Differential expression of neurotrophin and neurotrophin receptor mRNAs in and adjacent to fetal midbrain grafts implanted into the dopamine- denervated striatum

Journal of Comparative Neurology

Volumn 423, Issue 3, 2000, Pages 462-473

  Yurek, David M ^a   Seroogy, Kim B ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

BDNF; Neural transplantation; NT 3; Parkinson's disease; Rat; trkB; trkC

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; COMPLEMENTARY RNA; MESSENGER RNA; NEUROTROPHIN; NEUROTROPHIN RECEPTOR; OXIDOPAMINE; PROTEIN TYROSINE KINASE; RECEPTOR SUBTYPE; TYROSINE 3 MONOOXYGENASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN INJURY; BRAIN TRANSPLANTATION; CONTROLLED STUDY; CORPUS STRIATUM; DENERVATION; DISEASE COURSE; FETUS; MALE; MESENCEPHALON; NEUROTROPISM; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; POSTOPERATIVE PERIOD; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; RAT; RNA PROBE; TREATMENT OUTCOME;

ANIMALS; BRAIN TISSUE TRANSPLANTATION; BRAIN-DERIVED NEUROTROPHIC FACTOR; CEREBRAL CORTEX; CORPUS STRIATUM; DENERVATION; DOPAMINE; GENE EXPRESSION; IN SITU HYBRIDIZATION; MALE; MESENCEPHALON; NEURONS; NEUROTROPHIN 3; OXIDOPAMINE; PARKINSON DISEASE, SECONDARY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, TRKB; RECEPTOR, TRKC; RNA, MESSENGER; SYMPATHOLYTICS; TYROSINE 3-MONOOXYGENASE;

EID: 0034738777     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/1096-9861(20000731)423:3<462::AID-CNE9>3.0.CO;2-U     Document Type: Article

References (56)

1. Altar CA, DiStefano PS. 1998. Neurotrophin trafficking by anterograde transport. Trends Neurosci 21:433-437.
2. Altar CA, Boylan CB, Jackson C, Hershenson S, Miller J, Wiegand SJ, Lindsay RM, Hyman C. 1992. Brain-derived neurotrophic factor augments rotational behavior and nigrostriatal dopamine turnover in vivo. Proc Natl Acad Sci USA 89:11347-11351.
3. 125I]NT-3. Eur J Neurosci 6:1389-1404.
4. Altar CA, Boylan CB, Fritsche M, Jackson C, Hyman C, Lindsay RM. 1994b. The neurotrophins NT-4/5 and BDNF augment serotonin, dopamine and GABAergic systems during behaviorally effective infusions to the substantia nigra. Exp Neurol 130:31-40.
5. Altar CA, Cai N, Bliven T, Juhasz M, Conner JM, Acheson AL, Lindsay RM, Wiegand SJ. 1997. Anterograde transport of brain-derived neurotrophic factor and its role in the brain. Nature 389:856-860.
6. Berkemeier LR, Winslow J, Kaplan DR, Nikolics K, Goeddel D, Rosenthal A. 1991. Neurotrophin-5: a novel neurotrophic factor that activates trk and trkB. Neuron 7:857-866.
7. Brundin P, Strecker RE, Lindvall O, Isacson O, Nilsson OG, Bardin G, Prochiantz A, Forni C, Nieoullon A, Widner H, Gage FH, Björklund A. 1987. Intracerebral grafting of dopamine neurons. Ann N Y Acad Sci 495:473-496.
8. Carvey PM, Ptak LR, Nath ST, Sierens DK, Mufson EJ, Goetz CG, Klawans HL. 1993. Striatal extracts from patients with Parkinson's disease promote dopamine neuron growth in mesencephalic cultures. Exp Neurol 120:149-152.
9. Carvey PM, Lin DH, Faselis CJ, Notermann JK, Ling ZD. 1996. Loss of striatal DA innervation increases striatal trophic activity directed at DA neurons in culture. Exp Neurol 140:184-197.
10. Carvey PM, Vu TQ, Ling ZD, Lipton JW, Sortwell CE, Collier TJ. 1998. The compensatory increase in striatal trophic activity is reduced in the aged rat brain. Am Soc Neural Transplant 4:55.
11. Collier TJ, Steece-Collier K. 1996. 28 month old rats with a 16 month history of unilateral nigrostriatal lesion: drug-induced behavior and response to grafted dopamine neurons and Schwann cells. Soc Neurosci Abstr 22:1209.
12. Collier TJ, Sortwell CE, Daley BF. 1999. Diminished viability, growth, and behavioral efficacy of fetal dopamine neuron grafts in aging rats with long-term dopamine depletion: an argument for neurotrophic supplementation. J Neurosci 19:5563-5573.
13. Dragunow MN, Butterworth N, Waldvogel H, Faull RLM, Nicholson LFB. 1995. Prolonged expression of Fos-related antigens, JunB and TrkB in dopamine-denervated striatal neurons. Brain Res Mol Brain Res 30: 393-396.
14. Duan W-C, Widner H, Brundin P. 1995. Temporal pattern of host responses against intrastriatal grafts of syngeneic, allogeneic or xenogeneic embryonic neuronal tissue in rats. Exp Brain Res 104:227-242.
15. Frank L, Ventimiglia R, Anderson K, Lindsay RM, Rudge JS. 1996. BDNF down-regulates neurotrophin responsiveness, TrkB protein and TrkB mRNA levels in cultured rat hippocampal neurons. Eur J Neurosci 8:1220-1230.
16. Friedman WJ, Olson L, Persson J. 1991. Cells that express brain-derived neurotrophic factor mRNA in the developing postnatal brain. Eur J Neurosci 3:688-697.
17. Gall CM. 1993. Seizure-induced changes in neurotrophin expression: implications for epilepsy. Exp Neurol 124:150-166.
18. Gall CM, Gold SJ, Isackson PJ, Seroogy KB. 1992. Brain-derived neurotrophic factor and neurotrophin-3 mRNAs are expressed in ventral midbrain regions containing dopaminergic neurons. Mol Cell Neurosci 3:56-63.
19. Hagg T. 1998. Neurotrophins prevent death and differentially affect tyrosine hydroxylase of adult rat nigrostriatal neurons in vivo. Exp Neurol 149:183-192.
20. Hicks RR, Numan S, Dhillon HS, Prasad MR, Seroogy KB. 1997. Alterations in BDNF and NT-3 mRNAs in rat hippocampus after experimental brain trauma. Brain Res Mol Brain Res 48:401-406.
21. Humpel C, Giacobini MMJ, Wetmore C, Olson L. 1994. Brain-derived neurotrophic factor and trkB receptor mRNAs in grafts of cortex cerebri. Exp Neurol 127:171-177.
22. Humpel C, Strömberg I, Olson L. 1995. Expression of nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3 mRNAs in human cortical xenografts. J Neural Transplant Plast 5:257-264.
23. Hyman C, Hofer M, Barde Y-A, Juhasz M, Yancopoulos GD, Squinto SP, Lindsay RM. 1991. BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature 350:230-232.
24. Hyman C, Juhasz M, Jackson C, Wright P, Ip NY, Lindsay RM. 1994. Overlapping and distinct actions of the neurotrophins BDNF, NT-3 and NT-4/5 on cultured dopaminergic and GABAergic neurons of the ventral mesencephalon. J Neurosci 14:335-347.
25. Kawamoto Y, Nakamura S, Nakano S, Oka N, Akiguchi I, Kimura J. 1996. Immunohistochemical localization of brain-derived neurotrophic factor in adult brain. Neuroscience 74:1209-1226.
26. Klein R, Martin-Zanca D, Barbacid M, Parada LF. 1990. Expression of the tyrosine kinase receptor gene trkB is confined to the murine embryonic and adult nervous system. Development 109:845-850.
27. Knüsel B, Winslow JW, Rosenthal A, Burton LE, Seid DP, Nikolics K, Hefti F.. 1991. Promotion of central cholinergic and dopaminergic neuron differentiation by brain-derived neurotrophic factor but not neurotrophin 3 Proc Natl Acad Sci USA 88:961-965.
28. Kokaia Z, Andsberg G, Yan Q, Lindvall O. 1998. Rapid alterations of BDNF protein levels in rat brain after focal ischemia: evidence for increased synthesis and anterograde axonal transport. Exp Neurol 154:289-301.
29. Lamballe F, Klein R, Barbacid M. 1991. trkC, a new member of the trk family of tyrosine kinases, is a receptor for neurotrophin-3. Cell 66: 967-979.
30. Lamballe F, Smeyne RJ, Barbacid M. 1994. Developmental expression of trkC, the neurotrophin-3 receptor, in the mammalian nervous system. J Neurosci 14:14-28.
31. Lindvall O, Ernfors P, Bengzon J, Kokaia Z, Smith ML, Siesjö BK, Persson H. 1992. Differential regulation of mRNAs for nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3 in the adult rat brain following cerebral ischemia and hypoglycemic coma. Proc Natl Acad Sci USA 89:648-652.
32. Lindvall O, Kokaia Z, Bengzon J, Elmer E, Kokaia M. 1994. Neurotrophins and brain insults. TINS 17:490-496.
33. Mahalik TJ, Hahn WE, Clayton GH, Owens GP. 1994. Programmed cell death in developing grafts of fetal substantia nigra. Exp Neurol 129: 27-36.
34. Martin-Iverson MT, Altar CA. 1996. Spontaneous behaviors of rats are differentially affected by substantia nigra infusions of brain-derived neurotrophic factor and neurotrophin-3. Eur J Neurosci 8:1696-1706.
35. Masana Y, Wanaka A, Kato H, Asai T, Tohyama M. 1993. Localization of trkB mRNA in postnatal brain development. J Neurosci Res 35:468-479.
36. Merlio J-P, Ernfors P, Jaber M, Persson H. 1992. Molecular cloning of rat trkC and distribution of cells expressing messenger RNAs for members of the trk family in the rat central nervous system. Neuroscience 51:513-532.
37. Nawa NJ, Carnahan J, Gall C. 1995. BDNF protein measured by novel enzyme immunoassay in normal brain and after seizure: partial disagreement with mRNA levels. Eur J Neurosci 7:1527-1535.
38. Numan S. 1996. Neurotrophins and their receptors in the mesostriatal system. PhD dissertation, University of Kentucky, Lexington, KY.
39. Numan S, Seroogy KB, 1997. Increased expression of trkB mRNA in rat caudate-putamen following 6-OHDA lesions of the nigrostriatal pathway. Eur J Neurosci 9:489-495.
40. Numan S, Seroogy KB. 1999. Expression of trkB and trkC mRNAs by adult midbrain dopamine neurons: a double-label in situ hybridization study. J Comp Neurol 403:295-308.
41. Numan S, Lane-Ladd SB, Zhang L, Lundgren KH, Russell DS, Seruogy KB, Nestler EJ. 1998. Differential regulation of neurotrophin and trk receptor mRNAs in catecholaminergk nuclei during chronic opiate treatment and withdrawal. J Neurosci 18:10700-10708.
42. Okazawa H, Murata M, Watanabe M, Kamei M, Kanazawa I. 1992. Dopaminergic stimulation up-regulates the in vivo expression of brain-derived neurotrophic factor (BDNF) in the striatum. FEBS Lett 313: 138-142.
43. Paxinos G, Watson C. 1986. The rat brain in stereotaxic coordinates. New York: Academic Press.
44. Schmidt-Kastner R, Wetmore C, Olson L. 1996. Comparative study of brain-derived neurotrophic factor messenger RNA and protein at the cellular level suggests multiple roles in the hippocampus, striatum, and cortex. Neuroscience 74:161-183.
45. Seroogy KB, Gall CM. 1993. Expression of neurotrophins by midbrain dopaminergic neurons. Exp Neurol 124:119-128.
46. Seroogy KB, Herman JP. 1997. In situ hybridization approaches to the study of the nervous system. In: Turner AJ, Bachelard HS, editors. Neurochemistry - a practical approach. 2nd ed. Oxford: Oxford University Press. p 121-150.
47. Seroogy KB, Lundgren KH, Tran TMD, Guthrie KM, Isackson PJ, Gall CM. 1994. Dopaminergic neurons in rat ventral midbrain express brain-derived neurotrophic factor and neurotrophin-3 mRNAs. J Comp Neurol 342:321-334.
48. Son JH, Chun HS, Joh TH, Cho S, Conti B, Lee JW. 1999. Neuroprotection and neuronal differentiation studies using substantia nigra dopaminergic cells derived from transgenic mouse embryos. J Neurosci 19:10-20.
49. Soppet D, Escandon E, Maragos J, Middlemas DS, Reid SW, Blair J, Burton LE, Stanton BR, Kaplan DR, Hunter T, Nikolics K, Parada LF. 1991. The neurotrophic factors brain-derived neurotrophic factor and neurotrophin-3 are ligands for the trkB tyrosine kinase receptor. Cell 65:895-903.
50. Sponger C, Hyman C, Studer L, Egli M, Evtouchenko L, Jackson C, Dahl-Jørgensen A, Lindsay RM, Seiler SR. 1995. Effects of BDNF on dopaminergic, serotonergic, and GABAergic neurons in cultures of human fetal ventral mesencephalon. Exp Neurol 133:50-63.
51. Squinto SP, Stitt TN, Aldrich TH, Davis S, Bianco SM, Radziejewski C, Glass DJ, Masiakowski P, Furth ME, Valenzuela DM, DiStefano PS, Yancopoulos GD. 1991. trkB encodes a functional receptor for brain-derived neurotrophic factor and neurotrophin-3 but not nerve growth factor. Cell 65:885-893.
52. Strömberg I, Humpel C. 1995. Expression of BDNF and trkB mRNAs in comparison to dopamine D1 and D2 receptor mRNAs and tyrosine hydroxylase-immunoreactivity in nigrostriatal in oculo co-grafts. Brain Res Dev Brain Res 84:215-224.
53. Valenzuela DM, Maisonpierre PC, Glass DJ, Rojas E, Nuñez L, Kong Y, Gies DR, Stitt TN, Ip NY, Yancopoulos GD. 1993. Alternative forms of rat trkC with different functional capabilities. Neuron 10:963-974.
54. Wong JY, Liberatore GT, Donnan GA, Howells DW. 1997. Expression of brain-derived neurotrophic factor and TrkB neurotrophin receptors after striatal injury in the mouse. Exp Neurol 148:83-91.
55. Yurek DM, Fletcher-Turner A. 2000. Lesion-induced increase of BDNF is greater in the striatum of young versus old rat brain. Exp Neurol 161:392-396.
56. Zhou J, Pliego-Rivero B, Bradford HF, Stern GM. 1996. The BDNF content of postnatal and adult rat brain: the effects of 6-hydroxydopamine lesions in adult brain. Brain Res Dev Brain Res 97:297-303.