Temporal changes in Hox gene expression accompany endothelial cell differentiation of embryonic stem cells

Cell Adhesion and Migration

Volumn 5, Issue 2, 2011, Pages 133-141

  Bahrami, S Bahram ^a   Veiseh, Mandana ^b   Dunn, Ashley A ^a   Boudreau, Nancy J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Embryonic stem cell differentiation; Endothelial cells; Hox gene expression

Indexed keywords

BETA3 INTEGRIN; HOMEODOMAIN PROTEIN; MATRIX METALLOPROTEINASE 14; THROMBOSPONDIN 2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HOXA3; TRANSCRIPTION FACTOR HOXA5; TRANSCRIPTION FACTOR HOXD10; TRANSCRIPTION FACTOR HOXD3; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL INVASION; CELL MATURATION; CELL MIGRATION; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; GENE EXPRESSION; HOX GENE; MOUSE; NONHUMAN; PHENOTYPE; PLURIPOTENT STEM CELL; UPREGULATION;

EID: 79952341940     PISSN: 19336918     EISSN: 19336926     Source Type: Journal    
DOI: 10.4161/cam.5.2.14373     Document Type: Article

References (55)

1. Ema M, Rossant J. Cell fate decisions in early blood vessel formation. Trends Cardiovasc Med 2003; 13:254-9. (Pubitemid 36960174)
2. Carmeliet P. Blood vessels and nerves: common signals, pathways and diseases. Nat Rev Genet 2003; 4:710-20. (Pubitemid 37046138)
3. Wigle JT, Oliver G. Prox1 function is required for the development of the murine lymphatic system. Cell 1999; 98:769-78. (Pubitemid 29446894)
4. Cantile M, Schiavo G, Terracciano L, Cillo C. Homeobox genes in normal and abnormal vasculogenesis. Nutr Metab Cardiovasc Dis 2008; 18:651-8.
5. Choi K. The hemangioblast: a common progenitor of hematopoietic and endothelial cells. J Hematother Stem Cell Res 2002; 11:91-101. (Pubitemid 34163773)
6. Lacaud G, Keller G, Kouskoff V. Tracking mesoderm formation and specification to the hemangioblast in vitro. Trends Cardiovasc Med 2004; 14:314-7. (Pubitemid 41110610)
7. Vogeli KM, Jin SW, Martin GR, Stainier DY. A common progenitor for haematopoietic and endothelial lineages in the zebrafish gastrula. Nature 2006; 443:337-9. (Pubitemid 44435152)
8. Lugus JJ, Park C, Choi K. Developmental relationship between hematopoietic and endothelial cells. Immunol Res 2005; 32:57-74. (Pubitemid 41153614)
9. Tang DG, Conti CJ. Endothelial cell development, vasculogenesis, angiogenesis and tumor neovascularization: an update. Semin Thromb Hemost 2004; 30:109-17. (Pubitemid 38457305)
10. Jakobsson L, Kreuger J, Claesson-Welsh L. Building blood vessels - stem cell models in vascular biology. J Cell Biol 2007; 177:751-5. (Pubitemid 46873082)
11. Wang L. Endothelial and hematopoietic cell fate of human embryonic stem cells. Trends Cardiovasc Med 2006; 16:89-94.
12. Blancas AA, Lauer NE, McCloskey KE. Endothelial differentiation of embryonic stem cells. Curr Protoc Stem Cell Biol 2008; 1:5.
13. Doetschman TC, Eistetter H, Katz M, Schmidt W, Kemler R. The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol 1985; 87:27-45. (Pubitemid 15029925)
14. Messana JM, Hwang NS, Coburn J, Elisseeff JH, Zhang Z. Size of the embryoid body influences chondrogenesis of mouse embryonic stem cells. J Tissue Eng Regen Med 2008; 2:499-506.
15. Lu SJ, Hipp JA, Feng Q, Hipp JD, Lanza R, Atala A. GeneChip analysis of human embryonic stem cell differentiation into hemangioblasts: an in silico dissection of mixed phenotypes. Genome Biol 2007; 8:240.
16. Loring JF, Porter JG, Seilhammer J, Kaser MR, Wesselschmidt R. A gene expression profile of embryonic stem cells and embryonic stem cell-derived neurons. Restor Neurol Neurosci 2001; 18:81-8. (Pubitemid 33010629)
17. Martinez-Ceballos E, Chambon P, Gudas LJ. Differences in gene expression between wild type and Hoxa1 knockout embryonic stem cells after retinoic acid treatment or leukemia inhibitory factor (LIF) removal. J Biol Chem 2005; 280:16484-98. (Pubitemid 40616780)
18. Hansen SL, Myers CA, Charboneau A, Young DM, Boudreau N. HoxD3 accelerates wound healing in diabetic mice. Am J Pathol 2003; 163:2421-31. (Pubitemid 37466483)
19. Myers C, Charboneau A, Boudreau N. Homeobox B3 promotes capillary morphogenesis and angiogenesis. J Cell Biol 2000; 148:343-51. (Pubitemid 30078246)
20. Myers C, Charboneau A, Cheung I, Hanks D, Boudreau N. Sustained expression of homeobox D10 inhibits angiogenesis. Am J Pathol 2002; 161:2099-109. (Pubitemid 35434856)
21. Hansen SL, Young DM, Boudreau NJ. HoxD3 expression and collagen synthesis in diabetic fibroblasts. Wound Repair Regen 2003; 11:474-80. (Pubitemid 37467731)
22. Boudreau NJ, Varner JA. The homeobox transcription factor Hox D3 promotes integrin alpha5beta1 expression and function during angiogenesis. J Biol Chem 2004; 279:4862-8. (Pubitemid 38199081)
23. Mace KA, Hansen SL, Myers C, Young DM, Boudreau N. HOXA3 induces cell migration in endothelial and epithelial cells promoting angiogenesis and wound repair. J Cell Sci 2005; 118:2567-77. (Pubitemid 40932883)
24. Uyeno LA, Newman-Keagle JA, Cheung I, Hunt TK, Young DM, Boudreau N. Hox D3 expression in normal and impaired wound healing. J Surg Res 2001; 100:46-56. (Pubitemid 32802702)
25. Rhoads K, Arderiu G, Charboneau A, Hansen SL, Hoffman W, Boudreau N. A role for Hox A5 in regulating angiogenesis and vascular patterning. Lymphat Res Biol 2005; 3:240-52. (Pubitemid 43115793)
26. Carrio M, Arderiu G, Myers C, Boudreau NJ. Homeobox D10 induces phenotypic reversion of breast tumor cells in a three-dimensional culture model. Cancer Res 2005; 65:7177-85. (Pubitemid 41161248)
27. McGinnis W, Krumlauf R. Homeobox genes and axial patterning. Cell 1992; 68:283-302.
28. Scott MP. Vertebrate homeobox gene nomenclature. Cell 1992; 71:551-3.
29. Gorski DH, Walsh K. The role of homeobox genes in vascular remodeling and angiogenesis. Circ Res 2000; 87:865-72.
30. Botas J. Control of morphogenesis and differentiation by HOM/Hox genes. Curr Opin Cell Biol 1993; 5:1015-22.
31. Boudreau N, Andrews C, Srebrow A, Ravanpay A, Cheresh DA. Induction of the angiogenic phenotype by Hox D3. J Cell Biol 1997; 139:257-64. (Pubitemid 27444096)
32. Arderiu G, Cuevas I, Chen A, Carrio M, East L, Boudreau NJ. HoxA5 stabilizes adherens junctions via increased Akt1. Cell Adh Migr 2007; 1:185-95.
33. Ezhkova E, Pasolli HA, Parker JS, Stokes N, Su IH, Hannon G, et al. Ezh2 orchestrates gene expression for the stepwise differentiation of tissue-specific stem cells. Cell 2009; 136:1122-35.
34. Wu X, Gong Y, Yue J, Qiang B, Yuan J, Peng X. Cooperation between EZH2, NSPc1-mediated histone H2A ubiquitination and Dnmt1 in HOX gene silencing. Nucleic Acids Res 2008; 36:3590-9.
35. Laible G, Haynes AR, Lebersorger A, O'Carroll D, Mattei MG, Denny P, et al. The murine polycombgroup genes Ezh1 and Ezh2 map close to Hox gene clusters on mouse chromosomes 11 and 6. Mamm Genome 1999; 10:311-4. (Pubitemid 29390523)
36. Loh YH, Wu Q, Chew JL, Vega VB, Zhang W, Chen X, et al. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 2006; 38:431-40.
37. Wang J, Rao S, Chu J, Shen X, Levasseur DN, Theunissen TW, et al. A protein interaction network for pluripotency of embryonic stem cells. Nature 2006; 444:364-8. (Pubitemid 44764111)
38. Chen D, Ji X, Harris MA, Feng JQ, Karsenty G, Celeste AJ, et al. Differential roles for bone morphogenetic protein (BMP) receptor type IB and IA in differentiation and specification of mesenchymal precursor cells to osteoblast and adipocyte lineages. J Cell Biol 1998; 142:295-305. (Pubitemid 28341159)
39. Mercati F, Pascucci L, Ceccarelli P, Dall'aglio C, Pedini V, Gargiulo AM. Expression of mesenchymal stem cell marker CD90 on dermal sheath cells of the anagen hair follicle in canine species. Eur J Histochem 2009; 53:159-66.
40. Ji L, Allen-Hoffmann BL, de Pablo JJ, Palecek SP. Generation and differentiation of human embryonic stem cell-derived keratinocyte precursors. Tissue Eng 2006; 12:665-79. (Pubitemid 43726512)
41. Mariappan D, Winkler J, Chen S, Schulz H, Hescheler J, Sachinidis A. Transcriptional profiling of CD31(+) cells isolated from murine embryonic stem cells. Genes Cells 2009; 14:243-60.
42. Ferreira LS, Gerecht S, Shieh HF, Watson N, Rupnick MA, Dallabrida SM, et al. Vascular progenitor cells isolated from human embryonic stem cells give rise to endothelial and smooth muscle like cells and form vascular networks in vivo. Circ Res 2007; 101:286-94. (Pubitemid 47344078)
43. Mace KA, Yu DH, Paydar KZ, Boudreau N, Young DM. Sustained expression of Hif-1alpha in the diabetic environment promotes angiogenesis and cutaneous wound repair. Wound Repair Regen 2007; 15:636-45. (Pubitemid 47493890)
44. Chung N, Jee BK, Chae SW, Jeon YW, Lee KH, Rha HK. HOX gene analysis of endothelial cell differentiation in human bone marrow-derived mesenchymal stem cells. Mol Biol Rep 2009; 36:227-35.
45. Ackema KB, Charite J. Mesenchymal stem cells from different organs are characterized by distinct topographic Hox codes. Stem Cells Dev 2008; 17:979-91.
46. Fuller JF, McAdara J, Yaron Y, Sakaguchi M, Fraser JK, Gasson JC. Characterization of HOX gene expression during myelopoiesis: role of HOX A5 in lineage commitment and maturation. Blood 1999; 93:3391-400. (Pubitemid 29220906)
47. Crooks GM, Fuller J, Petersen D, Izadi P, Malik P, Pattengale PK, et al. Constitutive HOXA5 expression inhibits erythropoiesis and increases myelopoiesis from human hematopoietic progenitors. Blood 1999; 94:519-28. (Pubitemid 29323866)
48. Aubin J, Dery U, Lemieux M, Chailler P, Jeannotte L. Stomach regional specification requires Hoxa5-driven mesenchymal-epithelial signaling. Development 2002; 129:4075-87. (Pubitemid 35012493)
49. Aubin J, Lemieux M, Tremblay M, Berard J, Jeannotte L. Early postnatal lethality in Hoxa-5 mutant mice is attributable to respiratory tract defects. Dev Biol 1997; 192:432-45. (Pubitemid 28066945)
50. Krieger KE, Abbott MA, Joksimovic M, Lueth PA, Sonea IM, Jeannotte L, et al. Transgenic mice ectopically expressing HOXA5 in the dorsal spinal cord show structural defects of the cervical spinal cord along with sensory and motor defects of the forelimb. Brain Res Dev Brain Res 2004; 150:125-39. (Pubitemid 38639817)
51. Mandeville I, Aubin J, LeBlanc M, Lalancette-Hebert M, Janelle MF, Tremblay GM, et al. Impact of the loss of Hoxa5 function on lung alveogenesis. Am J Pathol 2006; 169:1312-27. (Pubitemid 351194366)
52. Aubin J, Chailler P, Menard D, Jeannotte L. Loss of Hoxa5 gene function in mice perturbs intestinal maturation. Am J Physiol 1999; 277:965-73.
53. Thorsteinsdottir U, Mamo A, Kroon E, Jerome L, Bijl J, Lawrence HJ, et al. Overexpression of the myeloid leukemia-associated Hoxa9 gene in bone marrow cells induces stem cell expansion. Blood 2002; 99:121-9.
54. Lawrence HJ, Christensen J, Fong S, Hu YL, Weissman I, Sauvageau G, et al. Loss of expression of the Hoxa-9 homeobox gene impairs the proliferation and repopulating ability of hematopoietic stem cells. Blood 2005; 106:3988-94. (Pubitemid 41739043)
55. Taniguchi Y, Komatsu N, Moriuchi T. Overexpression of the HOX4A (HOXD3) homeobox gene in human erythroleukemia HEL cells results in altered adhesive properties. Blood 1995; 85:2786-94.