Striatal dopaminergic afferents concentrate in GDNF-positive patches during development and in developing intrastriatal striatal grafts

Journal of Comparative Neurology

Volumn 406, Issue 2, 1999, Pages 199-206

  López Martín, Elena ^a   Caruncho, Hector J ^a   Rodríguez Pallares, Jannette ^a   Guerra, Mariáa José ^a   Labandeira García, José Luis ^a,b  

^a UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^b Facultad de Medicina   (Spain)

Author keywords

Basal ganglia; Neuronal transplants; Neurotrophic factors; Rat

Indexed keywords

GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; IBOTENIC ACID; PHOSPHOPROTEIN DARPP 32; TYROSINE 3 MONOOXYGENASE;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN DEVELOPMENT; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; FEMALE; FETUS; IMMUNOCYTOCHEMISTRY; INNERVATION; MESENCEPHALON; NERVE GRAFT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SENSORY NERVE;

ANIMALS; ANIMALS, NEWBORN; CELL TRANSPLANTATION; CORPUS STRIATUM; DOPAMINE; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; MESENCEPHALON; NERVE GROWTH FACTORS; NERVE TISSUE PROTEINS; NEURONS, AFFERENT; RATS; RATS, SPRAGUE-DAWLEY;

EID: 0033526078     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19990405)406:2<199::AID-CNE5>3.0.CO;2-Z     Document Type: Article

References (57)

1. Beck KD, Valverde J, Alexi T, Poulsen K, Moffat B, Vandlen RA, Rosenthal A, Hefti F. 1995. Mesencephalic dopaminergic neurons protected by GDNF from axotomy-induced degeneration in the adult brain. Nature 373:339-341.
2. Björklund A, Rosenblad C, Winkler C, Kirik D. 1997, Studies on neuroprotective and regenerative effects of GDNF in a partial lesion model of Parkinson's disease. Neurobiol Disease 4:186-200.
3. Bowenkamp KE, Hoffman AF, Gerhardt GA, Henry MA, Biddle PT, Hoffer BJ, Granholm ACE. 1995. Glial cell line-derived neurotrophic factor supports survival of injured midbrain dopaminergic neurons. J Comp Neurol 355:479-489.
4. Bowenkamp KE, Lapchak PA, Hoffer BJ, Miller PJ, Bickford PC. 1997. Intracerebroventricular glial cell line-derived neurotrophic factor improves motor function and supports nigrostriatal dopamine neurons in bilaterally 6-hydroxydopamine lesioned rats. Exp Xeurol 145:104-117.
5. Broaddus WC, Bennett JP. 1990. Postnatal development of striatal dopamine function. I. An examination of D1 and D2 receptors, adenylate cyclase regulation and pre-synaptic dopamine markers. Dev Brain Res 52:265-271.
6. Choi-Lundberg DL, Bohn MC. 1995. Ontogeny and distribution of glial cell line-derived neurotrophic factor (GDNF) mRNA in rat. Dev Brain Res;85:80-88.
7. Choi-Lundberg DL, Lin Q, Chang YN, Chiang YL, Hay CM, Mohajeri H, Davidson BL, Bohn MC. 1997. Dopaminergic neurons protected from degeneration by GDNF gene therapy. Science 275:838-841.
8. Constantini LC, Vozza RM, Snyder-Keller AM. 1994. Enhanced efficacy of nigral-striatal cotransplants in bilaterally dopamine-depleted rats: An anatomical and behavioural analysis. Exp Neurol 127:219-231.
9. De Beaurepaire R, Freed W. 1987. Embryonic substantia nigra grafts innervate embryonic striatal co-grafts in preference to mature host striatum. Exp Neurol 95:448-454.
10. Deckel AW, Robinson RG, Coyle JT, Sandberg PR. 1983. Reversal of longterm locomotor anormalities in the kainic acid model of Huntington's disease by day 18 fetal striatal implants. Eur J Pharmacol 93:287-288.
11. DiFiglia M, Schiff L, Deckel AW. 1988. Neuronal organization of fetal striatal grafts in kainate- and sham-lesioned rat caudate nucleus: light- and electron-microscopic observations. J Neurosci 8:1112-1130.
12. Dunnett SB, Björklund A. 1997. Basic neural transplantation techniques. I. Dissociated cell suspension grafts of embryonic ventral mesencephalon in the adult rat brain. Brain Res Protocols 1:91-99.
13. Dunnett SB, Isacson O, Sirinagthsinghji DHS, Clarke DJ, Björklund A. 1988. Striatal grafts in rats with unilateral striatal lesions. II. Recovery form dopamine dependent motor asymmetry deficits in skilled paw reaching. Neuroscience 24:813-820.
14. Foster GA, Schulzberg M, Hökfelt T, Goldstein M, Hemmings CH, Ouimet CC, Walaas SI, Greengard P. 1987. Development of a dopamine- and cyclid adenosine 3′:5′-monophosphate-regulated phosphoprotein (DARPP-32) in the prenatal rat central nervous system, and its relationship to the arrival of presumptive dopaminergic innervation. J Neurosci 7:1994-2018.
15. A-receptor subtypes during postnatal development and immunohistochemical study. J Neurosci 14:5302-5324.
16. Gash DM, Zhang Z, Ovadia A, Cass WA, Yi A, Simmerman L, Russell D, Martin D, Lapchak PA, Collins F, Hoffer BJ, Gerhardt GA. 1996. Functional recovery in Parkinsonian monkeys treated with GDNF. Nature 380:252-255.
17. Granholm AC, Mott JL, Bowenkamp K, Eken S, Henry S, Hoffer BJ, Lapchak PA, Palmer MR, Van Home C, Gerhardt GA. 1997. Glial cell line-derived neurotrophic factor improves survival of ventral mesencephalic grafts to the 6-hydroxydopamine lesioned striatum. Exp Brain Res 116:29-38.
18. Graybiel AM, Liu FC, Dunnett SB. 1989. Intrastriatal grafts derived from fetal striatal primordia: I. Phenotype and modular organization. J Neurosci 9:3250-3272.
19. Hudson J, Granholm AC, Gerhardt GA, Henry MA, Hoffma A, Biddle P, Leela NS, Mackerlova L, Lile JD, Collins F, Hoffer BJ. 1995. Glial cell line-derived neurotrophic factor augments dopaminergic circuits in vivo. Brain Res Bull 36:425-432.
20. Isacson O, Brundin P, Gage FH, Björklund A. 1984. Functional neural replacement by grafted neurons in the ibotenic acid-lesioned striatum. Nature 311:458-460.
21. Kearns CM, Gash DM. 1995. GDNF protects nigral dopamine neurons against 6-hydroxydopamine in vivo. Brain Res 672:104-111.
22. Labandeira-García JL, Guerra MJ. 1994. Cortical stimulation induces Fos expression in intrastriatal striatal grafts. Brain Res 2:87-97.
23. Labandeira-García JL, Liste I, Tobio JP, Rozas G, Lopez-Martin E, Guerra MJ. 1995. Intrathalamic striatal grafts survive and affect circling behaviour in adult rats with excitotoxically lesioned striatum. Neuroscience 68:737-749.
24. Labandeira-García JL, Tobio JP, Guerra MJ. 1994. Comparison between normal developing striatum and developing striatal grafts using drug-induced Fos expression and neuron-specific enolase immunohistochemistry. Neuroscience 60:399-415.
25. Labandeira-García JL, Wictorin K, Cunningham ET, Björklund A. 1991. Development of intrastriatal striatal grafts and their afferent innervation from the host. Neuroscience 42:407-426.
26. Lapchak PA, Miller PJ, Collins F, Jiao S. 1997. 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 78:61-72.
27. Lin LFH, Doherty DH, Lile JD, Bektesh S, Collins F. 1993. GDNF: A glial cell line-derived neurothropic factor for midbrain dopaminergic neurons. Science 260:1130-1132.
28. Lindsay RM, Yancopoulos GD. 1996. GDNF in a bind with known orphan: Accessory implicated in new twist. Neuron 17:571-574.
29. A receptor subunit expression in intrastriatal striatal grafts. Comparison between normal developing striatum and developing striatal grafts. Dev Brain Res;103:185-194.
30. Moore MW, Klein RD, Farinas I, Sauer H, Armanini M, Phillips H, Reichardt LF, Ryan AM, Carven-Moore K, Rosenthal A. 1996. Renal and neuronal abnormalities in mice lacking GDNF. Nature 382:76-79.
31. Nosrat CA, Tomac A, Lindqvist E, Lindskog S, Humpel C, Strömberg I, Ebendal T, Hoffer BJ, Olson L. 1996. Cellular expression of GDNF mRNA suggests multiple functions inside and outside the nervous system. Cell Tissue Res 286:191-207.
32. Olsson M, Campbell K, Wictorin K, Björklund A. 1995. Projection neurons in fetal striatal transplants are predominantly derived from the lateral ganglionic eminence. Neurocience 69:1169-1182.
33. Oppenheim RW, Houenou LJ, Johnson JE, Lin LFH, Li L, Lo AC, Newsome AL, Prevette DM, Wang S. 1995. Developing motor neurons rescued from programmed and axotomy-induced cell death by GDNF. Nature 373:344-346.
34. Pakzaban P, Deacon TW, Burns LH, Isacson O. 1993. Increased proportion of acetylcholinesterase-rich zones and improved morphological integration in host striatum of fetal grafts derived from the lateral but not meidal ganglionic eminence. Exp Brain Res 97:13-22.
35. Pichel JG, Shen L, Sheng HZ, Granholm AC, Drago J, Grinberg A, Lee EJ, Huang SP, Saarmas M, Hoffer BJ, Sariola H, Westphal H. 1996. Defects in enteric innervation and kidney development in mice lacking GDNF. Nature 382:73-76.
36. Pochon NAM, Menoud A, Tseng JL, Zum AD, Aebischer P. 1997. Neuronal GDNF expression in the adult rat nervous system identified by in situ hybridization. Eur J Neurosci 9:463-471.
37. Rosenblad C, Martinez-Serrano A, Björklund A. 1996. Glial cell line-derived neurotrophic factor increases survival, growth and function of intrastriatal fetal nigral dopaminergic grafts. Neuroscience 75:979-985.
38. Sánchez MP, Silos-Santiago I, Frisén J, He B, Lira SA, Barbacid M. 1996. Renal agenesis and the absence of enteric neurons in mice lacking GDNF. Nature 382:70-73.
39. Sauer H, Rosenblad C, Björklund A. 1995. Glial cell line-derived neurothropic factor but not transforming growth factor β3 prevents delayed degeneration of nigral dopaminergic neurons following striatal 6-hydroxydopamine lesion. Proc Natl Acad Sci 92:8935-8939.
40. Sautter J, Tseng JL, Braguglia D, Aebischer P, Spenger C, Seiler RW, Widmer HR, Zurn AD. 1998. Implants of polymer-encapsulated genetically modified cells releasing glial cell line-derived neurotrophic factor improve survival, growth, and function of fetal dopaminergic cells. Exp Neurol 149:230-236.
41. Schaar DG, Sieber BA, Dreyfus CF, Black IB. 1993. Regional and cell-specific expression of GDNF in rat brain. Exp Neurol 124:368-371.
42. Springer JE, Mu X, Bergmann LW, Trojanowski JQ. 1994. Expression of GDNF mRNA in rat and human nervous tissue. Exp Neurol 124:167-170.
43. Strömberg I, Björklund L, Johansson M, Tomac A, Collins F, Olson L, Hoffer B, Humpel C. 1993. Glial cell line-dervied neurotrophic factor is expressed in the developing but not adult striatum and stimulates developing dopamine neurons in vivo. Exp Neurol 124:401-412.
44. Suvanto P, Hiltunen JO, Arumäe U, Moshnyakov M, Sariola H, Sainio K, Saarma M. 1996. Localization of glial cell line-derived neurotrophic factor (GDNF) mRNA in embryonic rat by in situ hybridization. Eur J Neurosci 8:816-822.
45. Tomac A, Lindqvist E, Lin LFH, Ögren SO, Young D, Hoffer BH, Olson L. 1995a. Protection and repair of the nigrostriatal dopaminergic system by GDNF in vivo. Nature 373:335-339.
46. Tomac A, Widenfalk J, Lin LFH, Kohno T, Ebendal T, Hoffer BJ, Olson L. 1995b. Retrograde axonal transport of glial cell line-derived neurotrophic factor in the adult nigrostriatal system suggests a trophic role in the adult. Proc Natl Acad Sci USA 92:8274-8278.
47. Trok K, Hoffer B, Olson L. 1996. Glial cell line-derived neurotrophic factor enhances survival and growth of prenatal and postnatal spinal cord transplants. Neuroscience 71:231-241.
48. Trupp M, Belluardo N, Fukanoshi H, Ibáñez CF. 1997. Complementary and overlapping expression of glial cell line-derived neurotrophic factor (GDNF), c-ret proto-oncogene, and GDNF receptor-α indicates multiple mechanisms of thropic actions in the adult rat CNS. J Neurosci 17:3554-3567.
49. Unsicker K. 1996. GDNF: a cytokine at the interface of TGF-βs and neurothropins. Cell Tissue Res 286:175-178.
50. Voorn P, Kalsbeek A, Jorritsma-Byham B, Groenewegen HJ. 1988. The pre- and postnatal development of the dopaminergic cell groups in the ventral mesencephalon and dopamine innervation of the striatum of the rat. Neuroscience 25:857-887.
51. Wang Y, Tien LT, Lapchak PA, Hoffer BJ. 1996. GDNF triggers fiber outgrowth of fetal ventral mesencephalic grafts form nigra to striatum in 6-OHDA-lesioned rats. Cell Tissue Res 286:225-234.
52. Wictorin K, Ouimet CC, Björklund A. 1989a. Intrinsic organization and connectivity of intrastriatal striatal transplants as revealed by DARPP-32 immunohistochemistry: specificity of connections with the lesioned host brain. Eur J Neurosci 1:690-701.
53. Wictorin K, Simmerly RB, Isacson O, Swanson LW, Björklund A. 1989b. Connectivity of striatal grafts implanted into ibotenic acid lesioned striatum. III. Efferent projecting graft neurons and their relation to host afferents within the grafts. Neuroscience 30:313-330.
54. Winkler C, Sauer H, Lee CS, Björklund A. 1996. Short-term GDNF treatment provides long-term rescue of lesioned nigral dopaminergic neurons in a rat model of Parkinson's disease. J Neurosci 16:7206-7215.
55. Won L, Heller A, Hoffmann PC. 1989. Selective association of dopamine axons with their striatal target cells in vitro. Dev Brain Res;74:93-100.
56. Yan Q, Matheson C, Lopez OT. 1995. In vivo neurothropic effects of GDNF on neonatal and adult facial motor neurons. Nature;373:341-344.
57. Yurek D, Collier T, Sladek J. 1990. Embryonic mesencephalic and striatal co-grafts: Development of grafted dopamine neurons and functional recovery. Exp Neurol 109:191-199.