The GDNF family ligands and receptors - Implications for neural development

Current Opinion in Neurobiology

Volumn 10, Issue 1, 2000, Pages 103-110

  Baloh, Robert H ^a   Enomoto, Hideki ^a   Johnson Jr, Eugene M ^a   Milbrandt, Jeffrey ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GROWTH FACTOR RECEPTOR; NERVE GROWTH FACTOR; NEUROTROPHIC FACTOR; NEURTURIN;

MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW;

EID: 0033964411     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(99)00048-3     Document Type: Review

References (58)

1. Hamburger V., Levi-Montalcini R. Proliferation, differentiation and degeneration in the spinal ganglia of the chick embryo under normal and experimental conditions. J Exp Zool. 111:1949;457-501.
2. Levi-Montalcini R., Angeletti P.U. Nerve growth factor. Physiol Rev. 48:1968;534-569.
3. Levi-Montalcini R. The nerve growth factor 35 years later. Science. 237:1987;1154-1162.
4. Lin L.F., Doherty D.H., Lile J.D., Bektesh S., Collins F. GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science. 260:1993;1130-1132.
5. Trupp M., Ryden M., Jornvall H., Funakoshi H., Timmusk T., Arenas E., Ibanez C.F. Peripheral expression and biological activities of GDNF, a new neurotrophic factor for avian and mammalian peripheral neurons. J Cell Biol. 130:1995;137-148.
6. Ebendal T., Tomac A., Hoffer B.J., Olson L. Glial cell line-derived neurotrophic factor stimulates fiber formation and survival in cultured neurons from peripheral autonomic ganglia. J Neurosci Res. 40:1995;276-284.
7. Buj-Bello A., Buchman V.L., Horton A., Rosenthal A., Davies A.M. GDNF is an age-specific survival factor for sensory and autonomic neurons. Neuron. 15:1995;821-828.
8. Kotzbauer P.T., Lampe P.A., Heuckeroth R.O., Golden J.P., Creedon D.J., Johnson E.M., Milbrandt J.D. Neurturin, a relative of glial-cell-line-derived neurotrophic factor. Nature. 384:1996;467-470.
9. ••], established the necessary role of GFRα1 as a GDNF co-receptor in vivo. These authors also provided the first demonstration that NRTN-GFRα2 signaling supports parasympathetic submandibular neuron survival in culture.
10. Trupp M., Arenas E., Fainzilber M., Nilsson A-S., Sieber B-A., Grigoriou M., Kilkenny C., Salazar-Grueso E., Pachnis V., Arumae U.et al. Functional receptor for GDNF encoded by the c-ret proto-oncogene. Nature. 381:1996;785-789.
11. Durbec P., Marcos-Gutierrez C.V., Kilkenny C., Grigoriou M., Wartiowaara K., Suvanto P., Smith D., Ponder B., Costantini F., Saarma M.et al. GDNF signalling through the Ret receptor tyrosine kinase. Nature. 381:1996;789-793.
12. Jing S., Wen D., Yu Y., Holst P.L., Luo Y., Fang M., Tamir R., Antonio L., Hu Z., Cupples R.et al. GDNF-induced activation of the ret protein tyrosine kinase is mediated by GDNFR-α, a novel receptor for GDNF. Cell. 85:1996;1113-1124.
13. Treanor J.J.S., Goodman L., Sauvage F., Stone D.M., Poulsen K.T., Beck C.D., Gray C., Armanini M.P., Pollock R.A., Hefti F.et al. Characterization of a multicomponent receptor for GDNF. Nature. 382:1996;80-83.
14. Creedon D.J., Tansey M.G., Baloh R.H., Osborne P.A., Lampe P.A., Fahrner T.J., Heuckeroth R.O., Milbrandt J., Johnson E.M. Jr. Neurturin, shares receptors and signal transduction pathways with glial cell line-derived neurotrophic factor in sympathetic neurons. Proc Natl Acad Sci USA. 94:1997;7018-7023.
15. Ibanez C.F. Emerging themes in structural biology of neurotrophic factors. Trends Neurosci. 21:1998;438-444. A thorough review discussing major issues of the structural biology of the NGF and GDNF families, as well as ciliary neurotrophic factor (CNTF).
16. Grondin R., Gash D.M. Glial cell line-derived neurotrophic factor (GDNF): a drug candidate for the treatment of Parkinson's disease. J Neurol. 245:1998;35-42.
17. Airaksinen M.S., Titievsky A., Saarma M. GDNF family neurotrophic factor signaling: four masters, one servant? Mol Cell Neurosci. 13:1999;313-325. This is a recent comprehensive review covering issues of structural biology, therapeutic prospects, developmental roles, and ligand-interactions of the GFLs.
18. Takahashi M., Iwashita T., Santoro M., Lyonnet S., Lenoir G.M., Billaud M. Co-segregation of MEN2 and Hirschsprung's disease: the same mutation of RET with both gain and loss-of-function? Hum Mutat. 13:1999;331-336.
19. Ponder B.A. The phenotypes associated with ret mutations in the multiple endocrine neoplasia type 2 syndrome. Cancer Res. 59:1999;1736s-1741s.
20. Santoro M., Melillo R.M., Carlomagno F., Visconti R., De Vita G., Salvatore G., Lupoli G., Fusco A., Vecchio G. Molecular biology of the MEN2 gene. J Intern Med. 243:1998;505-508.
21. Baloh R.H., Tansey M.G., Golden J.P., Creedon D.J., Heuckeroth R.O., Keck C.L., Zimonjic D.B., Popescu N.C., Johnson E.M.J., Milbrandt J. TrnR2, a novel receptor that mediates neurturin and GDNF signaling through Ret. Neuron. 18:1997;793-802.
22. Jing S., Yu Y., Fang M., Hu Z., Holst P.L., Boone T., Delaney J., Schultz H., Zhou R., Fox G.M. GFRα-2 and GFRα-3 are two new receptors for ligands of the GDNF family. J Biol Chem. 272:1997;33111-33117.
23. Klein R.D., Sherman D., Ho W.H., Stone D., Bennett Gl, Moffat B., Vandlen R., Simmons L., Gu Q., Hongo J.A.et al. A GPI-linked protein that interacts with Ret to form a candidate neurturin receptor. Nature. 387:1997;717-721.
24. Baloh R.H., Tansey M.G., Lampe P.A., Fahrner T.J., Enomoto H., Simburger K., Leitner M.L., Araki T., Johnson E.M.J., Milbrandt J. Artemin, a novel member of the GDNF ligand family supports peripheral and central neurons and signals through the GFRα3-RET receptor complex. Neuron. 21:1998;1291-1302. This paper described the identification of ARTN, the most recently discovered GFL, and established that ARTN binds and signals through the former orphan receptor GFRα3-RET.
25. Enokido Y., de Sauvage F., Hongo J-A., Ninkina N., Rosenthal A., Buchman V.L., Davies A.M. GFRα4 and the tyrosine kinase Ret form a functional receptor complex for persephin. Curr Biol. 8:1998;1019-1022.
26. Suvanto P., Wartiovaara K., Lindahl M., Arumae U., Moshnyakov M., Horelli-Kuitunen N., Airaksinen M.S., Palotie A., Sariola H., Saarma M. Cloning, mRNA distribution and chromosomal localisation of the gene for glial cell line-derived neurotrophic factor receptor-β, a homologue to GDNFR-α Hum Molec Genet. 6:1997;1267-1273.
27. Sanicola M., Hession C., Worley D., Carmillo P., Ehrenfels C., Walus L., Robinson S., Jaworski G., Wei H., Tizard R.et al. Glial cell line-derived neurotrophic factor-dependent RET activation can be mediated by two different cell-surface accessory proteins. Proc Natl Acad Sci USA. 94:1997;6238-6243.
28. ••], demonstrated the critical role of NRTN-GFRα2 signaling in the development of parasympathetic neurons, and established that GFRα2-RET functions predominantly as a receptor for NRTN in vivo.
29. Schuchardt A., D'Agati V., Larsson-Blomberg L., Constantini F., Pachnis V. Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret. Nature. 367:1994;380-383.
30. Pachnis V., Mankoo B., Constantini F. Expression of the c-ret proto-oncogene during mouse embryogenesis. Development. 119:1993;1005-1017.
31. 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.
32. Pichel J.G., Shen L., Hui S.Z., Granholm A-C., Drago J., Grinberg A., Lee E.J., Huang S.P., Saarma M., Hoffer B.J.et al. Defects in enteric innervation and kidney development in mice lacking GDNF. Nature. 382:1996;73-76.
33. Sanchez M.P., Silos-Santiago I., Frisen J., He B., Lira S.A., Barbacid M. Renal agenesis and the absence of enteric neurons in mice lacking GDNF. Nature. 382:1996;70-73.
34. ••].
35. Sariola H., Sainio K. The tip-top branching ureter. Curr Opin Cell Biol. 9:1997;877-884.
36. Le Douarin N.M., Teillet M.A. Experimental analysis of the migration and differentiation of neuroblasts of the autonomic nervous system and of neuroectodermal mesenchymal derivatives, using a biological cell marking technique. Dev Biol. 41:1974;162-184.
37. Gershon M.D. Genes and lineages in the formation of the enteric nervous system. Curr Opin Neurobiol. 7:1997;101-109.
38. Lo L., Anderson D.J. Postmigratory neural crest cells expressing c-RET display restricted developmental and proliferative capacities. Neuron. 15:1995;527-539.
39. Hearn C.J., Murphy M., Newgreen D. GDNF and ET-3 differentially modulate the numbers of avian enteric neural crest cells and enteric neurons in vitro. Dev Biol. 197:1998;93-105.
40. Heuckeroth R.O., Lampe P.A., Johnson E.M., Milbrandt J. Neurturin and GDNF promote proliferation and survival of enteric neuron and glial progenitors in vitro. Dev Biol. 200:1998;116-129.
41. Chalazonitis A., Rothman T.P., Chen J., Gershon M.D. 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 GFRα-1 in vitro and in vivo. Dev Biol. 204:1998;385-406.
42. Taraviras S., Marcos-Gutierrez C.V., Durbec P., Jani H., Grigoriou M., Sukumaran M., Wang L.C., Hynes M., Raisman G., Pachnis V. Signalling by the RET receptor tyrosine kinase and its role in the development of the mammalian enteric nervous system. Development. 126:1999;2785-2797. This paper demonstrated that RET is a necessary receptor element for GDNF and NRTN to support neuronal survival in vitro, confirming that both RET and a GFRα are required for effective GFL signaling.
43. Molliver D.C., Wright D.E., Leitner M.L., Parsadanian A.S., Doster K., Wen D., Yan Q., Snider W.D. IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron. 19:1997;849-861.
44. Bennett D.L., Michael G.J., Ramachandran N., Munson J.B., Averill S., Yan Q., McMahon S.B., Priestley J.V. A distinct subgroup of small DRG cells express GDNF receptor components and GDNF is protective for these neurons after nerve injury. J Neurosci. 18:1998;3059-3072. This paper and [43] established that the IB4-binding non-TrkA expressing subset of nociceptive neurons in the DRG express RET, and respond to GDNF in vitro and after nerve injury.
45. -/- mice were selectively deficient in GFRα1-expressing neurons in the trigeminal ganglion.
46. Fundin B.T., Mikaels A., Westphal H., Ernfors P. A rapid and dynamic regulation of GDNF-family ligands and receptors correlate with the developmental dependency of cutaneous sensory innervation. Development. 126:1999;2597-2610.
47. Golden J.P., DeMaro J.A., Osborne P.A., Milbrandt J., Johnson E.M. Jr. Expression of Neurturin GDNF and GDNF family-receptor mRNA in the developing and mature mouse. Exp Neurol. 158:1999;504-528.
48. Henderson C.E., Phillips H.S., Pollock R.A., Davies A.M., Lemeulle C., Armanini M., Simpson L.C., Moffet B., Vandlen R.A., Koliatsos V.E., Rosenthal A. GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle. Science. 266:1994;1062-1064.
49. Nguyen Q.T., Parsadanian A.S., Snider W.D., Lichtman J.W. Hyperinnervation of neuromuscular junctions caused by GDNF overexpression in muscle. Science. 279:1998;1725-1729. This report demonstrates an interesting example of GDNF functioning in a non-canonical manner for a neurotrophic factor, using transgenic mice to demonstrate that GDNF, but not other neurotrophic factors, can regulate motor endplate innervation density.
50. ••], demonstrates the importance of NRTN as a target-derived trophic factor critical for the development of parasympathetic neurons signaling through the GFRα2-RET receptor.
51. Widenfalk J., Nosrat C., Tomac A., Westphal H., Hoffer B., Olson L. Neurturin and glial cell line-derived neurotrophic factor receptor-β (GDNFR-β), novel proteins related to GDNF and GDNFR-α with specific cellular patterns of expression suggesting roles in the developing and adult nervous system and in peripheral organs. J Neurosci. 17:1997;8506-8519.
52. Nosrat C.A., Tomac A., Hoffer B.J., Olson L. Cellular and developmental patterns of expression of Ret and glial cell line-derived neurotrophic factor receptor alpha mRNAs. Exp Brain Res. 115:1997;410-422.
53. Nishino J., Mochida K., Ohfuji Y., Shimazaki T., Meno C., Ohishi S., Matsuda Y., Fujii H., Saijoh Y., Hamada H. GFRα3, a component of the artemin receptor, is required for migration and survival of the superior cervical ganglion. Neuron. 23:1999;725-736. This paper provides the first insight into the developmental importance of ARTN-GFRα3 signaling, indicating that one of the major roles of GFRα3-RET appears to be for proper migration of sympathetic neurons of the superior cervical ganglion.
54. 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.
55. 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.et al. Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell. 76:1994;1001-1012.
56. Baloh R.H., Gorodinsky A., Golden J.P., Tansey M.G., Keck C.L., Popescu N.C., Johnson E.M. Jr., Milbrandt J. GFRα3 is an orphan member of the GDNF/neurturin/persephin receptor family. Proc Natl Acad Sci USA. 95:1998;5801-5806.
57. Durbec P.L., Larsson-Blomberg L.B., Schuchardt A., Costantini F., Pachnis V. Common origin and developmental dependence on c-ret of subsets of enteric and sympathetic neuroblasts. Development. 122:1996;349-358.
58. Snider W.D. Functions of the neurotrophins during nervous system development: What the knockouts are teaching us. Cell. 77:1994;627-638.