FoxO1 is required in endothelial but not myocardial cell lineages during cardiovascular development

Developmental Dynamics

Volumn 241, Issue 4, 2012, Pages 803-813

  Sengupta, Arunima ^a   Chakraborty, Santanu ^a   Paik, Jihye ^b   Yutzey, Katherine E ^a   Evans Anderson, Heather J ^c  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c WINTHROP UNIVERSITY   (United States)

Author keywords

Cardiac myocyte proliferation; Differentiation; Endothelial cells; Forkhead

Indexed keywords

TRANSCRIPTION FACTOR FKHR;

ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; EMBRYO; ENDOTHELIUM CELL; HEART DEVELOPMENT; HEART MUSCLE CELL; LOSS OF FUNCTION MUTATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; VASCULARIZATION;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; ENDOTHELIUM, VASCULAR; FORKHEAD TRANSCRIPTION FACTORS; GENE KNOCKDOWN TECHNIQUES; HEART; MICE; MYOCYTES, CARDIAC; ORGAN SPECIFICITY;

EID: 84858228682     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.23759     Document Type: Article

References (35)

1. Abid MR, Shih SC, Otu HH, Spokes KC, Okada Y, Curiel DT, Minami T, Aird WC. 2006. A novel class of vascular endothelial growth factor-responsive genes that require forkhead activity for expression. J Biol Chem 281: 35544-35553.
2. Bastide B, Neyses L, Ganten D, Paul M, Willecke K, Traub O. 1993. Gap junction protein connexin40 is preferentially expressed in vascular endothelium and conductive bundles of rat myocardium and is increased under hypertensive conditions. Circ Res 73: 1138-1149.
3. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96: 857-868.
4. Calnan DR, Brunet A. 2008. The FoxO code. Oncogene 27: 2276-2288.
5. Chakraborty S, Wirrig EE, Hinton RB, Merrill WH, Spicer DB, Yutzey KE. 2010. Twist1 promotes heart valve cell proliferation and extracellular matrix gene expression during development in vivo and is expressed in human diseased aortic valves. Dev Biol 347: 167-179.
6. Combs MD, Yutzey KE. 2009. Heart valve development: regulatory networks in development and disease. Circ Res 105: 408-421.
7. Conway SJ, Kruzynska-Frejtag A, Kneer PL, Machnicki M, Koushik SV. 2003. What cardiovascular defect does my prenatal mouse mutant have, and why? Genesis 35: 1-21.
8. de Lange WJ, Halabi CM, Beyer AM, Sigmund CD. 2008. Germ line activation of the Tie2 and SMMHC promoters causes noncell-specific deletion of floxed alleles. Physiol Genomics 35: 1-4.
9. De Val S, Black BL. 2009. Transcriptional control of endothelial cell development. Dev Cell 16: 180-195.
10. Evans-Anderson HJ, Alfieri CM, Yutzey KE. 2008. Regulation of cardiomyocyte proliferation and myocardial growth during development by FOXO transcription factors. Circ Res 102: 686-694.
11. Feng Q, Di R, Tao F, Chang Z, Lu S, Fan W, Shan C, Li X, Yang Z. 2010. PDK1 regulates vascular remodeling and promotes epithelial-mesenchymal transition in cardiac development. Mol Cell Biol 30: 3711-3721.
12. Ferdous A, Morris J, Abedin MJ, Collins S, Richardson JA, Hill JA. 2011. Forkhead factor FoxO1 is essential for placental morphogenesis in the developing embryo. Proc Natl Acad Sci USA 108: 16307-16312.
13. Furuyama T, Kitayama K, Yamashita H, Mori N. 2003. Forkhead transcription factor FOXO1 (FKHR)-dependent induction of PDK4 gene expression in skeletal muscle during energy deprivation. Biochem J 375: 365-371.
14. Furuyama T, Kitayama K, Shimoda Y, Ogawa M, Sone K, Yoshida-Araki K, HIsatsune H, Nishikawa S, Nakayama K, Nakayama K, Idkda K, Motoyama N, Mori N. 2004. Abnormal angiogenesis in FOXO1 (Fkhr)-deficient mice. J Biol Chem 279: 34741-34749.
15. Grego-Bessa J, Diez J, Timmerman L, de la Pompa JL. 2004. Notch and epithelial-mesenchyme transition in development and tumor progression: another turn of the screw. Cell Cycle 3: 718-721.
16. Hosaka T, Biggs WH, III, Tieu D, Boyer AD, Varki NM, Cavenee WK, Arden KC. 2004. Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification. Proc Natl Acad Sci USA 101: 2975-2980.
17. Kisanuki YY, Hammer RE, Miyazaki J, Williams SC, Richardson JA, Yanagisawa M. 2001. Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev Biol 230: 230-242.
18. Kitamura T, Kitamura YI, Funahashi Y, Shawber CJ, Castrillon DH, Kollipara R, DePinho RA, Kitajewski J, Accili D. 2007. A Foxo/Notch pathway controls myogenic differentiation and fiber type specification. J Clin Invest 117: 2477-2485.
19. Lee JW, Chen H, Pullikotil P, Quon MJ. 2011. Protein kinase A-{alpha} directly phosphorylates FoxO1 in vascular endothelial cells to regulate expression of vascular cellular adhesion molecule-1 mRNA. J Biol Chem 286: 6423-6432.
20. Ma L, Lu MF, Schwartz RJ, Martin JF. 2005. Bmp2 is essential for cardiac cushion epithelial-mesenchymal transition and myocardial patterning. Development 132: 5601-5611.
21. Matsukawa M, Sakamoto H, Kawasuji M, Furuyama T, Ogawa M. 2009. Different roles of Foxo1 and Foxo3 in the control of endothelial cell morphology. Genes Cells 14: 1167-1181.
22. Misfeldt AM, Boyle SC, Tompkins KL, Bautch VL, Labosky PA, Baldwin HS. 2009. Endocardial cells are a distinct endothelial lineage derived from Flk1+ multipotent cardiovascular progenitors. Dev Biol 333: 78-89.
23. Morgan SM, Samulowitz U, Darley L, Simmons DL, Vestweber D. 1999. Biochemical characterization and molecular cloning of a novel endothelial-specific sialomucin. Blood 93: 165-175.
24. Paik JH, Kollipara R, Chu G, Ji H, Xiao Y, Ding Z, Miao L, Tothova Z, Horner JW, Carrasco DR, Jiang S, Gilliland DG, Chin L, Wong WH, Castrillon DH, DePinho RA. 2007. FoxOs are lineage-restricted redundant tumor suppressors and regulate endothelial cell homeostasis. Cell 128: 309-323.
25. Palermo J, Gulick J, Colbert M, Fewell J, Robbins J. 1996. Transgenic remodeling of the contractile apparatus in the mammalian heart. Circ Res 78: 504-509.
26. Papanicolaou KN, Izumiya Y, Walsh K. 2008. Forkhead transcription factors and cardiovascular biology. Circ Res 102: 16-31.
27. Park SH, Sakamoto H, Tsuji-Tamura K, Furuyama T, Ogawa M. 2009. Foxo1 is essential for in vitro vascular formation from embryonic stem cells. Biochem Biophys Res Commun 390: 861-866.
28. Parsons SA, Millay DP, Wilkins BJ, Bueno OF, Tsika GL, Neilson JR, Liberatore CM, Yutzey KE, Crabtree GR, Tsika RW, Molkentin JD. 2004. Genetic loss of calcineurin blocks mechanical overload-induced skeletal muscle fiber type switching but not hypertrophy. J Biol Chem 279: 26192-26200.
29. Potente M, Urbich C, Sasaki K, Hofmann WK, Heeschen C, Aicher A, Kollipara R, DePinho RA, Zeiher AM, Dimmeler S. 2005. Involvement of Foxo transcription factors in angiogenesis and postnatal neovascularization. J Clin Invest 115: 2382-2392.
30. Sengupta A, Molkentin JD, Paik JH, DePinho RA, Yutzey KE. 2011. FoxO transcription factors promote cardiomyocyte survival upon induction of oxidative stress. J Biol Chem 286: 7468-7478.
31. Smith TK, Bader DM. 2007. Signals from both sides: Control of cardiac development by the endocardium and epicardium. Semin Cell Dev Biol 18: 84-89.
32. Timmerman LA, Grego-Bessa J, Raya A, Bertran E, Perez-Pomares JM, Diez J, Aranda S, Palomo S, McCormick F, Izpisua-Belmonte JC, de la Pompa JL. 2004. Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation. Genes Dev 18: 99-115.
33. Tirziu D, Simons M. 2009. Endothelium as master regulator of organ development and growth. Vascul Pharmacol 50: 1-7.
34. Wagner M, Siddiqui MA. 2007. Signal transduction in early heart development (II): ventricular chamber specification, trabeculation, and heart valve formation. Exp Biol Med (Maywood) 232: 866-880.
35. Warren CM, Iruela-Arispe ML. 2010. Signaling circuitry in vascular morphogenesis. Curr Opin Hematol 17: 213-218.