Aerobic exercise protects retinal function and structure from light-induced retinal degeneration

Journal of Neuroscience

Volumn 34, Issue 7, 2014, Pages 2406-2412

  Lawson, Eric C ^a,b   Han, Moon K ^b   Sellers, Jana T ^a   Chrenek, Micah A ^a   Hanif, Adam ^b   Gogniat, Marissa A ^b   Boatright, Jeffrey H ^a   Pardue, Machelle T ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ATLANTA VA MEDICAL CENTER   (United States)

Author keywords

Brain derived neurotrophic factor; Exercise; Neuroprotection; Photoreceptors; Retinal degeneration; Treadmill

Indexed keywords

BRAIN-DERIVED NEUROTROPHIC FACTOR; EXERCISE; NEUROPROTECTION; PHOTORECEPTORS; RETINAL DEGENERATION; TREADMILL;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; ENZYME-LINKED IMMUNOSORBENT ASSAY; LIGHT; MALE; MICE; MICE, INBRED BALB C; PHOTORECEPTOR CELLS, VERTEBRATE; PHYSICAL CONDITIONING, ANIMAL; RETINAL DEGENERATION;

EID: 84893652001     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2062-13.2014     Document Type: Article

References (50)

1. Aguiar AS Jr, Castro AA, Moreira EL, Glaser V, Santos AR, Tasca CI, Latini A, Prediger RD (2011) Short bouts of mild-intensity physical exercise improve spatial learning and memory in aging rats: involvement of hippocampal plasticity via AKT, CREB and BDNF signaling. Mech Ageing Dev 132:560-567. CrossRef Medline
2. Anderson BJ, Rapp DN, Baek DH, McCloskey DP, Coburn-Litvak PS, Robinson JK (2000) Exercise influences spatial learning in the radial arm maze. Physiol Behav 70:425-429. CrossRef Medline
3. Barone I, Novelli E, Piano I, Gargini C, Strettoi E (2012) Environmental enrichment extends photoreceptor survival and visual function in a mouse model of retinitis pigmentosa. PLo S One 7:e50726. CrossRef Medline
4. Berchtold NC, Chinn G, Chou M, Kesslak JP, Cotman CW (2005) Exercise primes a molecular memory for brain-derived neurotrophic factor protein induction in the rat hippocampus. Neuroscience 133:853-861. CrossRef Medline
5. Boatright JH, Moring AG, McElroy C, Phillips MJ, Do VT, Chang B, Hawes NL, Boyd AP, Sidney SS, Stewart RE, Minear SC, Chaudhury R, Ciavatta VT, Rodrigues CM, Steer CJ, Nickerson JM, Pardue MT (2006) Tool from ancient pharmacopoeia prevents vision loss. Mol Vis 12:1706-1714. Medline
6. Cazorla M, Prémont J, Mann A, Girard N, Kellendonk C, Rognan D (2011) Identification of a low-molecular weight Trk B antagonist with anxiolytic and antidepressant activity in mice. J Clin Invest 121:1846-1857. CrossRef Medline
7. Cellerino A, Kohler K (1997) Brain-derived neurotrophic factor/ neurotrophin-4 receptor Trk B is localized on ganglion cells and dopaminergic amacrine cells in the vertebrate retina. J Comp Neurol 386:149-160. CrossRef Medline
8. Chaddock L, Erickson KI, Prakash RS, Van Patter M, Voss MW, Pontifex MB, Raine LB, Hillman CH, Kramer AF (2010) Basal ganglia volume is associated with aerobic fitness in preadolescent children. Dev Neurosci 32: 249-256. CrossRef Medline
9. Cruise KE, Bucks RS, Loftus AM, Newton RU, Pegoraro R, Thomas MG (2011) Exercise and Parkinson's: benefits for cognition and quality of life. Acta Neurol Scand 123:13-19. CrossRef Medline
10. Di Polo A, Cheng L, Bray GM, Aguayo AJ (2000) Colocalization of Trk B and brain-derived neurotrophic factor proteins in green-red-sensitive cone outer segments. Invest Ophthalmol Vis Sci 41:4014-4021. Medline
11. Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L, Kim JS, Heo S, Alves H, White SM, Wojcicki TR, Mailey E, Vieira VJ, Martin SA, Pence BD, Woods JA, McAuley E, Kramer AF (2011) Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci U S A 108:3017-3022. CrossRef Medline
12. Filippin NT, da Costa PH, Mattioli R (2010) Effects of treadmill-walking training with additional body load on quality of life in subjects with Parkinson's disease. Rev Bras Fisioter 14:344-350. CrossRef Medline
13. Gomez-Pinilla F, Zhuang Y, Feng J, Ying Z, Fan G (2011) Exercise impacts brain-derived neurotrophic factor plasticity by engaging mechanisms of epigenetic regulation. Eur J Neurosci 33:383-390. CrossRef Medline
14. Griffin ÉW, Mullally S, Foley C, Warmington SA, O'Mara SM, Kelly AM (2011) Aerobic exercise improves hippocampal function and increases BDNF in the serum of young adult males. Physiol Behav 104:934-941. CrossRef Medline
15. Hood DC, Birch DG (1990) A quantitative measure of the electrical activity of human rod photoreceptors using electroretinography. Vis Neurosci 5:379-387. CrossRef Medline
16. Ikeda K, Tanihara H, Tatsuno T, Noguchi H, Nakayama C (2003) Brainderived neurotrophic factor shows a protective effect and improves recovery of the ERG b-wave response in light-damage. J Neurochem 87:290-296. CrossRef Medline
17. Intlekofer KA, Cotman CW (2013) Exercise counteracts declining hippocampal function in aging and Alzheimer's disease. Neurobiol Dis 57: 47-55. CrossRef Medline
18. Ke Z, Yip SP, Li L, Zheng XX, Tong KY (2011) The effects of voluntary, involuntary, and forced exercises on brain-derived neurotrophic factor and motor function recovery: a rat brain ischemia model. PLo S One 6:e16643. CrossRef Medline
19. Lavail MM (2005) Survival factors for treatment of retinal degenerative disorders: preclinical gains and issues for translation into clinical studies. Retina 25:S25-S26. CrossRef Medline
20. La Vail MM, Unoki K, Yasumura D, Matthes MT, Yancopoulos GD, Steinberg RH (1992) Multiple growth factors, cytokines, and neurotrophins rescue photoreceptors from the damaging effects of constant light. Proc Natl Acad Sci U S A 89:11249-11253. CrossRef Medline
21. Marais L, Stein DJ, Daniels WM (2009) Exercise increases BDNF levels in the striatum and decreases depressive-like behavior in chronically stressed rats. Metab Brain Dis 24:587-597. CrossRef Medline
22. McCrate ME, Kaspar BK (2008) Physical activity and neuroprotection in amyotrophic lateral sclerosis. Neuromolecular Med 10:108-117. CrossRef Medline
23. Mocko JA, Kim M, Faulkner AE, Cao Y, Ciavatta VT, Pardue MT (2011) Effects of subretinal electrical stimulation in mer-KO mice. Invest Ophthalmol Vis Sci 52:4223-4230. CrossRef Medline
24. Noell WK, Walker VS, Kang BS, Berman S (1966) Retinal damage by light in rats. Invest Ophthalmol 5:450-473. Medline
25. Okuno T, Sugiyama T, Kohyama M, Kojima S, Oku H, Ikeda T (2006) Ocular blood flow changes after dynamic exercise in humans. Eye 20:796-800. CrossRef Medline
26. Oliff HS, Berchtold NC, Isackson P, Cotman CW (1998) Exercise-induced regulation of brain-derived neurotrophic factor (BDNF) transcripts in the rat hippocampus. Brain Res Mol Brain Res 61:147-153. CrossRef Medline
27. Organisciak DT, Vaughan DK (2010) Retinal light damage: mechanisms and protection. Prog Retin Eye Res 29:113-134. CrossRef Medline
28. Paskowitz DM, Nune G, Yasumura D, Yang H, Bhisitkul RB, Sharma S, Matthes MT, Zarbin MA, Lavail MM, Duncan JL (2004) BDNF reduces the retinal toxicity of verteporfin photodynamic therapy. Invest Ophthalmol Vis Sci 45:4190-4196. CrossRef Medline
29. Penn RD, Hagins WA (1969) Signal transmission along retinal rods and the origin of the electroretinographic a-wave. Nature 223:201-204. CrossRef Medline
30. Ploughman M, Granter-Button S, Chernenko G, Attwood Z, Tucker BA, Mearow KM, Corbett D (2007) Exercise intensity influences the temporal profile of growth factors involved in neuronal plasticity following focal ischemia. Brain Res 1150:207-216. CrossRef Medline
31. Quirié A, Hervieu M, Garnier P, Demougeot C, Mossiat C, Bertrand N, Martin A, Marie C, Prigent-Tessier A (2012) Comparative effect of treadmill exercise on mature BDNF production in control versus stroke rats. PLo S One 7:e44218. CrossRef Medline
32. Radák Z, Kaneko T, Tahara S, Nakamoto H, Pucsok J, Sasvári M, Nyakas C, Goto S (2001) Regular exercise improves cognitive function and decreases oxidative damage in rat brain. Neurochem Int 38:17-23. CrossRef Medline
33. Rasmussen P, Brassard P, Adser H, Pedersen MV, Leick L, Hart E, Secher NH, Pedersen BK, Pilegaard H (2009) Evidence for a release of brain-derived neurotrophic factor from the brain during exercise. Exp Physiol 94:1062-1069. CrossRef Medline
34. Real CC, Ferreira AF, Chaves-Kirsten GP, Torrão AS, Pires RS, Britto LR (2013) BDNF receptor blockade hinders the beneficial effects of exercise in a rat model of Parkinson's disease. Neuroscience 237:118-129. CrossRef Medline
35. Remé CE, Grimm C, Hafezi F, Iseli HP, Wenzel A (2003) Why study rod cell death in retinal degenerations and how? Doc Ophthalmol 106:25-29. CrossRef Medline
36. Robson JG, Frishman LJ (1998) Dissecting the dark-adapted electroretinogram. Doc Ophthalmol 95:187-215. CrossRef Medline
37. Rohrer B, Ogilvie JM (2003) Retarded outer segment development in Trk B knockout mouse retina organ culture. Mol Vis 9:18-23. Medline
38. Rohrer B, Korenbrot JI, La Vail MM, Reichardt LF, Xu B (1999) Role of neurotrophin receptor Trk B in the maturation of rod photoreceptors and establishment of synaptic transmission to the inner retina. J Neurosci 19:8919-8930. Medline
39. Sabatier MJ, Redmon N, Schwartz G, English AW (2008) Treadmill training promotes axon regeneration in injured peripheral nerves. Exp Neurol 211:489-493. CrossRef Medline
40. Sabatier MJ, To BN, Nicolini J, English AW (2011) Effect of axon misdirection on recovery of electromyographic activity and kinematics after peripheral nerve injury. Cells Tissues Organs 193:298-309. CrossRef Medline
41. Spaeth AM, Kanoski SE, Hayes MR, Grill HJ (2012) Trk B receptor signaling in the nucleus tractus solitarius mediates the food intake-suppressive effects of hindbrain BDNF and leptin. Am J Physiol Endocrinol Metab 302:E1252-E1260. CrossRef Medline
42. Turner PV, Albassam MA (2005) Susceptibility of rats to corneal lesions after injectable anesthesia. Comp Med 55:175-182. Medline
43. Um HS, Kang EB, Koo JH, Kim HT, Jin L, Kim EJ, Yang CH, An GY, Cho IH, Cho JY (2011) Treadmill exercise represses neuronal cell death in an aged transgenic mouse model of Alzheimer's disease. Neurosci Res 69: 161-173. CrossRef Medline
44. Unoki K, La Vail MM (1994) Protection of the rat retina from ischemic injury by brain-derived neurotrophic factor, ciliary neurotrophic factor, and basic fibroblast growth factor. Invest Ophthalmol Vis Sci 35:907-915. Medline
45. van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci U S A 96:13427-13431. CrossRef Medline
46. Vassoler FM, White SL, Schmidt HD, Sadri-Vakili G, Pierce RC (2013) Epigenetic inheritance of a cocaine-resistance phenotype. Nat Neurosci 16: 42-47. CrossRef Medline
47. Vessal M, Darian-Smith C (2010) Adult neurogenesis occurs in primate sensorimotor cortex following cervical dorsal rhizotomy. J Neurosci 30: 8613-8623. CrossRef Medline
48. Vreugdenhil A, Cannell J, Davies A, Razay G (2012) A community-based exercise programme to improve functional ability in people with Alzheimer's disease: a randomized controlled trial. Scand J Caring Sci 26:12-19. CrossRef Medline
49. Williams PT (2009) Prospective study of incident age-related macular degeneration in relation to vigorous physical activity during a 7-year followup. Invest Ophthalmol Vis Sci 50:101-106. CrossRef Medline
50. Wood K, Wilhelm JC, Sabatier MJ, Liu K, Gu J, English AW (2012) Sex differences in the effectiveness of treadmill training in enhancing axon regeneration in injured peripheral nerves. Dev Neurobiol 72:688-698. CrossRef Medline