Short-term exercise increases GDNF protein levels in the spinal cord of young and old rats

Neuroscience

Volumn 240, Issue , 2013, Pages 258-268

  McCullough, M J ^a   Gyorkos, A M ^a   Spitsbergen, J M ^a  

^a WESTERN MICHIGAN UNIVERSITY   (United States)

Author keywords

Aging; Exercise; GDNF; Motor neuron; Neural plasticity; Spinal cord

Indexed keywords

CHOLINE ACETYLTRANSFERASE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXERCISE; IMMUNOHISTOCHEMISTRY; INVOLUNTARY RUNNING; LUMBAR SPINAL CORD; MALE; MOTONEURON; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN LOCALIZATION; RAT; RUNNING; SWIMMING; VOLUNTARY RUNNING; WESTERN BLOTTING;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; AUTOANTIGENS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; LOCOMOTION; MALE; MEMBRANE PROTEINS; MOTOR NEURONS; NERVE GROWTH FACTORS; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; SPINAL CORD INJURIES; SWIMMING; TIME FACTORS;

EID: 84876324158     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.02.063     Document Type: Article

References (81)

1. Aguiar A.S., Tuon T., Pinho C.A., Silva L.A., Andreazza A.C., Kapczinski F., Quevedo J., Streck E.L., Pinho R.A. Mitochondrial IV complex and brain neurotrophic derived factor response of mice brain cortex after downhill training. Neurosci Lett 2007, 426:171-174.
2. Al-Shawi R., Hafner A., Chun S., Raza S., Crutcher K., Thrasivoulou C., Simons P., Cowen T. ProNGF, sortilin, and age-related neurodegeneration. Ann N Y Acad Sci 2007, 1119:208-215.
3. Beattie M.S., Harrington A.W., Lee R., Kim J.Y., Boyce S.L., Longo F.M., Bresnahan J.C., Hempstead B.L., Yoon S.O. ProNGF induces p75-mediated death of oligodendrocytes following spinal cord injury. Neuron 2002, 36:375-386.
4. Bergman E., Kullberg S., Ming Y., Ulfhake B. Upregulation of GFRalpha-1 and c-ret in primary sensory neurons and spinal motoneurons of aged rats. J Neurosci Res 1999, 57:153-165.
5. Bierl M.A., Isaacson L.G. Increased NGF proforms in aged sympathetic neurons and their targets. Neurobiol Aging 2007, 28:122-134.
6. Blesch A., Tuszynski M.H. GDNF gene delivery to injured adult CNS motor neurons promotes axonal growth, expression of the trophic neuropeptide CGRP, and cellular protection. J Comp Neurol 2001, 436:399-410.
7. Cacalano G., Farinas I., Wang L.C., Hagler K., Forgie A., Moore M., Armanini M., Phillips H., Ryan A.M., Reichardt L.F., Hynes M., Davies A., Rosenthal A. GFRalpha1 is an essential receptor component for GDNF in the developing nervous system and kidney. Neuron 1998, 21:53-62.
8. Corse A.M., Bilak M.M., Bilak S.R., Lehar M., Rothstein J.D., Kuncl R.W. Preclinical testing of neuroprotective neurotrophic factors in a model of chronic motor neuron degeneration. Neurobiol Dis 1999, 6:335-346.
9. Deforges S., Branchu J., Biondi O., Grondard C., Pariset C., Lecolle S., Lopes P., Vidal P.-P., Chanoine C., Charbonnier F. Motoneuron survival is promoted by specific exercise in a mouse model of amyotrophic lateral sclerosis. J Physiol 2009, 587:3561-3571.
10. Domeniconi M., Hempstead B.L., Chao M.V. Pro-NGF secreted by astrocytes promotes motor neuron cell death. Mol Cell Neurosci 2007, 34:271-279.
11. Dupont-Versteegden E.E., Houle J.D., Dennis R.A., Zhang J., Knox M., Wagoner G., Peterson C.A. Exercise-induced gene expression in soleus muscle is dependent on time after spinal cord injury in rats. Muscle Nerve 2004, 29:73-81.
12. Engesser-Cesar C., Anderson A.J., Cotman C.J. Wheel running and fluoxetine antidepressant treatment have differential effects in the hippocampus and the spinal cord. Neuroscience 2007, 144:1033-1044.
13. Fabel K., Tam B., Kaufer D., Baiker A., Simmons N., Kuo C.J., Palmer T.D. VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur J Neurosci 2003, 18:2803-2812.
14. Fahnestock M., Yu G., Michalski B., Mathew S., Colquhoun A., Ross G.M., Coughlin M.D. The nerve growth factor precursor proNGF exhibits neurotrophic activity but is less active than mature nerve growth factor. J Neurochem 2004, 89:581-592.
15. Fediuc S., Campbell J.E., Riddell M.C. Effect of voluntary wheel running on circadian corticosterone release and on HPA axis responsiveness to restraint stress in Sprague-Dawley rats. J Appl Physiol 2006, 100:1867-1875.
16. Ferraiuolo L., De Bono J.P., Heath P.R., Holden H., Kasher P., Channon K.M., Kirby J., Shaw P.J. Transcriptional response of the neuromuscular system to exercise training and potential implications for ALS. J Neurochem 2009, 109:1714-1724.
17. Fries J.F., Singh G., Morfeld D., Hubert H.B., Lane N.E., Brown B.W. Running and the development of disability with age. Ann Intern Med 1994, 121:502-509.
18. Frontera W.R., Hughes V.A., Fielding R.A., Fiatarone M.A., Evans W.J., Roubenoff R. Aging of skeletal muscle: a 12-yr longitudinal study. J Appl Physiol 2000, 88:133-137.
19. Gomez-Pinilla F., Ying Z., Opazo P., Roy R.R., Edgerton V.R. Differential regulation by exercise of BDNF and NT-3 in rat spinal cord and skeletal muscle. Eur J Neurosci 2001, 13:1078-1084.
20. Gomez-Pinilla F., Ying Z., Roy R.R., Molteni R., Edgerton V.R. Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity. J Neurophysiol 2002, 88:2187-2195.
21. Hashizume K., Kanda K. Neuronal dropout is greater in hindlimb motor nuclei than in forelimb motor nuclei in aged rats. Neurosci Lett 1990, 113:267-269.
22. Henderson C.E., Phillips H.S., Pollock R.A., Davies A.M., Lemeulle C., Armanini M., Simpson L.C., Moffet B., Vandlen R.A., Koliatsos V.E., Rosenthal A. GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle. Science 1994, 266:1062-1064.
23. Hirofuji C., Ishihara A., Roy R.R., Itoh K., Itoh M., Edgerton V.R., Katsuta S. SDH activity and cell size of tibialis anterior motoneurons and muscle fibers in SAMP6. Neuroreport 2000, 11:823-828.
24. Huang E.J., Reichardt L.F. Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 2001, 24:677-736.
25. Ibanez C.F. Jekyll-hyde neurotrophins: the story of proNGF. Trends Neurosci 2002, 25:284-286.
26. Immonen T., Alakuijala A., Hytonen M., Sainio K., Poteryaev D., Saarma M., Pasternack M., Sariola H. A proGDNF-related peptide BEP increases synaptic excitation in rat hippocampus. Exp Neurol 2008, 210:793-796.
27. Jacob J.M. Lumbar motor neuron size and number is affected by age in male F344 rats. Mech Ageing Dev 1998, 106:205-216.
28. NTR, trkB and trkC in nonmanipulated and axotomized motoneurons of aged rats. Mol Brain Res 1999, 69:21-34.
29. Kallman D.A., Plato C.C., Tobin J.D. The role of muscle loss in the age-related decline of grip strength: cross-sectional and longitudinal perspectives. J Gerontol 1990, 45:M82-M88.
30. Kawamoto Y., Nakamura S., Matsuo A., Akiguchi I., Shibasaki H. Immunohistochemical localization of glial cell line-derived neurotrophic factor in the human central nervous system. Neuroscience 2000, 100:701-712.
31. Keller-Peck C.R., Feng G., Sanes J.R., Yan Q., Lichtman J.W., Snider W.D. Glial cell line-derived neurotrophic factor administration in postnatal life results in motor unit enlargement and continuous synaptic remodeling at the neuromuscular junction. J Neurosci 2001, 21:6136-6146.
32. Koo H., Choi B.H. Expression of glial cell line-derived neurotrophic factor (GDNF) in the developing human fetal brain. Int J Dev Neurosci 2001, 19:549-558.
33. Kullberg S., Ramirez-Leon V., Johnson H., Ulfhake B. Decreased axosomatic input to motoneurons and astrogliosis in the spinal cord of aged rats. J Gerontol A Biol Sci Med Sci 1998, 53:B369-B379.
34. Larsen K.E., Benn S.C., Ay I., Chian R.-J., Celia S.A., Remington M.P., Bejarano M., Liu M., Ross J., Carmillo P., Sah D., Phillips K.A., Sulzer D., Pepinsky R.B., Fishman P.S., Brown R.H., Francis J.W. A glial cell line-derived neurotrophic factor (GDNF):tetanus toxin fragment C protein conjugate improves delivery of GDNF to spinal cord motor neurons in mice. Brain Res 2006, 1120:1-12.
35. Leasure J.L., Jones M. Forced and voluntary exercise differentially affect brain and behavior. Neuroscience 2008, 156:456-465.
36. Lee R., Kermani P., Teng K.K., Hempstead B.L. Regulation of cell survival by secreted proneurotrophins. Science 2001, 294:1945-1948.
37. Li W., Brakefiled D., Pan Y., Hunter D., Myckatyn T.M., Parsadanian A. Muscle-derived but not centrally derived transgene GDNF is neuroprotective in G93A-SOD1 mouse model of ALS. Exp Neurol 2007, 203:457-471.
38. 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 1993, 260:1130-1132.
39. Lin L.-F.H., Zhang T.J., Collins F., Armes L.G. Purification and initial characterization of rat B49 glial cell line-derived neurotrophic factor. J Neurochem 1994, 63:758-768.
40. Lonka-Nevalaita L., Lume M., Leppanen S., Jokitalo E., Peranen J., Saarma M. Characterization of the intracellular localization, processing, and secretion of two glial cell line-derived neurotrophic factor splice isoforms. J Neurosci 2010, 30:11403-11413.
41. Macias M., Fehr S., Dwornik A., Sulejczak D., Wiater M., Czarkowska-Bauch J., Skup M., Schachner M. Exercise increases mRNA levels for adhesion molecules N-CAM and L1 correlating with BDNF response. Neuroreport 2002, 13:2527-2530.
42. McCullough M.J., Peplinski N.G., Kinnell K.R., Spitsbergen J.M. Glial cell line-derived neurotrophic factor protein content in rat skeletal muscle is altered by increased physical activity In vivo and In vitro. Neuroscience 2011, 174:234-244.
43. Molteni R., Ying Z., Gomez-Pinilla F. Differential effects of acute and chronic exercise on plasticity-related genes in the rat hippocampus revealed by microarray. Eur J Neurosci 2002, 16:1107-1117.
44. Moore M.W., Klein R.D., Farinas I., Sauer H., Armanini M., Phillips H., Reichardt L.F., Ryan A.M., Carver-Moore K., Rosenthal A. Renal and neuronal abnormalities in mice lacking GDNF. Nature 1996, 382:76-79.
45. Nair A., Bonneau R.H. Stress-induced elevation of glucocorticoids increases microglia proliferation through NMDA receptor activation. J Neuroimmunol 2006, 171:72-85.
46. Neeper S.A., Gomez-Pinilla F., Choi J., Cotman C.W. Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res 1996, 726:49-56.
47. Nguyen Q.T., Parsadanian A.S., Snider W.D., Lichtman J.W. Hyperinnervation of neuromuscular junctions caused by GDNF over-expression in muscle. Science 1998, 279:1725-1729.
48. Nicolopoulous-Stournaras S., Iles J.F. Motor neuron columns in the lumbar spinal cord of the rat. J Comp Neurology 1983, 217:75-85.
49. Nishi R. Neurotrophic factors: two are better than one. Science 1994, 265:1052-1053.
50. Nykjaer A., Lee R., Teng K.K., Jansen P., Madsen P., Nielsen M.S., Jacobsen C., Kliemannel M., Schwarz E., Willnow T.E., Hempstead B.L., Petersen C.M. Sortilin is essential for proNGF-induced neuronal cell death. Nature 2004, 427:843-848.
51. Oh-hashi K., Ito M., Tanaka T., Hirata Y., Kiuchi T. Biosynthesis, processing, and secretion of glial cell line-derived neurotrophic factor in astroglial cells. Mol Cell Biochem 2009, 323:1-7.
52. Ohta K., Inokuchi T., Gen E., Change J. Ultrastructural study of anterograde transport of glial cell line-derived neurotrophic factor from dorsal root ganglion neurons of rats towards the nerve terminal. Cells Tissues Organs 2001, 169:410-421.
53. Oppenheim R.W. Neurotrophic survival molecules for motoneurons: an embarrassment of riches. Neuron 1996, 17:195-197.
54. Oppenheim R.W., Houenou L.J., Johnson J.E., Lin L.F., 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 1995, 373:344-346.
55. Oppenheim R.W., Houenou L.J., Parsadanian A.S., Prevette D., Snider W.D., Shen L. Glial cell line-derived neurotrophic factor and developing mammalian motoneurons: regulation of programmed cell death among motoneuron subtypes. J Neurosci 2000, 20:5001-5011.
56. Peng S., Wuu J., Mufson E.J., Fahnestock M. Increased proNGF levels in subjects with mild cognitive impairment and mild Alzheimer disease. J Neuropathol Exp Neurol 2004, 63:641-649.
57. Ploughman M., Granter-Button S., Chernenko G., Attwood Z., Tucker B.A., Mearow K.M., Corbett D. Exercise intensity influences the temporal profile of growth factors involved in neuronal plasticity following focal ischemia. Brain Res 2007, 1150:207-216.
58. Ploughman N., Granter-Button S., Chernenko G., Tucker B.A., Mearow K.M., Corbett D. Endurance exercise regimens induce differential effects on brain-derived neurotrophic factor, synapsin-I and insulin-like growth factor I after focal ischemia. Neuroscience 2005, 136:991-1001.
59. Rind H.B., von Bartheld C.S. Anterograde axonal transport of internalized GDNF in sensory and motor neurons. Neuroreport 2002, 13:659-664.
60. Russell F.D., Koishi K., Jiang Y., McLennan I.S. Anterograde axonal transport of glial cell line-derived neurotrophic factor and its receptors in rat hypoglossal nerve. Neuroscience 2000, 97:575-580.
61. Siamilis S., Jakus J., Nyakas C., Costa A., Mihalik B., Falus A., Radak Z. The effect of exercise and oxidant-antioxidant intervention on the level of neurotrophins and free radicals in spinal cord of rats. Spinal Cord 2009, 47:453-457.
62. Skup M., Dwornik A., Macias M., Sulejczak D., Wiater M., Czarkowska-Bauch J. Long-term locomotor training up-regulates TrkB(FL) receptor-like proteins, brain-derived neurotrophic factor, and neurotrophin-4 with different topographies of expression in oligodendroglia and neurons in the spinal cord. Exp Neurol 2002, 176:289-307.
63. Springer J.E., Seeburger J.L., He J., Gabrea A., Blankenhorn E.P., Bergman L.W. CDNA sequence and differential mRNA regulation of two forms of glial cell line-derived neurotrophic factor in Schwann cells and rat skeletal muscle. Exp Neurol 1995, 131:47-52.
64. Stranahan A.M., Khalil D., Gould E. Social isolation delays the positive effects of running on adult neurogenesis. Nat Neurosci 2006, 9:526-533.
65. Sugama S., Fujita M., Hashimoto M., Conti B. Stress induced morphological microglial activation in the rodent brain: involvement of interleukin-18. Neuroscience 2007, 146:1388-1399.
66. Suter-Crazzolara C., Unsicker K. GDNF is expressed in two forms in many tissues outside the CNS. Neuroreport 1994, 5:2486-2488.
67. Suzuki H., Hase A., Miyata Y., Arahata K., Akazawa C. Prominent expression of glial cell line-derived neurotrophic factor in human skeletal muscle. J Comp Neurol 1998, 402:303-312.
68. Tokumine J., Kakinohana O., Cizkova D., Smith D.W., Marsala M. Changes in spinal GDNF, BDNF, and NT-3 expression after transient spinal cord ischemia in the rat. J Neurosci Res 2003, 74:552-561.
69. Toulotte C., Fabre C., Dangremont B., Lensel G., Thevenon A. Effects of physical training on the physical capacity of frail, demented patients with a history of falling: a randomised controlled trial. Age Aging 2003, 32:67-73.
70. Trejo J.L., Carro E., Torres-Aleman I. Circulating insulin-like growth factor 1 mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J Neurosci 2001, 21:1628-1634.
71. Trupp M., Belluardo N., Funakoshi H., Ibanez C.F. Complementary and overlapping expression of glial cell line-derived neurotrophic factor (GDNF), c-ret proto-oncogene, and GDNF receptor-alpha indicates multiple mechanisms of trophic actions in the adult rat CNS. J Neurosci 1997, 17:3554-3567.
72. Vianney J.-M., Spitsbergen J.M. Cholinergic neurons regulate secretion of glial cell line-derived neurotrophic factor by skeletal muscle cells in culture. Brain Res 2011, 1390:1-9.
73. Wang L.J., Lu Y.Y., Muramatsu S., Ikeguchi K., Fujimoto K., Okada T., Mizukami H., Matsushita T., Hanazono Y., Kime A., Nagatsu T., Ozawa K., Nakano I. Neuroprotective effects of glial cell line-derived neurotrophic factor mediated by an adeno-associated virus vector in a transgenic animal model of amyotrophic lateral sclerosis. J Neurosci 2002, 22:6920-6928.
74. Wehrwein E.A., Roskelley E.M., Spitsbergen J.M. GDNF is regulated in an activity-dependent manner in rat skeletal muscle. Muscle Nerve 2002, 26:206-211.
75. Wetts R., Vaughn J.E. Differential vulnerability to two subsets of spinal motor neurons in Amyotrophic Lateral Sclerosis. Exp Neurol 1996, 141:248-255.
76. Wu C.W., Chang Y.T., Yu L., Chen H.I., Jen C.J., Wu S.Y., Lo C.P., Kuo Y.M. Exercise enhances the proliferation of neural stem cells and neurite growth and survival of neuronal progenitor cells in dentate gyrus of middle-aged mice. J Appl Physiol 2008, 105:1585-1594.
77. Yamamoto M., Sobue G., Yamamoto K., Terao S., Mitsuma T. Expression of glial cell-line derived growth factor mRNA in the spinal cord and muscle in amyotrophic lateral sclerosis. Neurosci Lett 1996, 204:117-120.
78. Yan Q., Matheson C., Lopez O.T. In vivo neurotrophic effects of GDNF on neonatal and adult facial motor neurons. Nature 1995, 373:341-344.
79. Ying Z., Roy R.R., Edgerton R., Gomez-Pinilla F. Voluntary exercise increases neurotrophin-3 and its receptor TrkC in the spinal cord. Brain Res 2003, 987:93-99.
80. Zurn A.D., Baetge E.E., Hammang J.P., Tan S.A., Aebischer P. Glial cell line-derived neurotrophic factor (GDNF), a new neurotrophic factor for motoneurones. Neuroreport 1994, 6:113-118.
81. Zwick M., Teng L., Mu X., Springer J.E., Davis B.M. Overexpression of GDNF induces and maintains hyperinnervation of muscle fibers and multiple end-plate formations. Exp Neurol 2001, 171:342-350.