REVIEW

Choroid plexus trophic factors in the developing and adult brain

  • Karen Arnaud 1,2 ,
  • Ariel A. Di Nardo , 1
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  • 1. Center for Interdisciplinary Research in Biology (CIRB), CNRS UMR 7241/INSERM U1050, Labex Memolife, Collège de France, 75231 Paris, France
  • 2. Université Pierre et Marie Curie, Paris VI, Paris, France

Received date: 30 Jan 2016

Accepted date: 25 Apr 2016

Published date: 05 Jul 2016

Copyright

2016 Higher Education Press and Springer-Verlag Berlin Heidelberg

Abstract

The choroid plexus (CP), localized in brain ventricles, is the major source of cerebrospinal fluid (CSF) and participates in the blood-CSF barrier. It is essential for brain immunosurveillance and the clearance of toxics, and for brain development and activity. Indeed, the CP secretes a large variety of trophic factors in the CSF that impact the entire brain. These factors are mainly implicated in neurogenesis, but also in the maintenance of brain functions and the vasculature. In this mini-review, we provide an overview of the various trophic factors secreted by the CP in the CSF, and describe their roles in the developing, adult and diseased brain.

Cite this article

Karen Arnaud , Ariel A. Di Nardo . Choroid plexus trophic factors in the developing and adult brain[J]. Frontiers in Biology, 2016 , 11(3) : 214 -221 . DOI: 10.1007/s11515-016-1401-7

Compliance with ethics guidelines

K. Arnaud and A. A. Di Nardo declare they have no conflict of interest.
This article does not contain studies with human or animal subjects performed by the authors.
1
Alshehri B, D’Souza D G, Lee J Y, Petratos S, Richardson S J (2015). The diversity of mechanisms influenced by transthyretin in neurobiology: development, disease and endocrine disruption. J Neuroendocrinol, 27(5): 303–323

DOI PMID

2
Ashpole N M, Sanders J E, Hodges E L, Yan H, Sonntag W E (2015). Growth hormone, insulin-like growth factor-1 and the aging brain. Exp Gerontol, 68: 76–81

DOI PMID

3
Aurbach E L, Inui E G, Turner C A, Hagenauer M H, Prater K E, Li J Z, Absher D, Shah N, Blandino PJr, Bunney W E, Myers R M, Barchas J D, Schatzberg A F, Watson S JJr, Akil H (2015). Fibroblast growth factor 9 is a novel modulator of negative affect. Proc Natl Acad Sci USA, 112(38): 11953–11958

DOI PMID

4
Baruch K, Deczkowska A, David E, Castellano J M, Miller O, Kertser A, Berkutzki T, Barnett-Itzhaki Z, Bezalel D, Wyss-Coray T, Amit I, Schwartz M (2014). Aging. Aging-induced type I interferon response at the choroid plexus negatively affects brain function. Science, 346(6205): 89–93

DOI PMID

5
Ben-Hur T, Ben-Menachem O, Furer V, Einstein O, Mizrachi-Kol R, Grigoriadis N (2003). Effects of proinflammatory cytokines on the growth, fate, and motility of multipotential neural precursor cells. Mol Cell Neurosci, 24(3): 623–631

DOI PMID

6
Binder D K, Scharfman H E (2004). Brain-derived neurotrophic factor. Growth Factors, 22(3): 123–131

DOI PMID

7
Brinker T, Stopa E, Morrison J, Klinge P (2014). A new look at cerebrospinal fluid circulation. Fluids Barriers CNS, 11(1): 10

DOI PMID

8
Budni J, Bellettini-Santos T, Mina F, Garcez M L, Zugno A I (2015). The involvement of BDNF, NGF and GDNF in aging and Alzheimer’s disease. Aging Dis, 6(5): 331–341

DOI PMID

9
Carro E, Trejo J L, Spuch C, Bohl D, Heard J M, Torres-Aleman I (2006). Blockade of the insulin-like growth factor I receptor in the choroid plexus originates Alzheimer’s-like neuropathology in rodents: new cues into the human disease? Neurobiol Aging, 27(11): 1618–1631

DOI PMID

10
Chen C P C, Chen R L, Preston J E (2012). The influence of ageing in the cerebrospinal fluid concentrations of proteins that are derived from the choroid plexus, brain, and plasma. Exp Gerontol, 47(4): 323–328

DOI PMID

11
Cheng Y, Black I B, DiCicco-Bloom E (2002). Hippocampal granule neuron production and population size are regulated by levels of bFGF. Eur J Neurosci, 15(1): 3–12

DOI PMID

12
Chodobski A, Szmydynger-Chodobska J (2001). Choroid plexus: target for polypeptides and site of their synthesis. Microsc Res Tech, 52(1): 65–82

DOI PMID

13
Craig C G, Tropepe V, Morshead C M, Reynolds B A, Weiss S, van der Kooy D (1996). In vivogrowth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J Neurosci, 16(8): 2649–2658

PMID

14
Damkier H H, Brown P D, Praetorius J (2013). Cerebrospinal fluid secretion by the choroid plexus. Physiol Rev, 93(4): 1847–1892

DOI PMID

15
Das K P, Chao S L, White L D, Haines W T, Harry G J, Tilson H A, Barone SJr (2001). Differential patterns of nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3 mRNA and protein levels in developing regions of rat brain. Neuroscience, 103(3): 739–761

DOI PMID

16
Delgado A C, Ferrón S R, Vicente D, Porlan E, Perez-Villalba A, Trujillo C M, D’Ocón P, Fariñas I (2014). Endothelial NT-3 delivered by vasculature and CSF promotes quiescence of subependymal neural stem cells through nitric oxide induction. Neuron, 83(3): 572–585

DOI PMID

17
Doetsch F, Petreanu L, Caille I, Garcia-Verdugo J M, Alvarez-Buylla A (2002). EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron, 36(6): 1021–1034

DOI PMID

18
Dziegielewska K M, Ek J, Habgood M D, Saunders N R (2001). Development of the choroid plexus. Microsc Res Tech, 52(1): 5–20

DOI PMID

19
Emerich D F, Skinner S J M, Borlongan C V, Vasconcellos A V, Thanos C G (2005). The choroid plexus in the rise, fall and repair of the brain. BioEssays, 27(3): 262–274

DOI PMID

20
Emerich D F, Vasconcellos A V, Elliott R B, Skinner S J, Borlongan C V (2004). The choroid plexus: function, pathology and therapeutic potential of its transplantation. Expert Opin Biol Ther, 4(8): 1191–1201

DOI PMID

21
Engelhardt B, Wolburg-Buchholz K, Wolburg H (2001). Involvement of the choroid plexus in central nervous system inflammation. Microsc Res Tech, 52(1): 112–129

DOI PMID

22
Falcão A M, Marques F, Novais A, Sousa N, Palha J A, Sousa J C (2012). The path from the choroid plexus to the subventricular zone: go with the flow! Front Cell Neurosci, 6: 34

DOI PMID

23
Falk S, Wurdak H, Ittner L M, Ille F, Sumara G, Schmid M T, Draganova K, Lang K S, Paratore C, Leveen P, Suter U, Karlsson S, Born W, Ricci R, Götz M, Sommer L (2008). Brain area-specific effect of TGF-b signaling on Wnt-dependent neural stem cell expansion. Cell Stem Cell, 2(5): 472–483

DOI PMID

24
Forlenza O V, Diniz B S, Teixeira A L, Radanovic M, Talib L L, Rocha N P, Gattaz W F (2015). Lower cerebrospinal fluid concentration of brain-derived neurotrophic factor predicts progression from mild cognitive impairment to Alzheimer’s disease. Neuromolecular Med, 17(3): 326–332

DOI PMID

25
Gao L, Zhou S, Cai H, Gong Z, Zang D (2014). VEGF levels in CSF and serum in mild ALS patients. J Neurol Sci, 346(1-2): 216–220

DOI PMID

26
Gato A, Alonso M I, Martín C, Carnicero E, Moro J A, De la Mano A, Fernández J M, Lamus F, Desmond M E (2014). Embryonic cerebrospinal fluid in brain development: neural progenitor control. Croat Med J, 55(4): 299–305

DOI PMID

27
Gong Z, Gao L, Guo J, Lu Y, Zang D (2015). bFGF in the CSF and serum of sALS patients. Acta Neurol Scand, 132(3): 171–178

DOI PMID

28
González-Marrero I, Giménez-Llort L, Johanson C E, Carmona-Calero E M, Castañeyra-Ruiz L, Brito-Armas J M, Castañeyra-Perdomo A, Castro-Fuentes R (2015). Choroid plexus dysfunction impairs beta-amyloid clearance in a triple transgenic mouse model of Alzheimer’s disease. Front Cell Neurosci, 9: 17

DOI PMID

29
Greenwood S, Swetloff A, Wade A M, Terasaki T, Ferretti P (2008). Fgf2 is expressed in human and murine embryonic choroid plexus and affects choroid plexus epithelial cell behaviour. Cerebrospinal Fluid Res, 5(1): 20

DOI PMID

30
Hébert J M, Mishina Y, McConnell S K (2002). BMP signaling is required locally to pattern the dorsal telencephalic midline. Neuron, 35(6): 1029–1041

DOI PMID

31
Huang S L, Shi W, Jiao Q, He X J (2011). Change of neural stem cells in the choroid plexuses of developing rat. Int J Neurosci, 121(6): 310–315

DOI PMID

32
Huang X, Ketova T, Fleming J T, Wang H, Dey S K, Litingtung Y, Chiang C (2009). Sonic hedgehog signaling regulates a novel epithelial progenitor domain of the hindbrain choroid plexus. Development, 136(15): 2535–2543

DOI PMID

33
Iliff J J, Wang M, Liao Y, Plogg B A, Peng W, Gundersen G A, Benveniste H, Vates G E, Deane R, Goldman S A, Nagelhus E A, Nedergaard M (2012). A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid b. Sci Transl Med, 4(147): 147ra111PMID:22896675

DOI

34
Itokazu Y, Kitada M, Dezawa M, Mizoguchi A, Matsumoto N, Shimizu A, Ide C (2006). Choroid plexus ependymal cells host neural progenitor cells in the rat. Glia, 53(1): 32–42

DOI PMID

35
Jackson E L, Garcia-Verdugo J M, Gil-Perotin S, Roy M, Quinones-Hinojosa A, VandenBerg S, Alvarez-Buylla A (2006). PDGFR a-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron, 51(2): 187–199

DOI PMID

36
Jin K, Sun Y, Xie L, Batteur S, Mao X O, Smelick C, Logvinova A, Greenberg D A (2003). Neurogenesis and aging: FGF-2 and HB-EGF restore neurogenesis in hippocampus and subventricular zone of aged mice. Aging Cell, 2(3): 175–183

DOI PMID

37
Jin K, Zhu Y, Sun Y, Mao X O, Xie L, Greenberg D A (2002). Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci USA, 99(18): 11946–11950

DOI PMID

38
Johanson C, McMillan P, Tavares R, Spangenberger A, Duncan J, Silverberg G, Stopa E (2004). Homeostatic capabilities of the choroid plexus epithelium in Alzheimer’s disease. Cerebrospinal Fluid Res, 1(1): 3

DOI PMID

39
Johanson C, Stopa E, Baird A, Sharma H (2011a). Traumatic brain injury and recovery mechanisms: peptide modulation of periventricular neurogenic regions by the choroid plexus-CSF nexus. J Neural Transm (Vienna), 118(1): 115–133

DOI PMID

40
Johanson C, Stopa E, McMillan P, Roth D, Funk J, Krinke G (2011b). The distributional nexus of choroid plexus to cerebrospinal fluid, ependyma and brain: toxicologic/pathologic phenomena, periventricular destabilization, and lesion spread. Toxicol Pathol, 39(1): 186–212

DOI PMID

41
Johansson P A (2014). The choroid plexuses and their impact on developmental neurogenesis. Front Neurosci, 8: 340

DOI PMID

42
Krizhanovsky V, Ben-Arie N (2006). A novel role for the choroid plexus in BMP-mediated inhibition of differentiation of cerebellar neural progenitors. Mech Dev, 123(1): 67–75

DOI PMID

43
Krzyzanowska A, Carro E (2012). Pathological alteration in the choroid plexus of Alzheimer’s disease: implication for new therapy approaches. Front Pharmacol, 3: 75

DOI PMID

44
Kunis G, Baruch K, Rosenzweig N, Kertser A, Miller O, Berkutzki T, Schwartz M (2013). IFN-g-dependent activation of the brain’s choroid plexus for CNS immune surveillance and repair. Brain, 136(Pt 11): 3427–3440

DOI PMID

45
Lehtinen M K, Zappaterra M W, Chen X, Yang Y J, Hill A D, Lun M, Maynard T, Gonzalez D, Kim S, Ye P, D’Ercole A J, Wong E T, LaMantia A S, Walsh C A (2011). The cerebrospinal fluid provides a proliferative niche for neural progenitor cells. Neuron, 69(5): 893–905

DOI PMID

46
Li Y, Chen J, Chopp M (2002). Cell proliferation and differentiation from ependymal, subependymal and choroid plexus cells in response to stroke in rats. J Neurol Sci, 193(2): 137–146

DOI PMID

47
Licht T, Eavri R, Goshen I, Shlomai Y, Mizrahi A, Keshet E (2010). VEGF is required for dendritogenesis of newly born olfactory bulb interneurons. Development, 137(2): 261–271

DOI PMID

48
Liddelow S A (2015). Development of the choroid plexus and blood-CSF barrier. Front Neurosci, 9: 32

DOI PMID

49
Lun M P, Monuki E S, Lehtinen M K (2015). Development and functions of the choroid plexus-cerebrospinal fluid system. Nat Rev Neurosci, 16(8): 445–457

DOI PMID

50
Mackenzie F, Ruhrberg C (2012). Diverse roles for VEGF-A in the nervous system. Development, 139(8): 1371–1380

DOI PMID

51
Maharaj A S R, Walshe T E, Saint-Geniez M, Venkatesha S, Maldonado A E, Himes N C, Matharu K S, Karumanchi S A, D’Amore P A (2008). VEGF and TGF-b are required for the maintenance of the choroid plexus and ependyma. J Exp Med, 205(2): 491–501

DOI PMID

52
Maisonpierre P C, Belluscio L, Friedman B, Alderson R F, Wiegand S J, Furth M E, Lindsay R M, Yancopoulos G D (1990). NT-3, BDNF, and NGF in the developing rat nervous system: parallel as well as reciprocal patterns of expression. Neuron, 5(4): 501–509

DOI PMID

53
Marques F, Sousa J C, Coppola G, Gao F, Puga R, Brentani H, Geschwind D H, Sousa N, Correia-Neves M, Palha J A (2011). Transcriptome signature of the adult mouse choroid plexus. Fluids Barriers CNS, 8(1): 10

DOI PMID

54
Mashayekhi F, Azari M, Moghadam L M, Yazdankhah M, Naji M, Salehi Z (2009). Changes in cerebrospinal fluid nerve growth factor levels during chick embryonic development. J Clin Neurosci, 16(10): 1334–1337

DOI PMID

55
Mashayekhi F, Sadeghi M, Rajaei F (2011). Induction of perlecan expression and neural cell proliferation by FGF-2 in the developing cerebral cortex: an in vivo study. J Mol Neurosci, 45(2): 87–93

DOI PMID

56
McCoy M K, Tansey M G (2008). TNF signaling inhibition in the CNS: implications for normal brain function and neurodegenerative disease. J Neuroinflammation, 5(1): 45

DOI PMID

57
Meeker R B, Williams K, Killebrew D A, Hudson L C (2012). Cell trafficking through the choroid plexus. Cell Adhes Migr, 6(5): 390–396

DOI PMID

58
Mesquita S D, Ferreira A C, Gao F, Coppola G, Geschwind D H, Sousa J C, Correia-Neves M, Sousa N, Palha J A, Marques F (2015). The choroid plexus transcriptome reveals changes in type I and II interferon responses in a mouse model of Alzheimer’s disease. Brain Behav Immun, 49: 280–292

DOI PMID

59
Miyan J A, Nabiyouni M, Zendah M (2003). Development of the brain: a vital role for cerebrospinal fluid. Can J Physiol Pharmacol, 81(4): 317–328

DOI PMID

60
Moore L, Bain J M, Loh J M, Levison S W (2014). PDGF-responsive progenitors persist in the subventricular zone across the lifespan. ASN Neuro, 6(2): 65–81

DOI PMID

61
Nielsen C M, Dymecki S M (2010). Sonic hedgehog is required for vascular outgrowth in the hindbrain choroid plexus. Dev Biol, 340(2): 430–437

DOI PMID

62
Nilsson C, Hultberg B M, Gammeltoft S (1996). Autocrine role of insulin-like growth factor II secretion by the rat choroid plexus. Eur J Neurosci, 8(3): 629–635

DOI PMID

63
Pencea V, Bingaman K D, Freedman L J, Luskin M B (2001). Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain. Exp Neurol, 172(1): 1–16

DOI PMID

64
Pillai A, Kale A, Joshi S, Naphade N, Raju M S V K, Nasrallah H, Mahadik S P (2010). Decreased BDNF levels in CSF of drug-naive first-episode psychotic subjects: correlation with plasma BDNF and psychopathology. Int J Neuropsychopharmacol, 13(4): 535–539

DOI PMID

65
Prasongchean W, Vernay B, Asgarian Z, Jannatul N, Ferretti P (2015). The neural milieu of the developing choroid plexus: neural stem cells, neurons and innervation. Front Neurosci, 9: 103

DOI PMID

66
Preston J E (2001). Ageing choroid plexus-cerebrospinal fluid system. Microsc Res Tech, 52(1): 31–37

DOI PMID

67
Rabie M A, Mohsen M, Ibrahim M, El-Sawy Mahmoud R (2014). Serum level of brain derived neurotrophic factor (BDNF) among patients with bipolar disorder. J Affect Disord, 162: 67–72

DOI PMID

68
Redzic Z B, Preston J E, Duncan J A, Chodobski A, Szmydynger-Chodobska J (2005). “The Choroid Plexus‐Cerebrospinal Fluid System: From Development to Aging,” in Current Topics in Developmental Biology, ed. Gerald P. Schatten (Academic Press), 1–52. Available at: http://www.sciencedirect.com/science/article/pii/S0070215305710012 [<Date>Accessed November 15, 2013</Date>].

69
Redzic Z B, Segal M B (2004). The structure of the choroid plexus and the physiology of the choroid plexus epithelium. Adv Drug Deliv Rev, 56(12): 1695–1716

DOI PMID

70
Ruiz de Almodovar C, Coulon C, Salin P A, Knevels E, Chounlamountri N, Poesen K, Hermans K, Lambrechts D, Van Geyte K, Dhondt J, Dresselaers T, Renaud J, Aragones J, Zacchigna S, Geudens I, Gall D, Stroobants S, Mutin M, Dassonville K, Storkebaum E, Jordan B F, Eriksson U, Moons L, D’Hooge R, Haigh J J, Belin M F, Schiffmann S, Van Hecke P, Gallez B, Vinckier S, Chédotal A, Honnorat J, Thomasset N, Carmeliet P, Meissirel C (2010). Matrix-binding vascular endothelial growth factor (VEGF) isoforms guide granule cell migration in the cerebellum via VEGF receptor Flk1. J Neurosci, 30(45): 15052–15066

DOI PMID

71
Salehi Z, Mashayekhi F, Naji M, Pandamooz S (2009). Insulin-like growth factor-1 and insulin-like growth factor binding proteins in cerebrospinal fluid during the development of mouse embryos. J Clin Neurosci, 16(7): 950–953

DOI PMID

72
Sathyanesan M, Girgenti M J, Banasr M, Stone K, Bruce C, Guilchicek E, Wilczak-Havill K, Nairn A, Williams K, Sass S, Duman J G, Newton S S (2012). A molecular characterization of the choroid plexus and stress-induced gene regulation. Transl Psychiatry, 2(7): e139

DOI PMID

73
Saunders N R, Daneman R, Dziegielewska K M, Liddelow S A (2013). Transporters of the blood-brain and blood-CSF interfaces in development and in the adult. Mol Aspects Med, 34(2-3): 742–752

DOI PMID

74
Schänzer A, Wachs F P, Wilhelm D, Acker T, Cooper-Kuhn C, Beck H, Winkler J, Aigner L, Plate K H, Kuhn H G (2004). Direct stimulation of adult neural stem cells in vitro and neurogenesis in vivoby vascular endothelial growth factor. Brain Pathol, 14(3): 237–248

DOI PMID

75
Scola G, Andreazza A C (2015). The role of neurotrophins in bipolar disorder. Prog Neuropsychopharmacol Biol Psychiatry, 56: 122–128

DOI PMID

76
Segklia A, Seuntjens E, Elkouris M, Tsalavos S, Stappers E, Mitsiadis T A, Huylebroeck D, Remboutsika E, Graf D (2012). Bmp7 regulates the survival, proliferation, and neurogenic properties of neural progenitor cells during corticogenesis in the mouse. PLoS ONE, 7(3): e34088

DOI PMID

77
Serot J M, Béné M C, Foliguet B, Faure G C (1997). Altered choroid plexus basement membrane and epithelium in late-onset Alzheimer’s disease: an ultrastructural study. Ann N Y Acad Sci, 826(1 Cerebrovascul): 507–509

DOI PMID

78
Serot J M, Foliguet B, Béné M C, Faure G C (2001). Choroid plexus and ageing in rats: a morphometric and ultrastructural study. Eur J Neurosci, 14(5): 794–798

DOI PMID

79
Spatazza J, Lee H H C, Di Nardo A A, Tibaldi L, Joliot A, Hensch T K, Prochiantz A (2013). Choroid-plexus-derived Otx2 homeoprotein constrains adult cortical plasticity. Cell Reports, 3(6): 1815–1823

DOI PMID

80
Spector R, Johanson C E (2010). Vectorial ligand transport through mammalian choroid plexus. Pharm Res, 27(10): 2054–2062

DOI PMID

81
Spector R, Keep R F, Robert Snodgrass S, Smith Q R, Johanson C E (2015a). A balanced view of choroid plexus structure and function: Focus on adult humans. Exp Neurol, 267: 78–86

DOI PMID

82
Spector R, Robert Snodgrass S, Johanson C E (2015b). A balanced view of the cerebrospinal fluid composition and functions: Focus on adult humans. Exp Neurol, 273: 57–68

DOI PMID

83
Stolp H B, Molnár Z (2015). Neurogenic niches in the brain: help and hindrance of the barrier systems. Front Neurosci, 9: 20

DOI PMID

84
Storkebaum E, Carmeliet P (2004). VEGF: a critical player in neurodegeneration. J Clin Invest, 113(1): 14–18

DOI PMID

85
Strazielle N, Mutin M, Ghersi-Egea J F (2005). Les plexus choroïdes: une interface dynamique entre sang et liquide cephalo-rachidien. Morphologie, 89(285): 90–101

DOI PMID

86
Strelau J, Sullivan A, Böttner M, Lingor P, Falkenstein E, Suter-Crazzolara C, Galter D, Jaszai J, Krieglstein K, Unsicker K (2000). Growth/differentiation factor-15/macrophage inhibitory cytokine-1 is a novel trophic factor for midbrain dopaminergic neurons in vivo. J Neurosci, 20(23): 8597–8603

PMID

87
Tochitani S, Kondo S (2013). Immunoreactivity for GABA, GAD65, GAD67 and Bestrophin-1 in the meninges and the choroid plexus: implications for non-neuronal sources for GABA in the developing mouse brain. PLoS ONE, 8(2): e56901

DOI PMID

88
Turner C A, Thompson R C, Bunney W E, Schatzberg A F, Barchas J D, Myers R M, Akil H, Watson S J (2014). Altered choroid plexus gene expression in major depressive disorder. Front Hum Neurosci, 8: 238

DOI PMID

89
Vaccarino F M, Schwartz M L, Raballo R, Nilsen J, Rhee J, Zhou M, Doetschman T, Coffin J D, Wyland J J, Hung Y T (1999). Changes in cerebral cortex size are governed by fibroblast growth factor during embryogenesis. Nat Neurosci, 2(3): 246–253

DOI PMID

90
Wagner J P, Black I B, DiCicco-Bloom E (1999). Stimulation of neonatal and adult brain neurogenesis by subcutaneous injection of basic fibroblast growth factor. J Neurosci, 19(14): 6006–6016

PMID

91
Watanabe M, Kang Y J, Davies L M, Meghpara S, Lau K, Chung C Y, Kathiriya J, Hadjantonakis A K, Monuki E S (2012). BMP4 sufficiency to induce choroid plexus epithelial fate from embryonic stem cell-derived neuroepithelial progenitors. J Neurosci, 32(45): 15934–15945

DOI PMID

92
Werner H, LeRoith D (2014). Insulin and insulin-like growth factor receptors in the brain: physiological and pathological aspects. Eur Neuropsychopharmacol, 24(12): 1947–1953

DOI PMID

93
Xia Y X, Ikeda T, Xia X Y, Ikenoue T (2000). Differential neurotrophin levels in cerebrospinal fluid and their changes during development in newborn rat. Neurosci Lett, 280(3): 220–222

DOI PMID

94
Zappaterra M W, Lehtinen M K (2012). The cerebrospinal fluid: regulator of neurogenesis, behavior, and beyond. Cell Mol Life Sci, 69(17): 2863–2878

DOI PMID

95
Ziegler A N, Levison S W, Wood T L (2015). Insulin and IGF receptor signalling in neural-stem-cell homeostasis. Nat Rev Endocrinol, 11(3): 161–170

DOI PMID

96
Ziegler A N, Schneider J S, Qin M, Tyler W A, Pintar J E, Fraidenraich D, Wood T L, Levison S W (2012). IGF-II promotes stemness of neural restricted precursors. Stem Cells, 30(6): 1265–1276

DOI PMID

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