Phenotypic and gene expression modification with normal brain aging in GFAP-positive astrocytes and neural stem cells

Aging Cell

Volumn 10, Issue 3, 2011, Pages 466-482

  Bernal, Giovanna M ^a   Peterson, Daniel A ^a  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

Astrogliosis; FGF 2; Growth factors; Homeostasis; Neurogenesis; VEGF

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; GLIAL FIBRILLARY ACIDIC PROTEIN; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ADULT; AGED; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN FUNCTION; BRAIN REGION; CELL HETEROGENEITY; CELL STRUCTURE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HIPPOCAMPUS; HOMEOSTASIS; HUMAN; MITOSIS; MULTIPOTENT STEM CELL; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ADULT; AGING; ANIMALS; ASTROCYTES; CELL PROLIFERATION; FIBROBLAST GROWTH FACTOR 2; GENE EXPRESSION REGULATION; GENETIC VARIATION; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; HUMANS; IMMUNOHISTOCHEMISTRY; INTERMEDIATE FILAMENTS; NEURAL STEM CELLS; NEURONS; RATS; RATS, INBRED F344; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 79955951360     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2011.00694.x     Document Type: Article

References (91)

1. Alvarez-Buylla A, Lim DA (2004) For the long run: maintaining germinal niches in the adult brain. Neuron 41, 683-686.
2. Asahara T, Bauters C, Zheng LP, Takeshita S, Bunting S, Ferrara N, Symes JF, Isner JM (1995) Synergistic effect of vascular endothelial growth factor and basic fibroblast growth factor on angiogenesis in vivo. Circulation 92, II365-II371.
3. Ben Menachem-Zidon O, Avital A, Ben-Menahem Y, Goshen I, Kreisel T, Shmueli EM, Segal M, Ben Hur T, Yirmiya R (2010) Astrocytes support hippocampal-dependent memory and long-term potentiation via interleukin-1 signaling. Brain Behav. Immun. Epub ahead of print.
4. von Bernhardi RTJ, Eugenín J (2010) Aging-dependent changes of microglial cells and their relevance for neurodegenerative disorders. J. Neurochem. 112, 1099-1114.
5. Cansino S (2009) Episodic memory decay along the adult lifespan: a review of behavioral and neurophysiological evidence. Int. J. Psychophysiol. 71, 64-69.
6. Cevenini E, Caruso C, Candore G, Capri M, Nuzzo D, Duro G, Rizzo C, Colonna-Romano G, Lio D, Di Carlo D, Palmas MG, Scurti M, Pini E, Franceschi C, Vasto S (2010) Age-related inflammation: the contribution of different organs, tissues and systems. How to face it for therapeutic approaches. Curr. Pharm. Des. 16, 609-618.
7. Chadashvili T, Peterson DA (2006) Cytoarchitecture of fibroblast growth factor receptor 2 (FGFR-2) immunoreactivity in astrocytes of neurogenic and non-neurogenic regions of the young adult and aged rat brain. J. Comp. Neurol. 498, 1-15.
8. Cheng N, Brantley DM, Chen J (2002) The ephrins and Eph receptors in angiogenesis. Cytokine Growth Factor Rev. 13, 75-85.
9. Choi JS, Kim HY, Cha JH, Choi JY, Park SI, Jeong CH, Jeun SS, Lee MY (2007) Upregulation of vascular endothelial growth factor receptors Flt-1 and Flk-1 following acute spinal cord contusion in rats. J. Histochem. Cytochem. 55, 821-830.
10. Costantini C, Lorenzetto E, Cellini B, Buffelli M, Rossi F, Della-Bianca V (2010) Astrocytes regulate the expression of insulin-like growth factor 1 receptor (IGF1-R) in primary cortical neurons during in vitro senescence. J. Mol. Neurosci. 40, 342-352.
11. Croley AN, Zwetsloot KA, Westerkamp LM, Ryan NA, Pendergast AM, Hickner RC, Pofahl WE, Gavin TP (2005) Lower capillarization, VEGF protein, and VEGF mRNA response to acute exercise in the vastus lateralis muscle of aged vs. young women. J. Appl. Physiol. 99, 1872-1879.
12. Ding XM, Mao BY, Jiang S, Li SF, Deng YL (2005) Neuroprotective effect of exogenous vascular endothelial growth factor on rat spinal cord neurons in vitro hypoxia. Chin. Med. J. (Engl.) 118, 1644-1650.
13. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703-716.
14. Drogemuller K, Helmuth U, Brunn A, Sakowicz-Burkiewicz M, Gutmann DH, Mueller W, Deckert M, Schluter D (2008) Astrocyte gp130 expression is critical for the control of Toxoplasma encephalitis. J. Immunol. 181, 2683-2693.
15. During MJ, Cao L (2006) VEGF, a mediator of the effect of experience on hippocampal neurogenesis. Curr. Alzheimer Res. 3, 29-33.
16. Emsley J, Macklis J (2006) Astroglial heterogeneity closely reflects the neuronal-defined anatomy of the adult murine CNS. Neuron Glia Biol. 2, 175-186.
17. Eng LF, Ghirnikar RS, Lee YL (2000) Glial fibrillary acidic protein: GFAP-thirty-one years (1969-2000). Neurochem. Res. 25, 1439-1451.
18. Fabel K, Tam B, Kaufer D, Baiker A, Simmons N, Kuo CJ, Palmer TD (2003) VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur. J. Neurosci. 18, 2803-2812.
19. Faissner A, Pyka M, Geissler M, Sobik T, Frischknecht R, Gundelfinger ED, Seidenbecher C (2010) Contributions of astrocytes to synapse formation and maturation - Potential functions of the perisynaptic extracellular matrix. Brain Res. Rev. 63, 26-38.
20. Farrall AJ, Wardlaw JM (2009) Blood-brain barrier: ageing and microvascular disease--systematic review and meta-analysis. Neurobiol. Aging 30, 337-352.
21. Faulkner JR, Herrmann JE, Woo MJ, Tansey KE, Doan NB, Sofroniew MV (2004) Reactive astrocytes protect tissue and preserve function after spinal cord injury. J. Neurosci. 24, 2143-2155.
22. Ferrara N, Gerber HP, LeCouter J (2003) The biology of VEGF and its receptors. Nat. Med. 9, 669-676.
23. Filosa A, Paixão S, Honsek SD, Carmona MA, Becker L, Feddersen B, Gaitanos L, Rudhard Y, Schoepfer R, Klopstock T, Kullander K, Rose CR, Pasquale EB, Klein R (2009) Neuron-glia communication via EphA4/ephrin-A3 modulates LTP through glial glutamate transport. Nat. Neurosci. 12, 1285-1292.
24. Frinchi M, Bonomo A, Trovato-Salinaro A, Condorelli DF, Fuxe K, Spampinato MG, Mudo G (2008) Fibroblast growth factor-2 and its receptor expression in proliferating precursor cells of the subventricular zone in the adult rat brain. Neurosci. Lett. 447, 20-25.
25. Garcia AD, Doan NB, Imura T, Bush TG, Sofroniew MV (2004) GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat. Neurosci. 7, 1233-1241.
26. Gerber HP, Hillan KJ, Ryan AM, Kowalski J, Keller GA, Rangell L, Wright BD, Radtke F, Aguet M, Ferrara N (1999) VEGF is required for growth and survival in neonatal mice. Development 126, 1149-1159.
27. Giaume C (2010) Astroglial wiring is adding complexity to neuroglial networking. Front. Neuroenerg. 2, 129.
28. Giaume C, Koulakoff A, Roux L, Holcman D, Rouach N (2010) Astroglial networks: a step further in neuroglial and gliovascular interactions. Nat. Rev. Neurosci. 11, 87-99.
29. Gomez-Pinilla F, Lee JW, Cotman CW (1992) Basic FGF in adult rat brain: cellular distribution and response to entorhinal lesion and fimbria-fornix transection. J. Neurosci. 12, 345-355.
30. Gooney M, Messaoudi E, Maher FO, Bramham CR, Lynch MA (2004) BDNF-induced LTP in dentate gyrus is impaired with age: analysis of changes in cell signaling events. Neurobiol. Aging 25, 1323-1331.
31. Halassa MM, Haydon PG (2010) Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior. Annu. Rev. Physiol. 72, 335-355.
32. Hata Y, Rook SL, Aiello LP (1999) Basic fibroblast growth factor induces expression of VEGF receptor KDR through a protein kinase C and p44/p42 mitogen-activated protein kinase-dependent pathway. Diabetes 48, 1145-1155.
33. Islamov RR, Chintalgattu V, Pak ES, Katwa LC, Murashov AK (2004) Induction of VEGF and its Flt-1 receptor after sciatic nerve crush injury. Neuroreport 15, 2117-2121.
34. Jin K, Zhu Y, Sun Y, Mao XO, Xie L, Greenberg DA (2002) Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc. Natl. Acad. Sci. U S A 99, 11946-11950.
35. Kaul M, Lipton SA (2006) Mechanisms of neuroimmunity and neurodegeneration associated with HIV-1 infection and AIDS. J. Neuroimmune Pharmacol. 1, 138-151.
36. Kempermann G, Jessberger S, Steiner B, Kronenberg G (2004) Milestones of neuronal development in the adult hippocampus. Trends Neurosci. 27, 447-452.
37. Kilic E, Kilic U, Wang Y, Bassetti CL, Marti HH, Hermann DM (2006) The phosphatidylinositol-3 kinase/Akt pathway mediates VEGF's neuroprotective activity and induces blood brain barrier permeability after focal cerebral ischemia. FASEB J. 20, 1185-1187.
38. Kim HM, Hwang DH, Lee JE, Kim SU, Kim BG (2009) Ex vivo VEGF delivery by neural stem cells enhances proliferation of glial progenitors, angiogenesis, and tissue sparing after spinal cord injury. PLoS ONE 4, e4987.
39. Kimelberg HK (2004) The problem of astrocyte identity. Neurochem. Int. 45, 191-202.
40. Lalo U, Andrew J, Palygin O, Pankratov Y (2009) Ca2+-dependent modulation of GABAA and NMDA receptors by extracellular ATP: implication for function of tripartite synapse. Biochem. Soc. Trans. 37, 1407-1411.
41. Lindner AB, Demarez A (2009) Protein aggregation as a paradigm of aging. Biochim. Biophys. Acta 1790, 980-996.
42. Liu X, Zheng SX, Zhou LJ, Zhu XZ (2000) Basic fibroblast growth factor up-regulates the expression of vascular endothelial growth factor in primary cultured rat astrocytes. Acta Pharmacol. Sin. 21, 19-22.
43. Long JM, Kalehua AN, Muth NJ, Calhoun ME, Jucker M, Hengemihle JM, Ingram DK, Mouton PR (1998) Stereological analysis of astrocyte and microglia in aging mouse hippocampus. Neurobiol. Aging 19, 497-503.
44. Ma YY, Li KY, Wang JJ, Huang YL, Huang Y, Sun FY (2009) Vascular endothelial growth factor acutely reduces calcium influx via inhibition of the Ca2+ channels in rat hippocampal neurons. J. Neurosci. Res. 87, 393-402.
45. Maffei A, Turrigiano G (2008) The age of plasticity: developmental regulation of synaptic plasticity in neocortical microcircuits. Prog. Brain Res. 169, 211-223.
46. Magnus T, Carmen J, Deleon J, Xue H, Pardo AC, Lepore AC, Mattson MP, Rao MS, Maragakis NJ (2008) Adult glial precursor proliferation in mutant SOD1G93A mice. Glia 56, 200-208.
47. Maione P, Rossi A, Airoma G, Ferrara C, Castaldo V, Gridelli C (2004) The role of targeted therapy in non-small cell lung cancer. Crit. Rev. Oncol. Hematol. 51, 29-44.
48. Mani N, Khaibullina A, Krum JM, Rosenstein JM (2005) Astrocyte growth effects of vascular endothelial growth factor (VEGF) application to perinatal neocortical explants: receptor mediation and signal transduction pathways. Exp. Neurol. 192, 394-406.
49. Mouton PR, Long JM, Lei DL, Howard V, Jucker M, Calhoun ME, Ingram DK (2002) Age and gender effects on microglia and astrocyte numbers in brains of mice. Brain Res. 956, 30-35.
50. Murphy C, Nordin S, Acosta L (1997) Odor learning, recall, and recognition memory in young and elderly adults. Neuropsychology 11, 126-137.
51. Naidoo N (2009) ER and aging-protein folding and the ER stress response. Ageing Res. Rev. 8, 150-159.
52. Neves D, Santos J, Tomada N, Almeida H, Vendeira P (2006) Aging and orchidectomy modulate expression of VEGF receptors (Flt-1 and Flk-1) on corpus cavernosum of the rat. Ann. N Y Acad. Sci. 1067, 164-172.
53. Nicoletti JN, Shah SK, McCloskey DP, Goodman JH, Elkady A, Atassi H, Hylton D, Rudge JS, Scharfman HE, Croll SD (2008) Vascular endothelial growth factor is up-regulated after status epilepticus and protects against seizure-induced neuronal loss in hippocampus. Neuroscience 151, 232-241.
54. Ohba T, Haro H, Ando T, Wako M, Suenaga F, Aso Y, Koyama K, Hamada Y, Nakao A (2009) TNF-alpha-induced NF-kappaB signaling reverses age-related declines in VEGF induction and angiogenic activity in intervertebral disc tissues. J. Orthop. Res. 27, 229-235.
55. Palmer TD, Willhoite AR, Gage FH (2000) Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol. 425, 479-494.
56. Pascual O, Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, Sul JY, Takano H, Moss SJ, McCarthy K, Haydon PG (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310, 113-116.
57. Pati S, Orsi SA, Moore AN, Dash PK (2009) Intra-hippocampal administration of the VEGF receptor blocker PTK787/ZK222584 impairs long-term memory. Brain Res. 1256, 85-91.
58. Peterson DA, Lucidi-Phillipi CA, Murphy DP, Ray J, Gage FH (1996) Fibroblast growth factor-2 protects entorhinal layer II glutamatergic neurons from axotomy-induced death. J. Neurosci. 16, 886-898.
59. Picciotti P, Torsello A, Wolf FI, Paludetti G, Gaetani E, Pola R (2004) Age-dependent modifications of expression level of VEGF and its receptors in the inner ear. Exp. Gerontol. 39, 1253-1258.
60. Rai KS, Hattiangady B, Shetty AK (2007) Enhanced production and dendritic growth of new dentate granule cells in the middle-aged hippocampus following intracerebroventricular FGF-2 infusions. Eur. J. Neurosci. 26, 1765-1779.
61. Reuss B, Dono R, Unsicker K (2003) Functions of fibroblast growth factor (FGF)-2 and FGF-5 in astroglial differentiation and blood-brain barrier permeability: evidence from mouse mutants. J. Neurosci. 23, 6404-6412.
62. Seghezzi G, Patel S, Ren CJ, Gualandris A, Pintucci G, Robbins ES, Shapiro RL, Galloway AC, Rifkin DB, Mignatti P (1998) Fibroblast growth factor-2 (FGF-2) induces vascular endothelial growth factor (VEGF) expression in the endothelial cells of forming capillaries: an autocrine mechanism contributing to angiogenesis. J. Cell Biol. 141, 1659-1673.
63. Segi-Nishida E, Warner-Schmidt JL, Duman RS (2008) Electroconvulsive seizure and VEGF increase the proliferation of neural stem-like cells in rat hippocampus. Proc. Natl Acad. Sci. USA 105, 11352-11357.
64. Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J. Neurosci. 21, 7153-7160.
65. Shetty AK, Hattiangady B, Shetty GA (2005) Stem/progenitor cell proliferation factors FGF-2, IGF-1, and VEGF exhibit early decline during the course of aging in the hippocampus: role of astrocytes. Glia 51, 173-186.
66. Simón AM, de Maturana RL, Ricobaraza A, Escribano L, Schiapparelli L, Cuadrado-Tejedor M, Pérez-Mediavilla A, Avila J, Del Río J, Frechilla D (2009) Early changes in hippocampal eph receptors precede the onset of memory decline in mouse models of Alzheimer's disease. J. Alzheimers Dis. 17 (4), 773-786.
67. Sinclair DA, Oberdoerffer P (2009) The ageing epigenome: damaged beyond repair? Ageing Res. Rev. 8, 189-198.
68. Skold MK, von Gertten C, Sandberg-Nordqvist AC, Mathiesen T, Holmin S (2005) VEGF and VEGF receptor expression after experimental brain contusion in rat. J. Neurotrauma 22, 353-367.
69. Sofroniew MV (2005) Reactive astrocytes in neural repair and protection. Neuroscientist 11, 400-407.
70. Sofroniew MV (2009) Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci. 32, 638-647.
71. Sofroniew MV, Vinters HV (2010) Astrocytes: biology and pathology. Acta Neuropathol. 119, 7-35.
72. Song H, Stevens CF, Gage FH (2002) Astroglia induce neurogenesis from adult neural stem cells. Nature 417, 39-44.
73. Stavri GT, Zachary IC, Baskerville PA, Martin JF, Erusalimsky JD (1995) Basic fibroblast growth factor upregulates the expression of vascular endothelial growth factor in vascular smooth muscle cells. Synergistic interaction with hypoxia. Circulation 92, 11-14.
74. Steiner B, Klempin F, Wang L, Kott M, Kettenmann H, Kempermann G (2006) Type-2 cells as link between glial and neuronal lineage in adult hippocampal neurogenesis. Glia 54, 805-814.
75. Vasilevko V, Passos GF, Quiring D, Head E, Kim RC, Fisher M, Cribbs DH (2010) Aging and cerebrovascular dysfunction: contribution of hypertension, cerebral amyloid angiopathy, and immunotherapy. Ann. N Y Acad. Sci. 1207, 58-70.
76. Voskuhl RR, Peterson RS, Song B, Ao Y, Morales LB, Tiwari-Woodruff S, Sofroniew MV (2009) Reactive astrocytes form scar-like perivascular barriers to leukocytes during adaptive immune inflammation of the CNS. J. Neurosci. 29, 11511-11522.
77. Wang WY, Dong JH, Liu X, Wang Y, Ying GX, Ni ZM, Zhou CF (2005a) Vascular endothelial growth factor and its receptor Flk-1 are expressed in the hippocampus following entorhinal deafferentation. Neuroscience 134, 1167-1178.
78. Wang Y, Kilic E, Kilic U, Weber B, Bassetti CL, Marti HH, Hermann DM (2005b) VEGF overexpression induces post-ischaemic neuroprotection, but facilitates haemodynamic steal phenomena. Brain 128, 52-63.
79. Warner-Schmidt JL, Duman RS (2007) VEGF is an essential mediator of the neurogenic and behavioral actions of antidepressants. Proc. Natl. Acad. Sci. U S A 104, 4647-4652.
80. Warner-Schmidt JL, Duman RS (2008) VEGF as a potential target for therapeutic intervention in depression. Curr. Opin. Pharmacol. 8, 14-19.
81. Wilhelmsson U, Bushong EA, Price DL, Smarr BL, Phung V, Terada M, Ellisman MH, Pekny M (2006) Redefining the concept of reactive astrocytes as cells that remain within their unique domains upon reaction to injury. Proc. Natl. Acad. Sci. U S A 103, 17513-17518.
82. Wittko IM, Schanzer A, Kuzmichev A, Schneider FT, Shibuya M, Raab S, Plate KH (2009) VEGFR-1 regulates adult olfactory bulb neurogenesis and migration of neural progenitors in the rostral migratory stream in vivo. J. Neurosci. 29, 8704-8714.
83. Wolburg-Buchholz K, Mack AF, Steiner E, Pfeiffer F, Engelhardt B, Wolburg H (2009) Loss of astrocyte polarity marks blood-brain barrier impairment during experimental autoimmune encephalomyelitis. Acta Neuropathol. 118, 219-233.
84. Wolosker H, Dumin E, Balan L, Foltyn VN (2008) D-amino acids in the brain: D-serine in neurotransmission and neurodegeneration. FEBS J. 275, 3514-3526.
85. Wu Y, Zhang A-Q, Yew DT (2005) Age related changes of various markers of astrocytes in senescence-accelerated mice hippocampus. Neurochem. Int. 46, 565-574.
86. Xiao Z, Kong Y, Yang S, Li M, Wen J, Li L (2007) Upregulation of Flk-1 by bFGF via the ERK pathway is essential for VEGF-mediated promotion of neural stem cell proliferation. Cell Res. 17, 73-79.
87. Yang SZ, Zhang LM, Huang YL, Sun FY (2003) Distribution of Flk-1 and Flt-1 receptors in neonatal and adult rat brains. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 274, 851-856.
88. Yeh J, Kim BS, Peresie J (2008) Ovarian vascular endothelial growth factor and vascular endothelial growth factor receptor patterns in reproductive aging. Fertil. Steril. 89, 1546-1556.
89. Yoshimura S, Takagi Y, Harada J, Teramoto T, Thomas SS, Waeber C, Bakowska JC, Breakefield XO, Moskowitz MA (2001) FGF-2 regulation of neurogenesis in adult hippocampus after brain injury. Proc. Natl. Acad. Sci. U S A 98, 5874-5879.
90. Yoshimura S, Teramoto T, Whalen MJ, Irizarry MC, Takagi Y, Qiu J, Harada J, Waeber C, Breakefield XO, Moskowitz MA (2003) FGF-2 regulates neurogenesis and degeneration in the dentate gyrus after traumatic brain injury in mice. J. Clin. Invest. 112, 1202-1210.
91. Zhao M, Li D, Shimazu K, Zhou Y-X, Lu B, Deng C-X (2007) Fibroblast growth factor receptor-1 is required for long-term potentiation, memory consolidation, and neurogenesis. Biol. Psychiatry 62, 381-390.