Retinoic Acid Upregulates Ret and Induces Chain Migration and Population Expansion in Vagal Neural Crest Cells to Colonise the Embryonic Gut

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Simkin, Johanna E ^a   Zhang, Dongcheng ^a   Rollo, Benjamin N ^a   Newgreen, Donald F ^a  

^a ROYAL CHILDREN'S HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME P450 26A1; PROTEIN RET; RETINOIC ACID; RETINOIC ACID BINDING PROTEIN; RETINOIC ACID BINDING PROTEIN 1; RETINOIC ACID RECEPTOR; RETINOIC ACID RECEPTOR BETA; TAMIBAROTENE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CULTURE; CELL DENSITY; CELL MIGRATION; CELL POPULATION; CELL PROLIFERATION; EMBRYO; FLUORESCENCE ACTIVATED CELL SORTING; GANGLION; IN VITRO STUDY; INTESTINE; MESENCHYME; NEURAL CREST CELL; NONHUMAN; PROTEIN EXPRESSION; QUAIL; SIGNAL TRANSDUCTION; TISSUE CULTURE; UPREGULATION; VAGUS NERVE;

ANIMALS; APOPTOSIS; CELL MOVEMENT; CELL PROLIFERATION; CYTOCHROME P-450 ENZYME SYSTEM; EMIGRATION AND IMMIGRATION; ENTERIC NERVOUS SYSTEM; GANGLIA; GASTROINTESTINAL TRACT; MESODERM; NEURAL CREST; PROTO-ONCOGENE PROTEINS C-RET; QUAIL; RECEPTORS, NERVE GROWTH FACTOR; RECEPTORS, RETINOIC ACID; TRETINOIN; UP-REGULATION; VAGUS NERVE;

EID: 84878071162     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064077     Document Type: Article

References (85)

1. Yntema CL, Hammond WS, (1954) The origin of intrinsic ganglia of trunk viscera from vagal neural crest in the chick embryo. J Comp Neurol 101: 515-541.
2. LeDouarin NM, Teillet MA, (1973) Migration of Neural Crest Cells to Wall of Digestive Tract in Avian Embryo. Journal of Embryology and Experimental Morphology 30: 31-48.
3. Tucker GC, Ciment G, Thiery JP, (1986) Pathways of Avian Neural Crest Cell-Migration in the Developing Gut. Developmental Biology 116: 439-450.
4. Allan IJ, Newgreen DF, (1980) The origin and differentiation of enteric neurons of the intestine of the fowl embryo. American Journal of Anatomy 157: 137-154.
5. Connor PJ, Focke PJ, Noden DM, Epstein ML, (2003) Appearance of neurons and glia with respect to the wavefront during colonization of the avian gut by neural crest cells (vol 226, pg 91, 2003). Developmental Dynamics 226: 727-727.
6. Young HM, Bergner AJ, Anderson RB, Enomoto H, Milbrandt J, et al. (2004) Dynamics of neural crest-derived cell migration in the embryonic mouse gut. Developmental Biology 270: 455-473.
7. Druckenbrod NR, Epstein ML, (2005) The pattern of neural crest advance in the cecum and colon. Developmental Biology 287: 125-133.
8. Hackett-Jones EJ, Landman KA, Newgreen DF, Zhang DC, (2011) On the role of differential adhesion in gangliogenesis in the enteric nervous system. Journal of Theoretical Biology 287: 148-159.
9. Newgreen D, Young HM, (2002) Enteric nervous system: Development and developmental disturbances- Part 2. Pediatric and Developmental Pathology 5: 329-349.
10. Newgreen DF, Southwell B, Hartley L, Allan IJ, (1996) Migration of enteric neural crest cells in relation to growth of the gut in avian embryos. Acta Anat (Basel) 157: 105-115.
11. Simpson MJ, Zhang DC, Mariani M, Landman KA, Newgreen DF, (2007) Cell proliferation drives neural crest cell invasion of the intestine. Developmental Biology 302: 553-568.
12. Nishiyama C, Uesaka T, Manabe T, Yonekura Y, Nagasawa T, et al. (2012) Trans-mesenteric neural crest cells are the principal source of the colonic enteric nervous system. Nature Neuroscience 15: 1211-1218.
13. Simpson MJ, Landman KA, Hughes BD, Newgreen DF, (2006) Looking inside an invasion wave of cells using continuum models: Proliferation is the key. Journal of Theoretical Biology 243: 343-360.
14. Homma S, Oppenheim RW, Yaginuma H, Kimura S, (2000) Expression pattern of GDNF, c-ret, and GFR alpha s suggests novel roles for GDNF ligands during early organogenesis in the chick embryo. Developmental Biology 217: 121-137.
15. Robertson K, Mason I, (1995) Expression of ret in the chicken-embryo suggests roles in regionalization of the vagal neural-tube and somites and in development of multiple neural crest and placodal lineages. Mechanisms of Development 53: 329-344.
16. Sato Y, Heuckeroth RO, (2008) Retinoic acid regulates murine enteric nervous system precursor proliferation, enhances neuronal precursor differentiation, and reduces neurite growth in vitro. Developmental Biology 320: 185-198.
17. Young HM, Hearn CJ, Farlie PG, Canty AJ, Thomas P, et al. (2000) GDNF is a chemoattractant for migrating enteric neural crest-derived cells and neurites. Society for Neuroscience Abstracts 26: Abstract No.-602.608.
18. Hearn CJ, Murphy M, Newgreen D, (1998) GDNF and ET-3 differentially modulate the numbers of avian enteric neural crest cells and enteric neurons in vitro. Developmental Biology 197: 93-105.
19. Takahashi M, (2001) The GDNF/RET signaling pathway and human diseases. Cytokine & growth factor reviews 12: 361-373.
20. Yin MZ, King SK, Hutson JM, Chow CW, (2006) Multiple endocrine neoplasia type 2B diagnosed on suction rectal biopsy in infancy: A report of 2 cases. Pediatric and Developmental Pathology 9: 56-60.
21. Flynn B, Bergner AJ, Turner KN, Young HM, Anderson RB, (2007) Effect of Gdnf haploinsufficiency rate of migration and number of enteric neural crest-derived cells. Developmental Dynamics 236: 134-141.
22. Gianino S, Grider JR, Cresswell J, Enomoto H, Heuckeroth RO, (2003) GDNF availability determines enteric neuron number by controlling precursor proliferation. Development 130: 2187-2198.
23. Rhinn M, Dolle P, (2012) Retinoic acid signalling during development. Development 139: 843-858.
24. Pitera JE, Smith VV, Woolf AS, Milla PJ, (2001) Embryonic gut anomalies in a mouse model of retinoic acid-induced caudal regression syndrome- Delayed gut looping, rudimentary cecum, and anorectal anomalies. American Journal of Pathology 159: 2321-2329.
25. Niederreither K, Vermot J, Le Roux I, Schuhbaur B, Chambon P, et al. (2003) The regional pattern of retinoic acid synthesis by RALDH2 is essential for the development of posterior pharyngeal arches and the enteric nervous system. Development 130: 2525-2534.
26. Niederreither K, Vermot J, Messaddeq N, Schuhbaur B, Chambon P, et al. (2001) Embryonic retinoic acid synthesis is essential for heart morphogenesis in the mouse. Development 128: 1019-1031.
27. Bayha E, Jorgensen MC, Serup P, Grapin-Botton A, (2009) Retinoic acid signaling organizes endodermal organ specification along the entire antero-posterior axis. PloS one 4: e5845-e5845.
28. Cui J, Michaille JJ, Jianga WH, Zile MH, (2003) Retinoid receptors and vitamin A deficiency: differential patterns of transcription during early avian development and the rapid induction of RARs by retinoic acid. Developmental Biology 260: 496-511.
29. Dupe V, Ghyselinck NB, Wendling O, Chambon P, Mark M, (1999) Key roles of retinoic acid receptors alpha and beta in the patterning of the caudal hindbrain, pharyngeal arches and otocyst in the mouse. Development 126: 5051-5059.
30. Blentic A, Gale E, Maden M, (2003) Retinoic acid signalling centres in the avian embryo identified by sites of expression of synthesising and catabolising enzymes. Developmental Dynamics 227: 114-127.
31. Sonneveld E, van den Brink CE, Tertoolen LGJ, van der Burg P, van der Saag PT, (1999) Retinoic acid hydroxylase (CYP26) is a key enzyme in neuronal differentiation of embryonal carcinoma cells. Developmental Biology 213: 390-404.
32. Pijnappel WW, Hendriks HF, Folkers GE, van den Brink CE, Dekker EJ, et al. (1993) The retinoid ligand 4-oxo-retinoic acid is a highly active modulator of positional specification. Nature 366: 340-344.
33. Chang CL, Hong E, Lao-Sirieix P, Fitzgerald RC, (2008) A novel role for the retinoic acid-catabolizing enzyme CYP26A1 in Barrett's associated adenocarcinoma. Oncogene 27: 2951-2960.
34. Bellmeyer A, Krase J, Lindgren J, LaBonne C, (2003) The protooncogene c-Myc is an essential regulator of neural crest formation in Xenopus. Developmental Cell 4: 827-839.
35. Duong TD, Erickson CA, (2004) MMP-2 plays an essential role in producing epithelial-mesenchymal transformations in the avian embryo. Developmental Dynamics 229: 42-53.
36. Rossant J, Zirngibl R, Cado D, Shago M, Giguere V, (1991) Expression of a retinoic acid response element-hsplacZ transgene defines specific domains of transcriptional activity during mouse embryogenesis. Genes & development 5: 1333-1344.
37. Malpel S, Mendelsohn C, Cardoso WV, (2000) Regulation of retinoic acid signaling during lung morphogenesis. Development 127: 3057-3067.
38. Matt N, Ghyselinck NB, Wendling O, Chambon P, Mark M, (2003) Retinoic acid-induced developmental defects are mediated by RAR beta/RXR heterodimers in the pharyngeal endoderm. Development 130: 2083-2093.
39. Wendling O, Dennefeld C, Chambon P, Mark M, (2000) Retinoid signaling is essential for patterning the endoderm of the third and fourth pharyngeal arches. Development 127: 1553-1562.
40. Diman N, Remacle S, Bertrand N, Picard JJ, Zaffran S, et al. (2011) A Retinoic Acid Responsive Hoxa3 Transgene Expressed in Embryonic Pharyngeal Endoderm, Cardiac Neural Crest and a Subdomain of the Second Heart Field. Plos One 6.
41. Vermot J, Llamas JG, Fraulob V, Niederreither K, Chambon P, et al. (2005) Retinoic acid controls the bilateral symmetry of somite formation in the mouse embryo. Science 308: 563-566.
42. Vermot J, Pourquie O, (2005) Retinoic acid coordinates somitogenesis and left-right patterning in vertebrate embryos. Nature 435: 215-220.
43. Diez del Corral R, Olivera-Martinez I, Goriely A, Gale E, Maden M, et al. (2003) Opposing FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension. Neuron 40: 65-79.
44. Molotkov A, Molotkova N, Duester G, (2005) Retinoic acid generated by Raldh2 in mesoderm is required for mouse dorsal Endodermal pancreas development. Developmental Dynamics 232: 950-957.
45. Molotkova N, Molotkov A, Sirbu IO, Duester G, (2005) Requirement of mesodermal retinoic acid generated by Raldh2 for posterior neural transformation. Mechanisms of Development 122: 145-155.
46. Vermot J, Niederreither K, Garnier JM, Chambon P, Dolle P, (2003) Decreased embryonic retinoic acid synthesis results in a DiGeorge syndrome phenotype in newborn mice. Proceedings of the National Academy of Sciences of the United States of America 100: 1763-1768.
47. Lammer EJ, Chen DT, Hoar RM, Agnish ND, Benke PJ, et al. (1985) Retinoic acid embryopathy. The New England journal of medicine 313: 837-841.
48. Sinning AR, (1998) Role of vitamin A in the formation of congenital heart defects. Anatomical Record 253: 147-153.
49. Broekhuizen MLA, Gittenberger-de Groot AC, Baasten MJ, Wladimiroff JW, Poelmann RE, (1998) Disturbed vagal nerve distribution in embryonic chick hearts after treatment with all-trans retinoic acid. Anatomy and Embryology 197: 391-397.
50. Kirby ML, Aronstam RS, Buccafusco JJ, (1985) Changes in cholinergic parameters associated with failure of conotruncal septation in embryonic chick hearts after neural crest ablation. Circulation research 56: 392-401.
51. Young HM, Hearn CJ, Ciampoli D, Southwell BR, Brunet JF, et al. (1998) A single rostrocaudal colonization of the rodent intestine by enteric neuron precursors is revealed by the expression of Phox2b, Ret, and p75 and by explants grown under the kidney capsule or in organ culture. Developmental Biology 202: 67-84.
52. Patrone G, Puliti A, Bocciardi R, Ravazzolo R, Romeo G, (1997) Sequence and characterisation of the RET proto-oncogene 5 ' flanking region: analysis of retinoic acid responsiveness at the transcriptional level. Febs Letters 419: 76-82.
53. Angrisano T, Sacchetti S, Natale F, Cerrato A, Pero R, et al. (2011) Chromatin and DNA methylation dynamics during retinoic acid-induced RET gene transcriptional activation in neuroblastoma cells. Nucleic Acids Research 39: 1993-2006.
54. Smith CA, McClive PJ, Hudson Q, Sinclair AH, (2005) Male-specific cell migration into the developing gonad is a conserved process involving PDGF signalling. Developmental Biology 284: 337-350.
55. Newgreen DF, Murphy M, (2000) Neural crest cell outgrowth cultures and the analysis of cell migration. Methods Mol Biol 137: 201-211.
56. Hearn CJ, Young HM, Ciampoli D, Lomax AEG, Newgreen D, (1999) Catenary cultures of embryonic gastrointestinal tract support organ morphogenesis, motility, neural crest cell migration, and cell differentiation. Developmental Dynamics 214: 239-247.
57. Walters LC, Cantrell VA, Weller KP, Mosher JT, Southard-Smith EM Genetic background impacts developmental potential of enteric neural crest-derived progenitors in the Sox10(Dom) model of Hirschsprung disease. Human Molecular Genetics 19: 4353-4372.
58. Takahashi M, Buma Y, Taniguchi M, (1991) Identification of the ret proto-oncogene products in neuroblastoma and leukemia cells. Oncogene 6: 297-301.
59. O'Donnell AM, Mortell A, Giles J, Bannigan J, Puri P, (2004) The timing of enteric neural crest cell colonisation of the chick embryo cloaca. Pediatr Surg Int 20: 229-232.
60. Anderson RB, Turner KN, Nikonenko AG, Hemperly J, Schachner M, et al. (2006) The cell adhesion molecule L1 is required for chain migration of neural crest cells in the developing mouse gut. Gastroenterology 130: 1221-1232.
61. Zhang DC, Brinas IM, Binder BJ, Landman KA, Newgreen DF, (2010) Neural crest regionalisation for enteric nervous system formation: Implications for Hirschsprung's disease and stem cell therapy. Developmental Biology 339: 280-294.
62. Newgreen DF, Ritterman M, Peters EA, (1979) Morphology and behaviour of neural crest cells of chick embryo in vitro. Cell Tissue Res 203: 115-140.
63. Nagy N, Burns AJ, Goldstein AM, (2012) Immunophenotypic characterization of enteric neural crest cells in the developing avian colorectum. Dev Dyn 241: 842-851.
64. Tobita T, Takeshita A, Kitamura K, Ohnishi K, Yanagi M, et al. (1997) Treatment with a new synthetic retinoid, Am80, of acute promyelocytic leukemia relapsed from complete remission induced by all-trans retinoic acid. Blood 90: 967-973.
65. Kim MJ, Ciletti N, Michel S, Reichert U, Rosenfield RL, (2000) The role of specific retinoid receptors in sebocyte growth and differentiation in culture. Journal of Investigative Dermatology 114: 349-353.
66. Smith J, Cochard P, Ledouarin NM, (1977) Development of choline-acetyltransferase and cholinesterase activities in enteric ganglia derived from presumptive adrenergic and cholinergic levels of neural crest. Cell Differentiation 6: 199-216.
67. Newgreen DF, Jahnke I, Allan IJ, Gibbins IL, (1980) Differentiation of sympathetic and enteric neurons of the fowl embryo in grafts to the chorioallantoic membrane. Cell and Tissue Research 208: 1-19.
68. Reichenbach B, Delalande JM, Kolmogorova E, Prier A, Nguyen T, et al. (2008) Endoderm-derived Sonic hedgehog and mesoderm Hand2 expression are required for enteric nervous system development in zebrafish. Developmental Biology 318: 52-64.
69. Delalande JM, Barlow AJ, Thomas AJ, Wallace AS, Thapar N, et al. (2008) The receptor tyrosine kinase RET regulates hindgut colonization by sacral neural crest cells. Developmental Biology 313: 279-292.
70. Barlow AJ, Wallace AS, Thapar N, Burns AJ, (2008) Critical numbers of neural crest cells are required in the pathways from the neural tube to the foregut to ensure complete enteric nervous system formation. Development 135: 1681-1691.
71. Nikitina N, Sauka-Spengler T, Bronner-Fraser M, (2008) Dissecting early regulatory relationships in the lamprey neural crest gene network. Proceedings of the National Academy of Sciences of the United States of America 105: 20083-20088.
72. Nishiyama C, Uesaka T, Manabe T, Yonekura Y, Nagasawa T, et al. (2012) Trans-mesenteric neural crest cells are the principal source of the colonic enteric nervous system. Nat Neurosci 15: 1211-1218.
73. Kulesa PM, Fraser SE, (1998) Neural crest cell dynamics revealed by time-lapse video microscopy of whole embryo chick explant cultures. Developmental Biology 204: 327-344.
74. Kulesa PM, Fraser SE, (2000) In ovo time-lapse analysis of chick hindbrain neural crest cell migration shows cell interactions during migration to the branchial arches. Development 127: 1161-1172.
75. Testaz S, Duband JL, (2001) Central role of the alpha 4 beta 1 integrin in the coordination of avian truncal neural crest cell adhesion, migration, and survival. Developmental Dynamics 222: 127-140.
76. Breau MA, Dahmani A, Broders-Bondon F, Thiery JP, Dufour S, (2009) beta 1 integrins are required for the invasion of the caecum and proximal hindgut by enteric neural crest cells. Development 136: 2791-2801.
77. Broders-Bondon F, Paul-Gilloteaux P, Carlier C, Radice GL, Dufour S, (2012) N-cadherin and beta1-integrins cooperate during the development of the enteric nervous system. Dev Biol 364: 178-191.
78. Kuo BR, Erickson CA, (2011) Vagal Neural Crest Cell Migratory Behavior: A Transition Between the Cranial and Trunk Crest. Developmental Dynamics 240: 2084-2100.
79. Kuratani SC, Kirby ML, (1991) Initial Migration and Distribution of the Cardiac Neural Crest in the Avian Embryo- an Introduction to the Concept of the Circumpharyngeal Crest. American Journal of Anatomy 191: 215-227.
80. Young HM, Hearn CJ, Farlie PG, Canty AJ, Thomas PQ, et al. (2001) GDNF is a chemoattractant for enteric neural cells. Developmental Biology 229: 503-516.
81. Aquino JB, Lallemend F, Marmigere F, Adameyko, II, Golemis EA, et al. (2009) The Retinoic Acid Inducible Cas-Family Signaling Protein Nedd9 Regulates Neural Crest Cell Migration by Modulating Adhesion and Actin Dynamics. Neuroscience 162: 1106-1119.
82. Desai TJ, Malpel S, Flentke GR, Smith SM, Cardoso WV, (2004) Retinoic acid selectively regulates Fgf10 expression and maintains cell identity in the prospective lung field of the developing foregut. Developmental Biology 273: 402-415.
83. Fu M, Sato Y, Lyons-Warren A, Zhang B, Kane MA, et al. (2010) Vitamin A facilitates enteric nervous system precursor migration by reducing Pten accumulation. Development 137: 631-640.
84. Lee YM, Osumiyamashita N, Ninomiya Y, Moon CK, Eriksson U, et al. (1995) Retinoic Acid Stage-Dependently Alters the Migration Pattern and Identity of Hindbrain Neural Crest Cells. Development 121: 825-837.
85. Hotta R, Natarajan D, Burns AJ, Thapar N, (2011) Stem cells for GI motility disorders. Current Opinion in Pharmacology 11: 617-623.