Positive effects of aerobic exercise on learning and memory functioning, which correlate with hippocampal IGF-1 increase in adolescent rats

Neuroscience Letters

Volumn 549, Issue , 2013, Pages 177-181

  Cetinkaya, Caner ^a   Sisman, Ali Riza ^a   Kiray, Muge ^a   Camsari, Ulas Mehmet ^b   Gencoglu, Celal ^a   Baykara, Basak ^a   Aksu, Ilkay ^a   Uysal, Nazan ^a  

^a DOKUZ EYLUL UNIVERSITY   (Turkey)

^b Mayo Clinic   (United States)

Author keywords

Adolescent; Exercise; Hippocampus; IGF 1; Spatial learning and memory

Indexed keywords

SOMATOMEDIN C;

ADOLESCENT; AEROBIC EXERCISE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CELL DENSITY; COGNITION; CONTROLLED STUDY; DENTATE GYRUS; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; LIVER LEVEL; MALE; MEMORY; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN SECRETION; RAT; SPATIAL LEARNING; TREADMILL EXERCISE; VELOCITY;

ADOLESCENT; EXERCISE; HIPPOCAMPUS; IGF-1; SPATIAL LEARNING AND MEMORY;

ANIMALS; HIPPOCAMPUS; INSULIN-LIKE GROWTH FACTOR I; LEARNING; MALE; MAZE LEARNING; MEMORY; NEURONS; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, WISTAR;

EID: 84880746390     PISSN: 03043940     EISSN: 18727972     Source Type: Journal    
DOI: 10.1016/j.neulet.2013.06.012     Document Type: Article

References (52)

1. Aksu I., Ates M., Baykara B., Kiray M., Sisman A.R., Buyuk E., Baykara B., Cetinkaya C., Gumus H., Uysal N. Anxiety correlates to decreased blood and prefrontal cortex IGF-1 levels in streptozotocin induced diabetes. Neurosci. Lett. 2012, 531:176-181.
2. Aksu I., Baykara B., Kiray M., Gurpinar T., Sisman A.R., Ekerbicer N., Tas A., Gokdemir-Yazar O., Uysal N. Serum IGF-1 levels correlate negatively to liver damage in diabetic rats. Biotechnol. Histochem. 2013, 88:194-201.
3. Aleman A., Torres-Alemán I. Circulating insulin-like growth factor I and cognitive function: neuromodulation throughout the lifespan. Prog. Neurobiol. 2009, 89:256-265.
4. Arikawa A.Y., Kurzer M.S., Thomas W., Schmitz K.H. No effect of exercise on insulin-like growth factor-I insulin, and glucose in young women participating in a 16-week randomized controlled trial. Cancer Epidemiol. Biomarkers Prev. 2010, 19:2987-2990.
5. Arturi F., Succurro E., Procopio C., Pedace E., Mannino G.C., Lugarà M., Procopio T., Andreozzi F., Sciacqua A., Hribal M.L., Perticone F., Sesti G. Nonalcoholic fatty liver disease is associated with low circulating levels of insulin-like growth factor-I. J. Clin. Endocrinol. Metab. 2011, 96:E1640-E1644.
6. Arwert L.I., Deijen J.B., Drent M.L. The relation between insulin-like growth factor I levels and cognition in healthy elderly: a meta-analysis. Growth Horm. IGF Res. 2005, 15:416-422.
7. Barbieri M., Ferrucci L., Ragno E., Corsi A., Bandinelli S., Bonafè M., Olivieri F., Giovagnetti S., Franceschi C., Guralnik J.M., Paolisso G. Chronic inflammation and the effect of IGF-I on muscle strength and power in older persons. Am. J. Physiol. Endocrinol. Metab. 2003, 284:E481-E487.
8. Ben Ounis O., Elloumi M., Zouhal H., Makni E., Denguezli M., Amri M., Lac G., Tabka Z. Effect of individualized exercise training combined with diet restriction on inflammatory markers and IGF-1/IGFBP-3 in obese children. Ann. Nutr. Metab. 2010, 56:260-266.
9. Berg U., Bang P. Exercise and circulating insulin-like growth factor I. Horm. Res. 2004, 62:50-58.
10. Bonefeld K., Møller S. Insulin-like growth factor-I and the liver. Liver Int. 2011, 31:911-919.
11. Borst S.E., De Hoyos D.V., Garzarella L., Vincent K., Pollock B.H., Lowenthal D.T., Pollock M.L. Effects of resistance training on insulin-like growth factor-I and IGF binding proteins. Med. Sci. Sports Exerc. 2001, 33:648-653.
12. Carro E., Nuñez A., Busiguina S., Torres-Aleman I. Circulating insulin-like growth factor I mediates effects of exercise on the brain. J. Neurosci. 2000, 20:2926-2933.
13. Cassilhas R.C., Viana V.A., Grassmann V., Santos R.T., Santos R.F., Tufik S., Mello M.T. The impact of resistance exercise on the cognitive function of the elderly. Med. Sci. Sports Exerc. 2007, 39:1401-1407.
14. Cassilhas R.C., Lee K.S., Venâncio D.P., Oliveira M.G., Tufik S., de Mello M.T. Resistance exercise improves hippocampus-dependent memory. Braz. J. Med. Biol. Res. 2012, 45:1215-1220.
15. Cotman C.W., Engesser-Cesar C. Exercise enhances and protects brain function. Exerc. Sport Sci. Rev. 2002, 30:75-79.
16. DeVol D.L., Rotwein P., Sadow J.L., Novakofski J., Bechtel P.J. Activation of insulin-like growth factor gene expression during work-induced skeletal muscle growth. Am. J. Physiol. 1990, 259:E89-E95.
17. Duman R.S. Neurotrophic factors and regulation of mood: role of exercise diet and metabolism. Neurobiol. Aging 2005, 26:88-93.
18. Eliakim A., Brasel J.A., Mohan S., Wong W.L., Cooper D.M. Increased physical activity and the growth hormone-IGF-I axis in adolescent males. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1998, 275:R308-R314.
19. Eliakim A., Portal S., Zadik Z., Meckel Y., Nemet D. Training reduces catabolic and inflammatory response to a single practice in female volleyball players. J. Strength Cond. Res. 2013, (February (25)).
20. Fabel K., Kempermann G. Physical activity and the regulation of neurogenesis in the adult and aging brain. Neuromol. Med. 2008, 10:59-66.
21. Gatti R., De Palo E.F., Antonelli G., Spinella P. IGF-I/IGFBP system: metabolism outline and physical exercise. J. Endocrinol. Invest. 2012, 35:699-707.
22. Gluckman P.D., Guan J., Williams C., Scheepens A., Zhang R., Bennet L., Gunn A. Asphyxial brain injury - the role of the IGF system. Mol. Cell. Endocrinol. 1998, 140:95-99.
23. Gomes R.J., Mello M.A.R., Caetano F.H., Sibuya C.Y., Anaruma C.A., Rogatto G.P., Pauli J.R., Luciano E. Effects of swimming training on bone mass and the GH/IGF-1 axis in diabetic rats. Growth Horm. IGF Res. 2006, 16:326-331.
24. Gomes R.J., Caetano F.C., Mello M.A.R., Luciano E. Effect of chronic exercise on growth factors in diabetic rats. J. Exerc. Physiol. 2005, 8:16-23.
25. Guan J., Bennet L., Gluckman P.D., Gunn A.J. Insulin-like growth factor-1 and post-ischemic brain injury. Prog. Neurobiol. 2003, 70:443-462.
26. Gunnell D., Miller L.L., Rogers I., Holly J.M. ALSPAC Study Team Association of insulin-like growth factor I and insulin-like growth factor-binding protein-3 with intelligence quotient among 8- to 9-year-old children in the Avon Longitudinal Study of Parents and Children. Pediatrics 2005, 116:681-686.
27. Hodge R.D., D'Ercole A.J., O'Kusky J.R. Insulin-like growth factor accelerates the cell cycle by decreasing G1 phase length and increases cell cycle reentry in the embryonic cerebral cortex. J. Neurosci. 2004, 24:10201-10210.
28. Leme J.A., Gomes R.J., Mello M.A.R., Luciano E. Effects of short-term physical training on the liver IGF-I in diabetic rats. Growth Factors 2007, 25:9-14.
29. Leme J.A., Silveira R.F., Gomes R.J., Moura R.F., Sibuya C.A., Mello M.A., Luciano E. Long-term physical training increases liver IGF-I in diabetic rats. Growth Horm. IGF Res. 2009, 19:262-266.
30. Llorens-Martín M., Torres-Alemán I., Trejo J.L. Exercise modulates insulin-like growth factor 1-dependent and -independent effects on adult hippocampal neurogenesis and behaviour. Mol. Cell. Neurosci. 2010, 44:109-117.
31. Mitschelen M., Yan H., Farley J.A., Warrington J.P., Han S., Hereñú C.B., Csiszar A., Ungvari Z., Bailey-Downs L.C., Bass C.E., Sonntag W.E. Long-term deficiency of circulating and hippocampal insulin-like growth factor I induces depressive behavior in adult mice: a potential model of geriatric depression. Neuroscience 2011, 185:50-60.
32. O'Kusky J.R., Ye P., D'Ercole A.J. Insulin-like growth factor-I promotes neurogenesis and synaptogenesis in the hippocampal dentate gyrus during postnatal development. J. Neurosci. 2000, 20:8435-8442.
33. Ozdemir D., Baykara B., Aksu I., Kiray M., Sisman A.R., Cetin F., Dayi A., Gurpinar T., Uysal N., Arda M.N. Relationship between circulating IGF-1 levels and traumatic brain injury-induced hippocampal damage and cognitive dysfunction in immature rats. Neurosci. Lett. 2012, 507:84-89.
34. Reinhardt R.R., Bondy C.A. Insulin-like growth factors cross the blood-brain barrier. Endocrinology 1994, 135:1753-1761.
35. Rosendal L.H., Langberg A., Flyvbjerg A., Frystyk J., Orskov H., Kjaer M. Physical capacity influences the response of insulin-like growth factor and its binding proteins to training. J. Appl. Physiol. 2002, 93:1669-1675.
36. Rosenfeld R.G., Pham H., Cohen P. Insulin-like growth factor binding proteins and their regulation. Acta Paediatr. 1994, 83:61-67.
37. Ross A.P., Bruggeman E.C., Kasumu A.W., Mielke J.G., Parent M.B. Non-alcoholic fatty liver disease impairs hippocampal-dependent memory in male rats. Physiol. Behav. 2012, 106:133-141.
38. Schmitz K.H., Ahmed R.L., Yee D. Effects of a 9-month strength training intervention on insulin, insulin like growth factor (IGF)-I IGF-binding protein (IGFBP)-1, and IGFBP-3 in 30-50-year-old women. Cancer Epidemiol. Biomarkers Prev. 2002, 11:1597-1604.
39. Spear L.P. The adolescent brain and age related behavioral manifestations. Neurosci. Biobehav. Rev. 2000, 4:417-463.
40. Thissen J.P., Ketelslegers J.M., Underwood L.E. Nutritional regulation of the insulin-like growth factors. Endocr. Rev. 1994, 15:80-101.
41. Torres-Aleman I. Toward a comprehensive neurobiology of IGF-I. Dev. Neurobiol. 2010, 70:384-396.
42. Trejo J.L., Piriz J., Llorens-Martin M.V., Fernandez A.M., Bolos M., LeRoith D., Nunez A., Torres-Aleman I. Central actions of liver-derived insulin-like growth factor I underlying its pro-cognitive effects. Mol. Psychiatry 2007, 12:1118-1128.
43. Trejo J.L., Carro E., Torres-Aleman I. Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J. Neurosci. 2001, 21:1628-1634.
44. Trejo J.L., Llorens-Martín M.V., Torres-Alemán I. The effects of exercise on spatial learning and anxiety-like behavior are mediated by an IGF-I-dependent mechanism related to hippocampal neurogenesis. Mol. Cell. Neurosci. 2008, 37:402-411.
45. Uysal N., Tugyan K., Kayatekin B.M., Acikgoz O., Bagriyanik H.A., Gonenc S., Ozdemir D., Aksu I., Topcu A., Semin I. The effects of regular aerobic exercise in adolescent period on hippocampal neuron density apoptosis and spatial memory. Neurosci. Lett. 2005, 383:241-245.
46. Tugyan K., Uysal N., Ozdemir D., Sonmez U., Pekcetin C., Erbil G., Sonmez A. Protective effect of melatonin against maternal deprivation-induced acute hippocampal damage in infant rats. Neurosci. Lett. 2006, 398:145-150.
47. Uysal N., Gonenc S., Acikgoz O., Pekçetin C., Kayatekin B.M., Sonmez A., Semin I. Age-dependent effects of maternal deprivation on oxidative stress in infant rat brain. Neurosci. Lett. 2005, 384:98-101.
48. Uysal N., Sisman A.R., Dayi A., Ozbal S., Cetin F., Baykara B., Aksu I., Tas A., Cavus S.A., Gonenc-Arda S., Buyuk E. Acute footshock-stress increases spatial learning-memory and correlates to increased hippocampal BDNF and VEGF and cell numbers in adolescent male and female rats. Neurosci. Lett. 2012, 514:141-146.
49. van Praag H. Exercise and the brain: something to chew on. Trends Neurosci. 2009, 32:283-290.
50. Yan H., Mitschelen M., Bixler G.V., Brucklacher R.M., Farley J.A., Han S., Freeman W.M., Sonntag W.E. Circulating IGF-1 regulates hippocampal IGF-1 levels and brain gene expression during adolescence. J. Endocrinol. 2011, 211:27-37.
51. Zanconato S., Moromisato D.Y., Moromisato M.Y., Woods J., Brasel J.A., Leroith D., Roberts C.T., Cooper D.M. Effect of training and growth hormone suppression on insulin-like growth factor I mRNA in young rats. J. Appl. Physiol. 1994, 76:2204-2209.
52. Zhang J., Moats-Staats B.M., Ye P., D'Ercole A.J. Expression of insulin-like growth factor system genes during the early postnatal neurogenesis in the mouse hippocampus. J. Neurosci. Res. 2007, 85:1618-1627.