Endurance training upregulates the nitric oxide/soluble guanylyl cyclase/cyclic guanosine 3′,5′-monophosphate pathway in the striatum, midbrain and cerebellum of male rats

Brain Research

Volumn 1618, Issue , 2015, Pages 29-40

  Chalimoniuk, Małgorzata ^a   Chrapusta, Stanisław J ^a   Lukačova, Nadežda ^b   Langfort, Józef ^c  

^a MOSSAKOWSKI MEDICAL RESEARCH CENTRE   (Poland)

^b Center of Excellence for Brain Research   (Slovakia)

^c INSTITUTE OF SPORT SCIENCES   (Poland)

Author keywords

Brain derived neurotrophic factor; Endurance training; Locomotion; Nitric oxide synthase; Soluble guanylyl cyclase

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CYCLIC GMP; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GUANYLATE CYCLASE; GUANYLATE CYCLASE ALPHA 1; GUANYLATE CYCLASE ALPHA 2; GUANYLATE CYCLASE BETA 1; NEURONAL NITRIC OXIDE SYNTHASE; UNCLASSIFIED DRUG; CELL RECEPTOR; NITRIC OXIDE; SOLUBLE GUANYLYL CYCLASE;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CEREBELLUM; CONTROLLED STUDY; CORPUS STRIATUM; ENDURANCE TRAINING; ENZYME ACTIVITY; ENZYME INDUCTION; HIPPOCAMPUS; LOCOMOTION; MALE; MESENCEPHALON; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; YOUNG ADULT; ANIMAL; BRAIN; ENDURANCE; EXERCISE TEST; METABOLISM; NEOSTRIATUM; PHYSIOLOGY; SIGNAL TRANSDUCTION; UPREGULATION; WISTAR RAT;

RATTUS; RATTUS NORVEGICUS;

ANIMALS; BRAIN; CEREBELLUM; CYCLIC GMP; EXERCISE TEST; GUANYLATE CYCLASE; MALE; MESENCEPHALON; NEOSTRIATUM; NITRIC OXIDE; PHYSICAL ENDURANCE; RATS; RATS, WISTAR; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84938088232     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2015.05.020     Document Type: Article

References (69)

1. T. Abekawa, T. Ohmori, and T. Koyama Effect of NO synthesis inhibition on striatal dopamine release and stereotyped behavior induced by a single administration of methamphetamine Prog. Neuropsychopharmacol. Biol. Psychiatry 21 1997 831 838 10.1016/S0278-5846(97)00083-3
2. N.C. Berchtold, G. Chinn, M. Chou, J.P. Kesslak, and C.W. Cotman Exercise primes a molecular memory for brain-derived neurotrophic factor protein induction in the rat hippocampus Neuroscience 133 2005 853 861 10.1016/j.neuroscience.2005.03.026
3. J.M. Burgunder, and P.T. Cheung Expression of soluble guanylyl cyclase gene in adult rat brain Eur. J. Neurosci. 6 1994 211 217 10.1111/j.1460-9568.1994.tb00263.x
4. A. Calignano, P. Persico, F. Mancuso, and L. Sorrentino Endogenous nitric oxide modulates morphine-induced changes in locomotion and food intake in mice Eur. J. Pharmacol. 231 1993 415 419 10.1016/0014-2999(93)90118-2
5. M.C. Carreras, and J.J. Poderoso Mitochondrial nitric oxide in the signaling of cell integrated responses Am. J. Physiol. Cell Physiol. 292 2007 C1569 C1580 10.1152/ajpcell.00248.2006
6. E. Castrén, B. Berninger, A. Leingärtner, and D. Lindholm Regulation of brain-derived neurotrophic factor mRNA levels in hippocampus by neuronal activity Prog. Brain Res. 117 1998 57 64
7. F. Cechetti, C. Fochesatto, D. Scopel, P. Nardin, C.A. Gonçalves, C.A. Netto, and I.R. Siqueira Effect of a neuroprotective exercise protocol on oxidative state and BDNF levels in the rat hippocampus Brain Res. 1188 2008 182 188 10.1016/j.brainres.2007.10.012
8. M.J. Chen, A.S. Ivy, and A.A. Russo-Neustadt Nitric oxide synthesis is required for exercise-induced increases in hippocampal BDNF and phosphatidylinositol 3′ kinase expression Brain Res. Bull. 68 2006 257 268 10.1016/j.brainresbull.2005.08.013
9. M.J. Chen, and A.A. Russo-Neustadt Nitric oxide signaling participates in norepinephrine-induced activity of neuronal intracellular survival pathways Life Sci. 81 2007 1280 1290 10.1016/j.lfs.2007.09.003
10. A. Cheng, S. Wang, J. Cai, M.S. Rao, and M.P. Mattson Nitric oxide acts in a positive feedback loop with BDNF to regulate neural progenitor cell proliferation and differentiation in the mammalian brain Dev. Biol. 258 2003 319 333 10.1016/S0012-1606(03)00120-9
11. T. Collier, and C.E. Sortwell Therapeutic potential of nerve growth factors in Parkinson's disease Drugs Aging 14 1999 261 287 10.2165/00002512-199914040-00003
12. C. Cunha, R. Brambilla, and K.L. Thomas A simple role for BDNF in learning and memory? Front. Mol. Neurosci. 3 2010 1 10.3389/neuro.02.001.2010
13. A. Czurkó, H. Hirase, J. Csicsvari, and G. Buzsáki Sustained activation of hippocampal pyramidal cells by 'space clamping' in a running wheel Eur. J. Neurosci. 11 1999 344 352 10.1046/j.1460-9568.1999.00446.x
14. E.A. Del Bel, F.S. Guimarães, M. Bermúdez-Echeverry, M.Z. Gomes, A. Schiaveto-de-Souza, F.E. Padovan-Neto, V. Tumas, A.P. Barion-Cavalcanti, M. Lazzarini, L.P. Nucci-da-Silva, and D. de Paula-Souza Role of nitric oxide on motor behavior Cell. Mol. Neurobiol. 25 2005 371 392 10.1007/s10571-005-3065-8
15. C. Dessy, O. Feron, and J.L. Balligand The regulation of endothelial nitric oxide synthase by caveolin: a paradigm validated in vivo and shared by the 'endothelium-derived hyperpolarizing factor Pflugers Arch. 459 2010 817 827 10.1007/s00424-010-0815-3
16. P. Dobrzyn, A. Pyrkowska, M.K. Duda, T. Bednarski, M. Maczewski, J. Langfort, and A. Dobrzyn Expression of lipogenic genes is upregulated in the heart with exercise training-induced but not pressure overload-induced left ventricular hypertrophy Am. J. Physiol. Endocrinol. Metab. 304 2013 E1348 E1358 10.1152/ajpendo.00603.2012
17. M. Endres, K. Gertz, U. Lindauer, J. Katchanov, J. Schultze, H. Schrock, G. Nickenig, W. Kuschinsky, U. Dirnagl, and U. Laufs Mechanisms of stroke protection by physical activity Ann. Neurol. 54 2003 582 590 10.1002/ana.10722
18. A. Ghosh, J. Carnahan, and M.E. Greenberg Requirement for BDNF in activity-dependent survival of cortical neurons Science 263 1994 1618 1623 10.1126/science.7907431
19. B.J. Gibb, and J Garthwaite Subunits of the nitric oxide receptor, soluble guanylyl cyclase, expressed in rat brain Eur. J. Neurosci. 13 2001 539 544 10.1046/j.1460-9568.2001.01421.x
20. B.J. Gibb, V. Wykes, and J. Garthwaite Properties of NO-activated guanylyl cyclases expressed in cells Br. J. Pharmacol. 139 2003 1032 1040 10.1038/sj.bjp.0705318
21. M. Goekint, I. Bos, E. Heyan, R. Meeusen, Y. Michotte, and S. Sarre Acute running stimulates hippocampal dopaminergic neurotransmission in rats, but has no influence on brain-derived neurotrophic factor J. Appl. Physiol. 112 2012 535 541 10.1152/japplphysiol.00306.2011
22. S. Grillner Ion channels and locomotion Science 278 1997 1087 1088 10.1126/science.278.5340.1087
23. G. Gupta, M. Azam, L. Yang, and M.S. Danziger The β2 subunit inhibits stimulation of the α1/β1form of soluble guanylyl cyclase by nitric oxide. Potential relevance to regulation of blood pressure J. Clin. Invest. 100 1997 1488 1492 10.1172/JCI119670
24. M.M. Holmes, L.A. Galea, R.E. Mistlberger, and G. Kempermann Adult hippocampal neurogenesis and voluntary running activity: circadian and dose-dependent effects J. Neurosci. Res. 76 2004 216 222 10.1002/jnr.20039
25. Y. Itzhak, S.F. Ali, J.L. Martin, M.D. Black, and P.L. Huang Resistance of neuronal nitric oxide synthase-deficient mice to cocaine-induced locomotor sensitization Psychopharmacology (Berl) 140 1998 378 386 10.1007/s002130050779
26. K. Jahn, A. Deutschländer, T. Stephan, M. Wiesmann, and T. Brandt Brain activation patterns during imagined stance and locomotion in functional magnetic resonance imaging NeuroImage 22 2004 722 1731 10.1016/j.neuroimage.2004.05.017
27. K. Jahn, A. Deutschländer, T. Stephan, R. Kalla, M. Wiesmann, M. Strupp, and T. Brandt Imaging human supraspinal locomotor centers in brainstem and cerebellum NeuroImage 39 2008 786 792 10.1016/j.neuroimage.2007.09.047
28. L.M. Jordan, J. Liu, P.B. Hedlund, T. Akay, and K.G. Pearson Descending command system for the initiation of locomotion in mammals Brain Res. Rev. 57 2008 183 191 10.1016/j.brainresrev.2007.07.019
29. Z. Kazimierczuk, M. Chalimoniuk, A.E. Laudy, R. Moo-Puc, R. Cedillo-Rivera, B.J. Starosciak, and S.J. Chrapusta Synthesis and antimicrobial and nitric oxide synthase inhibitory activities of novel isothiourea derivatives Arch. Pharm. Res. 33 2010 821 830 10.1007/s12272-010-0604-8
30. H. Kim, Q. Li, B.L. Hempstead, and J.A. Madri Paracrine and autocrine functions of brain-derived neurotrophic factor (BDNF) and nerve growth factor (NGF) in brain-derived endothelial cells J. Biol. Chem. 279 2004 33538 33546 10.1074/jbc.M404115200
31. J.P. Kiss, and E.S. Vizi Nitric oxide: a novel link between synaptic and nonsynaptic transmission Trends Neurosci. 24 2001 211 215 10.1016/S0166-2236(00)01745-8
32. K. Knaepen, M. Goekint, EM. Heyman, and R. Meeusen Neuroplasticity - exercise-induced response of peripheral brain-derived neurotrophic factor: a systematic review of experimental studies in human subjects Sports Med. 40 2010 765 801 10.2165/11534530-000000000-00000
33. A.C. Lacerda, U. Marubayashi, C.H. Balthazar, and C.C. Coimbra Evidence that brain nitric oxide inhibition increases metabolic cost of exercise, reducing running performance in rats Neurosci. Lett. 393 2006 260 263 10.1016/j.neulet.2005.09.076
34. A.C. Lacerda, U. Marubayashi, C.H. Balthazar, L.H. Leite, and C.C. Coimbra Central nitric oxide inhibition modifies metabolic adjustments induced by exercise in rats Neurosci. Lett. 410 2006 152 156 10.1016/j.neulet.2006.09.067
35. J. Langfort, L. Budohoski, and E.A. Newsholme Effect of various types of acute exercise and exercise training on the insulin sensitivity of rat soleus muscle measured in vitro Pflugers Arch. 412 1988 101 105 10.1007/BF00583737
36. J. Langfort, D. Czarnowski, W. Pilis, B. Wojcik, and J. Gorski Effect of various types of exercise training on 5′-nucleotidase and adenosine deaminase activities in rat heart: influence of a single bout of endurance exercise Biochem. Mol. Med. 59 1996 28 32 10.1006/bmme.1996.0060
37. J. Langfort, E. Barańczuk, D. Pawlak, M. Chalimoniuk, N. Lukacova, J. Marsala, and J. Gorski The effect of endurance training on regional serotonin metabolism in the brain during early stage of detraining period in the female rat Cell. Mol. Neurobiol. 26 2006 1327 1342 10.1007/s10571-006-9065-5
38. W.D. Lust, G.K. Feussner, J.V. Passonneau, and D.W. McCandless Distribution of cyclic nucleotides in layers of the cerebellum after decapitation J. Cyclic Nucleotide Res. 7 1981 333 337
39. V.B. Matthews, M.B. Åström, M.H. Chan, C.R. Bruce, K.S. Krabbe, O. Prelovsek, T. Åckerström, C. Yfanti, C. Broholm, O.H. Mortensen, M. Penkowa, P. Hojman, A. Zankari, M.J. Watt, H. Bruunsgard, B.K. Pedersen, and M.A. Febbraio Brain-derived neurotrophic factor is produced by skeletal muscle cells in response to contraction and enhances fat oxidation via activation of AMP-activated protein kinase Diabetologia 52 2009 1409 1418 10.1007/s00125-009-1364-1
40. D.L. McLean, and K.T. Sillar Metamodulation of a spinal locomotor network by nitric oxide J. Neurosci. 24 2004 9561 9571 10.1523/JNEUROSCI.1817-04.2004
41. R. Meeusen, I. Smolders, S. Sarre, K. de Meirleir, H. Keizer, M. Serneels, G. Ebinger, and Y. Michotte Endurance training effects on neurotransmitter release in rat striatum: an in vivo microdialysis study Acta Physiol. Scand. 159 1997 335 341 10.1046/j.1365-201X.1997.00118.x
42. P.I. Nedvetsky, C. Kleinschnitz, and H.H. Schmidt Regional distribution of protein and activity of the nitric oxide receptor, soluble guanylyl cyclase, in rat brain suggests multiple mechanisms of regulation Brain Res. 950 2002 148 154 10.1016/S0006-8993(02)03015-9
43. E.A. Newsholme, and E. Blomstrand Tryptophan, 5-hydroxytryptamine and a possible explanation for central fatigue Adv. Exp. Med. Biol. 384 1995 315 320
44. M. Ono, Y. Itakura, T. Nonomura, T. Nakagawa, C. Nakayama, M. Taiji, and H. Noguchi Intermittent administration of brain-derived neurotrophic factor ameliorates glucose metabolism in obese diabetic mice Metabolism 49 2000 129 133 10.1016/S0026-0495(00)90988-0
45. W. Pan, W.A. Banks, M.B. Fasold, J. Bluth, and A.J. Ksatin Transport of brain-derived neurotrophic factor across the blood-brain barrier Neuropharmacology 37 1998 1553 1561 10.1016/S0028-3908(98)00141-5
46. S. Pastore, and D.A. Hood Endurance training ameliorates the metabolic and performance characteristics of circadian Clock mutant mice J. Appl. Physiol. 114 2013 1076 1084 10.1152/japplphysiol.01505.2012
47. B.K. Pedersen, and M.A. Febbraio Muscles, exercise and obesity: skeletal muscle as a secretory organ Nat. Rev. Endocrinol. 8 2012 457 465 10.1038/nrendo.2012.49
48. A.A. Petersen, K.E. Larsen, G.G. Behr, N. Romero, S. Przedborski, P. Brundin, and D. Sulzer Brain-derived neurotrophic factor inhibits apoptosis and dopamine-induced free radical production in striatal neurons but does not prevent cell death Brain Res. Bull. 56 2001 331 335 10.1016/S0361-9230(01)00580-9
49. A. Pietrelli, J.J. López-Costa, R. Goñi, E.M. López, A. Brusco, and N. Basso Effects of moderate and chronic exercise on the nitrergic system and behavioral parameters in rats Brain Res. 1389 2011 71 82 10.1016/j.brainres.2011.03.005
50. P. Pifarre, A. García, and G. Mengod Species differences in the localization of soluble guanylyl cyclase subunits in monkey and rat brain J. Comp. Neurol. 500 2007 942 957 10.1002/cne.21241
51. JF. Poduslo, and G.L. Curran Permeability at the blood-brain and blood-nerve barriers of the neurotrophic factors: NGF, CNTF, NT-3, BDNF Brain Res. Mol. Brain Res. 36 1996 280 286 10.1016/0169-328X(95)00250-V
52. P. Rasmussen, P. Brassard, H. Adser, MV. Pedersen, L. Leick, E. Hart, N.H. Secher, B.K. Pedersen, and H. Pilegaard Evidence for a release of brain-derived neurotrophic factor from the brain during exercise Exp. Physiol. 94 2009 1062 1069 10.1113/expphysiol.2009.048512
53. M. Russwurm, S. Behrends, C. Harteneck, and D. Koesling Functional properties of a naturally occurring isoform of soluble guanylyl cyclase Biochem. J. 335 1998 125 130
54. M. Russwurm, N. Wittau, and D. Koesling Guanylyl cyclase/PDS-95 interaction: targeting of the nitric oxide-sensitive α2β1 guanylyl cyclase to synaptic membranes J. Biol. Chem. 276 2001 44647 44652 10.1074/jbc.M105587200
55. E. Sadowska-Krępa, B. Kłapcińska, S. Jagsz, A. Sobczak, SJ. Chrapusta, M. Chalimoniuk, P. Grieb, S. Poprzęcki, and J. Langfort High-dose testosterone propionate treatment reverses the effects of endurance training on myocardial antioxidant defenses in adolescent male rats Cardiovasc. Toxicol. 11 2011 118 127 10.1007/s12012-011-9105-3
56. 2+ signals without involvement of de novo AP-1 synthesis Biochem. Biophys. Res. Commun. 229 1996 788 793 10.1006/bbrc.1996.1881
57. T.F. Seeger, B. Bartlett, T.M. Coskran, J.S. Culp, L.C. James, D.L. Krull, J. Lanfear, A.M. Ryan, C.J. Schmidt, C.A. Strick, A.H. Varghese, R.D. Williams, P.G. Wylie, and F.S. Menniti Immunohistochemical localization of PDE10A in the rat brain Brain Res. 985 2003 113 126 10.1016/S0006-8993(03)02754-9
58. J.A. Siuciak, S.A. McCarthy, D.S. Chapin, R.A. Fujiwara, L.C. James, R.D. Williams, J.L. Stock, J.D. McNeish, C.A. Strick, F.S. Menniti, and C.J. Schmidt Genetic deletion of the striatum-enriched phosphodiesterase PDE10A: evidence for altered striatal function Neuropharmacology 51 2006 374 385 10.1016/j.neuropharm.2006.01.012
59. M. Skup, A. Dwornik, M. Macias, D. Sulejczak, M. Wiater, and J. Czarkowska-Bauch 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. 176 2002 289 307 10.1006/exnr.2002.7943
60. J.C. Smith, and J.L. Feldman In vitro brainstem-spinal cord preparations for study of motor systems for mammalian respiration and locomotion J. Neurosci. Methods 21 1987 321 333 10.1016/0165-0270(87)90126-9
61. A.M. Teixeira, P. Reckziegel, L. Müller, R.P. Pereira, D.H. Roos, J.B. Rocha, and M.E. Bürger Intense exercise potentiates oxidative stress in striatum of reserpine-treated animals Pharmacol. Biochem. Behav. 92 2009 231 235 10.1016/j.pbb.2008.11.015
62. H. van Praag, G. Kempermann, and F.H. Gage Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus Nat. Neurosci. 2 1999 266 270 10.1038/6368
63. C. Villanueva, and C. Giulivi Subcellular and cellular locations of nitric oxide synthase isoforms as determinants of health and disease Free Radic. Biol. Med. 49 2010 307 316 10.1016/j.freeradbiomed.2010.04.004
64. X. Wang, and P.J. Robinson Cyclic GMP-dependent protein kinase and cellular signaling in the nervous system J. Neurochem. 68 1997 443 456 10.1046/j.1471-4159.1997.68020443.x
65. A.R. West, and M.P. Galloway Nitric oxide and potassium chloride-facilitated striatal dopamine efflux in vivo: role of calcium-dependent release mechanisms Neurochem. Int. 33 1998 493 501 10.1016/S0197-0186(98)00054-0
66. J. Widenfalk, L. Olson, and P. Thorén Deprived of habitual running, rats downregulate BDNF and TrkB messages in the brain Neurosci. Res. 34 1999 125 132 10.1016/S0168-0102(99)00051-6
67. H. Xiong, K. Yamada, D. Han, T. Nabeshima, G. Enikolopov, J. Carnahan, and H. Nawa Mutual regulation between the intercellular messengers nitric oxide and brain-derived neurotrophic factor in rodent neocortical neurons Eur. J. Neurosci. 11 1999 1567 1576 10.1046/j.1460-9568.1999.00567.x
68. R. Zarzeczny, W. Pilis, J. Langfort, H. Kaciuba-Us̈ciłko, and K. Nazar Influence of thyroid hormones on exercise tolerance and lactate threshold in rats J. Physiol. Pharmacol. 47 1996 503 513
69. L. Zhou, and D.Y. Zhu Neuronal nitric oxide synthase: structure, subcellular localization, regulation, and clinical implications Nitric Oxide 20 2009 223 230 10.1016/j.niox.2009.03.001