew J ^b   Kyba, Michael ^b   Daley, George Q ^b   Keller, Gordon ^b   Baron, Margaret H ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

HOMEODOMAIN PROTEIN; HOMEODOMAIN PROTEIN MMIX; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ACCELERATION; ANIMAL CELL; ARTICLE; BLOOD CELL; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; DEVELOPMENT; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; GENE; GENE ACTIVATION; GENE FUNCTION; GENE INDUCTION; GROWTH ACCELERATION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HOMEOBOX; MESODERM; MMIX GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

EID: 33645735014     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2005-10-4120     Document Type: Article

References (87)

1. Rossant J, Tam PPL. Mouse Development: Patterning, Morphogenesis, and Organogenesis. San Diego: Academic Press; 2002.
2. Epstein CJ, Erickson RP, Wynshaw-Boris A, eds. Inborn Errors of Development: The Molecular Basis of Clinical Disorders of Morphogenesis. New York, NY: Oxford University Press; 2004.
3. Tam PL, Behringer RR. Mouse gastrulation: the formation of a mammalian body plan. Mech Dev. 1997;68:3-25.
4. Lu CC, Brennan J, Robertson EJ. From fertilization to gastrulation: axis formation in the mouse embryo. Curr Opin Genet Develop. 2001;11:384-392.
5. Tam PP, Gad JM, Kinder SJ, Tsang TE, Behringer RR. Morphogenetic tissue movement and the establishment of body plan during development from blastocyst to gastrula in the mouse. Bioessays. 2001;23:508-517.
6. Shen MM, Pedersen RA. Developmental origins of the mammalian body plan. In: Epstein CJ, Erickson RP, Wynshaw-Boris A, eds. Inborn Errors of Development: The Molecular Basis of Clinical Disorders of Morphogenesis. New York, NY: Oxford University Press; 2004:53-66.
7. Lawson KA, Meneses JJ, Pedersen RA. Clonal analysis of epiblast fate during germ layer formation in the mouse embryo. Development. 1991;113:891-911.
8. Tam PPL, Beddington RSP. The formation of mesodermal tissues in the mouse embryo during gastrulation and early organogenesis. Development. 1987;99:109-126.
9. Kinder SJ, Loebel DA, Tam PP. Allocation and early differentiation of cardiovascular progenitors in the mouse embryo. Trends Cardiovasc Med. 2001;11:177-184.
10. Sun X, Meyers EN, Lewandoski M, Martin GR. Targeted disruption of Fgf8 causes failure of cell migration in the gastrulating mouse embryo. Genes Dev. 1999;13:1834-1846.
11. Rosa FM. Mix.1, a homebox mRNA inducible by mesoderm inducers, is expressed mostly in the presumptive endodermal cells of Xenopus embryos. Cell. 1989;57:965-974.
12. Vize P. DNA sequences mediating the transcriptional response of the Mix.2 homeobox gene to mesoderm induction. Dev Biol. 1996;177:226-231.
13. Huang H-C, Murtaugh LC, Vize PD, Whitman M. Identification of a potential regulator of early transcriptional responses to mesoderm inducers in the frog embryo. EMBO J. 1995;14:5965-5973.
14. Chen X, Rubock MJ, Whitman M. A transcriptional partner for MAD proteins in TGF-β signalling. Nature. 1996;383:691-696.
15. Chen X, Weisberg E, Fridmacher V, Watanabe M, Naco G, Whitman M. Smad4 and Fast-1 in the assembly of activin responsive factor. Nature. 1997;389:85-89.
16. Mead PE, Kelley CM, Hahn PS, Piedad O, Zon LI. SCL specifies hematopoietic mesoderm in Xenopus embryos. Development. 1998;125:2611-2620.
17. Ecochard V, Cayrol C, Rey S, et al. A novel Xenopus mix-like gene milk involved in the control of the endomesodermal fates. Development. 1998;125:2577-2585.
18. Henry GL, Melton DA. Mixer, a homeobox gene required for endoderm development. Science. 1998;281:91-96.
19. Lemaire P, Darras S, Caillol D, Kodjabachian L. A role for the vegetally expressed Xenopus gene Mix.1 in endoderm formation and in the restriction of mesoderm to the marginal zone. Development. 1998;125:2371-2380.
20. Tada M, Casey ES, Fairclough L, Smith JC. Bix1, a direct target of Xenopus T-box genes, causes formation of ventral mesoderm and endoderm. Development. 1998;125:3997-4006.
21. Alexander J, Stainier DY. A molecular pathway leading to endoderm formation in zebrafish. Curr Biol. 1999;9:1147-1157.
22. Kikuchi Y, Trinh LA, Reiter JF, Alexander J, Yelon D, Stainier DYR. The zebrafish bonnie and clyde gene encodes a Mix family homeodomain protein that regulates the generation of endodermal precursors. Genes Dev. 2000;14:1279-1289.
23. Reiter JF, Kikuchi Y, Stainier DYR. Multiple roles for Gata5 in zebrafish endoderm formation. Development. 2001;128:125-135.
24. Poulain M, Lepage T. Mezzo, a paired-like homeobox protein is an immediate target of Nodal signalling and regulates endoderm specification in zebrafish. Development. 2002;129:4901-4914.
25. Trinh LA, Meyer D, Stainier DY. The Mix family homeodomain gene bonnie and clyde functions with other components of the Nodal signaling pathway to regulate neural patterning in zebrafish. Development. 2003;130:4989-4998.
26. Mead PE, Brivanlou IH, Kelley CM, Zon LI. BMP-4-responsive regulation of dorsal-ventral patterning by the homeobox protein Mix.1. Nature. 1996;382:357-360.
27. Ng ES, Azzola L, Sourris K, Robb L, Stanley EG, Elefanty AG. The primitive streak gene Mixl1 is required for efficient haematopoiesis and BMP4-induced ventral mesoderm patterning in differentiating ES cells. Development. 2005;132:873-884.
28. Latinkic BV, Smith JC. Goosecoid and mix.1 repress Brachyury expression and are required for head formation in Xenopus. Development. 1999;126:1769-1779.
29. Sahr K, Dias D, Sanchez R, et al. Structure, upstream promoter region, and functional domains of a mouse and human Mix paired-like homeobox gene. Gene. 2002;291:135-147.
30. Peale FV, Sugden L, Bothwell M. Characterization of CMIX, a chicken homeobox gene related to the Xenopus gene mix1. Mech Dev. 1998;75:167-170.
31. Stein S, Roeser T, Kessel M. CMIX, a paired-type homeobox gene expressed before and during formation of the avian primitive streak. Mech Dev. 1998;75:163-165.
32. Pearce JJH, Evans MJ. Mml, a mouse Mix-like gene expressed in the primitive streak. Mech Dev. 1999;87:189-192.
33. Robb L, Hartley L, Begley CG, et al. Cloning, expression analysis, and chromosomal localization of murine and human homologues of a Xenopus mix gene. Dev Dyn. 2000;219:497-504.
34. Mohn D, Chen S, Dias D, et al. The mouse Mix gene is activated early during differentiation of ES and F9 stem cells and induces endoderm in frog embryos. Dev Dyn. 2003;226:446-459.
35. Hart AH, Hartley L, Sourris K, et al. Mixl1 is required for axial mesendoderm morphogenesis and patterning in the murine embryo. Development. 2002;129:3597-3608.
36. Keller G. Embryonic stem cell differentiation: emergence of a new era in biology and medicine. Genes Dev. 2005;19:1129-1155.
37. Choi K, Kennedy M, Kazarov A, Papadimitriou JC, Keller G. A common precursor for hematopoietic and endothelial cells. Development. 1998;125:725-732.
38. Robertson SM, Kennedy M, Shannon JM, Keller G. A transitional stage in the commitment of mesoderm to hematopoiesis requiring the transcription factor SCL/tal-1. Development. 2000;127:2447-2459.
39. Keller GA, Webb S, Kennedy M. Hematopoietic development of ES cells in culture. In: Klug CA, Jordan CT, eds. Hematopoietic Stem Cell Protocols. Totowa, NJ: Humana Press; 2001:209-230.
40. Fehling HJ, Lacaud G, Kubo A, et al. Tracking mesoderm induction and its specification to the hemangioblast during embryonic stem cell differentiation. Development. 2003;130:4217-4227.
41. Huber TL, Kouskoff V, Fehling HJ, Palis J, Keller G. Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature. 2004;432:625-630.
42. Kyba M, Perlingeiro RCR, Daley GQ. HoxB4 confers definitive lymphoid-myeloid engraftment potential on embryonic stem cell and yolk sac hematopoietic progenitors. Cell. 2002;109:29-37.
43. Dyer MA, Farrington SM, Mohn D, Munday JR, Baron MH. Indian hedgehog activates hematopoiesis and vasculogenesis and can respecify prospective neurectodermal cell fate in the mouse embryo. Development. 2001;128:1717-1730.
44. Kennedy M, Keller GM. Hematopoietic commitment of ES cells in culture. Methods Enzymol. 2003;365:39-59.
45. Baron MH, Mohn D. Mouse embryonic explant culture system for analysis of hematopoietic and vascular development. In: Baron MH, ed. Developmental Hematopoiesis: Methods and Protocols. Vol 105. Totowa, NJ: Humana Press; 2005:231-256.
46. Farrington SM, Belaoussoff M, Baron MH. Winged-Helix, Hedgehog and Bmp genes are differentially expressed in distinct cell layers of the murine yolk sac. Mech Dev. 1997;62:197-211.
47. Belaoussoff M, Farrington SM, Baron MH. Hematopoietic induction and respecification of A-P identity by visceral endoderm signaling in the mouse embryo. Development. 1998;125:5009-5018.
48. Rozen S, Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol. 2000;132:365-386.
49. Niswander L, Martin GR. Fgf-4 expression during gastrulation, myogenesis, limb and tooth development in the mouse. Development. 1992;114:755-768.
50. Blum M, Gaunt SJ, Cho KWY, et al. Gastrulation in the mouse: the role of the homeobox gene goosecoid. Cell. 1992;69:1097-1006.
51. Herrmann BG, Kispert A. The T genes in embryogenesis. Trends Genet. 1994;10:280-286.
52. Kispert A, Herrmann BG. Immunohistochemical analysis of the Brachyury protein in wild-type and mutant mouse embryos. Dev Biol. 1994;161:179-193.
53. Liu P, Wakamiya M, Shea MJ, Albrecht U, Behringer RR, Bradley A. Requirement for Wnt3 in vertebrate axis formation. Nat Genet. 1999;22:361-365.
54. Takada S, Stark K, Shea M, Vassileva G, McMahon J, McMahon A. Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev. 1994;8:174-189.
55. Wolf C, Thisse C, Stoetzel C, Thisse B, Gerlinger P, Perrin-Schmitt F. The M-twist gene of Mus is expressed in subsets of mesodermal cells and is closely related to the Xenopus X-twi and the Drosophila twist genes. Dev Biol. 1991;143:363-373.
56. Nieto MA, Gilardi-Hebenstreit P, Charnay P, Wilkinson DG. A receptor protein tyrosine kinase implicated in the segmental patterning of the hindbrain and mesoderm. Development. 1992;116:1137-1150.
57. Ang S-L, Wierda A, Wong D, et al. The formation and maintenance of the definitive endoderm lineage in the mouse: involvement of HNF3/forkhead proteins. Development. 1993;119:1301-1315.
58. Weinstein DC, Ruiz i Altaba A, Chen WS, et al. The winged-helix transcription factor HNF-3β is required for notochord development in the mouse embryo. Cell. 1994;78:575-588.
59. Dufort D, Schwartz L, Harpal K, Rossant J. The transcription factor HNF3β is required in visceral endoderm for normal primitive streak morphogenesis. Development. 1998;125:3015-3025.
60. Chapman DL, Agulnik I, Hancock S, Silver LM, Papaioannou VE. Tbx6, a mouse T-Box gene implicated in paraxial mesoderm formation at gastrulation. Dev Biol. 1996;180:534-542.
61. Candia AF, Hu J, Crosby J, et al. Mox-1 and Mox-2 define a novel homeobox gene subfamily and are differentially expressed during early mesodermal patterning in mouse embryos. Development. 1992;116:1123-1136.
62. Lints TJ, Parsons LM, Hartley L, Lyons I, Harvey RP. Nkx-2.5: a novel murine homeobox gene expressed in early heart progenitor cells and their myogenic descendants. Development. 1993;119:419-431.
63. North T, Gu TL, Stacy T, et al. Cbfa2 is required for the formation of intra-aortic hematopoietic clusters. Development. 1999;126:2563-2575.
64. Lacaud G, Kouskoff V, Trumble A, Schwantz S, Keller G. Haploinsufficiency of Runx1 results in the acceleration of mesodermal development and hemangioblast specification upon in vitro differentiation of ES cells. Blood. 2004;103:886-889.
65. Lacaud G, Gore L, Kennedy M, et al. Runx1 is essential for hematopoietic commitment at the hemangioblast stage of development in vitro. Blood. 2002;100:458-466.
66. Speck NA, Stacy T, Wang Q, et al. Core-binding factor: a central player in hematopoiesis and leukemia. Cancer Res. 1999;59(suppl 7):1789s-1793s.
67. North TE, de Bruijn MF, Stacy T, et al. Runx1 expression marks long-term repopulating hematopoietic stem cells in the midgestation mouse embryo. Immunity. 2002;16:661-672.
68. Ema M, Faloon P, Zhang WJ, et al. Combinatorial effects of Flk1 and Tal1 on vascular and hematopoietic development in the mouse. Genes Dev. 2003;17:380-393.
69. Park C, Afrikanova I, Chung YS, et al. A hierarchical order of factors in the generation of FLK1- and SCL-expressing hematopoietic and endothelial progenitors from embryonic stem cells. Development. 2004;131:2749-2762.
70. Davidson AJ, Ernst P, Wang Y, et al. Cdx4 mutants fail to specify blood progenitors and can be rescued by multiple hox genes. Nature. 2003;425:300-306.
71. Sauvageau G, Thorsteinsdottir U, Eaves C, et al. Overexpression of HOXB4 in hematopoietic cells causes the selective expansion of more primitive populations in vitro and in vivo. Genes Dev. 1995;9:1753-1765.
72. Antonchuk J, Sauvageau G, Humphries RK. HOXB4 overexpression mediates very rapid stem cell regeneration and competitive hematopoietic repopulation. Exp Hematol. 2001;29:1125-1134.
73. Bjornsson JM, Larsson N, Brun AC, et al. Reduced proliferative capacity of hematopoietic stem cells deficient in Hoxb3 and Hoxb4. Mol Cell Biol. 2003;23:3872-3883.
74. Brun AC, Bjornsson JM, Magnusson M, et al. Hoxb4-deficient mice undergo normal hematopoietic development but exhibit a mild proliferation defect in hematopoietic stem cells. Blood. 2004;103:4126-4133.
75. Cantor AB, Orkin SH. Hematopoietic development: a balancing act. Curr Opin Genet Dev. 2001;11:513-519.
76. Baumann CI, Bailey AS, Li W, Ferkowicz MJ, Yoder MC, Fleming WH. PECAM-1 is expressed on hematopoietic stem cells throughout ontogeny and identifies a population of erythroid progenitors. Blood. 2004;104:1010-1016.
77. Chung YS, Zhang WJ, Arentson E, Kingsley PD, Palis J, Choi K. Lineage analysis of the hemangioblast as defined by FLK1 and SCL expression. Development. 2002;129:5511-5520.
78. Hosler BA, LaRosa GJ, Grippo JF, Gudas LJ. Expression of REX-1, a gene containing zinc finger motifs, is rapidly reduced by retinoic acid in F9 teratocarcinoma cells. Mol Cell Biol. 1989;9:5623-5629.
79. Rogers MB, Hosler BA, Gudas LJ. Specific expression of a retinoic acid-regulated, zinc-finger gene, Rex-1, in preimplantation embryos, trophoblast and spermatocytes. Development. 1991;113:815-824.
80. Sato N, Meijer L, Skaltsounis L, Greengard P, Brivanlou AH. Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med. 2004;10:55-63.
81. Goolsby J, Marty MC, Heletz D, et al. Hematopoietic progenitors express neural genes. Proc Natl Acad Sci U S A. 2003;100:14926-14931.
82. D'Ippolito G, Diabira S, Howard GA, Menei P, Roos BA, Schiller PC. Marrow-isolated adult multilineage inducible (MIAMI) cells, a unique population of postnatal young and old human cells with extensive expansion and differentiation potential. J Cell Sci. 2004;117:2971-2981.
83. Baal N, Reisinger K, Jahr H, et al. Expression of transcription factor Oct-4 and other embryonic genes in CD133 positive cells from human umbilical cord blood. Thromb Haemost. 2004;92:767-775.
84. Yin Y, Que J, Teh M, Cao WP, El Oakley RM, Lim SK. Embryonic cell lines with endothelial potential: an in vitro system for studying endothelial differentiation. Arterioscler Thromb Vasc Biol. 2004;24:691-696.
85. Ben-Shushan E, Thompson JR, Gudas LJ, Bergman Y. Rex-1, a gene encoding a transcription factor expressed in the early embryo, is regulated via Oct-3/4 and Oct-6 binding to an octamer site and a novel protein, Rox-1, binding to an adjacent site. Mol Cell Biol. 1998;18:1866-1878.
86. Du Z, Cong H, Yao Z. Identification of putative downstream genes of Oct-4 by suppression-subtractive hybridization. Biochem Biophys Res Commun. 2001;282:701-706.
87. Guo W, Chan AP, Liang H, et al. A human Mix-like homeobox gene MIXL shows functional similarity to Xenopus Mix.1. Blood. 2002;100:89-95.