Intermittent fasting improves functional recovery after rat thoracic contusion spinal cord injury

Journal of Neurotrauma

Volumn 28, Issue 3, 2011, Pages 479-492

  Jeong, Mi Ae ^a,b   Plunet, Ward ^a   Streijger, Femke ^a   Lee, Jae H T ^a   Plemel, Jason R ^a   Park, Sophia ^a   Lam, Clarrie K ^a   Liu, Jie ^a   Tetzlaff, Wolfram ^a,c  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b Hanyang University Medical Center   (South Korea)

^c Blusson Spinal Cord Centre   (Canada)

Author keywords

calorie restriction; every other day fasting; functional recovery; intermittent fasting; spinal cord injury

Indexed keywords

SEROTONIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALORIC RESTRICTION; CONTROLLED STUDY; CORRELATION ANALYSIS; DIET RESTRICTION; FUNCTIONAL ASSESSMENT; FUNCTIONAL STATUS; GRAY MATTER; HINDLIMB; IMMUNOHISTOCHEMISTRY; LOCOMOTION; NONHUMAN; RAT; SPINAL CORD INJURY; WALKING;

ANALYSIS OF VARIANCE; ANIMALS; CALORIC RESTRICTION; FASTING; GAIT; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; SPINAL CORD INJURIES; THORACIC VERTEBRAE;

EID: 79952746670     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2010.1609     Document Type: Article

References (49)

1. Anson, R.M., Guo, Z., de Cabo, R., Iyun, T., Rios, M., Hagepanos, A., Ingram, D.K., Lane, M.A., and Mattson, M.P. (2003). Inter-mittent fasting dissociates beneficial effects of dietary restriction on glucose metabolism and neuronal resistance to injury from calorie intake. Proc Natl. Acad. Sci. USA 100, 6216-6220. (Pubitemid 36576956)
2. Bareyre, F.M., Kerschensteiner, M., Raineteau, O., Mettenleiter, T.C., Weinmann, O., and Schwab, M.E. (2004). The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat. Neurosci. 7, 269-277. (Pubitemid 38280451)
3. Basso, D.M. (2004). Behavioral testing after spinal cord injury: congruities, complexities, and controversies. J. Neurotrauma 21, 395-404. (Pubitemid 38509423)
4. Basso, D.M., Beattie, M.S., and Bresnahan, J.C. (1995). A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma 12, 1-21.
5. Basso, D.M., Beattie, M.S., and Bresnahan, J.C. (1996). Graded histological and locomotor outcomes after spinal cord contu-sion using the NYU weight-drop device versus transection. Exp. Neurol. 139, 244-256. (Pubitemid 26228093)
6. Beatty, W.W., Clouse, B.A., and Bierley, RA. (1987). Effects of long-term restricted feeding on radial maze performance by aged rats. Neurobiol. Aging 8, 325-327. (Pubitemid 17135592)
7. Bond, N.W., Everittm A.V., and Walton, J. (1989). Effects of di-etary restriction on radial-arm maze performance and flavor memory in aged rats. Neurobiol. Aging 10, 27-30. (Pubitemid 19164497)
8. Bough, K.J., Schwartzkroin, P.A., and Rho, J.M. (2003). Calorie restriction and ketogenic diet diminish neuronal excitability in rat dentate gyrus in vivo. Epilepsia 44, 752-760. (Pubitemid 36753999)
9. Bough, K.J., Valiyil, R., Han, F.T., and Eagles, D.A. (1999). Sei-zure resistance is dependent upon age and calorie restriction in rats fed a ketogenic diet. Epilepsy Res. 35, 21-28. (Pubitemid 29191491)
10. Bruce-Keller, A.J., Umberger, G., McFall, R., and Mattson, M.P. (1999). Food restriction reduces brain damage and improves behavioral outcome following excitotoxic and metabolic in-sults. Ann. Neurol. 45, 8-15. (Pubitemid 29036426)
11. Davis, L.M., Pauly, J.R., Readnower, R.D., Rho, J.M., and Sulli-van, P.G (2008). Fasting is neuroprotective following trau-matic brain injury. J. Neurosci. Res. 86, 1812-1822. (Pubitemid 351859431)
12. Deumens, R, Koopmans, GC., Honig, W.M., Hamers, F.P., Maquet, V., Jerome, R., Steinbusch, H.W., and Joosten, E.A. (2006). Olfactory ensheathing cells, olfactory nerve fibroblasts and biomatrices to promote long-distance axon regrowth and functional recovery in the dorsally hemisected adult rat spinal cord. Exp. Neurol. 200, 89-103. (Pubitemid 44080749)
13. Duan, W., Guo, Z., Jiang, H., Ware, M., Li, X.J., and Mattson, M.P. (2003). Dietary restriction normalizes glucose metabolism and BDNF levels, slows disease progression, and increases survival in huntingtin mutant mice. Proc Natl. Acad. Sci. USA 100, 2911-2916. (Pubitemid 36297597)
14. Fontan-Lozano, A., Saez-Cassanelli, J.L., Inda, M.C., de los Santos-Arteaga, M., Sierra-Dominguez, S.A., Lopez-Lluch, G., Delgado-Garcia, J.M., and Carrion, A.M. (2007). Caloric re-striction increases learning consolidation and facilitates syn-aptic plasticity through mechanisms dependent on NR2B subunits of the NMDA receptor. J. Neurosci. 27,10185-10195. (Pubitemid 47450454)
15. Halagappa, V.K., Guo, Z., Pearson, M., Matsuoka, Y., Cutler, R.G., Laferla, F.M., Mattson, M.P. (2007). Intermittent fasting and caloric restriction ameliorate age-related behavioral defi-cits in the triple-transgenic mouse model of Alzheimer's dis-ease. Neurobiol. Dis. 26, 212-220. (Pubitemid 46436499)
16. Hamers, F.P., Koopmans, GC., and Joosten, E.A. (2006). Cat-Walk-assisted gait analysis in the assessment of spinal cord injury. J. Neurotrauma 23, 537-548. (Pubitemid 43726327)
17. Hamers, F.P., Lankhorst, A.J., van Laar, T.J., Veldhuis, W.B., and Gispen, W.H. (2001). Automated quantitative gait analysis during overground locomotion in the rat: its application to spinal cord contusion and transection injuries. J. Neurotrauma 18,187-201. (Pubitemid 32173426)
18. Idrobo, F., Nandy, K., Mostofsky, D.I., Blatt, L., and Nandy, L. (1987). Dietary restriction: effects on radial maze learning and lipofuscin pigment deposition in the hippocampus and frontal cortex. Arch. Gerontol. Geriatr. 6, 355-362. (Pubitemid 18007956)
19. Jordan, L.M., Liu, J., Hedlund, P.B., Akay, T., and Pearson, K.G (2008). Descending command systems for the initiation of lo-comotion in mammals. Brain Res. Rev. 57, 183-191. (Pubitemid 350213101)
20. Koopmans, GC., Deumens, R, Buss, A., Geoghegan, L., Myint, A.M., Honig, W.H., Kern, N., Joosten, E.A., Noth, J., and Brook, GA. (2009). Acute rolipram/thalidomide treatment improves tissue sparing and locomotion after experimental spinal cord injury. Exp. Neurol. 216, 490-498.
21. Koopmans, G.C., Deumens, R., Honig, W.M., Hamers, F.P., Steinbusch, H.W., and Joosten, E.A. (2005). The assessment of locomotor function in spinal cord injured rats: the importance of objective analysis of coordination. J. Neurotrauma 22, 214-225. (Pubitemid 40333516)
22. Kwon, B.K., Okon, E.B., Tsai, E., Beattie, M.S., Bresnahan, I.C., Magnuson, D.K., Reier, P.J., McTigue, D.M., Popovich, P.G., Blight, A.R, Oudega, M., Guest, I.D., Weaver, L.C., Fehlings, M.G, Tetzlaff, W. (2010). A grading system to evaluate ob-jectively the strength of pre-clinical data of acute neuropro-tective therapies for clinical translation in spinal cord injury. J. Neurotrauma (E-pub ahead of print.)
23. Liu, K., Lu, Y., Lee, J.K., Samara, R, Willenberg, R, Sears-Kraxberger, I., Tedeschi, A., Park, K.K., Jin, D., Cai, B., Xu, B., Connolly, L., Steward, O., Zheng, B., and He, Z. (2010). PTEN deletion enhances the regenerative ability of adult corticosp-inal neurons. Nat. Neurosci. 13, 1075-1081.
24. Martin, B., Pearson, M., Brenneman, R, Golden, E., Keselman, A., Iyun, T., Carlson, O.D., Egan, J.M., Becker, K.G., Wood, W. 3rd., Prabhu, V., de Cabo, R, Maudsley, S., and Mattson, M.P. (2008). Conserved and differential effects of dietary energy intake on the hippocampal transcriptomes of females and males. PLoS One 3, e2398.
25. Martin, B., Pearson, M., Kebejian, L., Golden, E., Keselman, A., Bender, M., Carlson, O., Egan, J., Ladenheim, B., Cadet, J.L., Becker, K.G., Wood, W., Duffy, K., Vinayakumar, P., Maudsley, S., and Mattson, M.P. (2007). Sex-dependent met-abolic, neuroendocrine, and cognitive responses to dietary energy restriction and excess. Endocrinology 148, 4318-4333. (Pubitemid 47295690)
26. Maswood, N., Young, J., Tilmont, E., Zhang, Z., Gash, D.M., Gerhardt, G.A., Grondin, R., Roth, G.S., Mattison, J., Lane, M.A., Carson, RE., Cohen, R.M., Mouton, P.R., Quigley, C., Mattson, M.P., and Ingram, D.K. (2004). Caloric restriction increases neurotrophic factor levels and attenuates neuro-chemical and behavioral deficits in a primate model of Par-kinson's disease. Proc Natl. Acad. Sci. USA 101,18171-18176. (Pubitemid 40054092)
27. Mattson, M.P., Chan, S.L., and Duan, W. (2002). Modification of brain aging and neurodegenerative disorders by genes, diet, and behavior. Physiol. Rev. 82, 637-672. (Pubitemid 34743334)
28. Mattson, M.P., Duan, W., and Guo, Z. (2003). Meal size and fre-quency affect neuronal plasticity and vulnerability to disease: cellular and molecular mechanisms. J. Neurochem. 84,417-431. (Pubitemid 36182240)
29. Mattson, M.P. (2005). Energy intake, meal frequency, and health: a neurobiological perspective. Annu. Rev. Nutr. 25, 237-260. (Pubitemid 41209002)
30. Metz, GA., and Whishaw, I.Q. (2002). Cortical and subcortical lesions impair skilled walking in the ladder rung walking test: a new task to evaluate fore-and hindlimb stepping, placing, and co-ordination. J. Neurosci. Methods 115, 169-179. (Pubitemid 34461965)
31. Mouton, P.R, Chachich, M.E., Quigley, C., Spangler, E., and Ingram, D.K. (2009). Caloric restriction attenuates amyloid deposition in middle-aged dtg APP/PS1 mice. Neurosci. Lett. 464,184-187
32. Park, E., Velumian, A.A., and Fehlings, M.G (2004). The role of excitotoxicity in secondary mechanisms of spinal cord injury: a review with an emphasis on the implications for white matter degeneration. J. Neurotrauma 21, 754-774. (Pubitemid 38880247)
33. Patel, N.V., Gordon, M.N., Connor, K.E., Good, RA., Engelman, R.W., Mason, J., Morgan, D.G., Morgan, T.E., and Finch, C.E. (2005). Caloric restriction attenuates Abeta-deposition in Alz-heimer transgenic models. Neurobiol. Aging 26, 995-1000. (Pubitemid 40312661)
34. Pitsikas, N., and Algeri, S. (1992). Deterioration of spatial and nonspatial reference and working memory in aged rats: pro-tective effect of life-long calorie restriction. Neurobiol. Aging 13, 369-373.
35. Plunet, W.T., Lam, C.K., Lee, J.H., Liu, J., and Tetzlaff, W. (2010). Prophylactic dietary restriction may promote functional recovery and increase lifespan after spinal cord injury. Ann. NY Acad. Sci. 1198 (Suppl. 1), E1-E11.
36. Plunet, W.T., Streijger, F., Lam, C.K., Lee, J.H., Liu, J., and Tet-zlaff, W. (2008). Dietary restriction started after spinal cord injury improves functional recovery. Exp. Neurol. 213, 28-35.
37. Qin, W., Yang, T., Ho, L., Zhao, Z., Wang, J., Chen, L., Zhao, W., Thiyagarajan, M., MacGrogan, D., Rodgers, J.T., Puigserver, P., Sadoshima, J., Deng, H., Pedrini, S., Gandy, S., Sauve, A.A., and Pasinetti, GM. (2006). Neuronal SIRT1 activation as a novel mechanism underlying the prevention of Alzheimer disease amyloid neuropathology by calorie restriction. J. Biol. Chem. 281, 21745-21754. (Pubitemid 44181878)
38. Ramer, L.M., Ramer, M.S., and Steeves, J.D. (2005). Setting the stage for functional repair of spinal cord injuries: a cast of thousands. Spinal Cord 43, 134-161. (Pubitemid 40432659)
39. Saruhashi, Y., Matsusue, Y., and Fujimiya, M. (2009). The recov-ery of 5-HT transporter and 5-HT immunoreactivity in injured rat spinal cord. Arch. Orthop. Trauma Surg. 129, 1279-1285.
40. Saruhashi, Y., Young, W., and Perkins, R. (1996). The recovery of 5-HT immunoreactivity in lumbosacral spinal cord and locomotor function after thoracic hemisection. Exp. Neurol. 139, 203-213. (Pubitemid 26228089)
41. Schmidt, B.J., and Jordan, L.M. (2000). The role of serotonin in reflex modulation and locomotor rhythm production in the mammalian spinal cord. Brain Res. Bull. 53, 689-710. (Pubitemid 32114321)
42. Sharma, S., and Kaur, G (2005). Neuroprotective potential of dietary restriction against kainate-induced excitotoxicity in adult male Wistar rats. Brain Res. Bull 67, 482-491. (Pubitemid 41416743)
43. Streijger, E., Plunet, W.T., Lee, J.H.T., Liu, I., Lam, C.K., Park, S., Hilton, B.J., Fransen, B.J., Matheson, K.A.I., Assinck, P., Kwon, B.K., Tetzlaff, W. (2011). Post-injury ketogenic diet improves gross and skilled forelimb motor function after cervical cord contusion in rats (In submission).
44. Van Meeteren, N.L., Eggers, R, Lankhorst, A.J., Gispen, W.H., and Hamers, F.P. (2003). Locomotor recovery after spinal cord contusion injury in rats is improved by spontaneous exercise. J. Neurotrauma 20, 1029-1037. (Pubitemid 37288562)
45. Wang, J., Ho, L., Qin, W., Rocher, A.B., Seror, I., Humala, N., Maniar, K., Dolios, G., Wang, R, Hof, P.R, and Pasinetti, GM. (2005). Caloric restriction attenuates beta-amyloid neuropa-thology in a mouse model of Alzheimer's disease. FASEB J. 19, 659-661. (Pubitemid 40471277)
46. Wan, R., Camandola, S., and Mattson, M.P. (2003). Intermittent fasting and dietary supplementation with 2-deoxy-D-glucose improve functional and metabolic cardiovascular risk factors in rats. FASEB J. 17, 1133-1134.
47. Wu, P., Shen, Q., Dong, S., Xu, Z., Tsien, J.Z., and Hu, Y. (2008). Calorie restriction ameliorates neurodegenerative phenotypes in forebrain-specific presenilin-1 and presenilin-2 double knockout mice. Neurobiol. Aging 29, 1502-1511.
48. Yu, Z.F., and Mattson, M.P. (1999). Dietary restriction and 2-deoxyglucose administration reduce focal ischemic brain damage and improve behavioral outcome: evidence for a preconditioning mechanism. J. Neurosci. Res. 57, 830-839. (Pubitemid 29416113)
49. Zhu, H., Guo, Q., and Mattson, M.P. (1999). Dietary restriction protects hippocampal neurons against the death-promoting action of a presenilin-1 mutation. Brain Res. 842, 224-229. (Pubitemid 29447872)