Molecular fingerprinting delineates progenitor populations in the developing zebrafish enteric nervous system

Developmental Dynamics

Volumn 245, Issue 11, 2016, Pages 1081-1096

  Taylor, Charlotte R ^a   Montagne, William A ^a   Eisen, Judith S ^a   Ganz, Julia ^a,b  

^a UNIVERSITY OF OREGON   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

development; enteric glia; enteric neuron; gene expression; neural crest

Indexed keywords

PAIRED LIKE HOMEOBOX 2B PROTEIN; PROTEIN RET; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX10; UNCLASSIFIED DRUG; MESSENGER RNA; SOX10 PROTEIN, ZEBRAFISH; TRANSCRIPTION FACTOR SOX; ZEBRAFISH PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL LINEAGE; CELL MATURATION; CELL MIGRATION; CELL SUBPOPULATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ESSENTIAL GENE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE FUNCTION; GLIA CELL; IN VITRO STUDY; IN VIVO STUDY; INTESTINE FUNCTION; INTESTINE INNERVATION; MARKER GENE; MOLECULAR IMPRINTING; MOUSE; MULTIPOTENT STEM CELL; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; ZEBRA FISH; ANIMAL; CYTOLOGY; EMBRYOLOGY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NEURAL CREST;

ANIMALS; ENTERIC NERVOUS SYSTEM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; NEURAL CREST; RNA, MESSENGER; SOXE TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84988329666     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.24438     Document Type: Article

References (59)

1. Anderson RB, Stewart AL, Young HM. 2006. Phenotypes of neural-crest-derived cells in vagal and sacral pathways. Cell Tissue Res 323:11–25.
2. Baloh RH, Tansey MG, Golden JP, Creedon DJ, Heuckeroth RO, Keck CL, Zimonjic DB, Popescu NC, Johnson EM Jr, Milbrandt J. 1997. TrnR2, a novel receptor that mediates neurturin and GDNF signaling through Ret. Neuron 18:793–802.
3. Baloh RH, Tansey MG, Lampe PA, Fahrner TJ, Enomoto H, Simburger KS, Leitner ML, Araki T, Johnson EM Jr, Milbrandt J. 1998. Artemin, a novel member of the GDNF ligand family, supports peripheral and central neurons and signals through the GFRalpha3-RET receptor complex. Neuron 21:1291–1302.
4. Bisgrove BW, Raible DW, Walter V, Eisen JS, Grunwald DJ. 1997. Expression of c-ret in the zebrafish embryo: potential roles in motoneuronal development. J Neurobiol 33:749–768.
5. Bondurand N, Natarajan D, Barlow A, Thapar N, Pachnis V. 2006. Maintenance of mammalian enteric nervous system progenitors by SOX10 and endothelin 3 signalling. Development 133:2075–2086.
6. Bondurand N, Sham MH. 2013. The role of SOX10 during enteric nervous system development. Dev Biol 382:330–343.
7. Buj-Bello A, Adu J, Pinon LG, Horton A, Thompson J, Rosenthal A, Chinchetru M, Buchman VL, Davies AM. 1997. Neurturin responsiveness requires a GPI-linked receptor and the Ret receptor tyrosine kinase. Nature 387:721–724.
8. Chalazonitis A, Rothman TP, Chen J, Gershon MD. 1998. Age-dependent differences in the effects of GDNF and NT-3 on the development of neurons and glia from neural crest-derived precursors immunoselected from the fetal rat gut: expression of GFRalpha-1 in vitro and in vivo. Dev Biol 204:385–406.
9. Corpening JC, Cantrell VA, Deal KK, Southard-Smith EM. 2008. A Histone2BCerulean BAC transgene identifies differential expression of Phox2b in migrating enteric neural crest derivatives and enteric glia. Dev Dyn 237:1119–1132.
10. Durbec P, Marcos-Gutierrez CV, Kilkenny C, Grigoriou M, Wartiowaara K, Suvanto P, Smith D, Ponder B, Costantini F, Saarma M, et al. 1996a. GDNF signalling through the Ret receptor tyrosine kinase. Nature 381:789–793.
11. Durbec PL, Larsson-Blomberg LB, Schuchardt A, Costantini F, Pachnis V. 1996b. Common origin and developmental dependence on c-ret of subsets of enteric and sympathetic neuroblasts. Development 122:349–358.
12. Elworthy S, Pinto JP, Pettifer A, Cancela ML, Kelsh RN. 2005. Phox2b function in the enteric nervous system is conserved in zebrafish and is sox10-dependent. Mech Dev 122:659–669.
13. Emison ES, Garcia-Barcelo M, Grice EA, Lantieri F, Amiel J, Burzynski G, Fernandez RM, Hao L, Kashuk C, West K, Miao X, Tam PK, Griseri P, Ceccherini I, Pelet A, Jannot AS, de Pontual L, Henrion-Caude A, Lyonnet S, Verheij JB, Hofstra RM, Antinolo G, Borrego S, McCallion AS, Chakravarti A. 2010. Differential contributions of rare and common, coding and noncoding Ret mutations to multifactorial Hirschsprung disease liability. Am J Hum Genet 87:60–74.
14. Flames N, Pla R, Gelman DM, Rubenstein JL, Puelles L, Marin O. 2007. Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes. J Neurosci 27:9682–9695.
15. Furness JB. 2006. The enteric nervous system. Oxford Blackwell Publishing.
16. Ganz J, Kaslin J, Freudenreich D, Machate A, Geffarth M, Brand M. 2012. Subdivisions of the adult zebrafish subpallium by molecular marker analysis. J Comp Neurol 520:633–655.
17. Garcia-Barcelo M, Sham MH, Lui VC, Chen BL, Ott J, Tam PK. 2003. Association study of PHOX2B as a candidate gene for Hirschsprung's disease. Gut 52:563–567.
18. Guillemot F. 2005. Cellular and molecular control of neurogenesis in the mammalian telencephalon. Curr Opin Cell Biol 17:639–647.
19. Hafler BP, Surzenko N, Beier KT, Punzo C, Trimarchi JM, Kong JH, Cepko CL. 2012. Transcription factor Olig2 defines subpopulations of retinal progenitor cells biased toward specific cell fates. Proc Natl Acad Sci U S A 109:7882–7887.
20. Hagstrom C, Olsson C. 2010. Glial cells revealed by GFAP immunoreactivity in fish gut. Cell Tissue Res 341:73–81.
21. Harrison C, Wabbersen T, Shepherd IT. 2014. In vivo visualization of the development of the enteric nervous system using a Tg(-8.3bphox2b:Kaede) transgenic zebrafish. Genesis 52:985–990.
22. Heanue TA, Pachnis V. 2008. Ret isoform function and marker gene expression in the enteric nervous system is conserved across diverse vertebrate species. Mech Dev 125:687–699.
23. Herbarth B, Pingault V, Bondurand N, Kuhlbrodt K, Hermans-Borgmeyer I, Puliti A, Lemort N, Goossens M, Wegner M. 1998. Mutation of the Sry-related Sox10 gene in Dominant megacolon, a mouse model for human Hirschsprung disease. Proc Natl Acad Sci U S A 95:5161–5165.
24. Honjo Y, Kniss J, Eisen JS. 2008. Neuregulin-mediated ErbB3 signaling is required for formation of zebrafish dorsal root ganglion neurons. Development 135:2615–2625.
25. Jing S, Wen D, Yu Y, Holst PL, Luo Y, Fang M, Tamir R, Antonio L, Hu Z, Cupples R, Louis JC, Hu S, Altrock BW, Fox GM. 1996. GDNF-induced activation of the ret protein tyrosine kinase is mediated by GDNFR-alpha, a novel receptor for GDNF. Cell 85:1113–1124.
26. Kapur RP. 1999. Early death of neural crest cells is responsible for total enteric aganglionosis in Sox10(Dom)/Sox10(Dom) mouse embryos. Pediatr Dev Pathol 2:559–569.
27. Kim J, Lo L, Dormand E, Anderson DJ. 2003. SOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron 38:17–31.
28. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. 1995. Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310.
29. Klein RD, Sherman D, Ho WH, Stone D, Bennett GL, Moffat B, Vandlen R, Simmons L, Gu Q, Hongo JA, Devaux B, Poulsen K, Armanini M, Nozaki C, Asai N, Goddard A, Phillips H, Henderson CE, Takahashi M, Rosenthal A. 1997. A GPI-linked protein that interacts with Ret to form a candidate neurturin receptor. Nature 387:717–721.
30. Kohwi M, Doe CQ. 2013. Temporal fate specification and neural progenitor competence during development. Nat Rev Neurosci 14:823–838.
31. Kotzbauer PT, Lampe PA, Heuckeroth RO, Golden JP, Creedon DJ, Johnson EM, Jr., Milbrandt J. 1996. Neurturin, a relative of glial-cell-line-derived neurotrophic factor. Nature 384:467–470.
32. Lang D, Epstein JA. 2003. Sox10 and Pax3 physically interact to mediate activation of a conserved c-RET enhancer. Hum Mol Genet 12:937–945.
33. Leon TY, Ngan ES, Poon HC, So MT, Lui VC, Tam PK, Garcia-Barcelo MM. 2009. Transcriptional regulation of RET by Nkx2-1, Phox2b, Sox10, and Pax3. J Pediatr Surg 44:1904–1912.
34. Marusich MF, Furneaux HM, Henion PD, Weston JA. 1994. Hu neuronal proteins are expressed in proliferating neurogenic cells. J Neurobiol 25:143–155.
35. Masure S, Cik M, Hoefnagel E, Nosrat CA, Van der Linden I, Scott R, Van Gompel P, Lesage AS, Verhasselt P, Ibanez CF, Gordon RD. 2000. Mammalian GFRalpha-4, a divergent member of the GFRalpha family of coreceptors for glial cell line-derived neurotrophic factor family ligands, is a receptor for the neurotrophic factor persephin. J Biol Chem 275:39427–39434.
36. McLennan R, Schumacher LJ, Morrison JA, Teddy JM, Ridenour DA, Box AC, Semerad CL, Li H, McDowell W, Kay D, Maini PK, Baker RE, Kulesa PM. 2015. Neural crest migration is driven by a few trailblazer cells with a unique molecular signature narrowly confined to the invasive front. Development 142:2014–2025.
37. Milbrandt J, de Sauvage FJ, Fahrner TJ, Baloh RH, Leitner ML, Tansey MG, Lampe PA, Heuckeroth RO, Kotzbauer PT, Simburger KS, Golden JP, Davies JA, Vejsada R, Kato AC, Hynes M, Sherman D, Nishimura M, Wang LC, Vandlen R, Moffat B, Klein RD, Poulsen K, Gray C, Garces A, Johnson EM Jr, et al. 1998. Persephin, a novel neurotrophic factor related to GDNF and neurturin. Neuron 20:245–253.
38. Nagy N, Burns AJ, Goldstein AM. 2012. Immunophenotypic characterization of enteric neural crest cells in the developing avian colorectum. Dev Dyn 241:842–851.
39. Nechiporuk A, Linbo T, Poss KD, Raible DW. 2007. Specification of epibranchial placodes in zebrafish. Development 134:611–623.
40. Olden T, Akhtar T, Beckman SA, Wallace KN. 2008. Differentiation of the zebrafish enteric nervous system and intestinal smooth muscle. Genesis 46:484–498.
41. Paratore C, Eichenberger C, Suter U, Sommer L. 2002. Sox10 haploinsufficiency affects maintenance of progenitor cells in a mouse model of Hirschsprung disease. Hum Mol Genet 11:3075–3085.
42. Pattyn A, Morin X, Cremer H, Goridis C, Brunet JF. 1997. Expression and interactions of the two closely related homeobox genes Phox2a and Phox2b during neurogenesis. Development 124:4065–4075.
43. Pattyn A, Morin X, Cremer H, Goridis C, Brunet JF. 1999. The homeobox gene Phox2b is essential for the development of autonomic neural crest derivatives. Nature 399:366–370.
44. Pingault V, Bondurand N, Kuhlbrodt K, Goerich DE, Prehu MO, Puliti A, Herbarth B, Hermans-Borgmeyer I, Legius E, Matthijs G, Amiel J, Lyonnet S, Ceccherini I, Romeo G, Smith JC, Read AP, Wegner M, Goossens M. 1998. SOX10 mutations in patients with Waardenburg-Hirschsprung disease. Nat Genet 18:171–173.
45. Puelles L, Kuwana E, Puelles E, Bulfone A, Shimamura K, Keleher J, Smiga S, Rubenstein JL. 2000. Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr-1. J Comp Neurol 424:409–438.
46. Rothman TP, Gershon MD. 1982. Phenotypic expression in the developing murine enteric nervous system. J neuroSci 2:381–393.
47. Schiltz CA, Benjamin J, Epstein ML. 1999. Expression of the GDNF receptors ret and GFRalpha1 in the developing avian enteric nervous system. J Comp Neurol 414:193–211.
48. Schuchardt A, D'Agati V, Larsson-Blomberg L, Costantini F, Pachnis V. 1994. Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret. Nature 367:380–383.
49. Shepherd IT, Pietsch J, Elworthy S, Kelsh RN, Raible DW. 2004. Roles for GFRalpha1 receptors in zebrafish enteric nervous system development. Development 131:241–249.
50. Southard-Smith EM, Kos L, Pavan WJ. 1998. Sox10 mutation disrupts neural crest development in Dom Hirschsprung mouse model. Nat Genet 18:60–64.
51. Takahashi M, Cooper GM. 1987. ret transforming gene encodes a fusion protein homologous to tyrosine kinases. Mol Cell Biol 7:1378–1385.
52. Taraviras S, Marcos-Gutierrez CV, Durbec P, Jani H, Grigoriou M, Sukumaran M, Wang LC, Hynes M, Raisman G, Pachnis V. 1999. Signalling by the RET receptor tyrosine kinase and its role in the development of the mammalian enteric nervous system. Development 126:2785–2797.
53. Trimarchi JM, Stadler MB, Cepko CL. 2008. Individual retinal progenitor cells display extensive heterogeneity of gene expression. PloS One 3:e1588.
54. Trupp M, Arenas E, Fainzilber M, Nilsson AS, Sieber BA, Grigoriou M, Kilkenny C, Salazar-Grueso E, Pachnis V, Arumae U. 1996. Functional receptor for GDNF encoded by the c-ret proto-oncogene. Nature 381:785–789.
55. Westerfield M. 2000. The zebrafish book. a guide for the laboratory use of zebrafish (Danio rerio). Eugene, OR: University of Oregon Press.
56. Worby CA, Vega QC, Chao HH, Seasholtz AF, Thompson RC, Dixon JE. 1998. Identification and characterization of GFRalpha-3, a novel Co-receptor belonging to the glial cell line-derived neurotrophic receptor family. J Biol Chem 273:3502–3508.
57. Young HM, Bergner AJ, Muller T. 2003. Acquisition of neuronal and glial markers by neural crest-derived cells in the mouse intestine. J Comp Neurol 456:1–11.
58. Young HM, Ciampoli D, Hsuan J, Canty AJ. 1999. Expression of Ret-, p75(NTR)-, Phox2a-, Phox2b-, and tyrosine hydroxylase-immunoreactivity by undifferentiated neural crest-derived cells and different classes of enteric neurons in the embryonic mouse gut. Dev Dyn 216:137–152.
59. Young HM, Jones BR, McKeown SJ. 2002. The projections of early enteric neurons are influenced by the direction of neural crest cell migration. J Neurosci 22:6005–6018.