Development, Vol 119, Issue 4 1005-1017, Copyright © 1993 by Company of Biologists

JOURNAL ARTICLES

Expression of the c-ret proto-oncogene during mouse embryogenesis

V Pachnis, B Mankoo and F Costantini
Department of Genetics and Development, Columbia University, New York, NY 10032.

The c-ret proto-oncogene encodes a receptor tyrosine kinase whose normal function has yet to be determined. To begin to investigate the potential role of this gene in vertebrate development, we have isolated cDNA clones representing the murine c-ret gene, and have analyzed the pattern of expression during mouse embryogenesis, using northern blotting, in situ hybridization to histological sections and whole-mount hybridization histochemistry. c-ret transcripts were detected beginning at day 8.5 of embryogenesis, and were observed in a number of cell lineages in the developing peripheral and central nervous systems, as well as in the excretory system. In the cranial region at day 8.5-9.5, c-ret mRNA was restricted to a population of neural crest cells migrating from rhombomere 4 and forming the anlage of the facioacoustic ganglion, as well as to a closely associated domain of surface ectoderm and pharyngeal endoderm. At later stages (10.5-14.5 days), c-ret mRNA was observed in all cranial ganglia. In the peripheral nervous system of the trunk, c-ret was expressed in the autonomic ganglia and in subsets of cells in the dorsal root ganglia. In the enteric nervous system, c-ret was expressed in the presumptive enteric neuroblasts of the vagal crest (day 9.0-11.5), and in the myenteric ganglia of the gut (day 13.5-14.5). c-ret mRNA was observed in several regions of the central nervous system, including the undifferentiated neuroepithelial cells of the ventral neural tube (8.5 days), the motor neurons in the spinal cord and the hindbrain (10.5-14.5 days), the embryonic neuroretina (day 13.5) and the layers of the postnatal retina containing ganglion, amacrine and horizontal cells. Outside the nervous system, c-ret was expressed in the nephric (Wolffian) duct at day 8.5-10.5, the ureteric bud epithelium (but not the surrounding metanephric mesenchyme) at day 11.0-11.5, and the growing tips of the renal collecting ducts (but not the previously formed, subcortical portions of the collecting ducts, or the mesenchyme-derived renal vesicles) at day 13.5-17.5. Our results suggest that the c-ret gene may encode the receptor for a factor involved in the proliferation, migration, differentiation or survival of a variety of neuronal cell lineages, as well as in inductive interactions during organogenesis of the kidney.
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				A. Greenwood, E. Turner, and D. Anderson Identification of dividing, determined sensory neuron precursors in the mammalian neural crest Development, January 8, 1999; 126(16): 3545 - 3559. [Abstract] [PDF]

				J. Pisano and S. Birren Restriction of developmental potential during divergence of the enteric and sympathetic neuronal lineages Development, January 7, 1999; 126(13): 2855 - 2868. [Abstract] [PDF]

				S Taraviras, C. Marcos-Gutierrez, P Durbec, H Jani, M Grigoriou, M Sukumaran, L. Wang, M Hynes, G Raisman, and V Pachnis Signalling by the RET receptor tyrosine kinase and its role in the development of the mammalian enteric nervous system Development, January 6, 1999; 126(12): 2785 - 2797. [Abstract] [PDF]

				S Srinivas, Z Wu, C. Chen, V D'Agati, and F Costantini Dominant effects of RET receptor misexpression and ligand-independent RET signaling on ureteric bud development Development, January 4, 1999; 126(7): 1375 - 1386. [Abstract] [PDF]

				S. Perez, S Rebelo, and D. Anderson Early specification of sensory neuron fate revealed by expression and function of neurogenins in the chick embryo Development, January 4, 1999; 126(8): 1715 - 1728. [Abstract] [PDF]

				C Mendelsohn, E Batourina, S Fung, T Gilbert, and J Dodd Stromal cells mediate retinoid-dependent functions essential for renal development Development, January 3, 1999; 126(6): 1139 - 1148. [Abstract] [PDF]

				J. Wu, J. Chen, T. Rothman, and M. Gershon Inhibition of in vitro enteric neuronal development by endothelin-3: mediation by endothelin B receptors Development, January 3, 1999; 126(6): 1161 - 1173. [Abstract] [PDF]

				D Natarajan, M Grigoriou, C. Marcos-Gutierrez, C Atkins, and V Pachnis Multipotential progenitors of the mammalian enteric nervous system capable of colonising aganglionic bowel in organ culture Development, January 1, 1999; 126(1): 157 - 168. [Abstract] [PDF]

				K. Krieglstein, P. Henheik, L. Farkas, J. Jaszai, D. Galter, K. Krohn, and K. Unsicker Glial Cell Line-Derived Neurotrophic Factor Requires Transforming Growth Factor-beta for Exerting Its Full Neurotrophic Potential on Peripheral and CNS Neurons J. Neurosci., December 1, 1998; 18(23): 9822 - 9834. [Abstract] [Full Text] [PDF]

				E. Moreau, J. Vilar, M. Lelievre-Pegorier, C. Merlet-Benichou, and T. Gilbert Regulation of c-ret expression by retinoic acid in rat metanephros: implication in nephron mass control Am J Physiol Renal Physiol, December 1, 1998; 275(6): F938 - F945. [Abstract] [Full Text] [PDF]

				X.-X. Zeng, H. Zhang, R. R. Hardy, and R. Wasserman The Fetal Origin of B-Precursor Leukemia in the Eµ-ret Mouse Blood, November 15, 1998; 92(10): 3529 - 3536. [Abstract] [Full Text] [PDF]

				S. F. Leavey, L. J. Arend, H. Dare, G. R. Dressler, J. P. Briggs, and B. L. Margolis Expression of Grb7 growth factor receptor signaling protein in kidney development and in adult kidney Am J Physiol Renal Physiol, November 1, 1998; 275(5): F770 - F776. [Abstract] [Full Text] [PDF]

				M. P. Cosma, M. Cardone, F. Carlomagno, and V. Colantuoni Mutations in the Extracellular Domain Cause RET Loss of Function by a Dominant Negative Mechanism Mol. Cell. Biol., June 1, 1998; 18(6): 3321 - 3329. [Abstract] [Full Text]

				I. Berndt, M. Reuter, B. Saller, K. Frank-Raue, P. Groth, M. Grußendorf, F. Raue, M. M. Ritter, and W. Höppner A New Hot Spot for Mutations in the ret Protooncogene Causing Familial Medullary Thyroid Carcinoma and Multiple Endocrine Neoplasia Type 2A J. Clin. Endocrinol. Metab., March 1, 1998; 83(3): 770 - 774. [Abstract] [Full Text]

				S. Xing, T. L. Furminger, Q. Tong, and S. M. Jhiang Signal Transduction Pathways Activated by RET Oncoproteins in PC12 Pheochromocytoma Cells J. Biol. Chem., February 27, 1998; 273(9): 4909 - 4914. [Abstract] [Full Text] [PDF]

				V. Arce, R. A. Pollock, J.-M. Philippe, D. Pennica, C. E. Henderson, and O. deLapeyriere Synergistic Effects of Schwann- and Muscle-Derived Factors on Motoneuron Survival Involve GDNF and Cardiotrophin-1 (CT-1) J. Neurosci., February 15, 1998; 18(4): 1440 - 1448. [Abstract] [Full Text] [PDF]

				C. A. Worby, Q. C. Vega, H. H.-J. Chao, A. F. Seasholtz, R. C. Thompson, and J. E. Dixon Identification and Characterization of GFRalpha -3, a Novel Co-receptor Belonging to the Glial Cell Line-derived Neurotrophic Receptor Family J. Biol. Chem., February 6, 1998; 273(6): 3502 - 3508. [Abstract] [Full Text] [PDF]

				Y. Sagot, T. Rosse, R. Vejsada, D. Perrelet, and A. C. Kato Differential Effects of Neurotrophic Factors on Motoneuron Retrograde Labeling in a Murine Model of Motoneuron Disease J. Neurosci., February 1, 1998; 18(3): 1132 - 1141. [Abstract] [Full Text] [PDF]

				A. Burns and N. Douarin The sacral neural crest contributes neurons and glia to the post-umbilical gut: spatiotemporal analysis of the development of the enteric nervous system Development, January 11, 1998; 125(21): 4335 - 4347. [Abstract] [PDF]