Cardiac outflow tract development relies on the complex function of Sox4 and Sox11 in multiple cell types

Cellular and Molecular Life Sciences

Volumn 71, Issue 15, 2014, Pages 2931-2945

  Paul, Mandy H ^a   Harvey, Richard P ^b,c   Wegner, Michael ^a   Sock, Elisabeth ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b VICTOR CHANG CARDIAC RESEARCH INSTITUTE   (Australia)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Cardiac gene regulatory network; Common arterial trunk; Double outlet right ventricle; Neural crest; Sox factors

Indexed keywords

TRANSCRIPTION FACTOR SOX11; TRANSCRIPTION FACTOR SOX4;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTERIAL TRUNK; ARTICLE; CARDIAC OUTFLOW TRACT DEVELOPMENT; CELL ADHESION; CELL INTERACTION; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CELL TYPE; CONGENITAL HEART MALFORMATION; CONTROLLED STUDY; EMBRYO; ENZYME REGULATION; EXTRACELLULAR MATRIX; HEART DEVELOPMENT; HEART RIGHT VENTRICLE; HUMAN; HUMAN CELL; MESODERM; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL CREST; NEURAL TUBE; NONHUMAN; PROTEIN DEPLETION; PROTEIN FUNCTION;

ANIMALS; CELL LINE; GENE DELETION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART; HEART DEFECTS, CONGENITAL; HUMANS; MICE; MICE, INBRED C57BL; NEURAL CREST; SOXC TRANSCRIPTION FACTORS;

EID: 84904385694     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-013-1523-x     Document Type: Article

References (47)

1. Hoffman JI, Kaplan S (2002) The incidence of congenital heart disease. J Am Coll Cardiol 39:1890-1900 (Pubitemid 34628268)
2. Webb S, Qayyum SR, Anderson RH, Lamers WH, Richardson MK (2003) Septation and separation within the outflow tract of the developing heart. J Anat 202:327-342 (Pubitemid 36582300)
3. Snider P, Olaopa M, Firulli AB, Conway SJ (2007) Cardiovascular development and the colonizing cardiac neural crest lineage. Sci World J 7:1090-1113 (Pubitemid 47036152)
4. Srivastava D (2006) Making or breaking the heart: from lineage determination to morphogenesis. Cell 126:1037-1048
5. Kodo K, Yamagishi H (2011) A decade of advances in the molecular embryology and genetics underlying congenital heart defects. Circ J 75:2296-2304
6. Schilham MW, Oosterwegel MA, Moerer P, Ya J, Deboer PAJ, Vandewetering M, Verbeek S, Lamers WH, Kruisbeek AM, Cumano A, Clevers H (1996) Defects in cardiac outflow tract formation and pro-B-lymphocyte expansion in mice lacking Sox-4. Nature 380:711-714 (Pubitemid 26125470)
7. Sock E, Rettig SD, Enderich J, Bösl MR, Tamm ER, Wegner M (2004) Gene targeting reveals a widespread role for the high-mobility-group transcription factor Sox11 in tissue remodeling. Mol Cell Biol 24:6635-6644 (Pubitemid 38944343)
8. Thein DC, Thalhammer JM, Hartwig AC, Crenshaw EB 3rd, Lefebvre V, Wegner M, Sock E (2010) The closely related transcription factors Sox4 and Sox11 function as survival factors during spinal cord development. J Neurochem 115:131-141
9. Wegner M (1999) From head to toes: the multiple facets of Sox proteins. Nucleic Acids Res 27:1409-1420
10. Bhattaram P, Penzo-Méndez A, Sock E, Colmenares C, Kaneko KJ, DePamphilis ML, Wegner M, Lefebvre V (2010) Organogenesis relies on Sox4, Sox11, and Sox12 for survival of neural and mesenchymal progenitor cells. Nat Commun 1:9
11. Penzo-Mendez A, Dy P, Pallavi B, Lefebvre V (2007) Generation of mice harboring a Sox4 conditional null allele. Genesis 45:776-780 (Pubitemid 351158380)
12. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, Jessell TM, Costantini F (2001) Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1:4
13. Danielian PS, Muccino D, Rowitch DH, Michael SK, McMahon AP (1998) Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr Biol 8:1323-1326 (Pubitemid 29006707)
14. Stanley EG, Biben C, Elefanty A, Barnett L, Koentgen F, Robb L, Harvey RP (2002) Efficient Cre-mediated deletion in cardiac progenitor cells conferred by a 3′UTR-ires-Cre allele of the homeobox gene Nk2-5. Int J Dev Biol 46:431-439 (Pubitemid 36841010)
15. Macatee TL, Hammond BP, Arenkiel BR, Francis L, Frank DU, Moon AM (2003) Ablation of specific expression domains reveals discrete functions of ectoderm- and endoderm-derived FGF8 during cardiovascular and pharyngeal development. Development 130:6361-6374 (Pubitemid 38008833)
16. 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 (Pubitemid 32171420)
17. Hayashi S, Lewis P, Pevny L, McMahon AP (2002) Efficient gene modulation in mouse epiblast using a Sox2Cre transgenic mouse strain. Gene Expr Patterns 2:93-97 (Pubitemid 36356020)
18. Hoser M, Baader SL, Bosl MR, Ihmer A, Wegner M, Sock E (2007) Prolonged glial expression of Sox4 in the CNS leads to architectural cerebellar defects and ataxia. J Neurosci 27:5495-5505 (Pubitemid 46790178)
19. Kuhlbrodt K, Herbarth B, Sock E, Enderich J, Hermans-Borgmeyer I, Wegner M (1998) Cooperative function of POU proteins and Sox proteins in glial cells. J Biol Chem 273:16050-16057 (Pubitemid 28311373)
20. Ehrnsperger A, Rehli M, Thu-Hang P, Kreutz M (2005) Epigenetic regulation of the dendritic cell-marker gene ADAM19. Biochem Biophys Res Commun 332:456-464 (Pubitemid 40724999)
21. Peirano RI, Goerich DE, Riethmacher D, Wegner M (2000) Protein zero expression is regulated by the glial transcription factor Sox10. Mol Cell Biol 20:3198-3209 (Pubitemid 30215032)
22. Kellerer S, Schreiner S, Stolt CC, Bösl MR, Wegner M (2006) Replacement of the Sox10 transcription factor by Sox8 reveals incomplete functional equivalence. Development 133:2875-2886 (Pubitemid 44314265)
23. Schlierf B, Werner T, Glaser G, Wegner M (2006) Expression of Connexin47 in oligodendrocytes is regulated by the Sox10 transcription factor. J Mol Biol 361:11-21 (Pubitemid 44041452)
24. Olaopa M, Zhou HM, Snider P, Wang J, Schwartz RJ, Moon AM, Conway SJ (2011) Pax3 is essential for normal cardiac neural crest morphogenesis but is not required during migration nor outflow tract septation. Dev Biol 356:308-322
25. Hoser M, Potzner MR, Koch JMC, Bösl MR, Wegner M, Sock E (2008) Sox12 deletion in the mouse reveals non-reciprocal redundancy with the related Sox4 and Sox11 transcription factors. Mol Cell Biol 28:4675-4687
26. Bergsland M, Werme M, Malewicz M, Perlmann T, Muhr J (2006) The establishment of neuronal properties is controlled by Sox4 and Sox11. Genes Dev 20:3475-3486 (Pubitemid 44969164)
27. Mu L, Berti L, Masserdotti G, Covic M, Michaelidis TM, Doberauer K, Merz K, Rehfeld F, Haslinger A, Wegner M, Sock E, Lefebvre V, Couillard-Despres S, Aigner L, Berninger B, Lie DC (2012) SoxC transcription factors are required for neuronal differentiation in adult hippocampal neurogenesis. J Neurosci 32:3067-3080
28. Teddy JM, Kulesa PM (2004) In vivo evidence for short- and long-range cell communication in cranial neural crest cells. Development 131:6141-6151 (Pubitemid 40123927)
29. Young HM, Bergner AJ, Anderson RB, Enomoto H, Milbrandt J, Newgreen DF, Whitington PM (2004) Dynamics of neural crest-derived cell migration in the embryonic mouse gut. Dev Biol 270:455-473 (Pubitemid 38748565)
30. Koyanagi M, Urbich C, Chavakis E, Hoffmann J, Rupp S, Badorff C, Zeiher AM, Starzinski-Powitz A, Haendeler J, Dimmeler S (2005) Differentiation of circulating endothelial progenitor cells to a cardiomyogenic phenotype depends on E-cadherin. FEBS Lett 579:6060-6066 (Pubitemid 41546247)
31. Luo Y, High FA, Epstein JA, Radice GL (2006) N-cadherin is required for neural crest remodeling of the cardiac outflow tract. Dev Biol 299:517-528 (Pubitemid 44637279)
32. Komatsu K, Wakatsuki S, Yamada S, Yamamura K, Miyazaki J, Sehara-Fujisawa A (2007) Meltrin beta expressed in cardiac neural crest cells is required for ventricular septum formation of the heart. Dev Biol 303:82-92 (Pubitemid 46241090)
33. Dy P, Penzo-Mendez A, Wang H, Pedraza CE, Macklin WB, Lefebvre V (2008) The three SoxC proteins-Sox4, Sox11 and Sox12-exhibit overlapping expression patterns and molecular properties. Nucleic Acids Res 36:3101-3117 (Pubitemid 351737202)
34. Rochais F, Mesbah K, Kelly RG (2009) Signaling pathways controlling second heart field development. Circ Res 104:933-942
35. Goddeeris MM, Schwartz R, Klingensmith J, Meyers EN (2007) Independent requirements for Hedgehog signaling by both the anterior heart field and neural crest cells for outflow tract development. Development 134:1593-1604 (Pubitemid 46746311)
36. Park EJ, Ogden LA, Talbot A, Evans S, Cai CL, Black BL, Frank DU, Moon AM (2006) Required, tissue-specific roles for Fgf8 in outflow tract formation and remodeling. Development 133:2419-2433 (Pubitemid 44044562)
37. Sinha T, Wang B, Evans S, Wynshaw-Boris A, Wang J (2012) Disheveled mediated planar cell polarity signaling is required in the second heart field lineage for outflow tract morphogenesis. Dev Biol 370:135-144
38. Boogerd CJ, Wong LY, van den Boogaard M, Bakker ML, Tessadori F, Bakkers J, t Hoen PA, Moorman AF, Christoffels VM, Barnett P (2011) Sox4 mediates Tbx3 transcriptional regulation of the gap junction protein Cx43. Cell Mol Life Sci 68:3949-3961
39. Usui A, Mochizuki Y, Iida A, Miyauchi E, Satoh S, Sock E, Nakauchi H, Aburatani H, Murakami A, Wegner M, Watanabe S (2013) The early retinal progenitor-expressed gene Sox11 regulates the timing of the differentiation of retinal cells. Development 140:740-750
40. Jankowski MP, Cornuet PK, McIlwrath S, Koerber HR, Albers KM (2006) SRY-box containing gene 11 (Sox11) transcription factor is required for neuron survival and neurite growth. Neuroscience 143:501-514 (Pubitemid 44724937)
41. Lin L, Lee VM, Wang Y, Lin JS, Sock E, Wegner M, Lei L (2011) Sox11 regulates survival and axonal growth of embryonic sensory neurons. Dev Dyn 240:52-64
42. Bergsland M, Ramskold D, Zaouter C, Klum S, Sandberg R, Muhr J (2011) Sequentially acting Sox transcription factors in neural lineage development. Genes Dev 25:2453-2464
43. Conway SJ, Bundy J, Chen J, Dickman E, Rogers R, Will BM (2000) Decreased neural crest stem cell expansion is responsible for the conotruncal heart defects within the splotch (Sp(2H))/Pax3 mouse mutant. Cardiovasc Res 47:314-328 (Pubitemid 30625294)
44. Van de Putte T, Maruhashi M, Francis A, Nelles L, Kondoh H, Huylebroeck D, Higashi Y (2003) Mice lacking ZFHX1B, the gene that codes for Smad-interacting protein-1, reveal a role for multiple neural crest cell defects in the etiology of Hirschsprung disease-mental retardation syndrome. Am J Hum Genet 72:465-470 (Pubitemid 36194254)
45. Brewer S, Jiang X, Donaldson S, Williams T, Sucov HM (2002) Requirement for AP-2α in cardiac outflow tract morphogenesis. Mech Dev 110:139-149
46. Seo S, Kume T (2006) Forkhead transcription factors, Foxc1 and Foxc2, are required for the morphogenesis of the cardiac outflow tract. Dev Biol 296:421-436 (Pubitemid 44189349)
47. Vincentz JW, Firulli BA, Lin A, Spicer DB, Howard MJ, Firulli AB (2013) Twist1 controls a cell-specification switch governing cell fate decisions within the cardiac neural crest. PLoS Genet 9:e1003405