Loss of Hand2 in a population of Periostin lineage cells results in pronounced bradycardia and neonatal death

Developmental Biology

Volumn 388, Issue 2, 2014, Pages 149-158

  VanDusen, Nathan J ^a   Vincentz, Joshua W ^a   Firulli, Beth A ^a   Howard, Marthe J ^b   Rubart, Michael ^a   Firulli, Anthony B ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEDICAL COLLEGE OF OHIO   (United States)

Author keywords

Basic Helix loop Helix (bHLH) transcription factor; Bradycardia; Hand2; Heart development; Heart failure; Sympathetic neurogenesis

Indexed keywords

DOPAMINE BETA MONOOXYGENASE; PHENYLETHANOLAMINE N METHYLTRANSFERASE; TRANSCRIPTION FACTOR RUNX2; TYROSINE 3 MONOOXYGENASE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; HAND2 PROTEIN; UNCLASSIFIED DRUG;

ADRENAL MEDULLA; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOPAMINE BETA HYDROXYLASE GENE; ELECTROCARDIOGRAM; EMBRYO; EMBRYO DEVELOPMENT; GASTROINTESTINAL MOTILITY DISORDER; GENE EXPRESSION; HAND2 GENE; HEART DEVELOPMENT; HEART FAILURE; INTESTINE INNERVATION; LOSS OF FUNCTION MUTATION; MOUSE; NEWBORN; NEWBORN DEATH; NONHUMAN; PERIOSTIN GENE; PHENYLETHANOLAMINE N METHYLTRANSFERASE GENE; PRIORITY JOURNAL; PTERYGOPALATINE GANGLION; PUP (RODENT); SINUS BRADYCARDIA; SYMPATHETIC GANGLION; TYROSINE HYDROXYLASE GENE; ADRENERGIC SYSTEM; ALLELE; ANIMAL CELL; BRADYCARDIA; CAUSE OF DEATH; DBH GENE; HEART VALVE; HISTOLOGY; IN SITU HYBRIDIZATION; PHENOTYPE; PNMT GENE; PROTEIN DEPLETION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TH GENE;

BASIC HELIX-LOOP-HELIX (BHLH) TRANSCRIPTION FACTOR; BRADYCARDIA; HAND2; HEART DEVELOPMENT; HEART FAILURE; SYMPATHETIC NEUROGENESIS;

ANIMALS; ANIMALS, NEWBORN; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRADYCARDIA; CELL LINEAGE; IN SITU HYBRIDIZATION; MICE; MICE, KNOCKOUT; POLYMERASE CHAIN REACTION;

EID: 84895920187     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.02.010     Document Type: Article

References (44)

1. Abu-Issa R., Kirby M.L. Heart field: from mesoderm to heart tube. Annu. Rev. Cell Dev. Biol. 2007, 23:45-68.
2. Axelrod J., Reisine T.D. Stress hormones: their interaction and regulation. Science 1984, 224:452-459.
3. Barnes R.M., Firulli B.A., VanDusen N.J., Morikawa Y., Conway S.J., Cserjesi P., Vincentz J.W., Firulli A.B. Hand2 loss-of-function in Hand1-expressing cells reveals distinct roles in epicardial and coronary vessel development. Circ. Res. 2011, 108:940-949.
4. Coppola E., Rallu M., Richard J., Dufour S., Riethmacher D., Guillemot F., Goridis C., Brunet J.F. Epibranchial ganglia orchestrate the development of the cranial neurogenic crest. Proc. Natl. Acad. Sci. USA 2010, 107:2066-2071.
5. D'Autreaux F., Margolis K.G., Roberts J., Stevanovic K., Mawe G., Li Z., Karamooz N., Ahuja A., Morikawa Y., Cserjesi P., Setlick W., Gershon M.D. Expression level of Hand2 affects specification of enteric neurons and gastrointestinal function in mice. Gastroenterology 2011, 141:576-587. (p. 587, e571-e576).
6. Edwards B.S., Ackermann D.M., Lee M.E., Reeder G.S., Wold L.E., Burnett J.C. Identification of atrial natriuretic factor within ventricular tissue in hamsters and humans with congestive heart failure. J. Clin. Investig. 1988, 81:82-86.
7. Firulli B.A., Krawchuk D., Centonze V.E., Vargesson N., Virshup D.M., Conway S.J., Cserjesi P., Laufer E., Firulli A.B. Altered Twist1 and Hand2 dimerization is associated with Saethre-Chotzen syndrome and limb abnormalities. Nat. Genet. 2005, 37:373-381.
8. Fung, M.M.,Viveros,O.H.,O'Connor D.T. Diseases of the adrenal medulla. Acta Physiol. (Oxf.) 2008, 192:325-335.
9. Galli A., Robay D., Osterwalder M., Bao X., Benazet J.D., Tariq M., Paro R., Mackem S., Zeller R. Distinct roles of Hand2 in initiating polarity and posterior Shh expression during the onset of mouse limb bud development. PLoS Genet. 2010, 6:e1000901.
10. Hendershot T.J., Liu H., Clouthier D.E., Shepherd I.T., Coppola E., Studer M., Firulli A.B., Pittman D.L., Howard M.J. Conditional deletion of Hand2 reveals critical functions in neurogenesis and cell type-specific gene expression for development of neural crest-derived noradrenergic sympathetic ganglion neurons. Dev. Biol. 2008, 319:179-191.
11. Hendershot T.J., Liu H., Sarkar A.A., Giovannucci D.R., Clouthier D.E., Abe M., Howard M.J. Expression of Hand2 is sufficient for neurogenesis and cell type-specific gene expression in the enteric nervous system. Dev. Dyn. 2007, 236:93-105.
12. Hirsch M.R., Tiveron M.C., Guillemot F., Brunet J.F., Goridis C. Control of noradrenergic differentiation and Phox2a expression by MASH1 in the central and peripheral nervous system. Development 1998, 125:599-608.
13. Holler K.L., Hendershot T.J., Troy S.E., Vincentz J.W., Firulli A.B., Howard M.J. Targeted deletion of Hand2 in cardiac neural crest-derived cells influences cardiac gene expression and outflow tract development. Dev. Biol. 2010, 341:291-304.
14. Howard M., Foster D.N., Cserjesi P. Expression of HAND gene products may be sufficient for the differentiation of avian neural crest-derived cells into catecholaminergic neurons in culture. Dev. Biol. 1999, 215:62-77.
15. Howard M.J. Mechanisms and perspectives on differentiation of autonomic neurons. Dev. Biol. 2005, 277:271-286.
16. Keyte A., Hutson M.R. The neural crest in cardiac congenital anomalies. Differentiation 2012, 84:25-40.
17. Leblanc G.G., Landis S.C. Differentiation of noradrenergic traits in the principal neurons and small intensely fluorescent cells of the parasympathetic sphenopalatine ganglion of the rat. Dev. Biol. 1989, 131:44-59.
18. Lei J., Howard M.J. Targeted deletion of Hand2 in enteric neural precursor cells affects its functions in neurogenesis, neurotransmitter specification and gangliogenesis, causing functional aganglionosis. Development 2011, 138:4789-4800.
19. Lindsley A., Snider P., Zhou H., Rogers R., Wang J., Olaopa M., Kruzynska-Frejtag A., Koushik S.V., Lilly B., Burch J.B., Firulli A.B., Conway S.J. Identification and characterization of a novel Schwann and outflow tract endocardial cushion lineage-restricted periostin enhancer. Dev. Biol. 2007, 307:340-355.
20. Lucas M.E., Muller F., Rudiger R., Henion P.D., Rohrer H. The bHLH transcription factor Hand2 is essential for noradrenergic differentiation of sympathetic neurons. Development 2006, 133:4015-4024.
21. Malmejac J. Activity of the adrenal medulla and its regulation. Physiol. Rev. 1964, 44:186-218.
22. McFadden D.G., Barbosa A.C., Richardson J.A., Schneider M.D., Srivastava D., Olson E.N. The Hand1 and Hand2 transcription factors regulate expansion of the embryonic cardiac ventricles in a gene dosage-dependent manner. Development 2005, 132:189-201.
23. Morikawa Y., Cserjesi P. Cardiac neural crest expression of Hand2 regulates outflow and second heart field development. Circ. Res. 2008, 103:1422-1429.
24. Morikawa Y., D[U+05F3]Autreaux F., Gershon M.D., Cserjesi P. Hand2 determines the noradrenergic phenotype in the mouse sympathetic nervous system. Dev. Biol. 2007, 307:114-126.
25. Morikawa Y., Dai Y.S., Hao J., Bonin C., Hwang S., Cserjesi P. The basic helix-loop-helix factor Hand2 regulates autonomic nervous system development. Dev. Dyn. 2005, 234:613-621.
26. Ream M.A., Chandra R., Peavey M., Ray A.M., Roffler-Tarlov S., Kim H.G., Wetsel W.C., Rockman H.A., Chikaraishi D.M. High oxygen prevents fetal lethality due to lack of catecholamines. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 295:R942-R953.
27. Rychlik J.L., Gerbasi V., Lewis E.J. The interaction between dHAND and Arix at the dopamine beta-hydroxylase promoter region is independent of direct dHAND binding to DNA. J. Biol. Chem. 2003, 278:49652-49660.
28. Schmidt M., Lin S., Pape M., Ernsberger U., Stanke M., Kobayashi K., Howard M.J., Rohrer H. The bHLH transcription factor Hand2 is essential for the maintenance of noradrenergic properties in differentiated sympathetic neurons. Dev. Biol. 2009, 329:191-200.
29. Shen W.H., Chen Z., Shi S., Chen H., Zhu W., Penner A., Bu G., Li W., Boyle D.W., Rubart M., Field L.J., Abraham R., Liechty E.A., Shou W. Cardiac restricted overexpression of kinase-dead mammalian target of rapamycin (mTOR) mutant impairs the mTOR-mediated signaling and cardiac function. J. Biol. Chem. 2008, 283:13842-13849.
30. Srivastava D., Thomas T., Lin Q., Kirby M.L., Brown D., Olson E.N. Regulation of cardiac mesodermal and neural crest development by the bHLH transcription factor, dHAND. Nat. Genet. 1997, 16:154-160.
31. Suzuki N., Hardebo J.E., Kahrstrom J., Owman C. Selective electrical stimulation of postganglionic cerebrovascular parasympathetic nerve fibers originating from the sphenopalatine ganglion enhances cortical blood flow in the rat. J. Cereb. Blood Flow Metab. 1990, 10:383-391.
32. Takeda N., Manabe I., Uchino Y., Eguchi K., Matsumoto S., Nishimura S., Shindo T., Sano M., Otsu K., Snider P., Conway S.J., Nagai R. Cardiac fibroblasts are essential for the adaptive response of the murine heart to pressure overload. J. Clin. Investig. 2010, 120:254-265.
33. Ter Laan M., van Dijk J.M., Elting J.W., Staal M.J., Absalom A.R. Sympathetic regulation of cerebral blood flow in humans: a review. Br. J. Anaesth. 2013, 111(3):361-367.
34. Thomas S.A., Matsumoto A.M., Palmiter R.D. Noradrenaline is essential for mouse fetal development. Nature 1995, 374:643-646.
35. Tian H., Hammer R.E., Matsumoto A.M., Russell D.W., McKnight S.L. The hypoxia-responsive transcription factor EPAS1 is essential for catecholamine homeostasis and protection against heart failure during embryonic development. Genes Dev. 1998, 12:3320-3324.
36. Tronche F., Kellendonk C., Kretz O., Gass P., Anlag K., Orban P.C., Bock R., Klein R., Schutz G. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat. Genet. 1999, 23:99-103.
37. Tsuchihashi T., Maeda J., Shin C.H., Ivey K.N., Black B.L., Olson E.N., Yamagishi H., Srivastava D. Hand2 function in second heart field progenitors is essential for cardiogenesis. Dev. Biol. 2011, 351:62-69.
38. VanDusen N.J., Firulli A.B. Twist factor regulation of non-cardiomyocyte cell lineages in the developing heart. Differentiation 2012, 84:79-88.
39. Vincentz J.W., Barnes R.M., Firulli A.B. Hand factors as regulators of cardiac morphogenesis and implications for congenital heart defects. Birth Defects Res. A Clin. Mol. Teratol. 2011, 91:485-494.
40. Vincentz J.W., Barnes R.M., Rodgers R., Firulli B.A., Conway S.J., Firulli A.B. An absence of Twist1 results in aberrant cardiac neural crest morphogenesis. Dev. Biol. 2008, 320:131-139.
41. Vincentz J.W., Firulli B.A., Lin A., Spicer D.B., Howard M.J., Firulli A.B. Twist1 controls a cell-specification switch governing cell fate decisions within the cardiac neural crest. PLoS Genet. 2013, 9:e1003405.
42. Wildner H., Gierl M.S., Strehle M., Pla P., Birchmeier C. Insm1 (IA-1) is a crucial component of the transcriptional network that controls differentiation of the sympatho-adrenal lineage. Development 2008, 135:473-481.
43. Wu X., Howard M.J. Transcripts encoding HAND genes are differentially expressed and regulated by BMP4 and GDNF in developing avian gut. Gene Expr. 2002, 10:279-293.
44. Xu H., Firulli A.B., Zhang X., Howard M.J. HAND2 synergistically enhances transcription of dopamine-beta-hydroxylase in the presence of Phox2a. Dev. Biol. 2003, 262:183-193.