Fetal development of the enteric nervous system of transgenic mice that overexpress the Hoxa-4 gene

Developmental Dynamics

Volumn 211, Issue 3, 1998, Pages 269-291

  Tennyson, Virginia M ^a   Gershon, Michael D ^a   Wade, Paul R ^a   Crotty, David A ^a   Wolgemuth, Debra J ^a  

^a College of Physicians and Surgeons ^*  (United States)

Author keywords

Congenital megacolon; Enteric nervous system; Homeobox genes; Mutant mice; Neural crest; Peripheral nervous system

Indexed keywords

ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; FETUS; FETUS DEVELOPMENT; GENE EXPRESSION; INTESTINE INNERVATION; MEGACOLON; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSGENE; TRANSGENIC MOUSE;

NON-PROGRAMMATIC;

ANIMALS; COLON; DNA-BINDING PROTEINS; EMBRYONIC AND FETAL DEVELOPMENT; ENTERIC NERVOUS SYSTEM; GANGLIA; HOMEODOMAIN PROTEINS; INTESTINAL MUCOSA; MEGACOLON; MESODERM; MICE; MICE, TRANSGENIC; NEURONS; PELVIS; TYROSINE 3-MONOOXYGENASE;

ANIMALIA; LAMIINAE; MAMMALIA; MUS MUSCULUS;

EID: 0031923209     PISSN: 10588388     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0177(199803)211:3<269::AID-AJA8>3.0.CO;2-F     Document Type: Article

References (70)

1. Benson GV, Lim H, Paria BC, Satokata I, Dey SK, Maas RR. Mechanisms of reduced fertility in Hoxa-10 mutant mice: Uterine homeosis and loss of maternal Hoxa-10 expression. Development 1996;122:2687-2696.
2. Blaugrund E, Pham TD, Tennyson VM, Lo L, Sommer L, Anderson DJ, Gershon MD. Distinct subpopulations of enteric neuronal progenitors defined by time of development, sympathoadrenal lineage markers, and Mash-l-dependence. Development 1996;122:309-320.
3. Botas J. Control of morphogenesis and differentiation by HOM/Hox genes. Curr. Opin. Cell Biol. 1993;5:1015-1022.
4. Carpenter E, Goddard J, Chiska O, Manley N, Capecci M. Loss of Hox-a1 (Hox-1.6) function results in reorganization of the murine hindbrain. Development 1993;118:1063-1075.
5. Chalazonitis A, Tennyson VM, Kibbey MC, Rothman TP, Gershon MD. The α-1 subunit of laminin-1 promotes the development of neurons by interacting with LBP110 expressed by neural crest-derived cells immunoselected from the fetal mouse gut. J. Neurobiol. 1997;33:118-138.
6. Dail WG, Evan AP, Eason HR. The major ganglion in the pelvic plexus of the male rat: a histochemical and ultrastructural study. Cell Tissue Res. 1975;159:49-62.
7. Dollé P, Lufkin T, Krumlauf R, Mark M, Duboule D, Chambon P. Local alterations of Krox-20 and Hox gene expression in the hindbrain of Hox-a1 (Hox-1.6) homozygote null mutant embryos. Proc. Natl. Acad. Sci. USA 1993;90:7666-7670.
8. Durbec P, Marcos-Gutierrez CV, Kilkenny C, Grigoriou M, Wartiowaara K, Suvanto P, Smith D, Ponder B, Costantini F, Saarma M. GDNF signaling through the Ret receptor tyrosine kinase. Nature 1996a;381:789-793.
9. Durbec PL, Larsson-Blomberg LB, Schuschardt A, Costantini F, Pachnis V. Common origin and developmental dependence on c-ret of subsets of enteric and sympathetic neuroblasts. Development 1996b;122:349-358.
10. Echelard Y, Epstein DJ, St.-Jacques B, Shen L, Mohler J, McMahon JA, McMahon A. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 1993;75:1417-1430.
11. Fritsch C, Simon-Assmann P, Kedinger M, Evans GS. Cytokines modulate fibroblast phenotype and epithelial-stroma interactions in rat intestine. Gastroenterology 1997;112:826-838.
12. Furness JB, Costa M. "The Enteric Nervous System". New York: Churchill Livingstone. 1987;65-69.
13. Gabella G. Glial cells in the myenteric plexus. Z. Naturforsch. 1971;26B:244-245.
14. Gehring WJ. Homeoboxes in the study of development. Science 1987;236:1245-1252.
15. Gershon MD. Genes and lineages in the formation of the enteric nervous system. Curr. Opin. Neurobiol. 1996;7:101-109.
16. Gershon MD, Chalazonitis A, Rothman TP. From neural crest to bowel: development of the enteric nervous system. J. Neurobiol. 1993;24:199-214.
17. Gershon MD, Kirchgessner AL, Wade PR. Functional anatomy of the enteric nervous system. In: Johnson LR, Alpers DH, Jacobson ED, Walsh JH, eds. "Physiology of the Gastrointestinal Tract. Third Edition," 1, New York: Raven Press. 1994;381-422.
18. Gershon MD, Rothman TP. Enteric glia. Glia 1991;4:195-204.
19. Guillemot F, Joyner AL. Dynamic expression of the murine achaete-scute homolog (MASH-1) in the developing nervous system. Mech. Dev. 1993;42:171-185.
20. Guillemot F, Lo L-C, Johnson JE, Auerbach A, Anderson DJ, Joyner AL. Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell 1993;75:463-476.
21. Haffen K, Kedinger M, Simon-Assmann P. Mesenchyme-dependent differentiation of epithelial progenitor cells in the gut. J. Pediatr. Gastroenterol. Nutr. 1987;6:14-23.
22. Hökfelt T. Ultrastructural localization of interaneuronal monoaminessome aspects on methodology. Prog. Brain Res. 1971;34:213-222.
23. Horan GSB, Ramírez-Solis R, Featherstone MS, Wolgemuth DJ, Bradley A, Behringer RR. Compound mutants for the paraologous hoxa-4, hoxb-4, and hoxd genes show more complete homeotic transformations and a dose-dependent increase in the number of vertebrae transformed. Genes Dev. 1995;9:1667-1677.
24. Horan GSB, Wu K, Wolgemuth DJ, Behringer RR. Homeotic transformation of cervical vertebrae in Hoxa-4 mutant mice. Proc. Natl. Acad. Sci. USA 1994;91:12644-12648.
25. Jing S, Wen D, Yu Y, Holst PL, Luo Y, Fang M, Tamir R, Antonio L, Hu Z, Cupples R. GDNF-induced activation of the Ret protein tyrosine kinase is mediated by GDNFR-α, a novel receptor for GDNF. Cell 1996;85:1113-1124.
26. Keast JR, De Groat WC. Immunohistochemical characterization of pelvic neurons which project to the bladder, colon, or penis in rats. J. Comp. Neurol. 1989;288:387-400.
27. Kedinger M, Simon-Assmann P, Bouziges F, Arnold C, Alexandre E, Haffen K. Smooth muscle actin expression during rat gut development and induction in fetal skin fibroblastic cells associated with intestinal embryonic epithelium. Differentiation 1990;43:87-97.
28. Krumlauf R. Hox genes in vertebrate development. Cell 1994;78:191-201.
29. Le Douarin NM. The Neural Crest. Cambridge: Cambridge University Press, 1982.
30. Le Douarin NM. Cell line segregation during peripheral nervous system ontogeny. Science 1986;231:1515-1522.
31. Le Douarin NM, Teillet MA. The migration of neural crest cells to the wall of the digestive tract in avian embryo. J. Embryol. Exp. Morphol. 1973;30:31-48.
32. Le Douarin NM, Teillet MA. Experimental analysis of the migration and differentiation of neuroblasts of the autonomic nervous system and of neurectodermal mesenchymal derivatives, using a biological cell marking technique. Dev. Biol. 1974;41:162-184.
33. Lo L, Guillemot F, Joyner AL, Anderson DJ. MASH-1: A marker and a mutation for mammalian neural crest development. Persp. Dev. Neurobiol. 1994;2:191-201.
34. Luckenbill-Edds L, vanHorn C. Development of chick paravertebral sympathetic ganglia. I. Fine structure and correlative histofluorescence of catecholaminergic cells. J. Comp. Neurol. 1980;191:65-76.
35. Mark M, Lufkin T, Vonesch J-L, Ruberte E, Olivo J-C, Dolló P, Gorry P, Lumsden A, Chambon P. Two rhombomeres are altered in Hoxa-1 null mutant mice. Development 1993;119:319-338.
36. Matthews MR, Raisman G. A light and electron microscopic study of cellular response to axonal injury in the superior cervical ganglion of the rat. Proc. R. Soc. Lond. B. 1972;181:43-79.
37. Mawe GM, Gershon MD. Structure, afferent innervation, and transmitter content of ganglia of the guinea pig gallbladder: relationship to the enteric nervous system. J. Comp. Neurol. 1989;283:374-390.
38. McGinnis W, Krumlauf R. Homeobox genes and axial patterning. Cell 1992;68:283-302.
39. McLean IW, Nakane PK. Periodate-lysine paraformaldehyde fixative: a new fixative for immunoelectron microscopy. J. Histochem. Cytochem. 1974;22:1077-1083.
40. Orian-Rousseau V, Aberdam D, Fontao L, Chevalier L, Meneguzzi G, Kedinger M, Simon-Assmann P. Developmental expression of laminin-5 and HD1 in the intestine: epithelial to mesenchymal shift for the laminin gamma-2 chain subunit deposition. Dev. Dyn. 1996;206:12-23.
41. Papka RE. Ultrastructural and fluorescence histochemical studies of developing sympathetic ganglia in the rabbit. Am. J. Anat. 1972;134:337-364.
42. Pichel JG, Shen L, Sheng HZ, Granholm A-C, Drago J, Grinberg A, Lee EJ, Huang SB, Saarma M, Hoffer BJ. Defects in enteric innervation and kidney development in mice lacking GDNF. Nature 1996;382:73-76.
43. Pomeranz HD, Gershon MD. Colonization of the avian hindgut by cells derived from the sacral neural crest. Dev. Biol. 1990;137:378-394.
44. Pomeranz HD, Rothman TP, Gershon MD. Colonization of the postumbilical bowel by cells derived from the sacral neural crest: Direct tracing of cell migration using an intercalating probe and a replication-deficient retrovirus. Development 1991a;111:647-655.
45. Pomeranz HD, Sherman DL, Smalheiser NR, Tennyson VM, Gershon MD. Expression of a neurally related laminin binding protein by neural crest-derived cells that colonize the gut: Relationship to the formation of enteric ganglia. J. Comp. Neurol. 1991b;313:625-642.
46. Riddle RD, Johnson RL, Laufer E, Tabin C. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 1993;75:1401-1416.
47. Roberts DJ, Johnson RL, Burke AC, Nelson CE, Morgan BA, Tabin C. Sonic hedgehog is an endodermal signal inducing Bmp-4 and Hox genes during induction and regionalization of the chick hindgut. Development 1995;121:3163-3174.
48. Rosenbluth J. Subsurface cisterns and their relationship to the neuronal plasma membrane. J. Cell Biol. 1962;13:405-421.
49. Rothman TP, Chen J, Howard MJ, Costantini FD, Pachnis V, Gershon MD. Increased expression of laminin-1 and collagen (IV) subunits in the aganglionic bowel of ls/ls, but not c-ret % mice. Dev. Biol. 1986;178:498-513.
50. Schuchardt A, D'Agati V, Larsson-Blomberg L, Costantini F, Pachnis V. Defect in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret. Nature 1994;367:380-383.
51. Sénchez M, Silos-Santiago I, Frisén J, He B, Lira S, Barbacid M. Renal agenesis and the absence of enteric neurons in mice lacking GDNF. Nature 1996;382:70-73.
52. Serbedzija GN, Burgan S, Fraser SE, Bronner-Fraser M. Vital dye labeling demonstrates a sacral neural crest contribution to the enteric nervous system of chick and mouse embryos. Development 1991;111:857-866.
53. Simionescu N, Simionescu M. Galloylglucoses of low molecular weight as mordant in electron microscopy. I. Procedure, and evidence for mordanting effect. J. Cell Biol. 1976;70:608-621.
54. Simo P, Bouziges F, Lissitzky J-C, Sorokin L, Kedinger M, Simon-Assman P. Dual and asynchronous deposition of laminin chains at the epithelial-mesenchymal interface in the gut. Gastroenterology 1992;102:1835-1845.
55. Simon-Assman P, Bouziges F, Freund JN, Perin-Schmitt F, Kedinger M. Type IV collagen mRNA accumulates in the mesenchymal compartment at early stages of murine developing intestine. J. Cell Biol. 1990;110:849-857.
56. Simon-Assmann P, Kedinger M, De Arcangelis A, Rousseau V, Simo P. Extracellular matrix components in intestinal development. Experientia 1995;51:883-900.
57. Sudhof T. The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 1995;375:645-653.
58. Tennyson VM, Gershon MD. Light and electron microscopy of dorsal root, sympathetic and enteric ganglia. In: 1, Dyck PJ, Thomas PK, Lamber PK, Bunge RP, eds. Peripheral Neuropathy. Philadelphia: W.B. Saunders Co. 1984;121-155.
59. Tennyson VM, Gershon MD, Sherman DL, Behringer RR, Raz R, Crotty DA, Wolgemuth DJ. Structural abnormalities associated with congenital megacolon in transgenic mice that overexpress the Hoxa-4 gene. Dev. Dyn. 1993;198:28-53.
60. Tennyson VM, Mytilineou C. Fluorescence and electron microscopic studies of sympathoblasts in the fetal rabbit. In: Eränko O., ed. SIF cells, Structure and Function of Small Intensely Fluorescent Sympathetic Cells, Chapter 4. Fogarty Internat. Center Proc. 30, Washington, D.C.: DHEW Publication (NIH). 1997;76-492:35-53.
61. Theiler K. The House Mouse. Development and Normal Stages from Fertilization to 4 Weeks of Age. New York: Springer-Verlag, 1972.
62. Thureson-Klein AK, Klein RL. Exocytosis from neuronal large dense cored vesicles. Int. Rev. Cytol. 1990;121:67-126.
63. Toth LE, Slawin KL, Pintar JE, Nguyen Hun MC. Region-specific expression of mouse homeobox genes in the embryonic mesoderm and central nervous system. Proc. Natl. Acad. Sci. USA 1987;84:6790-6793.
64. Treanor JJS, Goodman L, de Sauvage F, Stone DM, Poulsen KT, Beck CD, Gray C, Armanini MP, Pollock RA, Hefti F. Characterization of a multicomponent receptor for GDNF. Nature 1996;382:80-83.
65. Trupp M, Arenas E, Fainzilber M, Nilsson A-S, Sieber B-A, Grigoriou M, Kilkenny C, Salazar-Grueso E, Pachnis V, Arumäe U. Functional receptor for GDNF encoded by the c-ret proto-oncogene. Nature 1996;381:785-789.
66. Trupp M, Rydén M, Jörnvall H, Funakoshi H, Timmusk T, Arenas E, Ibäñez CF. Peripheral expression and biological activities of GDNF, a new neurotrophic factor for avian and mammalian peripheral neurons. J. Cell Biol. 1995;130:137-148.
67. Wolgemuth DJ, Behringer RR, Mostoller MP, Brinster RL, Palmiter RD. Transgenic mice overexpressing the mouse homoeobox-containing gene Hox-1.4 exhibit abnormal gut development. Nature 1989; 337:464-467.
68. Yntema CL, Hammond WS. The origin of intrinsic ganglia of trunk viscera from vagal neural crest in the chick embryo. J. Comp. Neurol. 1954;101:515-542.
69. Yntema CL, Hammond WS. Experiments on the origin and development of the sacral autonomic nerves in the chick embryo. J. Exp. Zool. 1995;129:375-414.
70. Yokouchi Y, Sakiyama J, Kuroiwa A. Coordinated expression of Abd-B subfamily of the HoxA cluster in the developing digestive tract of chick embryo. Dev. Biol. 1995;169:76-89.