Human FGF1 promoter is active in ependymal cells and dopaminergic neurons in the brains of F1B-GFP transgenic mice

Developmental Neurobiology

Volumn 75, Issue 3, 2015, Pages 232-248

  Chen, Mei Shu ^a   Lin, Hua Kuo ^a   Chiu, Hsun ^a   Lee, Don Ching ^a   Chung, Yu Fen ^a   Chiu, Ing Ming ^a,b,c  

^a NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^b NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^c THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

Author keywords

Adult brain; Dopaminergic neurons; FGF1; Human FGF1 promoter; Transgenic mice

Indexed keywords

FIBROBLAST GROWTH FACTOR 1; TYROSINE 3 MONOOXYGENASE; FIBROBLAST GROWTH FACTOR RECEPTOR 1; GREEN FLUORESCENT PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN VENTRICLE; CELL ACTIVITY; CELL POPULATION; CELL SUBPOPULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EPENDYMA CELL; HUMAN; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RAPHE NUCLEUS; REPORTER GENE; TRANSGENIC MOUSE; VENTRAL TEGMENTUM; ANIMAL; BRAIN; CYTOLOGY; EPENDYMA; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

ANIMALS; BRAIN; CEREBRAL VENTRICLES; DOPAMINERGIC NEURONS; EPENDYMA; FIBROBLAST GROWTH FACTOR 1; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; HUMANS; MICE; MICE, TRANSGENIC; PROMOTER REGIONS, GENETIC; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; TYROSINE 3-MONOOXYGENASE;

EID: 84922763762     PISSN: 19328451     EISSN: 1932846X     Source Type: Journal    
DOI: 10.1002/dneu.22225     Document Type: Article

References (66)

1. Alam KY, Frostholm A, Hackshaw KV, Evans JE, Rotter A, Chiu IM. 1996. Characterization of the 1B promoter of fibroblast growth factor 1 and its expression in the adult and developing mouse brain. J Biol Chem 271:30263-30271.
2. Bean AJ, Elde R, Cao YH, Oellig C, Tamminga C, Goldstein M, Pettersson RF, et al. 1991. Expression of acidic and basic fibroblast growth factors in the substantia nigra of rat, monkey, and human. Proc Natl Acad Sci USA 88:10237-10241.
3. Beenken A, Mohammadi M. 2009. The FGF family: Biology, pathophysiology and therapy. Nat Rev Drug Discov 8:235-253.
4. Bennett L, Yang M, Enikolopov G, Iacovitti L. 2009. Circumventricular organs: A novel site of neural stem cells in the adult brain. Mol Cell Neurosci 41:337-347.
5. Canteras NS. 2002. The medial hypothalamic defensive system: Hodological organization and functional implications. Pharmacol Biochem Behav 71:481-491.
6. Canteras NS, Simerly RB, Swanson LW. 1995. Organization of projections from the medial nucleus of the amygdala: A PHAL study in the rat. J Comp Neurol 360:213-245.
7. Carlen M, Meletis K, Goritz C, Darsalia V, Evergren E, Tanigaki K, Amendola M, et al. 2009. Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke. Nat Neurosci 12:259-267.
8. Chauvet N, Prieto M, Alonso G. 1998. Tanycytes present in the adult rat mediobasal hypothalamus support the regeneration of monoaminergic axons. Exp Neurol 151:1-13.
9. Chen CW, Liu CS, Chiu IM, Shen SC, Pan HC, Lee KH, Lin SZ, et al. 2010. The signals of FGFs on the neurogenesis of embryonic stem cells. J Biomed Sci 17:33.
10. Chiu IM, Touhalisky K, Liu Y, Yates A, Frostholm A. 2000. Tumorigenesis in transgenic mice in which the SV40 T antigen is driven by the brain-specific FGF1 promoter. Oncogene 19:6229-6239.
11. Chiu IM, Wang WP, Lehtoma K. 1990. Alternative splicing generates two forms of mRNA coding for human heparin-binding growth factor 1. Oncogene 5:755-762.
12. Codega P, Silva-Vargas V, Paul A, Maldonado-Soto AR, Deleo AM, Pastrana E, Doetsch F. 2014. Prospective identification and purification of quiescent adult neural stem cells from their in vivo niche. Neuron 82:545-559.
13. Cuevas P, Revilla C, Herreras O, Largo C, Gimenez-Gallego G. 1994. Neuroprotective effect of acidic fibroblast growth factor on seizure-associated brain damage. Neurol Res 16:365-369.
14. Date I, Notter MF, Felten SY, Felten DL. 1990. MPTP-treated young mice but not aging mice show partial recovery of the nigrostriatal dopaminergic system by stereotaxic injection of acidic fibroblast growth factor (aFGF). Brain Res 526:156-160.
15. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. 1997. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17:5046-5061.
16. Eckenstein F, Woodward WR, Nishi R. 1991. Differential localization and possible functions of aFGF and bFGF in the central and peripheral nervous systems. Ann NY Acad Sci 638:348-360.
17. Fallon JH, Di Salvo J, Loughlin SE, Gimenez-Gallego G, Seroogy KB, Bradshaw RA, Morrison RS, et al. 1992. Localization of acidic fibroblast growth factor within the mouse brain using biochemical and immunocytochemical techniques. Growth Factors 6:139-157.
18. Ferri AL, Cavallaro M, Braida D, Di Cristofano A, Canta A, Vezzani A, Ottolenghi S, et al. 2004. Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain. Development 131:3805-3819.
19. Flores JA, Galan-Rodriguez B, Rojo AI, Ramiro-Fuentes S, Cuadrado A, Fernandez-Espejo E. 2010. Fibroblast growth factor-1 within the ventral tegmental area participates in motor sensitizing effects of morphine. Neuroscience 165:198-211.
20. Gates MA, Thomas LB, Howard EM, Laywell ED, Sajin B, Faissner A, Gotz B, et al. 1995. Cell and molecular analysis of the developing and adult mouse subventricular zone of the cerebral hemispheres. J Comp Neurol 361:249-266.
21. Gerdes J, Schwab U, Lemke H, Stein H. 1983. Production of a mouse monoclonal antibody reactive with a human nuclear antigen associated with cell proliferation. Int J Cancer 31:13-20.
22. Ghielli M, Verstrepen W, Nouwen E, De Broe ME. 1998. Regeneration processes in the kidney after acute injury: Role of infiltrating cells. Exp Nephrol 6:502-507.
23. Giacobini MM, Stromberg I, Almstrom S, Cao Y, Olson L. 1993. Fibroblast growth factors enhance dopamine fiber formation from nigral grafts. Brain Res Dev Brain Res 75:65-73.
24. Hamilton LK, Truong MK, Bednarczyk MR, Aumont A, Fernandes KJ. 2009. Cellular organization of the central canal ependymal zone, a niche of latent neural stem cells in the adult mammalian spinal cord. Neuroscience 164:1044-1056.
25. Hanai K, Oomura Y, Kai Y, Nishikawa K, Shimizu N, Morita H, Plata-Salaman CR. 1989. Central action of acidic fibroblast growth factor in feeding regulation. Am J Physiol 256:R217-R223.
26. Hashimoto M, Sagara Y, Langford D, Everall IP, Mallory M, Everson A, Digicaylioglu M, et al. 2002. Fibroblast growth factor 1 regulates signaling via the glycogen synthase kinase-3beta pathway. Implications for neuroprotection. J Biol Chem 277:32985-32991.
27. Hermann A, Maisel M, Wegner F, Liebau S, Kim DW, Gerlach M, Schwarz J, et al. 2006. Multipotent neural stem cells from the adult tegmentum with dopaminergic potential develop essential properties of functional neurons. Stem Cells 24:949-964.
28. Hermann A, Suess C, Fauser M, Kanzler S, Witt M, Fabel K, Schwarz J, et al. 2009. Rostro-caudal gradual loss of cellular diversity within the periventricular regions of the ventricular system. Stem Cells 27:928-941.
29. Ho YC, Cheng JK, Chiou LC. 2013. Hypofunction of glutamatergic neurotransmission in the periaqueductal gray contributes to nerve-injury-induced neuropathic pain. J Neurosci 33:7825-7836.
30. Jin BK, Iacovitti L. 1995. Dopamine differentiation factors produce partial motor recovery in 6-hydroxydopamine lesioned rats. Neurobiol Dis 2:1-12.
31. Jin BK, Iacovitti L. 1996. Dopamine differentiation factors increase striatal dopaminergic function in 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-lesioned mice. J Neurosci Res 43:331-334.
32. Kimura H, Tooyama I, McGeer PL. 1994. Acidic FGF expression in the surroundings of senile plaques. Tohoku J Exp Med 174:279-293.
33. Lee DC, Hsu YC, Chung YF, Hsiao CY, Chen SL, Chen MS, Lin HK, et al. 2009. Isolation of neural stem/progenitor cells by using EGF/FGF1 and FGF1B promoter-driven green fluorescence from embryonic and adult mouse brains. Mol Cell Neurosci 41:348-363.
34. Lou G, Zhang Q, Xiao F, Xiang Q, Su Z, Zhang L, Yang P, et al. 2012. Intranasal administration of TAT-haFGF((1)(4)(-)(1)(5)(4)) attenuates disease progression in a mouse model of Alzheimer's disease. Neuroscience 223:225-237.
35. Luo J, Shook BA, Daniels SB, Conover JC. 2008. Subventricular zone-mediated ependyma repair in the adult mammalian brain. J Neurosci 28:3804-3813.
36. Luskin MB. 1993. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173-189.
37. Maingay M, Romero-Ramos M, Carta M, Kirik D. 2006. Ventral tegmental area dopamine neurons are resistant to human mutant alpha-synuclein overexpression. Neurobiol Dis 23:522-532.
38. Mashayekhi F, Hadavi M, Vaziri HR, Naji M. 2010. Increased acidic fibroblast growth factor concentrations in the serum and cerebrospinal fluid of patients with Alzheimer's disease. J Clin Neurosci 17:357-359.
39. McLay RN, Freeman SM, Zadina JE. 2001. Administration of FGF-1 through transfected cells alleviates MPTP toxicity in mice. Neurotox Res 3:249-253.
40. Mena MA, Casarejos MJ, Gimenez-Gallego G, Garcia de Yebenes J. 1995. Fibroblast growth factors: Structure-activity on dopamine neurons in vitro. J Neural Transm Park Dis Dement Sect 9:1-14.
41. Miller DL, Ortega S, Bashayan O, Basch R, Basilico C. 2000. Compensation by fibroblast growth factor 1 (FGF1) does not account for the mild phenotypic defects observed in FGF2 null mice. Mol Cell Biol 20:2260-2268.
42. Mirzadeh Z, Doetsch F, Sawamoto K, Wichterle H, Alvarez-Buylla A. 2010. The subventricular zone en-face: Wholemount staining and ependymal flow. J Vis Exp.
43. Mullen RJ, Buck CR, Smith AM. 1992. NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211.
44. Myers RL, Chedid M, Tronick SR, Chiu IM. 1995a. Different fibroblast growth factor 1 (FGF-1) transcripts in neural tissues, glioblastomas and kidney carcinoma cell lines. Oncogene 11:785-789.
45. Myers RL, Payson RA, Chotani MA, Deaven LL, Chiu IM. 1993. Gene structure and differential expression of acidic fibroblast growth factor mRNA: Identification and distribution of four different transcripts. Oncogene 8:341-349.
46. Myers RL, Ray SK, Eldridge R, Chotani MA, Chiu IM. 1995b. Functional characterization of the brain-specific FGF-1 promoter, FGF-1.B. J Biol Chem 270:8257-8266.
47. Ni HC, Tseng TC, Chen JR, Hsu SH, Chiu IM. 2013. Fabrication of bioactive conduits containing the fibroblast growth factor 1 and neural stem cells for peripheral nerve regeneration across a 15 mm critical gap. Biofabrication 5:035010.
48. Oomura Y, Sasaki K, Suzuki K, Muto T, Li AJ, Ogita Z, Hanai K, et al. 1992. A new brain glucosensor and its physiological significance. Am J Clin Nutr 55:278S-282S.
49. Patrie K, Botelho MJ, Ray SK, Mehta VB, Chiu IM. 1997. Amphibian FGF-1 is structurally and functionally similar to but antigenically distinguishable from its mammalian counterpart. Growth Factors 14:39-57.
50. Presta M, Dell'Era P, Mitola S, Moroni E, Ronca R, Rusnati M. 2005. Fibroblast growth factor/fibroblast growth factor receptor system in angiogenesis. Cytokine Growth Factor Rev 16:159-178.
51. Ray SK, Yang XQ, Chiu IM. 1997. Transcriptional activation of fibroblast growth factor 1.B promoter is mediated through an 18-base pair cis-acting element. J Biol Chem 272:7546-7555.
52. Russell JC, Szuflita N, Khatri R, Laterra J, Hossain MA. 2006. Transgenic expression of human FGF-1 protects against hypoxic-ischemic injury in perinatal brain by intervening at caspase-XIAP signaling cascades. Neurobiol Dis 22:677-690.
53. Sasaki K, Li AJ, Oomura Y, Muto T, Hanai K, Tooyama I, Kimura H, et al. 1994. Effects of fibroblast growth factors and related peptides on food intake by rats. Physiol Behav 56:211-218.
54. Sasaki K, Oomura Y, Li AJ, Hanai K, Tooyama I, Kimura H, Yanaihara N, et al. 1995. Actions of acidic fibroblast growth factor fragments on food intake in rats. Obes Res 3 Suppl 5:697S-706S.
55. Sasaki K, Oomura Y, Suzuki K, Muto T, Hanai K, Tooyama I, Kimura H, et al. 1991. Effects of fibroblast growth factors and platelet-derived growth factor on food intake in rats. Brain Res Bull 27:327-332.
56. Stock A, Kuzis K, Woodward WR, Nishi R, Eckenstein FP. 1992. Localization of acidic fibroblast growth factor in specific subcortical neuronal populations. J Neurosci 12:4688-4700.
57. Teng YD, Mocchetti I, Wrathall JR. 1998. Basic and acidic fibroblast growth factors protect spinal motor neurones in vivo after experimental spinal cord injury. Eur J Neurosci 10:798-802.
58. Thorns V, Masliah E. 1999. Evidence for neuroprotective effects of acidic fibroblast growth factor in Alzheimer disease. J Neuropathol Exp Neurol 58:296-306.
59. Tooyama I, Hara Y, Yasuhara O, Oomura Y, Sasaki K, Muto T, Suzuki K, et al. 1991. Production of antisera to acidic fibroblast growth factor and their application to immunohistochemical study in rat brain. Neuroscience 40:769-779.
60. Tsai MC, Shen LF, Kuo HS, Cheng H, Chak KF. 2008. Involvement of acidic fibroblast growth factor in spinal cord injury repair processes revealed by a proteomics approach. Mol Cell Proteomics 7:1668-1687.
61. Wang WP, Myers RL, Chiu IM. 1991. Single primer-mediated polymerase chain reaction: Application in cloning of two different 5′-untranslated sequences of acidic fibroblast growth factor mRNA. DNA Cell Biol 10:771-777.
62. Weiss WA, Israel M, Cobbs C, Holland E, James CD, Louis DN, Marks C, et al. 2002. Neuropathology of genetically engineered mice: Consensus report and recommendations from an international forum. Oncogene 21:7453-7463.
63. Wojtowicz JM, Kee N. 2006. BrdU assay for neurogenesis in rodents. Nat Protoc 1:1399-1405.
64. Xu Y, Tamamaki N, Noda T, Kimura K, Itokazu Y, Matsumoto N, Dezawa M, et al. 2005. Neurogenesis in the ependymal layer of the adult rat 3rd ventricle. Exp Neurol 192:251-264.
65. Yun YR, Won JE, Jeon E, Lee S, Kang W, Jo H, Jang JH, et al. 2010. Fibroblast growth factors: Biology, function, and application for tissue regeneration. J Tissue Eng 2010:218142.
66. Zhao C, Suh H, Gage FH. 2009. Notch keeps ependymal cells in line. Nat Neurosci 12:243-245.