NT-3, like NGF, is required for survival of sympathetic neurons, but not their precursors

Developmental Biology

Volumn 210, Issue 2, 1999, Pages 411-427

  Francis, Nicole ^a   Farinas, Isabel ^c   Brennan, Christine ^b   Rivas Plata, Kimberly ^b   Backus, Carey ^c   Reichardt, Louis ^c   Landis, Story ^b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell death; Neurotrophin; Survival; Sympathetic neuron

Indexed keywords

NERVE GROWTH FACTOR; NEUROTROPHIC FACTOR; NEUROTROPHIN 3;

ANIMAL CELL; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; MOUSE; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPORTER GENE; STEM CELL; SUPERIOR CERVICAL GANGLION; SYMPATHETIC NERVE; SYMPATHETIC NERVE CELL;

EID: 0033564479     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1999.9269     Document Type: Article

References (51)

1. Albers K. M., Wright D. E., Davis B. M. Overexpression of nerve growth factor in epidermis of transgenic mice causes hypertrophy of the peripheral nervous system. J. Neurosci. 14:1994;1422-1432.
2. Barbacid M. The Trk family of neurotrophin receptors. J. Neurobiol. 25:1994;1386-1403.
3. Belliveau D. J., Krivko I., Kohn J., Lachance C., Pozniak C., Rusakov D., Kaplan D., Miller F. NGF and neurotrophin-3 both activate TrkA on sympathetic neurons but differentially regulate survival and neuritogenesis. J. Cell Biol. 136:1997;375-388.
4. Benedetti M., Levi A., Chao M. V. Differential expression of nerve growth factor receptors leads to altered binding affinity and neurotrophin responsiveness. Proc. Natl. Acad. Sci. USA. 90:1993;7859-7863.
5. Birren S. J., Lo L., Anderson D. J. Sympathetic neuroblasts undergo a developmental switch in trophic dependence. Development. 119:1993;597-610.
6. Bothwell M. Functional interactions of neurotrophins and neurotrophin receptors. Annu. Rev. Neurosci. 18:1995;223-253.
7. Buchman V. L., Davies A. M. Different neurotrophins are expressed and act in a developmental sequence to promote the survival of embryonic sensory neurons. Development. 118:1993;989-1001.
8. Buj-Bello A. M., Pinon L., Davies A. M. The survival of NGF-dependent but not BDNF-dependent cranial sensory neurons is promoted by several different neurotrophins early in their development. Development. 120:1994;1573-1580.
9. Campenot R. Local control of neurite development by nerve growth factor. Proc. Natl. Acad. Sci. USA. 74:1977;4516-4519.
10. Chun L. L. Y., Patterson P. H. Role of nerve growth factor in the development of rat sympathetic neurons in vitro. I. Survival, growth, and differentiation of catecholamine production. J. Cell Biol. 75:1977;694-704.
11. Clary D. O., Reichardt L. F. An alternatively spliced form of the nerve growth factor receptor TrkA confers enhanced response to neurotrophin 3. Proc. Natl. Acad. Sci. USA. 91:1994;11133-11137.
12. Cordon-Cardo C., Tapley P., Jing S., Nanduri V., O'Rourke E., Lamballe F., Kovary K., Klein R., Jones K. R., Reichardt L. F., Barbacid M. The trk tyrosine protein kinase mediates the mitogenic properties of nerve growth factor and neurotrophin-3. Cell. 66:1991;173-183.
13. Coughlin M. D., Collins M. B. Nerve growth factor-independent development of embryonic mouse sympathetic neurons in dissociated cell culture. Dev. Biol. 110:1985;392-401.
14. Crowley C., Spencer S. D., Nishimura M. C., Chen K. S., Pitts-Meek S., Armanini M. P., Ling L. H., McMahon S. B., Shelton D. L., Levinson A. D., Phillips H. S. Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell. 76:1994;1001-1011.
15. Davies A. Neurotrophin switching: Where does it stand? Curr. Opin. Neurobiol. 7:1997;110-118.
16. Davies A. M. Switching neurotrophin dependence. Curr. Biol. 4:1994;273-276.
17. Davies A. M., Minichiello L., Klein R. Developmental changes in NT-3 signalling via TrkA and TrkB in embryonic neurons. EMBO J. 14:1995;4482-4489.
18. DiCicco-Bloom E., Friedman W. J., Black I. B. NT-3 stimulates sympathetic neuroblast proliferation by promoting neuroblast survival. Neuron. 11:1993;1101-1111.
19. Durbec P., Marcos-Gutierrez C. V., Kilkenny C., Grigoriou M., Wartiowaara K., Suvanto P., Smith D., Ponder B., Costantini F., Saarma M., Sariola H., Pachnis V. GDNF signalling through the Ret receptor tyrosine kinase. Nature. 381:1996a;789-793.
20. Durbec P. L., Larsson-Blomberg L. B., Schuchardt A., Constantini F., Pachnis V. Common origin and developmental dependence on c-ret of subsets of enteric and sympathetic neurons. Development. 122:1996b;349-358.
21. ElShamy W., Linnarsson S., Lee K., Jaenisch R., Ernfors P. Prenatal and postnatal requirements of NT-3 for sympathetic neuroblast survival and innervation of specific targets. Development. 122:1996;491-500.
22. Ernfors P., Lee K.-F., Kucera J., Jaenisch R. Lack of neurotrophin-3 leads to deficiencies in the peripheral nervous system and loss of limb proprioceptive afferents. Cell. 77:1994;503-512.
23. Ernfors P., Wetmore C., Olson L., Persson H. Identification of cells in rat brain and peripheral tissues expressing mRNA for members of the nerve growth factor family. Neuron. 5:1990;511-526.
24. Fagan A., Zhang H., Landis S., Smeyne R., Silos-Santiago I., Barbacid M. TrkA, but not TrkC, receptors are essential for survival of sympathetic neurons in vivo. J. Neurosci. 16:1996;6208-6218.
25. Farinas I., Jones K., Backus C., Wang X., Reichardt L. Severe sensory and sympathetic deficits in mice lacking neurotrophin-3. Nature. 369:1994;658-661.
26. Farinas I., Wilkinson G. A., Backus C., Reichardt L. F., Patapoutian A. Characterization of neurotrophin and Trk receptor functions in developing sensory ganglia: Direct NT-3 activation of TrkB neurons in vivo. Neuron. 21:1998;325-334.
27. Farinas I., Yoshida C. K., Backus C., Reichardt L. F. Lack of neurotrophin-3 results in death of spinal sensory neurons and premature differentiation of their precursors. Neuron. 17:1996;1065-1078.
28. Fernholm M. On the development of the sympathetic chain and the adrenal medulla in the mouse. Z. Anat. Entwickl. Gesch. 133:1971;305-317.
29. Greene L. A. Quantitative in vitro studies on the nerve growth factor (NGF) requirement of neurons. I. Sympathetic neurons. Dev. Biol. 58:1977;96-106.
30. Hall A. K., Landis S. C. Division and migration of satellite glia in the embryonic rat superior cervical ganglion. J. Neurocytol. 21:1992;635-647.
31. Hendry I. A. Cell division in the developing sympathetic nervous system. J. Neurocytol. 6:1977;299-309.
32. Hendry I. A., Stockel K., Thoenen H., Iverson L. L. The retrograde axonal transport of nerve growth factor. Brain Res. 68:1974;103-121.
33. Hoyle G. W., Mercer E. H., Palmiter R. D., Brinster R. L. Expression of NGF in sympathetic neurons leads to excessive axon outgrowth from ganglia but decreased terminal innervation within tissues. Neuron. 10:1993;1019-1034.
34. Korsching S., Thoenen H. Nerve growth factor in sympathetic ganglia and corresponding target organs of the rat: Correlation with density of sympathetic innervation. Proc. Natl. Acad. Sci. USA. 80:1983;3513-3516.
35. Lee K.-F., Davies A. M., Jaenisch R. p75-deficient embryonic dorsal root sensory and neonatal sympathetic neurons display a decreased sensitivity to NGF. Development. 120:1994;1027-1033.
36. Levi-Montalcini R. The nerve growth factor: Thirty-five years later. EMBO J. 6:1987;1145-1154.
37. Levi-Montalcini R., Angeletti P. Essential role of the nerve growth factor in the survival and maintenance of dissociated sensory and sympathetic neurons in vitro. Dev. Biol. 7:1963;653-659.
38. Maina F., Hilton M. C., Andres R., Wyatt S., Klein R., Davies A. M. Multiple roles for hepatocyte growth factor in sympathetic neuron development. Neuron. 20:1998;835-846.
39. Moore M. W., Klein R. D., Farinas I., Sauer H., Armanini M., Phillips H., Reichart L. F., Ryan A. M., Carver-Moore K., Rosenthal A. Renal and neuronal abnormalities in mice lacking GDNF. Nature. 382:1996;76-79.
40. Rubin E. Development of the rat superior cervical ganglion: Ganglion cell maturation. J. Neurosci. 5:1985;673.
41. Scarisbrick I. A., Jones E. G., Isackson P. J. Coexpression of mRNAs for NGF, BDNF, and NT-3 in the cardiovascular system of the pre- and postnatal rat. J. Neurosci. 13:1993;875-893.
42. Smeyne R. J., Klein R., Schnapp A., Long L. K., Bryant S., Lewin A., Lira S. A., Barbacid M. Severe sensory and sympathetic neuropathies in mice carrying a disrupted trk/NGF receptor gene. Nature. 368:1994;246-249.
43. Tessarollo L., Tsoulfas P., Donovan M. J., Palko M. E., Blair-Flynn J., Hempstead B. L., Parada L. F. Targeted deletion of all isoforms of the trkC gene suggests the use of alternate receptors by its ligand neurotrophin-3 in neuronal development and implicates trkC in normal cardiogenesis. Proc. Natl. Acad. Sci. USA. 94:1997;14776-14781.
44. Theiler K. The House Mouse. Development and Normal Stages from Fertilization to 4 Weeks of Age. 1972;Springer-Verlag, Berlin/Heidelberg/New York.
45. Thoenen H., Barde Y.-A. Physiology of nerve growth factor. Physiol. Rev. 60:1980;1284-1335.
46. Verdi J., Groves A., Farinas I., Jones K., Marchionni M., Reichardt L., Anderson D. A reciprocal cell-cell interaction mediated by NT-3 and neuregulins controls the early survival and development of sympathetic neuroblasts. Neuron. 16:1996;515-527.
47. Verdi J. M., Anderson D. J. Neurotrophins regulate sequential changes in neurotrophin receptor expression by sympathetic neuroblasts. Neuron. 13:1994;1359-1372.
48. Wright L. L., Cunninham T. J., Smolen A. J. Developmental neuron death in the rat superior cervical sympathetic ganglion: Cell counts and ultrastructure. J. Neurocytol. 12:1983;727-738.
49. Wyatt S., Davies A. Regulation of nerve growth factor receptor gene expression in sympathetic neurons during development. J. Cell Biol. 130:1995;1435-1446.
50. Wyatt S., Pinon L. G. P., Ernfors P., Davies A. M. Sympathetic neuron survival and TrkA expression in NT-3 deficient mouse embryos. EMBO J. 16:1997;3115-3123.
51. Zhou X., Rush R. Sympathetic neurons in neonatal rats require endogenous neurotrophin-3 for survival. J. Neurosci. 15:1995;6521-6530.