Expression of neurotrophin and its tropomyosin-related kinase receptors (Trks) during axonal regeneration following spinal cord injury in larval lamprey

Neuroscience

Volumn 183, Issue , 2011, Pages 265-277

  Laramore, C ^a,c   Maymind, E ^b   Shifman, M I ^a,c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Identifiable neurons; Lamprey; Microglia; Molecular cloning; Neurotrophins; Spinal cord injury

Indexed keywords

MEMBRANE PROTEIN; MESSENGER RNA; NEUROTROPHIN; TROPOMYOSIN RELATED KINASE RECEPTOR; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION REGULATION; LAMPREY; MACROPHAGE; MICROGLIA; NERVE FIBER REGENERATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; RETICULOSPINAL TRACT; RNA PROBE; SEQUENCE HOMOLOGY; SPINAL CORD INJURY; UPREGULATION;

ANALYSIS OF VARIANCE; ANIMALS; AXONS; BRAIN; CELL COUNT; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; LAMPREYS; LARVA; LECTINS; MICROGLIA; NERVE GROWTH FACTORS; NERVE REGENERATION; RECEPTOR, TRKA; RNA, MESSENGER; SPINAL CORD; SPINAL CORD INJURIES; TIME FACTORS;

EID: 79955615259     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.03.024     Document Type: Article

References (78)

1. Barreiro-Iglesias A., Villar-Cheda B., Abalo X.M., Anadon R., Rodicio M.C. The early scaffold of axon tracts in the brain of a primitive vertebrate, the sea lamprey. Brain Res Bull 2008, 75:42-52.
2. Batchelor P.E., Porritt M.J., Martinello P., Parish C.L., Liberatore G.T., Donnan G.A., Howells D.W. Macrophages and microglia produce local trophic gradients that stimulate axonal sprouting toward but not beyond the wound edge. Mol Cell Neurosci 2002, 21:436-453.
3. Benito-Gutierrez E., Garcia-Fernandez J., Comella J.X. Origin and evolution of the Trk family of neurotrophic receptors. Mol Cell Neurosci 2006, 31:179-192.
4. Bertolini B. Ultrastructure of the spinal cord of the lamprey. J Ultrastruct Res 1964, 11:1-24.
5. Bibel M., Barde Y.-A. Neurotrophins: key regulators of cell fate and cell shape in the vertebrate nervous system. Genes Dev 2000, 14:2919-2937.
6. Boya J., Carbonell A.L., Calvo J.L., Borregon A. Microglial cells in the central nervous system of the rabbit and rat: cytochemical identification using two different lectins. Acta Anat (Basel) 1991, 140:250-253.
7. Boyd J.G., Gordon T. Neurotrophic factors and their receptors in axonal regeneration and functional recovery after peripheral nerve injury. Mol Neurobiol 2003, 27:277-324.
8. Brown A., Ricci M.J., Weaver L.C. NGF message and protein distribution in the injured rat spinal cord. Exp Neurol 2004, 188:115-127.
9. Bullock T.H., Moore J.K., Fields R.D. Evolution of myelin sheaths: both lamprey and hagfish lack myelin. Neurosci Lett 1984, 48:145-148.
10. Chen Z.-L., Yu W.-M., Strickland S. Peripheral regeneration. Annu Rev Neurosci 2007, 30:209-233.
11. Cohen A.H., Mackler S.A., Selzer M.E. Behavioral recovery following spinal transection: functional regeneration in the lamprey CNS. Trends Neurosci 1988, 11:227-231.
12. Davis G.R., McClellan A.D. Extent and time course of restoration of descending brainstem projections in spinal cord-transected lamprey. J Comp Neurol 1994, 344:65-82.
13. Davis G.R.J., McClellan A.D. Time course of anatomical regeneration of descending brainstem neurons and behavioral recovery in spinal-transected lamprey. Brain Res 1993, 602:131-137.
14. Dougherty K.D., Dreyfus C.F., Black I.B. Brain-derived neurotrophic factor in astrocytes, oligodendrocytes, and microglia/macrophages after spinal cord injury. Neurobiol Dis 2000, 7:574-585.
15. Dusart I., Schwab M.E. Secondary cell death and the inflammatory reaction after dorsal hemisection of the rat spinal cord. Eur J Neurosci 1994, 6:712-724.
16. Ebadi M., Bashir R.M., Heidrick M.L., Hamada F.M., Refaey H.E., Hamed A., Helal G., Baxi M.D., Cerutis D.R., Lassi N.K. Neurotrophins and their receptors in nerve injury and repair. Neurochem Int 1997, 30:347-374.
17. Giehl K.M., Rohrig S., Bonatz H., Gutjahr M., Leiner B., Bartke I., Yan Q., Reichardt L.F., Backus C., Welcher A.A., Dethleffsen K., Mestres P., Meyer M. Endogenous brain-derived neurotrophic factor and neurotrophin-3 antagonistically regulate survival of axotomized corticospinal neurons in vivo. J Neurosci 2001, 21:3492-3502.
18. Gomes-Leal W., Corkill D.J., Freire M.A., Picanco-Diniz C.W., Perry V.H. Astrocytosis, microglia activation, oligodendrocyte degeneration, and pyknosis following acute spinal cord injury. Exp Neurol 2004, 190:456-467.
19. Gordon T., Sulaiman O., Boyd J.G. Experimental strategies to promote functional recovery after peripheral nerve injuries. J Peripher Nerv Syst 2003, 8:236-250.
20. Graeber M.B. Changing face of microglia. Science 2010, 330:783-788.
21. Graeber M.B., Streit W.J. Microglia: biology and pathology. Acta Neuropathol 2010, 119:89-105.
22. Hains B.C., Waxman S.G. Activated microglia contribute to the maintenance of chronic pain after spinal cord injury. J Neurosci 2006, 26:4308-4317.
23. Hallbook F., Lundin L.G., Kullander K. Lampetra fluviatilis neurotrophin homolog, descendant of a neurotrophin ancestor, discloses the early molecular evolution of neurotrophins in the vertebrate subphylum. J Neurosci 1998, 18:8700-8711.
24. Hashimoto M., Nitta A., Fukumitsu H., Nomoto H., Shen L., Furukawa S. Inflammation-induced GDNF improves locomotor function after spinal cord injury. Neuroreport 2005, 16:99-102.
25. Huang E.J., Reichardt L.F. Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 2003, 72:609-642.
26. Ikeda O., Murakami M., Ino H., Yamazaki M., Nemoto T., Koda M., Nakayama C., Moriya H. Acute up-regulation of brain-derived neurotrophic factor expression resulting from experimentally induced injury in the rat spinal cord. Acta Neuropathol (Berl) 2001, 102:239-245.
27. Ip N.Y., Maisonpierre P., Alderson R., Friedman B., Furth M.E., Panayotatos N., Squinto S., Yancopoulos G.D., Lindsay R.M. The neurotrophins and CNTF: specificity of action towards PNS and CNS neurons. J Physiol 1991, 85:123-130.
28. Ip N.Y., Yancopoulos G.D. Neurotrophic factors and their receptors. Ann Neurol 1994, 35:S13-S16.
29. Jacobs A.J., Swain G.P., Snedeker J.A., Pijak D.S., Gladstone L.J., Selzer M.E. Recovery of neurofilament expression selectively in regenerating reticulospinal neurons. J Neurosci 1997, 17:5206-5220.
30. Jones L.L., Tuszynski M.H. Spinal cord injury elicits expression of keratan sulfate proteoglycans by macrophages, reactive microglia, and oligodendrocyte progenitors. J Neurosci 2002, 22:4611-4624.
31. Kaplan D.R., Miller F.D. Neurotrophin signal transduction in the nervous system. Curr Opin Neurobiol 2000, 10:381-391.
32. Koshinaga M., Whittemore S.R. The temporal and spatial activation of microglia in fiber tracts undergoing anterograde and retrograde degeneration following spinal cord lesion. J Neurotrauma 1995, 12:209-222.
33. Ladeby R., Wirenfeldt M., Garcia-Ovejero D., Fenger C., Dissing-Olesen L., Dalmau I., Finsen B. Microglial cell population dynamics in the injured adult central nervous system. Brain Res Rev 2005, 48:196-206.
34. Lee P.-G., Zhuo H., Helke C.J. Axotomy alters neurotrophin and neurotrophin receptor mRNAs in the vagus nerve and nodose ganglion of the rat. Mol Brain Res 2001, 87:31-41.
35. Leme R.J., Chadi G. Distant microglial and astroglial activation secondary to experimental spinal cord lesion. Arq Neuro Psiquiatr 2001, 59:483-492.
36. Lewin G.R., Barde Y.A. Physiology of the neurotrophins. Annu Rev Neurosci 1996, 19:289-317.
37. Liebl D.J., Huang W., Young W., Parada L.F. Regulation of Trk receptors following contusion of the rat spinal cord. Exp Neurol 2001, 167:15-26.
38. Loane D.J., Byrnes K.R. Role of microglia in neurotrauma. Neurotherapeutics 2010, 7:366-377.
39. Lurie D.I., Pijak D.S., Selzer M.E. The structure of reticulospinal axon growth cones and their cellular environment during regeneration in the lamprey spinal cord. J Comp Neurol 1994, 344:559-580.
40. Lurie D.I., Selzer M.E. The need for cellular elements during axonal regeneration in the sea lamprey spinal cord. Exp Neurol 1991, 112:64-71.
41. Lurie D.I., Selzer M.E. Preferential regeneration of spinal axons through the scar in hemisected lamprey spinal cord. J Comp Neurol 1991, 313:669-679.
42. Mackler S.A., Selzer M.E. Specificity of synaptic regeneration in the spinal cord of the larval sea lamprey. J Physiol (Lond) 1987, 388:183-198.
43. Merrick S.E., Pleasure S.J., Lurie D.I., Pijak D.S., Selzer M.E., Lee V.M. Glial cells of the lamprey nervous system contain keratin-like proteins. J Comp Neurol 1995, 355:199-210.
44. Morino T., Ogata T., Horiuchi H., Takeba J., Okumura H., Miyazaki T., Yamamoto H. Delayed neuronal damage related to microglia proliferation after mild spinal cord compression injury. Neurosci Res 2003, 46:309-318.
45. Mueller C.A., Schluesener H.J., Conrad S., Pietsch T., Schwab J.M. Spinal cord injury-induced expression of the immune-regulatory chemokine interleukin-16 caused by activated microglia/macrophages and CD8+ cells. J Neurosurg Spine 2006, 4:233-240.
46. Nakamura M., Bregman B.S. Differences in neurotrophic factor gene expression profiles between neonate and adult rat spinal cord after injury. Exp Neurol 2001, 169:407-415.
47. Napoli I., Neumann H. Microglial clearance function in health and disease. Neuroscience 2009, 158:1030-1038.
48. Pancer Z., Amemiya C.T., Ehrhardt G.R., Ceitlin J., Gartland G.L., Cooper M.D. Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 2004, 430:174-180.
49. Patapoutian A., Reichardt L.F. Trk receptors: mediators of neurotrophin action. Curr Opin Neurobiol 2001, 11:272-280.
50. Popovich P.G., Wei P., Stokes B.T. Cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats. J Comp Neurol 1997, 377:443-464.
51. Priestley J.V. Promoting anatomical plasticity and recovery of function after traumatic injury to the central or peripheral nervous system. Brain 2007, 130:895-897.
52. Prinz M., Mildner A. Microglia in the CNS: immigrants from another world. Glia 2011, 59:177-187.
53. Rabchevsky A.G., Streit W.J. Grafting of cultured microglial cells into the lesioned spinal cord of adult rats enhances neurite outgrowth. J Neurosci Res 1997, 47:34-48.
54. Rovainen C.M. Regeneration of Müller and Mauthner axons after spinal transection in larval lampreys. J Comp Neurol 1976, 168:545-554.
55. Rovainen C.M. Neurobiology of lampreys. Physiol Rev 1979, 59:1007-1077.
56. Sandvig A., Berry M., Barrett L.B., Butt A., Logan A. Myelin-, reactive glia-, and scar-derived CNS axon growth inhibitors: expression, receptor signaling, and correlation with axon regeneration. Glia 2004, 46:225-251.
57. Schultz R., Berkowitz E.C., Pease D.C. The electron microscopy of the lamprey spinal cord. J Morphol 1956, 98:251-273.
58. Selzer M.E. Mechanisms of functional recovery and regeneration after spinal cord transection in larval sea lamprey. J Physiol (Lond) 1978, 277:395-408.
59. Shifman M.I., Selzer M.E. Expression of netrin receptor UNC-5 in lamprey brain; modulation by spinal cord transection. NeuroRehabil Neural Repair 2000, 14:49-58.
60. Shifman M.I., Selzer M.E. In situ hybridization in wholemounted lamprey spinal cord: localization of netrin mRNA expression. J Neurosci Methods 2000, 104:19-25.
61. Shifman M.I., Selzer M.E. Semaphorins and their receptors in lamprey CNS: cloning, phylogenetic analysis and developmental changes during metamorphosis. J Comp Neurol 2006, 497:115-132.
62. Shifman M.I., Selzer M.E. Differential expression of class 3 and 4 semaphorins and netrin in the lamprey spinal cord during regeneration. J Comp Neurol 2007, 501:631-646.
63. Shifman M.I., Yumul R.E., Laramore C., Selzer M.E. Expression of the repulsive guidance molecule RGM and its receptor neogenin after spinal cord injury in sea lamprey. Exp Neurol 2009, 217:242-251.
64. Sroga J.M., Jones T.B., Kigerl K.A., McGaughy V.M., Popovich P.G. Rats and mice exhibit distinct inflammatory reactions after spinal cord injury. J Comp Neurol 2003, 462:223-240.
65. Stock D.W., Whitt G.S. Evidence from 18S ribosomal RNA sequences that lampreys and hagfishes form a natural group. Science 1992, 257:787-789.
66. Streit W. An improved staining method for rat microglial cells using the lectin from Griffonia simplicifolia (GSA I-B4). J Histochem Cytochem 1990, 38:1683-1686.
67. Streit W.J. The role of microglia in regeneration. Eur Arch Otorhinolaryngol 1994, S69-S70.
68. Streit W.J. The role of microglia in brain injury. Neurotoxicology 1996, 17:671-678.
69. Streit W.J. Microglia and the response to brain injury. Ernst Schering Res Found Workshop 2002, 11-24.
70. Streit W.J. Microglia as neuroprotective, immunocompetent cells of the CNS. Glia 2002, 40:133-139.
71. Streit W.J., Kreutzberg G.W. Lectin binding by resting and reactive microglia. J Neurocytol 1987, 16:249-260.
72. Vidal Pizarro I., Swain G.P., Selzer M.E. Cell proliferation in the lamprey central nervous system. J Comp Neurol 2004, 469:298-310.
73. Villar-Cheda B., Perez-Costas E., Melendez-Ferro M., Abalo X.M., Rodriguez-Munoz R., Anadon R., Rodicio M.C. Cell proliferation in the forebrain and midbrain of the sea lamprey. J Comp Neurol 2006, 494:986-1006.
74. Widenfalk J., Lundstromer K., Jubran M., Brene S., Olson L. Neurotrophic factors and receptors in the immature and adult spinal cord after mechanical injury or kainic acid. J Neurosci 2001, 21:3457-3475.
75. Wood M.R., Cohen M.J. Synaptic regeneration in identified neurons of the lamprey spinal cords. Science 1979, 206:344-347.
76. Wu D., Miyamoto O., Shibuya S., Okada M., Igawa H., Janjua N.A., Norimatsu H., Itano T. Different expression of macrophages and microglia in rat spinal cord contusion injury model at morphological and regional levels. Acta Med Okayama 2005, 59:121-127.
77. Xu M., Ng Y.K., Leong S.K. Induction of microglial reaction and expression of nitric oxide synthase I in the nucleus dorsalis and red nucleus following lower thoracic spinal cord hemisection. Brain Res 1998, 808:23-30.
78. Yin H.S., Selzer M.E. Axonal regeneration in lamprey spinal cord. J Neurosci 1983, 3:1135-1144.