Localization of GDNF/neurturin receptor (c-ret, GFRα-1 and α-2) mRNAs in postnatal rat brain: Differential regional and temporal expression in hippocampus, cortex and cerebellum

Molecular Brain Research

Volumn 73, Issue 1-2, 1999, Pages 151-171

  Burazin, Tanya C D ^a   Gundlach, Andrew L ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Development; GDNF; Gene expression; GFR 1 and GFR 2; GPI linked receptor; In situ hybridization histochemistry; Neurturin; Ret tyrosine kinase

Indexed keywords

GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA; NEURTURIN;

ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN REGION; CEREBELLUM; GENE EXPRESSION; HIPPOCAMPUS; HISTOCHEMISTRY; IN SITU HYBRIDIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; RNA ANALYSIS;

ANIMALS; ANIMALS, NEWBORN; BRAIN; CEREBELLUM; CEREBRAL CORTEX; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR RECEPTORS; HIPPOCAMPUS; IN SITU HYBRIDIZATION; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-RET; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR PROTEIN-TYROSINE KINASES; RNA, MESSENGER;

ANIMALIA;

EID: 0032751610     PISSN: 0169328X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0169-328X(99)00217-X     Document Type: Article

References (71)

1. Arenas E., Trupp M., Akerud P., Ibáñez C. GDNF prevents degeneration and promotes the phenotype of brain noradrenergic neurons in vivo. Neuron. 15:1995;1465-1473.
2. 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., Milbrandt J. TrnR2, a novel receptor that mediates neurturin and GDNF signaling through Ret. Neuron. 18:1997;793-802.
3. S.A. Bayer, J. Altman, Neurogenesis and neuronal migration, in: G. Paxinos (Ed.), The Rat Nervous System, Vol. 2, Academic Press, Sydney, 1995, pp. 1041-1078.
4. Buj-Bello A., Adu J., Piñón L.G.P., Horton A., Thompson J., Rosenthal A., Chinchetru M., Buchman V.L., Davies A.M. Neurturin responsiveness requires a GPI-linked receptor and the Ret receptor tyrosine kinase. Nature. 387:1997;721-724.
5. Buj-Bello A., Buchman V.L., Horton A., Rosenthal A., Davies A.M. GDNF is an age-specific factor for sensory and autonomic neurons. Neuron. 15:1995;821-828.
6. Burazin T.C.D., Gundlach A.L. Rapid and transient increases in cellular immediate early gene and neuropeptide mRNAs in cortical and limbic areas after amygdaloid kindling seizures in the rat. Epilepsy Res. 26:1996;281-293.
7. Burazin T.C.D., Gundlach A.L. Differential distribution, developmental profile and regulation of GDNFR-α and -β mRNA expression in rat brain. Eur. J. Neurosci. 10:1998;121.
8. Burazin T.C.D., Gundlach A.L. Up-regulation of GDNFR-α and c-ret mRNA in facial motor neurons following facial nerve injury in the rat. Mol. Brain Res. 55:1998;331-336.
9. Canzian F., Ushijima T., Nagao M., Matera I., Romeo G., Ceccherini I. Genetic mapping of the RET protooncogene on rat chromosome 4. Mamm. Genome. 6:1995;433-435.
10. Castrén E., Thoenen H., Lindholm D. Brain-derived neurotrophic factor messenger RNA is expressed in the septum, hypothalamus and in adrenergic brain stem nuclei of adult rat brain and is increased by osmotic stimulation in the paraventricular nucleus. Neuroscience. 64:1995;71-80.
11. Choi-Lundberg D.L., Bohn M.C. Ontogeny and distribution of glial cell line-derived neurotrophic factor (GDNF) mRNA in rat. Dev. Brain Res. 85:1995;80-88.
12. Enokido Y., de Sauvage F., Hongo J.-A., Ninkina N., Rosenthal A., Buchman V.L., Davies A.M. GFRα-4 and the tyrosine kinase Ret form a functional receptor complex for persephin. Curr. Biol. 8:1998;1019-1022.
13. Giehl K.M., Schacht C.M., Yan Q., Mestres P. GDNF is a trophic factor for adult rat corticospinal neurons and promotes their long-term survival after axotomy in vivo. Eur. J. Neurosci. 9:1997;2479-2489.
14. Glazner G.W., Mu X., Springer J.E. Localization of glial cell line-derived neurotrophic factor receptor alpha and c-ret mRNA in rat central nervous system. J. Comp. Neurol. 391:1998;42-49.
15. Golden J.P., Baloh R.H., Kotzbauer P.T., Lampe P.A., Osborne P.A., Milbrandt J., Johnson E.M. Jr. Expression of neurturin, GDNF, and their receptors in the adult mouse CNS. J. Comp. Neurol. 398:1998;139-150.
16. Haglund L., Swanson L.W., Köhler C. The projection of the supramammillary nucleus to the hippocampal formation: an immunohistochemical and anterograde transport study with the lectin PHA-L in the rat. J. Comp. Neurol. 229:1984;171-185.
17. Henderson C.E., Phillips H.S., Pollock R.A., Davies A.M., Lemeulle C., Armanini M., Simpson L.C., Moffat 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.
18. Herkenham M., Nauta W.J.H. Efferent connections of the habenular nuclei in the rat. J. Comp. Neurol. 187:1979;19-48.
19. Horger B.A., Nishimura M.C., Armanini M.P., Wang L.-C., Poulsen K.T., Rosenbald C., Kirik D., Moffat B., Simmons L., Johnson E. Jr., Milbrandt J., Rosenthal A., Bjorklund A., Vandlen R.A., Hynes M.A., Phillips H.S. Neurturin exerts potent actions on survival and function of midbrain dopaminergic neurons. J. Neurosci. 18:1998;4929-4937.
20. Humpel C., Hoffer B., Stromberg I., Bektesh S., Collins F., Olson L. Neurons of the hippocampal formation express glial cell line-derived neurotrophic factor messenger RNA in response to kainate-induced excitation. Neuroscience. 59:1994;791-795.
21. 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.
22. Jing S.J., Wen D., Yu Y., Holst P.L., Luo Y., Fang M., Tamir R., Antonio L., Hu Z., Cupples R., Louis J.-C., Hu S., Altrock B., Fox G.M. GDNF-induced activation of the ret protein tyrosine kinase is mediated by GDNFR-alpha, a novel receptor for GDNF. Cell. 85:1996;1113-1124.
23. Kitagawa H., Hayashi T., Mitsumoto Y., Koga N., Itoyama Y., Abe K. Reduction of ischemic brain injury by topical application of glial cell line-derived neurotrophic factor after permanent middle cerebral artery occlusion in rats. Stroke. 29:1998;1417-1422.
24. Klein R.D., Sherman D., Ho W.-H., Stone D., Bennett G.L., 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 C.E., Takahashi M., Rosenthal A. A GPI-linked protein that interacts with Ret to form a candidate neurturin receptor. Nature. 387:1997;717-721.
25. Kokaia Z., Airaksinen M.S., Nanobashvili A., Larsson E., Kujamäki E., Lindvall O., Saarma M. GDNF family ligands and receptors are differentially regulated after brain insults in the rat. Eur. J. Neurosci. 11:1999;1202-1216.
26. Kokaia Z., Gido G., Ringstedt T., Bengzon J., Kokaia M., Siesjo B.K., Persson H., Lindvall O. Rapid increase of BDNF mRNA levels in cortical neurons following spreading depression: regulation by glutamatergic mechanisms independent of seizure activity. Mol. Brain Res. 19:1993;277-286.
27. Kotzbauer P.T., Lampe P.A., Heuckeroth R.O., Golden J.P., Creedon D.J., Johnson E.M. Jr., Milbrandt J. Neurturin, a relative of glial-cell-line-derived neurotrophic factor. Nature. 384:1996;467-470.
28. Lapchak P.A., Miller P.J., Collins F., Jiao S. Glial cell line-derived neurotrophic factor attenuates behavioural deficits and regulates nigrostriatal dopaminergic and peptidergic markers in 6-hydroxydopamine-lesioned adult rats: comparison of intraventricular and intranigral delivery. Neuroscience. 78:1997;61-72.
29. Li L., Wutian W., Lin L.-F., Lei M., Oppenheim R.W., Houenou L.J. Rescue of adult mouse motoneurons from injury-induced cell death by glial cell line-derived neurotrophic factor. Proc. Natl. Acad. Sci. U. S. A. 92:1995;9771-9775.
30. Lin L.-F.H., 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.
31. Martin D., Miller G., Rosendahl M., Russell D.A. Potent inhibitory effects of glial derived neurotrophic factor against kainic acid mediated seizures in the rat. Brain Res. 683:1995;172-178.
32. Masure S., Cik M., Pangalos M.N., Bonaventure P., Verhasselt P., Lesage A.S.J., Leysen J.E., Gordon R.D. Molecular cloning, expression and tissue distribution of glial-cell-line-derived neurotrophic factor family receptor α-3 (GFRα-3). Eur. J. Biochem. 251:1998;622-630.
33. Matheson C.R., Carnahan J., Urich J.L., Bocangel D., Zhang T.J., Yan Q. Glial cell line-derived neurotrophic factor (GDNF) is a neurotrophic factor for sensory neurons: comparison with the effects of the neurotrophins. J. Neurobiol. 32:1997;22-32.
34. Milbrandt J., de Sauvage F.J., Fahmer T.J., Baloh R.H., Leitner M.L., Tansey M.G., Lampe P.A., Heuckeroth R.O., Kotzbauer P.T., Simburger K.S., Golden J.P., Davies J.A., Vejsada R., Kato A.C., Hynes M., Sherman D., Nishimura M., Wang L.-C., Vandlen R., Moffat B., Klein R.D., Poulsen K., Gray C., Garces A., Henderson C.E., Philips H.S., Johnson E.M. Jr. Persephin, a novel neurotrophic factor related to GDNF and neurturin. Neuron. 20:1998;245-253.
35. Mount H.T.J., Dean D.O., Alberch J., Dreyfus C.F., Black I.B. Glial cell line-derived neurotrophic factor promotes the survival and morphologic differentiation of Purkinje cells. Proc. Natl. Acad. Sci. U. S. A. 92:1995;9092-9096.
36. Naveilhan P., ElShamy W.M., Ernfors P. Differential regulation of mRNAs for GDNF and its receptors ret and GDNFRα after sciatic nerve lesion in the mouse. Eur. J. Neurosci. 9:1997;1450-1460.
37. 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.
38. Nosrat C.A., Tomac A., Lindqvist E., Lindskog S., Humpel C., Stromberg I., Ebendal T., Hoffer B.J., Olson L. Cellular expression of GDNF mRNA suggests multiple functions inside and outside the nervous system. Cell Tissue Res. 286:1996;191-207.
39. Oppenheim R.W., Houenou L.J., Johnson J.E., Lin L.-F.H., Li L., Lo A.C., Newsome A.L., Prevette D.M., Wang S. Developing motor neurons rescued from programmed and axotomy-induced cell death by GDNF. Nature. 373:1995;344-346.
40. G. Paxinos, K.W.S. Ashwell, I. Tork, Atlas of the Developing Rat Nervous System., 2nd edn., Academic Press, Sydney, 1994.
41. G. Paxinos, C. Watson, The Rat Brain in Stereotaxic Coordinates, 2nd edn., Academic Press, Sydney, 1986.
42. Pochon N.A.-M., Menoud A., Tseng J.L., Zurn A.D., Aebischer P. Neuronal GDNF expression in the adult rat nervous system identified by in situ hybridization. Eur. J. Neurosci. 9:1997;463-471.
43. J.L. Price, Thalamus, in: G. Paxinos (Ed.), The Rat Nervous System, Academic Press, Sydney, 1995, pp. 629-648.
44. Reeben M., Laurikainen A., Hiltunen J.O., Castrén E., Saarma M. The messenger RNAs for both glial cell line-derived neurotrophic factor receptors, c-ret and GDNFRα, are induced in the rat brain in response to kainate-induced excitation. Neuroscience. 83:1998;151-159.
45. Rønnekleiv O.K., Kelly M.J., Wuttke W. Single unit recordings in the rat pineal gland: evidence for habenulo-pineal neural connections. Exp. Brain Res. 39:1980;187-192.
46. Rønnekleiv O.K., Møller M. Brain-pineal nervous connections in the rat: an ultrastructure study following habenular lesion. Exp. Brain Res. 37:1979;551-562.
47. Ryan M.C., Gundlach A.L. Localization of preprogalanin messenger RNA in rat brain: identification of transcripts in a subpopulation of cerebellar Purkinje cells. Neuroscience. 70:1996;709-728.
48. Ryan M.C., Gundlach A.L. Differential regulation of angiotensinogen and natriuretic peptide mRNAs in rat brain by osmotic stimuli: focus on anterior hypothalamus and supraoptic nucleus. Peptides. 18:1997;1365-1375.
49. Ryan M.C., Loiacono R.E., Gundlach A.L. Galanin messenger RNA during postnatal development of the rat brain: expression patterns in Purkinje cells differentiate anterior and posterior lobes of cerebellum. Neuroscience. 78:1997;1113-1127.
50. Sanicola M., Hession C., Worley D., Carmillo P., Ehrenfels C., Walus L., Robinson S., Jaworski G., Wei H., Tizard R., Whitty A., Pepinsky R.B., Cate R.L. Glial cell line-derived neurotrophic factor-dependent RET activation can be mediated by two different cell-surface accessory proteins. Proc. Natl. Acad. Sci. U. S. A. 94:1997;6238-6243.
51. Shen P.-J., Gundlach A.L. Differential increases in chromogranins, but not synapsin I, in cortical neurons following spreading depression: implications for functional roles and transmitter peptide release. Eur. J. Neurosci. 10:1998;2217-2230.
52. 1B-adrenoceptors. Exp. Neurol. 154:1998;612-627.
53. Stromberg I., Bjorklund L., Johansson M., Tomac A., Collins F., Olson L., Hoffer B., Humpel C. Glial cell line-derived neurotrophic factor is expressed in the developing but not adult striatum and stimulates developing dopamine neurons in vivo. Exp. Neurol. 124:1993;401-412.
54. Sutherland R.J. The dorsal diencephalic conduction system: a review of the anatomy and functions of the habenular complex. Neurosci. Biobehav. Rev. 6:1982;1-13.
55. Suvanto P., Wartiovaara K., Lindahl M., Arumäi 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. Mol. Genet. 6:1997;1267-1273.
56. Thompson J., Doxakis E., Piñón L.G.P., Strachan P., Bujbello A., Wyatt S., Buchman V.L., Davies A.M. GFR α-4, a new GDNF family receptor. Mol. Cell. Neurosci. 11:1998;117-126.
57. Tomac A., Lindqvist E., Lin L.-H., Ogren S.O., Young D., Hoffer B.J., Olson L. Protection and repair of the nigrostriatal dopaminergic system by GDNF in vivo. Nature. 373:1995;335-339.
58. Treanor J.J.S., Goodman L., de Sauvage F., Stone D.M., Poulsen K.T., Beck C.D., Gray C., Armanini M.P., Pollock R.A., Hefti F., Phillips H.S., Goddard A., Moore M.W., Buj-Bello A., Davies A.M., Asai N., Takahashi M., Vandlen R., Henderson C.E., Rosenthal A. Characterization of a multicomponent receptor for GDNF. Nature. 382:1996;80-83.
59. Trupp M., Belluardo N., Funakoshi H., Ibáñez C.F. Complementary and overlapping expression of glial cell line-derived neurotrophic factor (GDNF), c-ret proto-oncogene, and GDNF receptor-α indicates multiple mechanisms of trophic actions in the adult rat CNS. J. Neurosci. 17:1997;3554-3567.
60. Trupp M., Raynoschek C., Belluardo N., Ibáñez C.F. Multiple GPI-anchored receptors control GDNF-dependent and independent activation of the c-ret receptor tyrosine kinase. Mol. Cell. Neurosci. 11:1998;47-63.
61. Trupp M., Ryden M., Jornvall H., Funakoshi H., Timmusk T., Arenas E., Ibáñez 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.
62. Wang C.-Y., Ni J., Jiang H., Hsu T.-A., 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. 83:1998;7-14.
63. Wang Y., Lin S.-Z., Chiou A.-L., Williams L.R., Hoffer B.J. Glial cell line-derived neurotrophic factor protects against ischemia-induced injury in the cerebral cortex. J. Neurosci. 17:1997;4341-4348.
64. 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 GNDFR-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.
65. Widenfalk J., Tomac A., Lindqvist E., Hoffer B., Olson L. GFRα-3, a protein related to GFRα-1, is expressed in developing peripheral neurons and ensheathing cells. Eur. J. Neurosci. 10:1998;1508-1517.
66. Williams L.R., Inouye G., Cummins V., Pelleymounter M.A. Glial cell line-derived neurotrophic factor sustains axotomized basal forebrain cholinergic neurons in vivo: dose-response comparison to nerve growth factor and brain-derived neurotrophic factor. J. Pharmacol. Exp. Ther. 277:1996;1140-1151.
67. Winkler C., Sauer H., Lee C.S., Björklund A. Short-term GDNF treatment provides long-term rescue of lesioned nigral dopaminergic neurons in a rat model of Parkinson's disease. J. Neurosci. 16:1996;7206-7215.
68. W. Wisden, B.J. Morris, In situ hybridization with synthetic oligonucleotide probes, in: W. Wisden, B.J. Morris (Eds.), In Situ Hybridization Protocols for the Brain, Academic Press, London, 1994, pp. 9-34.
69. Yan Q., Matheson C., Lopez O.T. In vivo neurotrophic effects of GDNF on neonatal and adult facial motor neurons. Nature. 373:1995;341-344.
70. Yu T., Scully S., Yu Y., Fox G.M., Jing S., Zhou R. Expression of GDNF family receptor components during development: implications in the mechanisms of interaction. J. Neurosci. 18:1998;4684-4696.
71. Zurn A.D., Winkel L., Menoud A., Djabali K., Aebischer P. Combined effects of GDNF, BDNF and CNTF on motoneuron differentiation in vitro. J. Neurosci. Res. 44:1996;133-141.