Neurturin mRNA expression suggests roles in trigeminal innervation of the first branchial arch and in tooth formation

Developmental Dynamics

Volumn 213, Issue 2, 1998, Pages 207-219

  Luukko, Keijo ^a,b   Saarma, Mart ^a   Thesleff, Irma ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

GDNF; Innerration; Neurons; Neurotrophic factors; NTN; Odontogenesis; Tooth; Trigeminal

Indexed keywords

GLYCOSYLPHOSPHATIDYLINOSITOL; NEUROTROPHIC FACTOR; NEURTURIN; RECEPTOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRANCHIAL ARCH; EMBRYO; EMBRYO DEVELOPMENT; EPITHELIUM CELL; IN SITU HYBRIDIZATION; INNERVATION; MOUSE; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; TOOTH DEVELOPMENT; TRIGEMINAL NERVE; VIBRISSA;

ANIMALS; APOPTOSIS; BASE SEQUENCE; BRANCHIAL REGION; CELL DIVISION; DNA, COMPLEMENTARY; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR RECEPTORS; IN SITU HYBRIDIZATION; MEMBRANE GLYCOPROTEINS; MESODERM; MICE; MICE, INBRED CBA; NERVE GROWTH FACTORS; NERVE TISSUE PROTEINS; NEURTURIN; ODONTOGENESIS; ORGAN CULTURE TECHNIQUES; PREGNANCY; RECEPTORS, CELL SURFACE; RECEPTORS, NERVE GROWTH FACTOR; RNA, MESSENGER; TOOTH; TRIGEMINAL NERVE;

ANIMALIA; MAMMALIA; STAPHYLOCOCCUS PHAGE 3A;

EID: 0031719356     PISSN: 10588388     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0177(199810)213:2<207::AID-AJA6>3.0.CO;2-K     Document Type: Article

References (75)

1. Airaksinen M, Suvanto P, Moshnyakov M, Saarma M. Expression and sequence homology of GDNF family receptors suggest roles in cell-cell interactions. Abstract in the 3rd International Meeting: Hirschsprung disease and related neurocristopathies. Evian, France, 1998.
2. Arenas E, Trupp M, Åkerud P, Ibáñez C. GDNF prevents degeneration and promotes the phenotype of brain noradrenergic neurons in vivo. Neuron 1995;15:1465-1473.
3. Arumäe U, Pirvola U, Palgi J, Kiema T-L, Palm K, Moshnyakov M, Ylikoski J, Saarma M. Neurotrophins and their receptors in rat peripheral trigeminal system during maxillary nerve growth. J. Cell Biol. 1993;122:1953-1065.
4. Atkinson M, Mohammed S. A histochemical study of the cholinergic and adrenergic innervation of the developing teeth and oral tissues in the mouse. Arch. Oral Biol. 1983;28:353-357.
5. Baloh RH, Tansey MG, Golden JP, Creedon DJ, Heuckeroth RO, Keck CL, Zimonjic DB, Popescu NC, Johnson EM, Milbrandt J. TrnR2, a novel receptor that mediates neuturin and GDNF signalling through ret. Neuron 1997;18:793-802.
6. Baloh RH, Gorodinsky A, Golden JP, Tansey MG, Keck CL, Popescu NC, Johnson EM, Milbrandt J. GFRα-3 is an orphan member of the GDNF/neuturin/persephin receptor family. Proc. Natl. Acad. Sci. USA 1998;95:5801-5806.
7. Buj-Bello A, Buchman VL, Horton A, Rosenthal A, Davies AM. GDNF is an age-specific survival factor for sensory and autonomic neurons. Neuron 1995;15:821-828.
8. Buj-Bello A, Adu J, Piñón LGP, Horton A, Thompson J, Rosenthal A, Chinchetru M, Buchman VL, Davies AM. Neurturin responsiveness requires a GPI-linked receptor and the Ret receptor tyrosine kinase. Nature 1997;387:721-724.
9. Byers M, Shatteman GC, Bothwell M. Multiple function for NGF receptor in developing, aging and injured rat teeth are suggested by epithelial, mesenchymal and neural immunoreactivity. Development 1990;109:461-471.
10. Creedon DJ, Tansey MG, Baloh RH, Osborne PA, Lampe PA, Fahrner TJ, Heuckeroth RO, Milbrandt J, Johnson EM. (1997) Neurturin shares receptors and signal transduction pathways with glial cell line-derived neurotrophic factor in sympathetic neurons. Proc. Natl. Acad. Sci. USA 1997;94:7018-7023.
11. Davies AM. The trigeminal system: An advantageous experimental model for studying neuronal development. Development 1988;103: 175-183.
12. Davies AM. Neurotrophin switching: Where does it stand. Curr. Opin. Neurobiol. 1997;7:110-118.
13. Davies AM, Lumsden AGS, Slavkin HC, Burnstock G. Influence of nerve growth factor on the embryonic mouse trigeminal ganglion in culture. Dev. Neurosci 1981;4:150-156.
14. Ebendal T. Use of collagen gels to bioassay nerve growth factor activity. In: Rush RA. ed. Nerve Growth Factors. Chichester: John Wiley and Sons, 1989:81-93.
15. Ebendal T, Tomac A, Hoffer BJ, Olson L. Glial cell-line-derived neurotrophic factor stimulates fiber formation and survival in cultured neurons from peripheral autonomic ganglia. J. Neurosci. Res. 1995;40:276-284.
16. Fristad I, Heyeraas KJ, Kvinnsland I. Nerve fibres and cells immunoreactive to neurochemical markers in developing rat molars and supporting tissues. Arch. Oral Biol. 1994;39:633-646.
17. Gavrieli Y, Sherman Y, Ben-Sasson SA. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol.1992;119:493-501.
18. Hellmich HL, Kos L, Cho ES, Mahon KA, Zimmer A. Embryonic expression of glial cell-line derived neurotrophic factor (GDNF) suggests multiple developmental roles in neural differentiation and epithelial-mesenchymal interactions. Mech. Dev. 1996;54:95-105.
19. Henderson CE, Phillips HS, Pollock RA, Davies AM, Lemeulle C, Armanini M, Simpson LC, Moffet B, Vandlen RA, Koliatsos VE, Rosenthal A. GDNF: A potent survival factor for motoneurons present in peripheral nerve and muscle. Science 1994;266:1062-1064.
20. Hildebrand C, Fried K, Tuisku F, Johansson CS. Teeth and tooth nerves. Prog. Neurobiol. 1995;45:165-222.
21. Jernvall J, Kettunen P, Karavanova I, Martin LB, Thesleff I. Evidence for the role of the enamel knot as a control center in mammalian tooth cusp formation: Non-dividing cells express growth stimulating Fgf-4 gene. Int. J. Dev. Biol. 1994;38:463-469.
22. Jernvall J, Åberg T, Kettunen P, Keränen S, Thesleff I. The life history of an embryonic signalling center: BMP-4 induces p21 and is associated with apoptosis in the mouse toota enamel knot. Development 1998;125:161-169.
23. Jing SQ, Wen DZ, Yu YB, Holst PL, Luo Y, Fang M, Tamir R, Antonio L, Hu Z, Cupples R, Louis JC, Hu S, Altrock BW, Fox GM. GDNF-induced activation of the Ret protein tyrosine kinase is mediated by GDNFR-a, a novel receptor for GDNF. Cell 1996;85:1113-1124.
24. Jing SQ, Hu Z, Fang M, Hu S, Holst PL, Boone T, Delaney J, Schultz H, Zhou R, Fox GM. GFRα-2 and GFRα-3 are two new receptors for ligands of the GDNF family. J. Biol Chem. 1997;272:33111-33117.
25. Kettunen P, Thesleff I. Expression and functions of FGFs-4, -8 and -9 suggest functional redundancy and repetitive use as epithelial signals during tooth morphogenesis. Dev. Dyn. 1998;211:256-268.
26. Kettunen P, Thesleff I. Responsiveness of developing dental tissues to fibroblast growth factors: Expression of splicing alternatives of FGFR1, -2, -3 and of FGFR4; and stimulation of cell proliferation by FGF-2, -4, -8 and -9. Dev. Genet. 1998;22:374-385.
27. Klein RD, Sherman D, Ho W-H, Stone D, Bennett GL, Moffat B, Vandlen R, Simmons L, Gu Q, Hongo J-A Devaux B, Poulsen K, Armanini M, Nozaki C, Asai N, Goddard A, Phillips H, Henderson CE, Takahashi M, Rosenthal A. A GPI-linked protein that interacts with Ret to form a candidate neurturin receptor. Nature 1997;387: 717-721.
28. Kotzbauer PT, Lampe PA, Heuckeroth RO, Golden JP, Greedon DJ, Johnson EM, Mildrandt JD. Neurturin, a relative of glial-cell-line-derived neurotrophic factor. Nature 1996;384:467-470.
29. Lewin GR, Barde Y-A. Physiology of neurotrophins. Annu. Rev. Neurosci. 1996;19:289-317.
30. Lin L-FH, Doherty DH, Lile JD, Bektesh S, Collins F. GDNF: A glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 1993;260:1130-1132.
31. Lumsden AGS. Spatial organization of the epithelium and the role of neural crest cells in the initiation of the mammalian tooth germ. Development 1988;103:155-169.
32. Lumsden AGS, Davies AM. Earliest sensory nerve fibers are guided to peripheral targets by attractants other than nerve growth factor. Nature 1983;306:786-788.
33. Luukko K. Immunohistochemical localisation of nerve fibres during the development of the embryonic rat molar using peripherin and PGP 9.5 antibodies. Arch. Oral Biol. 1997;42:189-195.
34. Luukko K. Neuronal cells and neurotrophins in odontogenesis. Eur. J. Oral Sci. 1998;106:80-93.
35. Luukko K, Moshnyakov M, Sainio K, Saarma M, Sariola H, Thesleff I. Expression of neurotrophin receptors during rat tooth development is developmentally regulated, independent of innervation and suggests functions in the regulation of morphogenesis and innervation. Dev. Dyn. 1996;206:87-99.
36. Luukko K, Arumäe U, Karavanov A, Moshnyakov M, Sainio K, Sariola H, Saarma M, Thesleff I. Neurotrophin mRNA expression in the developing tooth suggests multiple roles in nnervation and organogenesis. Dev. Dyn. 1997a;210:117-129.
37. Luukko K, Suvanto P, Saarma M, Thesleff I. Expression of GDNF and its receptors in developing tooth is developmentally regulated and suggests multiple roles in innervation and organogenesis. Dev. Dyn. 1997b;210:463-471.
38. Masure S, Cik M, Pangalos MN, Bonaventure P, Verhasselt P, Lesage ASJ, Leysen JE, Gordon RD. Molecular cloning, expression and tissue distribution of glial-cell-line-derived neurotrophic factor family receptor α-3 (GFRα-3). Eur J Biochem 1998;251:622-630.
39. 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, Vejseda R, Kato AC, Hynes M, Sherman D, Nishimura M, Wang L-C, Vandlen R Mofrat B, Klein RD, Poulsen K, Gray C, Garces A, Henderson CE, Phillips HS, Johnson EM. Persephin, a novel neurotrophic factor related to GDNF and neurturin. Neuron 1998;20:1-20.
40. Mina M, Kollar EJ. The induction of odontogenesis in non-dental mesenchyme combined with early murine mandibular arch epithelium. Arch. Oral Biol. 1987;32:123-127.
41. Mitsiadis TA, Dicou E, Joffre A, Magloire H. Immunohistochemical localization of nerve growth factor (NGF) and NGF receptor (NGF-R) in the developing first molar tooth of the rat. Differentiation 1992;49:47-61.
42. Mohamed SS, Atkinson ME. A histological study of the innervation of developing mouse teeth. J. Anat. 1983;136:735-749.
43. Molliver DC, Wright DE, Leitner ML, Parsadanian ASH, Doster K, Wen D, Van Q, Snider WD. IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron 1997;19: 849-861.
44. Moore MW, Klein RD, Farinas I, Sauer H, Armanini M, Phillips H, Reichardt LF, Ryan AM, Carver-Moore K, Rosenthal A. Renal and neuronal abnormalities in mice lacking GDNF. Nature 1996;382:76-79.
45. Naftel JP, Qian X-B, Bernanke JM. Effects of postnatal anti-nerve growth factor serum exposure on development of apical nerves of the rat molar. Dev. Brain Res. 1994;80:54-62.
46. Naveilhan P, Baudet C, Mikaeis Å, Shen L, Westphal H, Ernfors P. Expression and regulation of GFRα-3, a glial cell line-derived neurotrophic factor family receptor. Proc. Natl. Acad. Sci. USA 1998;95:1295-1300.
47. Neubüser A, Peters H, Balling R, Martin GR. Antagonistic interactions between FGF and BMP signaling pathways: A mechanism for positioning the sites of tooth formation. Cell 1997;90:247-255.
48. Nomoto S, Ito S, Yang LX, Kiuchi K. Molecular cloning and expression analysis of GFR alpha-3, a novel cDNA related to GDNFR alpha and NTNR alpha. Biochem. Biophys. Res. Commun. 1998;244:849-853.
49. Nosrat CA, Tomac A, Lindquist E, Lindskog S, Humpel C, Strömberg I, Ebendal T, Hoffer B, Olson L. Cellular expression of GDNF mRNAs suggest multiple functions inside and outside the nervous system. Cell. Tissue Res. 1996;286:191-207.
50. Nosrat CA, Tomac A, Hoffer BJ, Olson L. Cellular and developmental patterns of expression of Ret and glial cell line-derived neurotrophic factor receptors alpha mRNAs. Exp. Brain Res. 1997;115:410-422.
51. Nosrat CA, Fried K, Ebendal T, Olson, L. NGF, BDNF, NT3, NT4 and GDNF in tooth development. Eur. J. Oral Sci. 1998;106:94-99.
52. Olson L. The coming of age of the GDNF family and its receptors: Gene delivery in a rat Parkinson mode may have clinical implications. Trends Neurosci. 1997;20:277-279.
53. Oppenheim RW, Houenou LJ, Johnson JE, Lin LF, Li L, Lo AC, Newsome AL, Prevette DM, Wang S. Developing motor neurons rescued from programmed and axotomy-induced cell death by GDNF. Nature 1995;373:344-346.
54. Pichel JG, Shen L, Sheng HZ, Granholm A-C, Drago J, Grinberg A, Lee EJ, Huang SP, Saarma M, Hoffer BJ, Sariola H, Westphal H. Defects in enteric innervation and kidney development in mice lacking GDNF. Nature 1996;382:73-76.
55. Qian X-B, Naftel JP. The effects of anti-nerve growth factor on retrograde labeling of superior cervical ganglion neurones projecting to the molar pulp in the rat. Arch. Oral Biol. 1994;39:1041-1047.
56. Sainio K, Suvanto P, Saarma M, Arumäe U, Meng X, Lindahl M, Davies J, Pachnis V, Sariola H. Glial cell-line derived neurotrophic factor is required for bud initiation from the ureteric epithelium. Development 1997;124:3919-3928.
57. Sánchez MP, Silos-Santiago I, Frisén J, He B, Lira SA, Barbacid M. Renal agenesis and the absence of enteric neurons in mice lacking GDNF. Nature 1996;382:70-73.
58. Sanicola M, Hession C, Worley D, Carmillo P, Ehrenfels C, Walus L, Robinson S, Jaworski G, Wei H, Tizard R, Whitty A, Pepinsky RB, Cate RL. Glial cell line-derived neurotrophic factor-dependent Ret activation can be mediated by two different cell-surface accessory proteins. Proc. Natl. Acad. Sci. USA 1997;94:6238-6243.
59. Schuchardt A, D'Agati V, Larsson-Blomberg L, Costantini F, Pachnis V. Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret. Nature 1994;367:380-383.
60. Suvanto P, Hiltunen JO, Arumäe U, Moshnyakov M, Sariola H, Saarma M. Localization of glial cell line-derived neurotrophic factor (GDNF) mRNA in embryonic rat by in situ hybridization. Eur. J. Neurosci. 1996;8:816-822.
61. Suvanto P, Wartiovaara K, Lindahl M, Arumäe U, Moshnyakov M, Horelli-Kuitunen N, Airaksinen MS, Palotie A, Sariola H, Saarma M. Cloning, mRNA distribution and chromosomal localization of the gene for glial cell line-derived neurotrophic factor receptor β, a homologue to GDNFR-α. Hum. Mol. Genet. 1997;6:1267-1273.
62. Thesleff I, Vaahtokari A, Partanen A-M. Regulation of organogenesis: Common molecular mechanisms regulating the development of the teeth and other organs. Int. J. Dev. Biol. 1995;39:35-50.
63. Tomac A, Lindqvist E, Lin L-FH, Ögren SO, Young D, Hoffer BJ, Olson L. Protection and repair of the nigrostriatal dopaminergic system by GDNF in vivo. Nature 1995;373:335-339.
64. Treanor JSS, Goodman L, Desauvage F, Stone DM, Poulsen KT, Beck CD, Gray C, Armanini MP, Pollock RA, Hefti F, Phillips HS, Goddard A, Moore MW, Bujbello A. Davies AM, Asai N, Takahashi M, Vandlen R, Henderson CE, Rosenthal A. Characterization of a multicomponent receptor for GDNF. Nature 1996;382:80-83.
65. Trupp M, Ryden M, Jornvall H. Funakoshi H, Timmusk T, Arenas E, Ibáñez 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.
66. Trupp M, Arenas E, Fainzilber M, Nilsson AS, Sieber BA, Grigoriou M, Kilkenny C, Salazar-Grueso E, Pachnis V, Arumäe U, Saarma M, Ibáñez, CF. Functional receptor for GDNF encoded by c-Ret protooncogene. Nature 1996;381:785-789.
67. Tsuzuki H, Kitamura H. Immunohistochemical analysis of pulpal innervation in developing rat molars. Arch. Oral Biol. 1991;36:139-146.
68. Vaahtokari A, Aberg T, Jernvall J, Keränen S, Thesleff I. The enamel knot as a signaling center in the developing mouse tooth. Mech. Dev. 1996;54:39-43.
69. Vainio S, Karavanova I, Jowett A, Thesleff I. Identification of BMP-4 as a signal mediating secondary induction between epithelial and mesenchymal tissues during early tooth development. Cell 1993;75: 45-58.
70. Wang CY, Ni J, Jiang H, Hsu TA, Dugich-Djordjevic M, Feng L, Zhang M, Mei L, Gentz R, Lu B. Cloning and characterization of glial cell line-derived neurotrophic factor receptor-B: A novel receptor for members of glial cell line-derived neurotrophic factor family of neurotrophic factors. Neuroscience 1998;83:7-14
71. 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-a with specific cellular patterns of expression suggesting roles in the developing and adult nervous system and in peripheral organs. J. Neurosci. 1997;17:8506-8519.
72. Widenfalk J, Tomac A, Lindquist E, Hoffer B, Olson L. GFR-alpha-3, a protein related to GFR-alpha-1, is expressed in developing peripheral neurons and ensheating cells. Eur. J. Neurosci. 1998;10:1508-1517.
73. Wilkinson DG, Green J. In situ hybridization and the three-dimensional reconstruction of serial sections. In: Copp AJ, Cockroft DL, eds. Postimplantation Mammalian Embryos: A Practical Approach. Oxford: IRL Press, 1990:155-171.
74. Worby CA, Vega QC, Chao HH-J, SeasholtzAF, Thopson RC, Dixon JE. Identification and characterization of GFRα-3, a novel co-receptor belonging to the glial cell line-derived neurotrophic receptor family. J. Biol. Chem 1998;283:3502-3508.
75. Yan Q, Matheson C, Lopez OT. In vivo neurotrophic effects of GDNF on neonatal and adult facial motor neurons. Nature 1995;373:341-344.