Fibroblast Growth Factor-2 Induced by Enriched Environment Enhances Angiogenesis and Motor Function in Chronic Hypoxic-Ischemic Brain Injury

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Seo, Jung Hwa ^a,b   Yu, Ji Hea ^a,b   Suh, Hwal ^a,b   Kim, Myung Sun ^a,c,d   Cho, Sung Rae ^a,b,d  

^a Yonsei University College of Medicine   (South Korea)

^b Yonsei University   (South Korea)

^c Hanyang University   (South Korea)

^d Yonsei Stem Cell Center   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN A; ALPHA SMOOTH MUSCLE ACTIN; CD31 ANTIGEN; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 2 ANTIBODY; NEUTRALIZING ANTIBODY; OXYGEN; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN DAMAGE; CELL DENSITY; CEREBELLUM; CHRONIC DISEASE; CONTROLLED STUDY; CORPUS STRIATUM; FORELIMB; FRONTAL CORTEX; GRIP STRENGTH; HIPPOCAMPUS; HYPOXIC ISCHEMIC ENCEPHALOPATHY; MOTOR PERFORMANCE; MOUSE; NEUROPSYCHOLOGY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; ROTAROD TEST; UPREGULATION; WALKING;

ACTINS; ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS, CD31; BLOTTING, WESTERN; DNA PRIMERS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FIBROBLAST GROWTH FACTOR 2; HOUSING, ANIMAL; HYPOXIA-ISCHEMIA, BRAIN; IMMUNOHISTOCHEMISTRY; MICE; MUSCLE STRENGTH; NEOVASCULARIZATION, PHYSIOLOGIC; REAL-TIME POLYMERASE CHAIN REACTION; ROTAROD PERFORMANCE TEST;

EID: 84884746880     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074405     Document Type: Article

References (48)

1. Vannucci RC, Connor JR, Mauger DT, Palmer C, Smith MB, et al. (1999) Rat model of perinatal hypoxic-ischemic brain damage. J Neurosci Res 55: 158-163.
2. Yager JY, (2004) Animal models of hypoxic-ischemic brain damage in the newborn. Semin Pediatr Neurol 11: 31-46.
3. Komitova M, Mattsson B, Johansson BB, Eriksson PS, (2005) Enriched environment increases neural stem/progenitor cell proliferation and neurogenesis in the subventricular zone of stroke-lesioned adult rats. Stroke 36: 1278-1282.
4. Gobbo OL, O'Mara SM, (2004) Impact of enriched-environment housing on brain-derived neurotrophic factor and on cognitive performance after a transient global ischemia. Behav Brain Res 152: 231-241.
5. Skalak TC, Price RJ, Zeller PJ, (1998) Where do new arterioles come from? Mechanical forces and microvessel adaptation. Microcirculation 5: 91-94.
6. Brown MD, Hudlicka O, (2003) Modulation of physiological angiogenesis in skeletal muscle by mechanical forces: involvement of VEGF and metalloproteinases. Angiogenesis 6: 1-14.
7. Bengoetxea H, Argandona EG, Lafuente JV, (2008) Effects of visual experience on vascular endothelial growth factor expression during the postnatal development of the rat visual cortex. Cereb Cortex 18: 1630-1639.
8. Franklin TB, Murphy JA, Myers TL, Clarke DB, Currie RW, (2006) Enriched environment during adolescence changes brain-derived neurotrophic factor and TrkB levels in the rat visual system but does not offer neuroprotection to retinal ganglion cells following axotomy. Brain Res 1095: 1-11.
9. Ickes BR, Pham TM, Sanders LA, Albeck DS, Mohammed AH, et al. (2000) Long-term environmental enrichment leads to regional increases in neurotrophin levels in rat brain. Exp Neurol 164: 45-52.
10. Folkman J, Klagsbrun M, (1987) Angiogenic factors. Science 235: 442-447.
11. Gomez-Pinilla F, Dao L, So V, (1997) Physical exercise induces FGF-2 and its mRNA in the hippocampus. Brain Res 764: 1-8.
12. Im SH, Yu JH, Park ES, Lee JE, Kim HO, et al. (2010) Induction of striatal neurogenesis enhances functional recovery in an adult animal model of neonatal hypoxic-ischemic brain injury. Neuroscience 169: 259-268.
13. Ekstrand J, Hellsten J, Tingström A, (2008) Environmental enrichment, exercise and corticosterone affect endothelial cell proliferation in adult rat hippocampus and prefrontal cortex. Neurosci Lett 442: 203-207.
14. Cho SH, Yao Z, Wang SW, Alban RF, Barbers RG, et al. (2003) Regulation of Activin A Expression in Mast Cells and Asthma: Its Effect on the Proliferation of Human Airway Smooth Muscle Cells. J Immunol 170: 4045-4052.
15. Tretter YP, Hertel M, Munz B, ten Bruggencate G, Werner S, et al. (2000) Induction of activin A is essential for the neuroprotective action of basic fibroblast growth factor in vivo. Nat Med 6: 812-815.
16. Macko RF, Ivey FM, Forrester LW, Hanley D, Sorkin JD, et al. (2005) Treadmill exercise rehabilitation improves ambulatory function and cardiovascular fitness in patients with chronic stroke: a randomized, controlled trial. Stroke 36: 2206-2211.
17. Frazzitta G, Maestri R, Uccellini D, Bertotti G, Abelli P, (2009) Rehabilitation treatment of gait in patients with Parkinson's disease with freezing: a comparison between two physical therapy protocols using visual and auditory cues with or without treadmill training. Mov Disord 24: 1139-1143.
18. Risedal A, Mattsson B, Dahlqvist P, Nordborg C, Olsson T, et al. (2002) Environmental influences on functional outcome after a cortical infarct in the rat. Brain Res Bull 58: 315-321.
19. Pang TY, Stam NC, Nithianantharajah J, Howard ML, Hannan AJ, (2006) Differential effects of voluntary physical exercise on behavioral and brain-derived neurotrophic factor expression deficits in Huntington's disease transgenic mice. Neuroscience 141: 569-584.
20. Wolf SA, Kronenberg G, Lehmann K, Blankenship A, Overall R, et al. (2006) Cognitive and physical activity differently modulate disease progression in the amyloid precursor protein (APP)-23 model of Alzheimer's disease. Biol Psychiatry 60: 1314-1323.
21. Kempermann G, Kuhn HG, Gage FH, (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386: 493-495.
22. Nilsson M, Perfilieva E, Johansson U, Orwar O, Eriksson PS, (1999) Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. J Neurobiol 39: 569-578.
23. Soffie M, Hahn K, Terao E, Eclancher F, (1999) Behavioural and glial changes in old rats following environmental enrichment. Behav Brain Res 101: 37-49.
24. Rampon C, Tang YP, Goodhouse J, Shimizu E, Kyin M, et al. (2000) Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice. Nat Neurosci 3: 238-244.
25. Torasdotter M, Metsis M, Henriksson BG, Winblad B, Mohammed AH, (1998) Environmental enrichment results in higher levels of nerve growth factor mRNA in the rat visual cortex and hippocampus. Behav Brain Res 93: 83-90.
26. Mora F, Segovia G, del Arco A, (2007) Aging, plasticity and environmental enrichment: structural changes and neurotransmitter dynamics in several areas of the brain. Brain Res Rev 55: 78-88.
27. Carro E, Nunez A, Busiguina S, Torres-Aleman I, (2000) Circulating insulin-like growth factor I mediates effects of exercise on the brain. J Neurosci 20: 2926-2933.
28. Gomez-Pinilla F, So V, Kesslak JP, (1998) Spatial learning and physical activity contribute to the induction of fibroblast growth factor: neural substrates for increased cognition associated with exercise. Neuroscience 85: 53-61.
29. Endres M, Gertz K, Lindauer U, Katchanov J, Schultze J, et al. (2003) Mechanisms of stroke protection by physical activity. Ann Neurol 54: 582-590.
30. Schallert T, Leasure JL, Kolb B, (2000) Experience-associated structural events, subependymal cellular proliferative activity, and functional recovery after injury to the central nervous system. J Cereb Blood Flow Metab 20: 1513-1528.
31. Cohen AD, Tillerson JL, Smith AD, Schallert T, Zigmond MJ, (2003) Neuroprotective effects of prior limb use in 6-hydroxydopamine-treated rats: possible role of GDNF. J Neurochem 85: 299-305.
32. Bikfalvi A, Klein S, Pintucci G, Rifkin DB, (1997) Biological roles of fibroblast growth factor-2. Endocr Rev 18: 26-45.
33. Comeau WL, Hastings E, Kolb B, (2007) Pre- and postnatal FGF-2 both facilitate recovery and alter cortical morphology following early medial prefrontal cortical injury. Behav Brain Res 180: 18-27.
34. Monfils MH, Driscoll I, Kamitakahara H, Wilson B, Flynn C, et al. (2006) FGF-2-induced cell proliferation stimulates anatomical, neurophysiological and functional recovery from neonatal motor cortex injury. Eur J Neurosci 24: 739-749.
35. Li Q, Stephenson D, (2002) Postischemic administration of basic fibroblast growth factor improves sensorimotor function and reduces infarct size following permanent focal cerebral ischemia in the rat. Exp Neurol 177: 531-537.
36. Rowntree S, Kolb B, (1997) Blockade of basic fibroblast growth factor retards recovery from motor cortex injury in rats. Eur J Neurosci 9: 2432-2441.
37. Reuss B, von Bohlen und Halbach O, (2003) Fibroblast growth factors and their receptors in the central nervous system. Cell Tissue Res 313: 139-157.
38. Kleim JA, Cooper NR, VandenBerg PM, (2002) Exercise induces angiogenesis but does not alter movement representations within rat motor cortex. Brain Res 934: 1-6.
39. Swain RA, Harris AB, Wiener EC, Dutka MV, Morris HD, et al. (2003) Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience 117: 1037-1046.
40. Ding Y, Li J, Lai Q, Rafols JA, Luan X, et al. (2004) Motor balance and coordination training enhances functional outcome in rat with transient middle cerebral artery occlusion. Neuroscience 123: 667-674.
41. Gertz K, Priller J, Kronenberg G, Fink KB, Winter B, et al. (2006) Physical activity improves long-term stroke outcome via endothelial nitric oxide synthase-dependent augmentation of neovascularization and cerebral blood flow. Circ Res 99: 1132-1140.
42. Krupinski J, Kaluza J, Kumar P, Kumar S, Wang JM, (1994) Role of angiogenesis in patients with cerebral ischemic stroke. Stroke 25: 1794-1798.
43. Wei L, Erinjeri JP, Rovainen CM, Woolsey TA, (2001) Collateral growth and angiogenesis around cortical stroke. Stroke 32: 2179-2184.
44. Heil M, Eitenmuller I, Schmitz-Rixen T, Schaper W, (2006) Arteriogenesis versus angiogenesis: Similarities and differences. J Cell Mol Med 10: 45-55.
45. Buschmann I, Schaper W, (1999) Arteriogenesis Versus Angiogenesis: Two Mechanisms of Vessel Growth. News Physiol Sci 14: 121-125.
46. Takakusaki K, Habaguchi T, Ohtinata-Sugimoto J, Saitoh K, Sakamoto T, (2003) Basal ganglia efferents to the brainstem centers controlling postural muscle tone and locomotion: a new concept for understanding motor disorders in basal ganglia dysfunction. Neuroscience 119: 293-308.
47. Alexander GE, Crutcher MD, (1990) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13: 266-271.
48. Mizutani K, Sonoda S, Karasawa N, Yamada K, Shimpo K, et al. (2012) Effects of exercise after focal cerebral cortex infarction on basal ganglion. Neurol Sci 34: 861-867.