Differential regulation of the expression of neurotrophin receptors in rat extraocular motoneurons after lesion

Journal of Comparative Neurology

Volumn 519, Issue 12, 2011, Pages 2335-2352

  Morcuende, Sara ^a   Matarredona, Esperanza R ^a   Benítez Temiño, Beatriz ^a   Muñoz Hernández, Rocío ^a   Pastor, Ángel M ^a   De la Cruz, Rosa R ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

Author keywords

Abducens; Axotomy; CGRP; ChAT; Oculomotor; Trk receptor

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CALCITONIN GENE RELATED PEPTIDE; CHOLINE ACETYLTRANSFERASE; MESSENGER RNA; NEUROTROPHIN 3 RECEPTOR; NEUROTROPHIN RECEPTOR; PROTEIN TYROSINE KINASE A;

ABDUCENS NUCLEUS; ANIMAL TISSUE; ANTIBODY DETECTION; ARTICLE; CELL REGENERATION; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; EXTRAOCULAR MUSCLE; FEMALE; IMMUNOREACTIVITY; MALE; MORPHOLOGY; MOTONEURON; NERVE FIBER TRANSECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OCULOMOTOR NUCLEUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RAT; TROCHLEAR NUCLEUS;

ANIMALS; AXOTOMY; CALCITONIN GENE-RELATED PEPTIDE; CHOLINE O-ACETYLTRANSFERASE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MESENCEPHALON; MOTOR NEURONS; OCULOMOTOR MUSCLES; RATS; RATS, WISTAR; RECEPTOR, TRKA; RECEPTOR, TRKB; RECEPTOR, TRKC;

EID: 79959733644     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22630     Document Type: Article

References (86)

1. Abercrombie M. 1946. Estimation of the nuclear population from microtome sections. Anat Rec 94: 239-247.
2. Allen SJ, Dawbarn D. 2006. Clinical relevance of the neurotrophins and their receptors. Clin Sci (Lond) 110: 175-191.
3. Barbacid M. 1994. The Trk family of neurotrophin receptors. J Neurobiol 25: 1386-1414.
4. Benítez-Temiño B, de la Cruz RR, Pastor AM. 2002. Firing properties of axotomized central nervous system neurons recover after graft reinnervation. J Comp Neurol 444: 324-344.
5. Benítez-Temiño B, Morcuende S, Mentis GZ, de la Cruz RR, Pastor AM. 2004. Expression of Trk receptors in the oculomotor system of the adult cat. J Comp Neurol 473: 538-552.
6. Benítez-Temiño B, de la Cruz RR, Tena J, Pastor AM. 2005 Cerebellar grafting in the oculomotor system as a model to study target influence on adult neurons. Brain Res Brain Res Rev 49: 317-329.
7. Borke RC, Curtis M, Ginsberg C. 1993. Choline acetyltransferase and calcitonin gene-related peptide immunoreactivity in motoneurons after different types of nerve injury. J Neurocytol 22: 141-153.
8. Boyd JG, Gordon T. 2003. Neurotrophic factors and their receptors in axonal regeneration and function recovery after peripheral nerve injury. Mol Neurobiol 27: 277-324.
9. Bruce G, Wainer BH, Hersh LB. 1985. Immunoaffinity purification of human choline acetyltransferase: comparison of the brain and placental enzymes. J Neurochem 45: 611-620.
10. Brunelli G, Spano P, Barlati S, Guarneri B, Barbon A, Bresciani R, Pizzi M. 2005. Glutamatergic reinnervation through peripheral nerve graft dictates assembly of glutamatergic synapses at rat skeletal muscle. Proc Natl Acad Sci U S A 102: 8752-8757.
11. Büttner-Ennever JA. 2006. Neuroanatomy of the oculomotor system. Progress in brain research, vol. 151. Amsterdam: Elsevier.
12. Calderó J, Casanovas A, Sorribas A, Esquerda JE. 1992. Calcitonin gene related peptide in rat spinal cord motoneurons: subcellular distribution and changes induced by axotomy. Neuroscience 48: 449-461.
13. Canals JM, Checa N, Marco S, Michels A, Perez-Navarro E, Alberch J. 1999. The neurotrophin receptors trkA, trkB and trkC are differentially regulated after excitotoxic lesion in the rat striatum. Brain Res Mol Brain Res 69: 242-248.
14. Chang HM, Wei IH, Tseng ChY, Lue JH, Wen CY, Shieh JY. 2004. Differential expression of calcitonin gene related peptide (CGRP) and choline acetyltransferase (ChAT) in the axotomized motoneurons of normoxic and hypoxic rats. J Chem Neuroanat 28: 239-251.
15. Chao MV. 2003. Neurotrophins and their receptors: a convergence point for many signaling pathways. Nat Rev 4: 299-309.
16. Connor B, Young D, Lawlor P, Gai W, Waldvogel H, Faull RL, Dragunow M. 1996. Trk receptor alteration in Alzheimer's disease. Brain Res Mol Brain Res 42: 1-17.
17. Corcoran JPT, So PL, Maden M. 2004. Disruption of the retinoid signalling pathway causes a deposition of amyloid in the adult rat brain. Eur J Neurosci 20: 896-902.
18. Costigan M, Befort K, Karchewski L, Griffin RS, D'Urso D, Allchorne A, Sitarski J, Mannion JW, Pratt RE, Woolf CJ. 2002. Replicate high-density rat genome oligonucleotide microarrays reveal hundreds of regulated genes in the dorsal root ganglion after peripheral nerve injury. BMC Neurosci 3: 16.
19. Curtis R, Tonra JR, Stark JL, Adryan KM, Park JS, Cliffer KD, Lindsay M, DiStefano PS. 1998. Neuronal injury increases retrograde axonal transport of neurotrophins to spinal sensory neurons and motor neurons via multiple receptor mechanisms. Mol Cell Neurosci 12: 105-118.
20. Davis-López de Carrizosa MA, Morado-Díaz CJ, Tena JJ, Benítez-Temiño B, Pecero ML, Morcuende S, de la Cruz RR, Pastor AM. 2009. Complementary actions of BDNF and neurotrophin-3 on the firing patterns and synaptic composition of motoneurons. J Neurosci 29: 575-587.
21. Davis-López de Carrizosa MA, Morado-Díaz CJ, Morcuende S, de la Cruz RR, Pastor AM. 2010. Nerve growth factor regulates the firing patterns and synaptic composition of motoneurons. J Neurosci 30: 8308-8319.
22. de la Cruz RR, Pastor AM, Delgado-García JM. 1994a. Effects of target depletion on adult mammalian central neurons: morphological correlates. Neuroscience 58: 59-79.
23. de la Cruz RR, Pastor AM, Delgado-García JM. 1994b. Effects of target depletion on adult mammalian central neurons: functional correlates. Neuroscience 58: 81-97.
24. de la Cruz RR, Pastor AM, Delgado-García JM. 1996. Influence of the postsynaptic target on the functional properties of neurons in the adult mammalian central nervous system. Rev Neurosci 7: 115-149.
25. de la Cruz RR, Delgado-García JM, Pastor AM. 2000. Discharge characteristics of axotomized abducens internuclear neurons in the adult cat. J Comp Neurol 427: 391-404.
26. Delgado-García JM, del Pozo F, Spencer RF, Baker R. 1988. Behavior of neurons in the abducens nucleus of the alert cat. III. Axotomized motoneurons. Neuroscience 24: 143-160.
27. DiStefano PS, Friedman B, Radziejewski C, Alexander C, Boland P, Schick CM, Lindsay RM, Wiegand SJ. 1992. The neurotrophins BDNF, NT-3 and NGF display distinct patterns of retrograde axonal transport in peripheral and central neurons. Neuron 8: 983-993.
28. Dumoulin FL, Raivich G, Haas CA, Lazar P, Reddington M, Streit WJ, Kreutzberg GW. 1992. Calcitonin gene-related peptide and peripheral nerve regeneration. Ann N Y Acad Sci 657: 351-360.
29. Duprey-Díaz MV, Soto I, Blagburn JM, Blanco RE. 2002. Changes in brain-derived neurotrophic factor and trkB receptor in adult Rana pipiens retina and optic tectum after optic nerve injury. J Comp Neurol 454: 456-469.
30. Fernandes KJL, Kobayashi NR, Jasmin BJ, Tetzlaff W. 1998. Acetylcholinesterase gene expression in axotomized rat facial motoneurons is differentially regulated by neurotrophins: correlation with trkB and trkC mRNA levels and isoforms. J Neurosci 18: 9936-9947.
31. Friedman B, Kleinfeld D, Ip NY, Verge VMK, Moulton R, Boland P, Zlotchenko E, Lindsay RM, Liu L. 1995. BDNF and NT-4/5 exert neurotrophic influences on injured adult spinal motor neurons. J Neurosci 15: 1044-1056.
32. Fukuoka T, Tokunaga A, Kondo E, Miki K, Tachibana T, Noguchi K. 1999. Differential regulation of alpha- and beta-CGRP mRNAs within oculomotor, trochlear, abducens, and trigeminal motoneurons in response to axotomy. Brain Res Mol Brain Res 63: 304-315.
33. Funakoshi H, Frisén J, Barbany G, Timmusk T, Zachrisson O, Verge VMK, Persson H. 1993. Differential expression of mRNAs for neurotrophins and their receptors after axotomy of the sciatic nerve. J Cell Biol 123: 455-465.
34. Geerling JC, Shin JW, Chimenti PC, Joel C, Loewv AD. 2010. Pararaventricular hypothalamic nucleus: axonal projections to the brainstem. J Comp Neurol 518: 1460-1499.
35. Giehl KM, Schütte A, Mestres P, Yan Q. 1998. The survival-promoting effect of glial cell line-derived neurotrophic factor on axotomized corticospinal neurons in vivo is mediated by an endogenous brain-derived neurotrophic factor mechanism. J Neurosci 18: 7351-7360.
36. Giehl KM, Röhrig S, Bonatz H, Gutjahr M, Leiner B, Bartke i, Yan Q, Reichardt LF, Backus C, Welcher AA, Dethleffsen K, Mestres M, Meyer M. 2001. Endogenous brain-derived neurotrophic factor and neurotrophin-3 antagonistically regulate survival of axotomized corticospinal neurons in vivo. J Neurosci 21: 3492-3502.
37. Glicksman MA. 1980. Localization of motoneurons controlling the extraocular muscles of the rat. Brain Res 188: 53-62.
38. González-Forero D, de La Cruz RR, Delgado-García JM, Álvarez FJ, Pastor AM. 2002. Correlation between CGRP immunoreactivity and firing activity in cat abducens motoneurons. J Comp Neurol 451: 201-212.
39. Hammarberg H, Piehl F, Risling M, Cullheim S. 2000. Differential regulation of trophic factor receptor mRNAs in spinal motoneurons after sciatic nerve transection and ventral root avulsion in the rat. J Comp Neurol 426: 587-601.
40. Hughes RA, Sendtner M, Thoenen H. 1993. Members of several gene families influence survival of rat motoneurons in vitro and in vivo. J Neurosci Res 36: 663-671.
41. Ip NY, Ibáñez CF, Nye SH, McClain J, Jones PF, Gies DR, Belluscio L, Le Beau MM, Espinosa R III, Squinto SP, Persson H, Yancopoulos GD. 1992. Mammalian neurotrophin-4: structure, chromosomal localization, tissue distribution, and receptor specificity. Proc Natl Acad Sci U S A 89: 3060-3064.
42. Johnson H, Hökfelt T, Ulfhake B. 1999. Expression of p75(NTR), trkB and trkC in nonmanipulated and axotomized motoneurons of aged rats. Brain Res Mol Brain Res 69: 21-34.
43. Jones KR, Reichardt LF. 1990. Molecular cloning of a human gene that is a member of the nerve growth factor family. Proc Natl Acad Sci U S A 87: 8060-8064.
44. Kaplan DR, Miller FD. 2000. Neurotrophin signal transduction in the nervous system. Curr Opin Neurobiol 10: 381-391.
45. Kobayashi NR, Bedard AM, Hinchke MT, Tetzlaff W. 1996. Increased expression of BDNF and TrkB mRNA in rat facial motoneurons after axotomy. Eur J Neurosci 8: 1018-1029.
46. Koliatsos VE, Crawford TO, Price DL. 1991. Axotomy induces nerve growth factor receptor immunoreactivity in spinal motor neurons. Brain Res 549: 297-304.
47. Koliatsos VE, Clatterbuck RE, Winslow JW, Cayouette MH, Price DL. 1993. Evidence that brain-derived neurotrophic factor is a trophic factor for motor neurons in vivo. Neuron 10: 359-367.
48. Kosaras B, Jakubowski M, Kainz V, Burstein R. 2009. Sensory innervation of the calvarial bones of the mouse. J Comp Neurol 515: 331-348.
49. Kotulska K, Larysz-Brysz M, Marcol W, Jozwiak S, Lewin-Kowalik J. 2006. The role of trkB receptor in the formation of post-traumatic neuroma. Folia Neuropathol 44: 221-227
50. Kryger GS, Kriger Z, Zhang F, Shelton DL, Leneaweaver WC, Buncke HJ. 2001. Nerve growth factor inhibition prevents traumatic neuroma formation in the rat. J Hand Surg Am 26: 635-644.
51. Kubo T, Yamashita T, Yamaguchi A, Hosokawa K, Tohyama M. 2002. Analysis of genes induced in peripheral nerve after axotomy using cDNA microarrays. J Neurochem 82: 1129-1136.
52. Lams BE, Isacson O, Sofroniew MV. 1988. Loss of transmitter-associated enzyme staining following axotomy does not indicate death of brainstem cholinergic neurons. Brain Res 475: 401-406.
53. Leibrock J, Lottspeich F, Hohn A, Hofer M, Hengerer B, Masiakowski P, Thoenen H, Barde Y-A. 1989. Molecular cloning and expression of brain-derived neurotrophic factor. Nature 341: 149-152.
54. Levi-Montalcini R. 1982. Developmental biology and the natural history of nerve growth factor. Annu Rev Neurosci 5: 341-362.
55. Ma W, Quirion R. 2006. Increased calcitonin gene-related peptide in neuroma and invading macrophages is involved in the up-regulation of interleukin-6 and thermal hyperalgesia in a rat model of mononeuropathy. J Neurochem 98: 180-192.
56. Márquez-Ruiz J, Morcuende S, Navarro-López JD, Escudero M. 2007. Anatomical and pharmacological relationship between acetylcholine and nitric oxide in the prepositus hypoglossi nucleus of the cat: functional implications for eye-movement control. J Comp Neurol 503: 407-20.
57. Matsuura J, Ajiki K, Ichikawa T, Misawa H. 1997. Changes of expression levels of choline acetyltransferase and vesicular acetylcholine transporter mRNAs after transection of the hypoglossal nerve in adult rats. Neurosci Lett 236: 95-98.
58. McAllister AK, Katz LC, Lo DC. 1997. Opposing roles for endogenous BDNF and NT-3 in regulating cortical dendritic growth. Neuron 18: 767-778.
59. Meakin SO, Suter U, Drinkwater CC, Welcher AA, Shooter EM. 1992. The rat trk protooncogene product exhibits properties characteristic of the slow nerve growth factor receptor. Proc Natl Acad Sci U S A 89: 2374-2378.
60. Merlio JP, 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.
61. Meyer M, Matsuoka I, Wetmore C, Olson L, Thoenen H. 1992. Enhanced synthesis of brain-derived neurotrophic factor in the lesioned peripheral nerve: differential mechanisms are responsible for the regulation of BDNF and NGF mRNA. J Cell Biol 119: 45-54.
62. Middlemas DS, Lindberg RA, Hunter T. 1991. trkB, a neural receptor protein-tyrosine kinase: evidence for a full-length and two truncated receptors. Mol Cell Biol 11: 143-153.
63. Miyazaki S. 1985. Location of motoneurons in the oculomotor nucleus and the course of their axons in the oculomotor nerve. Brain Res 348: 57-63.
64. Morcuende S, Benítez-Temiño B, Pecero ML, Pastor AM, de la Cruz RR. 2005. Abducens internuclear neurons depend on their target motoneurons for survival during early postnatal development. Exp Neurol 195: 244-256.
65. Navarro X, Vivó M, Valero-Cabré A. 2007. Neural plasticity after peripheral nerve injury and regeneration. Prog Neurobiol 82: 163-201.
66. Okura Y, Arimoto H, Tanuma N, Matsumoto K, Nakamura T, Yamashima T, Miyazawa T, Matsumoto Y. 1999. Analysis of neurotrophic effects of hepatocyte growth factor in the adult hypoglossal nerve axotomy model. Eur J Neurosci 11: 4139-4144.
67. Omura T, Sano M, Omura K, Hasegawa T, Doi M, Sawada T, Nagano A. 2005. Different expressions of BDNF, NT3 and NT4 in muscle and nerve after various types of peripheral nerve injuries. J Peripher Nerv Syst 10: 293-300.
68. Oppenheim RW, Yin QW, Prevette D, Yan Q. 1992. Brain-derived neurotrophic factor rescues developing avian motoneurons from cell death. Nature 360: 755-757.
69. Pastor AM, Delgado-García JM, Martínez-Guijarro FJ, López-García C, de la Cruz RR. 2000. Response of abducens internuclear neurons to axotomy in the adult cat. J Comp Neurol 427: 370-390.
70. Patapoutian A, Reichardt lf. 2001. Trk receptors: mediators of neurotrophin action. Curr Opin Neurobiol 11: 272-280.
71. Piehl F, Arvidsson U, Johnson H, Cullheim S, Dagerlind A, Ulfhake B, Cao Y, Elde R, Pettersson RF, Terenius L, Hökfelt T. 1993. GAP-43, Afgf, CCK and alpha- and beta-CGRP in rat spinal motoneurons subjected to axotomy and/or dorsal root severance. Eur J Neurosci 5: 1321-1333.
72. Piehl F, Frisen J, Risling M, Hökfelt T, Cullheim S. 1994. Increased trkB mRNA expression by axotomized motoneurons. Neuroreport 5: 697-700.
73. Sala C, Andreose JS, Fumagalli G, Lomo T. 1995. Calcitonin gene-related peptide: possible role in formation and maintenance of neuromuscular junctions. J Neurosci 15: 520-528.
74. Schmitt AB, Breuer S, Liman J, Buss A, Schlangen C, Pech K, Hol EM, Brook GA, Noth J, Schwaiger FW. 2003. Identification of regeneration-associated genes after central and peripheral nerve injury in the adult rat. BMC Neurosci 4: 8.
75. Sendtner M, Hotmann G, Hughes RA. 1996. The response of motoneurons to neurotrophins. Neurochem Res 21: 831-841.
76. Sofroniew MV, Howe CL, Mobley WC. 2001. Nerve growth factor signaling, neuroprotection, and neural repair. Annu Rev Neurosci 24: 1217-1281.
77. Sumner BE. 1975. A quantitative analysis of boutons with different types of synapse in normal and injured hypoglossal nuclei. Exp Neurol 49: 406-417.
78. Suneja SK, Yan L, Potasher SJ. 2005. Regulation of NT-3 and BDNF levels in guinea pig auditory brain stem nuclei after unilateral cochlear ablation. J Neurosci Res 80: 381-390.
79. Tuszynsky MH, Mafong E, Meyer S. 1996. Central infusion of brain-derived neurotrophic factor and neurotrophin-4/5, but not nerve growth factor and neurotrophin-3, prevent loss of the cholinergic phenotype in injured adult motor neurons. Neuroscience 71: 761-771.
80. Venero JL, Vizuete ML, Revuelta M, Vargas C, Cano J, Machado A. 2000. Upregulation of BDNF mRNA and trkB mRNA in the nigrostriatal system and in the lesion site following unilateral transection of the medial forebrain bundle. Exp Neurol 161: 38-48.
81. Wang HL, Morales M. 2009. Pedunculopontine and laterodorsal tegmental nuclei contain distinct populations of cholinergic, glutamatergic and GABAergic neurons in the rat. Eur J Neurosci 29: 340-358.
82. Wang H, Wei F, Dubner R, Ren K. 2006. Selective distribution and function of primary afferent nociceptive inputs from deep muscle tissue to the brainstem trigeminal transition zone. J Comp Neurol 498: 390-402.
83. Wang W, Salvaterra PM, Loera S, Chiu AY. 1997. Brain-derived neurotrophic factor spares choline acetyltransferase mRNA following axotomy of motor neurons in vivo. J Neurosci Res 47: 134-143.
84. Wisden W, Morris BJ. 2002. In situ hybridization with oligonucleotide probes. Int Rev Neurobiol 2002; 47: 3-59.
85. Yan Q, Matheson C, Lopez OT, Miller JA. 1994. The biological responses of axotomized adult motoneurons to BDNF. J Neurosci 14: 5281-5291.
86. Yang L, Zhang FX, Huang F, Lu YJ, Li GD, Bao L, Xiao HS, Zhang X. 2004. Peripheral nerve injury induces trans-synaptic modification of channels, receptors and signal pathways in rat dorsal spinal cord. Eur J Neurosci 19: 871-883.