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Acute normobaric hypoxia does not affect the simultaneous exercise-induced increase in circulating BDNF and GDNF in young healthy men: A feasibility study


Autoři: Zofia Piotrowicz aff001;  Małgorzata Chalimoniuk aff002;  Kamila Płoszczyca K aff003;  Miłosz Czuba aff003;  Józef Langfort aff001
Působiště autorů: Institute of Sport Sciences, The Jerzy Kukuczka Academy of Physical Education, Katowice, Poland aff001;  Department of Tourism and Health in Biała Podlaska, The Józef Piłsudski University of Physical Education, Warsaw, Poland aff002;  Department of Kinesiology, Institute of Sport, Warsaw, Poland aff003;  Department of Sports Theory, The Jerzy Kukuczka Academy of Physical Education, Katowice, Poland aff004
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0224207

Souhrn

Physical exercise has a neuromodulatory effect on the central nervous system (CNS) partially by modifying expression of neuropeptides produced and secreted by neurons and glial cells, among which the best examined are brain-derived neurotrophic factor (BDNF) and glial cell line-derived neurotrophic factor (GDNF). Because both neurotrophins can cross the brain-blood barrier (BBB), their blood levels indirectly reflect their production in the CNS. Moreover, both neuropeptides are involved in modulation of dopaminergic and serotoninergic system function. Because limited information is available on the effects of exercise to volition exhaustion and acute hypoxia on CNS, BDNF and GDNF formation, the aims of the present study were to verify whether 1) acute exercise to exhaustion in addition to neurons also activates glial cells and 2) additional exposure to acute normobaric moderate hypoxia affects their function. In this feasibility study we measured blood concentrations of BDNF, GDNF, and neuropeptides considered as biomarkers of brain damage (bFGF, NGF, S100B, GFAP) in seven sedentary healthy young men who performed a graded exercise test to volitional exhaustion on a cycle ergometer under normoxic (N) and hypoxic conditions: 2,000 m (H2; FiO2 = 16.6%) and 3,000 m altitude (H3; FiO2 = 14.7%). In all conditions serum concentrations of both BDNF and GDNF increased immediately after cessation of exercise (p<0.01). There was no effect of condition or interaction (condition x time of measurement) and exercise on any of the brain damage biomarkers: bFGF, NGF, S100B, GFAP. Moreover, in N (0<0.01) and H3 (p<0.05) exercise caused elevated serum 5-HT concentration. The results suggest that a graded effort to volitional exhaustion in normoxia, as well as hypoxia, simultaneously activates both neurons and astrocytes. Considering that s100B, GFAP, bFGF, and NGF (produced mainly by astrocytes) are markers of brain damage, it can be assumed that a maximum effort in both conditions is safe for the CNS.

Klíčová slova:

Astrocytes – Blood – Central nervous system – Exercise – Hypoxia – Medical hypoxia – Neurons – Serotonin


Zdroje

1. Voss MV, Vivar C, Kramer AF, van Praag H. Bridging animal and human models of exercise-induced brain plasticity. Trrends Cogn Sci. 2013; 17: 525–544.

2. Lin C, Wu CJ, Wei IH, Tsai MH, Chang NW, Yang TT, et al. Chronic treadmill running protects hippocampal neurons from hypobaric hypoxia-induced apoptosis in rats. Neuroscience. 2013; 231: 216–224. doi: 10.1016/j.neuroscience.2012.11.051 23219906

3. Verburgh L, Königs M, Scherder EJ, Oosterlaan J. Physical exercise and executive functions in preadolescent children, adolescents and young adults: a meta-analysis. Br J Sports Med. 2014; 48: 973–979. doi: 10.1136/bjsports-2012-091441 23467962

4. Heijnen S, Hommel B, Kibele A, Colzato LS. Neuromodulation of aerobic exercise-A review. Front Psychol. 2016; 6: 1890. doi: 10.3389/fpsyg.2015.01890 26779053

5. Morland C, Andersson KA, Haugen ØP, Hadzic A, Kleppa L, Gille A, et al. Exercise induces cerebral VEGF and angiogenesis via the lactate receptor HCAR1. Nat Commun. 2017; 23: 8: 15557.

6. van Praag H. Exercise and the brain: something to chew on. Trends Neurosci. 2009; 32: 283–290. doi: 10.1016/j.tins.2008.12.007 19349082

7. Hohn A, Leibrock J, Bailey K, Barde YA. Identification and characterization of a novel member of the nerve growth factor/brain-derived neurotrophic factor family. Nature. 1990; 344: 339–341. doi: 10.1038/344339a0 2314473

8. Binder DK, Scharfman HE. Brain-derived neurotrophic factor. Growth Factors. 2004; 22: 123–131. doi: 10.1080/08977190410001723308 15518235

9. Popova NK, Iichibaeva TV, Naumenko VS. Neurotrophic factors (BDNF and GDNF) and serotonergic system of the brain. Biochemistry (Moscow). 2017; 82: 308–317.

10. Żołądź JA, Pilc A. The effect of physical activity on the brain derived neurotrophic factor: from animal to human studies. J Physiol Pharmacol. 2010; 61: 533–541. 21081796

11. Dinoff A, Herrmann N, Swardfager W, Lanctot KL. The effect of acute exercise on blood concentrations of brain-derived neurotrophic factor in healthy adults: a meta-analysis. Eur J Neurosci. 2017; 46: 1635–1646. doi: 10.1111/ejn.13603 28493624

12. Żołądź JA, Pilc A, Majerczak J, Grandys M, Zapart-Bukowska J, Duda K. Endurance training increases plasma brain-derived neurotrophic factor concentration in young healthy men. J Physiol Pharmacol. 2008; 59: 119–132. 19258661

13. Cho HC, Kim J, Kim S, Son YH, Lee N, Jung SH. The concentrations of serum, plasma and platelet BDNF are all increased by treadmill VO2max performance in healthy college men. Neurosci Lett. 2012; 519: 78–83. doi: 10.1016/j.neulet.2012.05.025 22617010

14. Knaepen K, Goekint M, Heyman EM, Meeusen R. Neuroplasticity-exercise-induced response of peripheral brain-derived neurotrophic factor. A systematic review of experimental studies in human subjects. Sports Med. 2010; 40: 766–801.

15. Pan W, Banks WA, Fasold MB, Bluth J, Kastin AJ. Transport of brain-derived neurotrophic factor across the blood-brain barrier. Neuropharmacology. 1998; 37: 1553–1561. doi: 10.1016/s0028-3908(98)00141-5 9886678

16. McCullough MJ, Gyorkos AM, Spitsbergen JM. Short-term exercise increases GDNF protein levels in the spinal cord of young and old rats. Neuroscience. 2013; 240: 258–268. doi: 10.1016/j.neuroscience.2013.02.063 23500094

17. Lin F, Doherty DH, Lile JD, Bektesh S, Collins F. GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science. 1993; 260: 1130–1132. doi: 10.1126/science.8493557 8493557

18. Salvatore MF, Zhang JL, Large DM, Wilson PE, Gash CR, Thomas TC, et al. Striatal GDNF administration increases tyrosine hydroxylase phosphorylation in the rat striatum and substantia nigra. J Neurochem. 2004; 90: 245–54. doi: 10.1111/j.1471-4159.2004.02496.x 15198683

19. DiStefano PS, Friedman B, Radziejewski C, Alexander C, Boland P, Schick CM, et al. The neurotrophins BDNF, NT-3, and NGF display distinct patterns of retrograde axonal transport in peripheral and central neurons. Neuron. 1992; 8: 983–993. doi: 10.1016/0896-6273(92)90213-w 1375039

20. Liu P, Nusslock R. Exercise-Mediated Neurogenesis in the Hippocampus via BDNF. Front Neurosci. 2018; 12: 52. doi: 10.3389/fnins.2018.00052 29467613

21. Yang H, An JJ, Sun C, Xu B. Regulation of Energy Balance via BDNF Expressed in Non paraventricular Hypothalamic. Neurons Mol Endocrinol. 2016; 30: 494–503. doi: 10.1210/me.2015-1329 27003443

22. Cotman CW, Berchtold NC, Christie LA. Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci. 2007; 30: 464–472. doi: 10.1016/j.tins.2007.06.011 17765329

23. Wrann CD, White JP, Salogiannnis J, Laznik-Bogoslavski D, Wu J, Ma D, et al. Exercise induces hippocampal BDNF through a PGC-1α/FNDC5 pathway. Cell Metab. 2013; 18: 649–59. doi: 10.1016/j.cmet.2013.09.008 24120943

24. Gomez-Pinilla F, Hillman Ch. The influence of exercise on cognitive abilities. Comp Physiol. 2013; 3: 403–442.

25. DaSilva PG, Domingues DD, de Carvalho LA, Allodi S, Correa CL. Neurotrophic factors in Parkinson's disease are regulated by exercise: Evidence-based practice. J Neurol Sci. 2016; 363: 5–15. doi: 10.1016/j.jns.2016.02.017 27000212

26. Małczyńska P, Piotrowicz Z, Drabarek D, Langfort J, Chalimoniuk M. The role of the brain-derived neurotrophic factor (BDNF) in neurodegenerative processes and in the neuroregeneration mechanisms induced by increased physical activity. Postepy Biochem. 2019; 65: 2–8. 30901514

27. Gibson GE, Duffy TE. Impaired synthesis of acetylcholine by mild hypoxic hypoxia or nitrous oxide. J Neurochem. 1981; 36: 28–33. doi: 10.1111/j.1471-4159.1981.tb02373.x 7463052

28. Meder D, Herz DM, Rowe JB, Lehericy S, Siebner HR. The role of dopamine in the brain—lessons learned from Parkinson's disease. Neuroimage. 2019; 190: 79–93. doi: 10.1016/j.neuroimage.2018.11.021 30465864

29. Cordeiro LMS, Rabelo PCR, Moraes MM, Teixeira-Coelho F, Coimbra CC, Wanner SP, et al. Physical exercise-induced fatigue: the role of serotonergic and dopaminergic systems. Braz J Med Biol Res. 2017; 50: e6432. doi: 10.1590/1414-431X20176432 29069229

30. Foley TE, Fleshner M. Neuroplasticity of dopamine circuits after exercise: implications for central fatigue. Neuromol Med. 2008; 10: 67–80.

31. Newsholme EA, Acworth IN, Blomstrand E. Amino acids, brain neurotransmitters and a functional link between muscle brain that is important in sustained exercise. In: Benzi G (Ed), Advances in Biochemistry. John LibbyEurotex; 1987. Pp. 21–28.

32. Illes P, Verkhratsky A, Burnstock G, Franke H. P2X receptors and their roles in astroglia in the central and peripheral nervous system. Neuroscientist. 2012; 18: 422–38. doi: 10.1177/1073858411418524 22013151

33. Ma Z, Stork T, Bergles DE, Freeman MR. Neuromodulators signal through astrocytes to alter neural circuit activity and behaviour. Nature. 2016; 538: 428–432.

34. Freitas-Andrade M, Naus CC. Astrocytes in neuroprotection and neurodegeneration: The role of connexin43 and pannexin1. Neuroscience. 2016; 323: 207–221. doi: 10.1016/j.neuroscience.2015.04.035 25913636

35. Dreingen R, Gebhardt R, Hamprecht B. Glycogen in astrocytes: Possible function as lactate supply for neighboring cells. Brain Res. 1993; 623: 208–214. doi: 10.1016/0006-8993(93)91429-v 8221102

36. Suh SW, Bergher JP, Anderson CM, Treadway JL, Fosgerau K, Swanson RA. Astrocyte glycogen sustains neuronal activity during hypoglycemia: studies with the glycogen phosphorylase inhibitor CP-316,819([R-R*,S*]-5-chloro-N-[2-hydroxy-3-(methoxymethylamino)-3-oxo-1-(phenylmethyl) propyl]-1 h-indole-2-carboxamide). J Pharmacol Exp Ther. 2007; 321: 45–50. doi: 10.1124/jpet.106.115550 17251391

37. Wender R, Brown AM, Fern R, Swanson RA, Farrell K, Ransom BR. Astrocytic glycogen influences axon function and survival during glucose deprivation in central white matter. J Neurosci. 2000; 20: 6804–6810. doi: 10.1523/JNEUROSCI.20-18-06804.2000 10995824

38. Chen Y, Swanson RA. Astrocytes and brain injury. J Cereb Blood Fow Metab. 2003; 23: 137–149.

39. Nedergaard M, Dirnagl U. Role of glial cells in cerebral ischemia. Glia. 2005, 50(4):281–286. doi: 10.1002/glia.20205 15846807

40. Abbott NJ, Rönnbäck L, Hansson E. Astrocyte–endothelial interactions at the blood–brain barrier. Nat Rev Neurosci. 2006; 7: 41–53. doi: 10.1038/nrn1824 16371949

41. Kirkley KS, Popichak KA, Afzali MF, Legare ME, Tjalkens RB. Microglia amplify inflammatory activation of astrocytes in manganese neurotoxicity. J Neuroinflammation. 2017; 14: 99. doi: 10.1186/s12974-017-0871-0 28476157

42. Kusy K, Zieliński J. Sprinters versus long-distance runners: how to grow old healthy. Exerc Sport Sci Rev. 2015; 43: 57–64. doi: 10.1249/JES.0000000000000033 25390294

43. Rupp T, Perrey S. Prefrontal cortex oxygenation and neuromuscular responses to exhaustive exercise. Eur J Appl Physiol. 2008; 102: 153–63. doi: 10.1007/s00421-007-0568-7 17882449

44. Dillon GH, Waldrop TG. In vitro responses of caudal hypothalamic neurons to hypoxia and hypercapnia. Neuroscience. 1992; 51: 941–950. doi: 10.1016/0306-4522(92)90531-6 1336828

45. Cohen PJ, Alexander SC, Smith TC, Reivich M, Wollman H. Effects of hypoxia and normocarbia on cerebral blood flow and metabolism in conscious man. J Appl Physiol. 1967; 23: 183–189. doi: 10.1152/jappl.1967.23.2.183 6031186

46. Amann M, Kayser B. Nervous system function during exercise in hypoxia. High Alt Med Biol. 2009; 10: 149–164. doi: 10.1089/ham.2008.1105 19555297

47. Terraneo L, Samaja M. Comparative response of brain to chronic hypoxia and hyperoxia. Int J Mol Sci. 2017; 18: 1914

48. Navarrete-Opazo A, Mitchell GS. Therapeutic potential of intermittent hypoxia: a matter of dose. Am J Physiol Regul Integr Comp Physiol. 2014; 307: R1181–R1197. doi: 10.1152/ajpregu.00208.2014 25231353

49. Wilson M, Newman S, Imray CH. The cerebral effects of ascent to high altitudes. Neurology. 2009; 8: 175–191. doi: 10.1016/S1474-4422(09)70014-6 19161909

50. Viscor G, Torrella JR, Corral L, Ricart A, Javierre C, Pages T, et al. Physiological and biological responses to short-term intermittent hypobaric hypoxia exposure: from sports and mountain medicine to new biomedical applications. Front Physiol. 2018; 9: 814. doi: 10.3389/fphys.2018.00814 30038574

51. Dewan NA, Nieto FJ, Somers VK. Intermittent hypoxemia and OSA: implications for comorbidities. Chest. 2015; 147: 266–274. doi: 10.1378/chest.14-0500 25560865

52. Czuba M. Wilk R. Karpiński J, et al. Intermittent hypoxic training improves anaerobic performance in competitive swimmers when implemented into a direct competition mesocycle. PLoS One. 2017; 12: e0180380. doi: 10.1371/journal.pone.0180380 28763443

53. Millet GP, Roels B, Schmitt L, Woorons X, Richalet JP. Combining hypoxic methods for peak performance. Sports Med. 2010; 40: 1–25. doi: 10.2165/11317920-000000000-00000 20020784

54. Czuba M, Bril G, Płoszczyca K, Piotrowicz Z, Chalimoniuk M, Roczniok R, et al. Intermittent hypoxic training at lactate threshold intensity improves aiming performance in well-trained biathletes with little change of cardiovascular variables. Biomed Res Int. 2019; 2019: 1287506

55. Czuba M, Zając A, Maszczyk A, Roczniok R, Poprzęcki S, Garbaciak W, et al. The effects of high intensity interval training in normobaric hypoxia on aerobic capacity in basketball players. J Hum Kinet. 2013; 39: 103–114. doi: 10.2478/hukin-2013-0073 24511346

56. Lieberman P, Protopapas A, Reed E, Youngs JW, Kanki BG. Cognitive defects at altitude. Nature. 1994; 372: 325. doi: 10.1038/372325a0 7969487

57. Amann M, Romer LM, Subudhi AW, Pegelow DF, Dempsey JA. Severity of arterial hypoxaemia affects the relative contributions of peripheral muscle fatigue to exercise performance in healthy humans. J Physiol. 2007; 581: 389–403. doi: 10.1113/jphysiol.2007.129700 17317739

58. Kuipers H, Verstappen FTJ, Keizer HA, Guerten P, van Kranenburg G. Variability of aerobic performance in the laboratory and its physiological correlates. Int J Sports Med. 1985; 6: 197–201. doi: 10.1055/s-2008-1025839 4044103

59. Edvardsen E, Hem E, Anderssen SA. End criteria for reaching maximal oxygen uptake must be strict and adjusted to sex and age: a cross-sectional study. PLoS One. 2014; 9: e85276. doi: 10.1371/journal.pone.0085276 24454832

60. Cohen J. Statistical Power Analysis for the Behavioral Sciences (2nd ed.). Hillsdale, NJ: L. Erlbaum Associates; 1988.

61. Karege F, Schwald M, Cisse M. Postnatal developmental profile of brain-derived neurotrophic factor in rat brain and platelets. Neurosci Lett. 2002; 328: 261–264. doi: 10.1016/s0304-3940(02)00529-3 12147321

62. Rasmussen P, Brassard P, Adser H, Pedersen MV, Leick L, Hart E, et al. Evidence for a release of brain-derived neurotrophic factor from the brain during exercise. Exp Physiol. 2009; 94: 1062–1069. doi: 10.1113/expphysiol.2009.048512 19666694

63. Hawley JA, Hargreaves M, Joyner MJ, Zierath JR. Integrative biology of exercise. Cell 2014; 159: 738–749. doi: 10.1016/j.cell.2014.10.029 25417152

64. Pedersen BK, Febbraio MA. Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Phys Rev. 2008; 88: 1379–1406.

65. Schmolesky MT, Webb DL, Hansen RA. The effects of aerobic exercise intensity and duration on levels of brain-derived neurotrophic factor in healthy men. J Sports Sci Med. 2013; 12: 502–511. 24149158

66. Marston KJ, Newton MJ, Brown BM, Rainey-Smith SR, Bird S, Martins RN et al. Intense resistance exercise increases peripheral brain-derived neurotrophic factor. Sci Med Sport. 2017; 20: 899–903.

67. Roach RC, Maes D, Sandoval RA, Robergs M, Icenogle M, Hinghofer-Szalkay H, et al. Exercise exacerbates acute mountain sickness at simulated high altitude. J Appl Physiol. 2000; 88: 581–585. doi: 10.1152/jappl.2000.88.2.581 10658026

68. Becke A, Müller P, Dordevic M, Lessmann V, Brigadski T, Müller NG. Daily Intermittent Normobaric Hypoxia Over 2 Weeks Reduces BDNF Plasma Levels in Young Adults—A Randomized Controlled Feasibility Study. Front Physiol. 2018; 9: 1337. doi: 10.3389/fphys.2018.01337 30327610

69. Hubold C, Lang UE, Gehring H, Schultes B, Schweiger U, Peters A, et al. Increased serum brain-derived neurotrophic factor protein upon hypoxia in healthy young men. J Neural Transm (Vienna). 2009; 116: 1221–1225.

70. Gao YX, Li P, Jiang CH, Liu C, Chen Y, Chen L, et al. Psychological and cognitive impairment of long-term migrators to high altitudes and the relationship to physiological and biochemical changes. Eur J Neurol. 2015; 22: 1363–1369. doi: 10.1111/ene.12507 25040466

71. Hartman W, Helan M, Smelter D, Sathish V, Thompson M, Pabelick CM, et al. Role of hypoxia-induced brain derived neurotrophic factor in human pulmonary artery smooth muscle. PLoS One. 2015; 10: e0129489. doi: 10.1371/journal.pone.0129489 26192455

72. Schega L, Peter B, Brigadski T, Leßmann V, Isermann B, Hamacher D, et al. Effect of intermittent normobaric hypoxia on aerobic capacity and cognitive function in older people. J Sci Med Sport. 2016; 19: 941–945. doi: 10.1016/j.jsams.2016.02.012 27134133

73. Zhu L, Wu L, Yew DT, Fan M. Effects of hypoxia on the proliferation and differentiation of NSCs. Mol Neurobiol. 2005; 31: 231–242. doi: 10.1385/MN:31:1-3:231 15953824

74. Calbet JA, Boushel R, Radegran G, Sondergaard H, Wagner PD, Saltin B. Determinants of maximal oxygen uptake insevere acute hypoxia. Am J Physiol. 2002; 284: 291–303.

75. Płoszczyca K, Langfort J, Czuba M. The effects of altitude training on erythropoietic response and hematological variables in adult athletes: A narrative review. Front Physiol. 2018; 9: 375. doi: 10.3389/fphys.2018.00375 29695978

76. Czuba M, Waśkiewicz Z, Zajac A, Poprzecki S, Cholewa J, Roczniok R. The effects of intermittent hypoxic training on aerobic capacity and endurance performance in cyclists. J Sport Sci Med. 2011; 10: 175–183.

77. Czuba M, Fidos-Czuba O, Płoszczyca K, Zając A, Langfort J. Comparison of the effect of intermittent hypoxic training vs. the live high, train low strategy on aerobic capacity and sports performance in cyclists in normoxia. Biol Sport. 2018; 35: 39–48. doi: 10.5114/biolsport.2018.70750 30237660

78. Connett RJ, Honig CR, Gayeski TE, Brooks GA. Defining hypoxia: a systems view of VO2, glycolysis, energetics, and intracellular PO2. J Appl Physiol. 1990; 68: 833–842. doi: 10.1152/jappl.1990.68.3.833 2187852

79. Hughson RL, Green HJ, Sharratt MT. Gas exchange, blood lactate and plasma catecholamines during incremental exercise in hypoxia and normoxia. J Appl Physiol. 1995; 79: 1134–1141. doi: 10.1152/jappl.1995.79.4.1134 8567554

80. Pedersen BK, Febraio MA. Muscle exercise and obesity: skeletal muscle as a secretory organ. Nat Rev Endocrinol. 2012; 8: 457–465. doi: 10.1038/nrendo.2012.49 22473333

81. Van den Berghe G, Bontemps F, Vincent MF, Van den Bergh F. The purine nucleotide cycle and its molecular defects. Prog Neurobiol. 1992; 39: 547–561. 1529104

82. Chalimoniuk M, Wronski Z, Gilewski K, Stolecka A, Langfort J. Does exercise training affect NO/GC/cGMP pathway in the brain? J Hum Kinet. 2005; 13: 27–40.

83. Norenberg MD, Rama Rao KV, Jayakumar AR. Signaling factors in the mechanism of ammonia neurotoxicity. Metab Brain Dis. 2009; 24: 103–117. doi: 10.1007/s11011-008-9113-6 19104923

84. Cudalbu C. In vivo studies of brain metabolism in animal models of hepatic encephalopathy using 1 h magnetic resonance spectroscopy. Metab Brain Dis. 2013; 28: 167–174. doi: 10.1007/s11011-012-9368-9 23254563

85. Pan W, Kastin AJ. Adipokines and the brain barrier: Peptides. 2007; 28: 1317–1330. doi: 10.1016/j.peptides.2007.04.023 17540480

86. Steensberg A, Febbraio MA, Osada T, Schjerling P, Van Hall G, Saltin B, et al. Interleukin-6 production in contracting human skeletal muscles is influenced by pre-exercise muscle glycogen content. J Physiol. 2001; 537: 633–639. doi: 10.1111/j.1469-7793.2001.00633.x 11731593

87. Steensberg A, Keller C, Starkie RL, Osada T, Febbraio MA, Pedersen BK. IL-6 and TNF-alpha expression in, and release from, contracting human skeletal muscle. Am J Physiol Endocrinol Metab. 2002; 283: E1272–E1278. doi: 10.1152/ajpendo.00255.2002 12388119

88. Van Wagoner NJ, Benveniste EN. Interleukin-6 expression and regulation in astrocytes. J Neurol. 1999; 100: 124–139.

89. Nybo L, Nielsen B, Pedersen BK, Moller K, Secher NH. Interleukin-6 release from the human brain during prolonged exercise. J Physiol. 2002; 542: 991–995. doi: 10.1113/jphysiol.2002.022285 12154196

90. Sopova K, Gatsiou K, Stellos K, Laske C. Dysregulation of neurotrophic and haematopoietic growth factors in Alzheimer's disease: from pathophysiology to novel treatment strategies. Curr Alzheimer Res. 2014; 11: 27–39. 24251394

91. Hui YP, Han LN, Li LB, Sun YN, Liu J, Qiao HF, et al. Anxiolytic effects of prelimbic 5-HT1A receptor activation in the hemiparkinsonian rat. Behav Brain Res. 2015; 277: 211–220. doi: 10.1016/j.bbr.2014.04.053 24906197

92. Sutoo D, Akiyama K. Regulation of brain function by exercise. Neurobiol Dis. 2003; 13: 1–14. 12758062

93. Zieliński J, Kusy K, Słoińska E. Alterations in purine metabolism in middle-aged elite, amateur, and recreational runners across a 1-year training cycle. Eur J Appl Physiol. 2013; 113: 763–773. doi: 10.1007/s00421-012-2488-4 22965897

94. Langfort J, Barańczuk E, Pawlak D, Chalimoniuk M, Lukacova N, Marsala J, et al. 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. 2006; 26: 1327–1342. doi: 10.1007/s10571-006-9065-5 16897368

95. Mir IN, Chalak LF. Serum biomarkers to evaluate the integrity of the neurovascular unit. Early Hum Dev. 2014; 90: 707–711. doi: 10.1016/j.earlhumdev.2014.06.010 25064445

96. Abe K, Saito H. Effects of basic fibroblast growth factor on central nervous system functions. Pharmacol Res 2001; 43: 307–312. doi: 10.1006/phrs.2000.0794 11352534

97. Ishitsuka K, Ago T, Arimura K, Nakamura K, Tokami H, Makihara N, et al. Neurotrophin production in brain pericytes during hypoxia: a role of pericytes for neuroprotection. Microvasc Res. 2012; 83: 352–359. doi: 10.1016/j.mvr.2012.02.009 22387236

98. Vos PE, Jacobs B, Andriessen TMJC, Lamners KJB, Borm GF, Beems T, et al. GFAP and S100B are biomarkers of traumatic brain injury. Neurology. 2010; 75: 1786–1793. doi: 10.1212/WNL.0b013e3181fd62d2 21079180

99. Winter CD, Whyte TR, Cardinal J, Rose SE, O'Rourke PK, Kenny RG. Elevated plasma S100B levels in high altitude hypobaric hypoxia do not correlate with acute mountain sickness. Neurol Res. 2014; 36: 779–785. doi: 10.1179/1743132814Y.0000000337 24620985

100. Jensen L, Bangsbo J, Hellsten Y. Effect of high intensity training on capillarization and presence of angiogenic factors in human skeletal muscle. J Physiol. 2004; 557: 571–582. doi: 10.1113/jphysiol.2003.057711 15020701

101. Yardan T, Erenler AK, Baydin A, Aydin K, Cokluk C. Usefulness of S100B protein in neurological disorders. J Pak Med Assoc. 2011; 61: 276–281. 21465945

102. Middeldorp J, Hol EM. GFAP in health and disease. Prog Neurobiol. 2011; 93: 421–43. doi: 10.1016/j.pneurobio.2011.01.005 21219963

103. Van Eldik LJ, Wainwright MS. The Janus face of glial-derived S100B: beneficial and detrimental functions in the brain. Restor Neurol Neurosci. 2003; 21: 97–108. 14530573

104. Koh SX, Lee KW. S100B as a marker for brain damage and blood–brain barrier disruption following exercise. Sports Med. 2014; 44: 369–385. doi: 10.1007/s40279-013-0119-9 24194479

105. Otto M, Holthusen S, Bahn E, Söhnchen N, Wiltfang J, Geese R, et al. Boxing and running lead to a rise in serum levels of S-100B protein. Int J Sports Med. 2000; 21: 551–555. doi: 10.1055/s-2000-8480 11156273

106. Hasselblatt M, Mooren FC, von Ahsen N, Keyvani K, Fromme A, Schwarze-Eicker K, et al. Serum S100beta increases in marathon runners reflect extracranial release rather than glial damage. Neurology. 2004; 62: 1634–1636. doi: 10.1212/01.wnl.0000123092.97047.b1 15136701

107. Eng LF, Ghirnikar RS, Lee YL. Glial fibrillary acidic protein: GFAP-thirty-one years (1969–2000). Neurochem Res. 2000; 25: 1439–1451. doi: 10.1023/a:1007677003387 11059815

108. Levi-Montalcini R, Skaper SD, Dal Toso R, Petrelli L, Leon A. Nerve growth factor: From neurotrophin to neurokine. Trends Neurosci. 1996; 19: 514–520. doi: 10.1016/S0166-2236(96)10058-8 8931279

109. Aloe L, Bracci-Laudiero L, Alleva E, Lambiase A, Micera A, Tirassa P. Emotional stress induced by parachute jumping enhances blood nerve growth factor levels and the distribution of nerve growth factor receptors in lymphocytes. Proc Natl Acad Sci. 1994; 91: 10440–10444.97. doi: 10.1073/pnas.91.22.10440 7937971

110. Bogetti ME, Pozo Devoto VM, Rapacioli M, Flores V, Fiszer de Plazas S. NGF, TrkA-P and neuroprotection after a hypoxic event in the developing central nervous system. Int J Dev Neurosci. 2018; 71: 111–121 doi: 10.1016/j.ijdevneu.2018.08.007 30165176


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