Maternal aerobic exercise during pregnancy can increase spatial learning by affecting leptin expression on offspring's early and late period in life depending on gender

The Scientific World Journal

Volumn 2012, Issue , 2012, Pages

  Dayi, Ayfer ^a   Agilkaya, Sinem ^a   Ozbal, Seda ^a   Cetin, Ferihan ^a   Aksu, Ilkay ^a   Gencoglu, Celal ^a   Cingoz, Sultan ^a   Pekcetin, Cetn ^a   Tugyan, Kazim ^a   Kayatekin, Berkant Muammer ^a   Uysal, Nazan ^a  

^a DOKUZ EYLUL UNIVERSITY   (Turkey)

Author keywords

[No Author keywords available]

Indexed keywords

LEPTIN; LEPTIN RECEPTOR;

AEROBIC EXERCISE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; FEMALE; HIPPOCAMPUS; HISTOLOGY; LEARNING; MALE; MEMORY; NERVE CELL PLASTICITY; NONHUMAN; PREGNANCY; PREPUBERTY; PROGENY; PROTEIN EXPRESSION; PUP (RODENT); RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RUNNING; SEX DIFFERENCE; SPATIAL LEARNING; AGE; ANIMAL; DENTATE GYRUS; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; MAZE TEST; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONPARAMETRIC TEST; PHYSIOLOGY; WISTAR RAT;

AGE FACTORS; ANIMALS; CA1 REGION, HIPPOCAMPAL; CA3 REGION, HIPPOCAMPAL; CELL SURVIVAL; DENTATE GYRUS; FEMALE; MALE; MAZE LEARNING; MEMORY; NEUROGENESIS; NEURONAL PLASTICITY; NEURONS; PHYSICAL CONDITIONING, ANIMAL; PREGNANCY; RATS; RATS, WISTAR; RECEPTORS, LEPTIN; SEX FACTORS; STATISTICS, NONPARAMETRIC;

EID: 84867829806     PISSN: None     EISSN: 1537744X     Source Type: Journal    
DOI: 10.1100/2012/429803     Document Type: Article

References (51)

1. Cotman C. W., Engesser-Cesar C., Exercise enhances and protects brain function. Exercise and Sport Sciences Reviews 2002 30 2 75 79 2-s2.0-0036214846 (Pubitemid 34298808)
2. Swain R. A., Harris A. B., Wiener E. C., Dutka M. V., Morris H. D., Theien B. E., Konda S., Engberg K., Lauterbur P. C., Greenough W. T., Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience 2003 117 4 1037 1046 2-s2.0-0345700667 10.1016/S0306-4522(02)00664-4 (Pubitemid 36332321)
3. Black J. E., Isaacs K. R., Anderson B. J., Alcantara A. A., Greenough W. T., Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proceedings of the National Academy of Sciences of the United States of America 1990 87 14 5568 5572 2-s2.0-0025180876 10.1073/pnas.87.14.5568 (Pubitemid 20260222)
4. Pysh J. J., Weiss G. M., Exercise during development induces an increase in Purkinje cell dendritic tree size. Science 1979 206 4415 230 231 2-s2.0-0018672051 (Pubitemid 10242039)
5. Howe M. L., Stones M. J., Brainerd C. J., Cognitive and Behavioral Performance Factors in a Typical Aging 1990 New York, NY, USA Springer
6. 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. Neuroscience Letters 2005 383 3 241 245 2-s2.0-20444389396 10.1016/j.neulet.2005.04.054 (Pubitemid 40805563)
7. Rezaie P., Trillo-Pazos G., Everall I. P., Male D. K., Expression of β -chemokines and chemokine receptors in human fetal astrocyte and microglial co-cultures: potential role of chemokines in the developing CNS. GLIA 2002 37 1 64 75 2-s2.0-0036006723 10.1002/glia.1128 (Pubitemid 34103095)
8. Marco E. M., Adriani W., Llorente R., Laviola G., Viveros M. P., Detrimental psychophysiological effects of early maternal deprivation in adolescent and adult rodents: altered responses to cannabinoid exposure. Neuroscience and Biobehavioral Reviews 2009 33 4 498 507 2-s2.0-61849119556 10.1016/j.neubiorev.2008.03.008
9. 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. Neuroscience Letters 2006 398 1-2 145 150 2-s2.0-33645983914 10.1016/j.neulet.2005.12.090
10. Rosenzweig M. R., Bennett E. L., Psychobiology of plasticity: effects of training and experience on brain and behavior. Behavioural Brain Research 1996 78 1 57 65 2-s2.0-0029893652 10.1016/0166-4328(95)00216-2 (Pubitemid 26179783)
11. O'Keefe J., Nadel L., The Hippocampus as a Cognitive Map 1978 Oxford, UK Clarendon
12. Van Praag H., Christie B. R., Sejnowski T. J., Gage F. H., Running enhances neurogenesis, learning, and long-term potentiation in mice. Proceedings of the National Academy of Sciences of the United States of America 1999 96 23 13427 13431 2-s2.0-0033539607 10.1073/pnas.96.23.13427
13. Gould E., Tanapat P., Stress and hippocampal neurogenesis. Biological Psychiatry 1999 46 11 1472 1479 2-s2.0-0032721988 10.1016/S0006-3223(99)00247-4
14. Uysal N., Ozdemir D., Dayi A., Yalaz G., Baltaci A. K., Bediz C. S., Effects of maternal deprivation on melatonin production and cognition in adolescent male and female rats. Neuroendocrinology Letters 2005 26 5 555 560 2-s2.0-29544431706 (Pubitemid 43013731)
15. Bungum T. J., Peaslee D. L., Jackson A. W., Perez M. A., Exercise during pregnancy and type of delivery in nulliparae. Journal of Obstetric, Gynecologic, and Neonatal Nursing 2000 29 3 258 264 2-s2.0-0034182813
16. Parnpiansil P., Jutapakdeegul N., Chentanez T., Kotchabhakdi N., Exercise during pregnancy increases hippocampal brain-derived neurotrophic factor mRNA expression and spatial learning in neonatal rat pup. Neuroscience Letters 2003 352 1 45 48 2-s2.0-0242711665 10.1016/j.neulet.2003.08.023 (Pubitemid 37412322)
17. Ahima R. S., Leptin and the neuroendocrinology of fasting. Frontiers of Hormone Research 2000 26 42 56 2-s2.0-0033657074
18. Morash B., Li A., Murphy P. R., Wilkinson M., Ur E., Leptin gene expression in the brain and pituitary gland. Endocrinology 1999 140 12 5995 5998 2-s2.0-0033304752 (Pubitemid 30645391)
19. Schwartz M. W., Peskind E., Raskind M., Boyko E. J., Porte D. Jr., Cerebrospinal fluid leptin levels: relationship to plasma levels and to adiposity in humans. Nature Medicine 1996 2 5 589 593 2-s2.0-0029881125 10.1038/nm0596-589 (Pubitemid 26151520)
20. Banks W. A., Kastin A. J., Huang W., Jaspan J. B., Maness L. M., Leptin enters the brain by a saturable system independent of insulin. Peptides 1996 17 2 305 311 2-s2.0-0029864416 10.1016/0196-9781(96)00025-3 (Pubitemid 26124406)
21. Couce M. E., Burguera B., Parisi J. E., Jensen M. D., Lloyd R. V., Localization of leptin receptor in the human brain. Neuroendocrinology 1997 66 3 145 150 2-s2.0-0030806382 (Pubitemid 27356895)
22. Elmquist J. K., Bjorbaek C., Ahima R. S., Flier J. S., Saper C. B., Distributions of leptin receptor mRNA isoforms in the rat brain. Journal of Comparative Neurology 1998 395 535 547 (Pubitemid 28226097)
23. Håkansson M.-L., Brown H., Ghilardi N., Skoda R. C., Meister B., Leptin receptor immunoreactivity in chemically defined target neurons of the hypothalamus. Journal of Neuroscience 1998 18 1 559 572 2-s2.0-0031963436 (Pubitemid 28046812)
24. Bereiter D. A., Jeanrenaud B., Altered neuroanatomical organization in the central nervous system of the genetically obese (ob/ob) mouse. Brain Research 1979 165 2 249 260 2-s2.0-0018409557 10.1016/0006-8993(79)90557-2 (Pubitemid 9153505)
25. Sena A., Sarliève L. L., Rebel G., Brain myelin of genetically obese mice. Journal of the Neurological Sciences 1985 68 2-3 233 244 2-s2.0-0021814756 (Pubitemid 15031493)
26. Steppan C. M., Swick A. G., A role for leptin in brain development. Biochemical and Biophysical Research Communications 1999 256 3 600 602 2-s2.0-0033599509 10.1006/bbrc.1999.0382 (Pubitemid 29301152)
27. Ahima R. S., Bjorbæk C., Osei S., Flier J. S., Regulation of neuronal and glial proteins by leptin: implications for brain development. Endocrinology 1999 140 6 2755 2762 2-s2.0-17744375347 10.1210/en.140.6.2755 (Pubitemid 32245155)
28. Anderson M. F., Åberg M. A. I., Nilsson M., Eriksson P. S., Insulin-like growth factor-I and neurogenesis in the adult mammalian brain. Developmental Brain Research 2002 134 1-2 115 122 2-s2.0-0037204590 10.1016/S0165-3806(02)00277-8 (Pubitemid 34310242)
29. Holmes M. M., Galea L. A. M., Mistlberger R. E., Kempermann G., Adult hippocampal neurogenesis and voluntary running activity: circadian and dose-dependent effects. Journal of Neuroscience Research 2004 76 2 216 222 2-s2.0-1842426537 10.1002/jnr.20039 (Pubitemid 38451209)
30. Hummel K. P., Dickie M. M., Coleman D. L., Diabetes, a new mutation in the mouse. Science 1966 153 3740 1127 1128 2-s2.0-0014004384
31. Stranahan A. M., Lee K., Martin B., Maudsley S., Golden E., Cutler R. G., Mattson M. P., Voluntary exercise and caloric restriction enhance hippocampal dendritic spine density and BDNF levels in diabetic mice. Hippocampus 2009 19 10 951 961 2-s2.0-70349262248 10.1002/hipo.20577
32. Aksu I., Baykara B., Ozbal S., Maternal treadmill exercise during pregnancy decreases anxiety and increases prefrontal cortex VEGF and BDNF levels of rat pups in early and late periods of life. Neuroscience Letters 2012 516 221 225
33. Paxinos G., Watson C., The Rat Brain in Stereotaxic Coordinates 1982 New York, NY, USA Academic Press
34. Kramer A. F., Hahn S., Cohen N. J., Banich M. T., McAuley E., Harrison C. R., Chason J., Vakil E., Bardell L., Boileau R. A., Colcombe A., Ageing, fitness and neurocognitive function. Nature 1999 400 6743 418 419 2-s2.0-0033614960 10.1038/22682 (Pubitemid 29361788)
35. Kleim J. A., Cooper N. R., VandenBerg P. M., Exercise induces angiogenesis but does not alter movement representations within rat motor cortex. Brain Research 2002 934 1 1 6 2-s2.0-0037177439 10.1016/S0006-8993(02) 02239-4 (Pubitemid 34286562)
36. Bland B. H., Bird J., Jackson J., Natsume K., Medial septal modulation of the ascending brainstem hippocampal synchronizing pathways in the freely moving rat. Hippocampus 2006 16 1 11 19 2-s2.0-33644860636 10.1002/hipo.20136
37. Ma Q., Beneficial effects of moderate voluntary physical exercise and its biological mechanisms on brain health. Neuroscience Bulletin 2008 24 4 265 270 2-s2.0-48749097234 10.1007/s12264-008-0402-1
38. Trejo J. L., Carro E., Torres-Alemán I., Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. Journal of Neuroscience 2001 21 5 1628 1634 2-s2.0-0035283153 (Pubitemid 32182203)
39. Fabel K., 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. European Journal of Neuroscience 2003 18 10 2803 2812 2-s2.0-0346751060 10.1111/j.1460-9568.2003.03041.x (Pubitemid 37542133)
40. Shioda S., Funahashi H., Nakajo S., Yada T., Maruta O., Nakai Y., Immunohistochemical localization of leptin receptor in the rat brain. Neuroscience Letters 1998 243 13 41 44 2-s2.0-0031887488 10.1016/S0304-3940(98) 00082-2 (Pubitemid 28109406)
41. Shanley L. J., Irving A. J., Harvey J., Leptin enhances NMDA receptor function and modulates hippocampal synaptic plasticity. Journal of Neuroscience 2001 21 24 RC186 2-s2.0-0035893251
42. Wayner M. J., Armstrong D. L., Phelix C. F., Oomura Y., Orexin-A (Hypocretin-1) and leptin enhance LTP in the dentate gyrus of rats in vivo. Peptides 2004 25 6 991 996 2-s2.0-2942620246 10.1016/j.peptides.2004.03.018 (Pubitemid 38760287)
43. Li X. L., Aou S., Oomura Y., Hori N., Fukunaga K., Hori T., Impairment of long-term potentiation and spatial memory in leptin receptor-deficient rodents. Neuroscience 2002 113 3 607 615 2-s2.0-0037008873 10.1016/S0306-4522(02)00162-8 (Pubitemid 34874684)
44. Oomura Y., Hori N., Shiraishi T., Fukunaga K., Takeda H., Tsuji M., Matsumiya T., Ishibashi M., Aou S., Li X. L., Kohno D., Uramura K., Sougawa H., Yada T., Wayner M. J., Sasaki K., Leptin facilitates learning and memory performance and enhances hippocampal CA1 long-term potentiation and CaMK II phosphorylation in rats. Peptides 2006 27 11 2738 2749 2-s2.0-33750091967 10.1016/j.peptides.2006.07.001 (Pubitemid 44584418)
45. Bliss T. V. P., Collingridge G. L., A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993 361 6407 31 39 2-s2.0-0027476024 10.1038/361031a0 (Pubitemid 23020772)
46. Winocur G., Greenwood C. E., Piroli G. G., Grillo C. A., Reznikov L. R., Reagan L. P., McEwen B. S., Memory impairment in Obese Zucker rats: an investigation of cognitive function in an animal model of insulin resistance and obesity. Behavioral Neuroscience 2005 119 5 1389 1395 2-s2.0-27744486073 10.1037/0735-7044.119.5.1389 (Pubitemid 41598751)
47. Farr S. A., Banks W. A., Morley J. E., Effects of leptin on memory processing. Peptides 2006 27 6 1420 1425 2-s2.0-33646789779 10.1016/j.peptides. 2005.10.006 (Pubitemid 43767004)
48. Brun V. H., Otnæss M. K., Molden S., Steffenach H. A., Witter M. P., Moser M. B., Moser E. I., Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 2002 296 5576 2243 2246 2-s2.0-0037150644 10.1126/science.1071089 (Pubitemid 34680313)
49. Amaral D. G., Witter M. P., The Hippocampal Formation: The Rat Nervous System 1995 San Diego, Calif, USA Academic Press
50. Eriksson P. S., Perfilieva E., Björk-Eriksson T., Alborn A. M., Nordborg C., Peterson D. A., Gage F. H., Neurogenesis in the adult human hippocampus. Nature Medicine 1998 4 11 1313 1317 2-s2.0-0031789814 10.1038/3305 (Pubitemid 28512114)
51. Kronenberg G., Lippoldt A., Kempermann G., Two genetic rat models of arterial hypertension show different mechanisms by which adult hippocampal neurogenesis is increased. Developmental Neuroscience 2006 29 1-2 124 133 2-s2.0-33845588118 10.1159/000096217 (Pubitemid 44934968)