The molecular basis of the cooperation between EGF, FGF and eCB receptors in the regulation of neural stem cell function

Molecular and Cellular Neuroscience

Volumn 52, Issue , 2013, Pages 20-30

  Sütterlin, Philipp ^a   Williams, Emma J ^a   Chambers, David ^a   Saraf, Kathryn ^c   von Schack, David ^b   Reisenberg, Melina ^a   Doherty, Patrick ^a   Williams, Gareth ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b PFIZER GLOBAL RESEARCH AND DEVELOPMENT   (United Kingdom)

^c PFIZER INC   (United States)

Author keywords

EGF; Endocannabinoid; ERK; FGF; Neural stem cells; Neurogenesis

Indexed keywords

ACTIN; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C GAMMA; PROTEIN KINASE B; TRANSCRIPTOME;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; RECEPTOR UPREGULATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ADULT STEM CELLS; ANIMALS; BLOTTING, WESTERN; CELL LINE; ENDOCANNABINOIDS; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTORS; MICE; NEURAL STEM CELLS; NEUROGENESIS; PROTEIN ARRAY ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 84870330631     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2012.10.006     Document Type: Article

References (64)

1. Aguado T., Monory K., Palazuelos J., Stella N., Cravatt B., Lutz B., Marsicano G., Kokaia Z., Guzman M., Galve-Roperh I. The endocannabinoid system drives neural progenitor proliferation. FASEB J. 2005, 19:1704-1706.
2. Alessi D.R., Cuenda A., Cohen P., Dudley D.T., Saltiel A.R. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J. Biol. Chem. 1995, 270:27489-27494.
3. Callen L., Moreno E., Barroso-Chinea P., Moreno-Delgado D., Cortes A., Mallol J., Casado V., Lanciego J.L., Franco R., Lluis C., Canela E.I., McCormick P.J. Cannabinoid receptors CB1 and CB2 form functional heteromers in brain. J. Biol. Chem. 2012, 287:20851-20865.
4. Capdevila J., Elez E., Macarulla T., Ramos F.J., Ruiz-Echarri M., Tabernero J. Anti-epidermal growth factor receptor monoclonal antibodies in cancer treatment. Cancer Treat. Rev. 2009, 35:354-363.
5. Choi Y.S., Cho H.Y., Hoyt K.R., Naegele J.R., Obrietan K. IGF-1 receptor-mediated ERK/MAPK signaling couples status epilepticus to progenitor cell proliferation in the subgranular layer of the dentate gyrus. Glia 2008, 56:791-800.
6. Ciccolini F., Svendsen C.N. Fibroblast growth factor 2 (FGF-2) promotes acquisition of epidermal growth factor (EGF) responsiveness in mouse striatal precursor cells: identification of neural precursors responding to both EGF and FGF-2. J. Neurosci. 1998, 18:7869-7880.
7. Conti L., Pollard S.M., Gorba T., Reitano E., Toselli M., Biella G., Sun Y., Sanzone S., Ying Q.L., Cattaneo E., Smith A. Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol. 2005, 3:e283.
8. Craig C.G., Tropepe V., Morshead C.M., Reynolds B.A., Weiss S., van der Kooy D. In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J. Neurosci. 1996, 16:2649-2658.
9. Cunningham J.T., Rodgers J.T., Arlow D.H., Vazquez F., Mootha V.K., Puigserver P. mTOR controls mitochondrial oxidative function through a YY1-PGC-1alpha transcriptional complex. Nature 2007, 450:736-740.
10. de Graauw M., Hensbergen P., van de Water B. Phospho-proteomic analysis of cellular signaling. Electrophoresis 2006, 27:2676-2686.
11. Doetsch F. A niche for adult neural stem cells. Curr. Opin. Genet. Dev. 2003, 13:543-550.
12. Doetsch F., Petreanu L., Caille I., Garcia-Verdugo J.M., Alvarez-Buylla A. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 2002, 36:1021-1034.
13. Dougherty J.D., Garcia A.D., Nakano I., Livingstone M., Norris B., Polakiewicz R., Wexler E.M., Sofroniew M.V., Kornblum H.I., Geschwind D.H. PBK/TOPK, a proliferating neural progenitor-specific mitogen-activated protein kinase kinase. J. Neurosci. 2005, 25:10773-10785.
14. Felder C.C., Joyce K.E., Briley E.M., Glass M., Mackie K.P., Fahey K.J., Cullinan G.J., Hunden D.C., Johnson D.W., Chaney M.O., Koppel G.A., Brownstein M. LY320135, a novel cannabinoid CB1 receptor antagonist, unmasks coupling of the CB1 receptor to stimulation of cAMP accumulation. J. Pharmacol. Exp. Ther. 1998, 284:291-297.
15. Frinchi M., Bonomo A., Trovato-Salinaro A., Condorelli D.F., Fuxe K., Spampinato M.G., Mudo G. Fibroblast growth factor-2 and its receptor expression in proliferating precursor cells of the subventricular zone in the adult rat brain. Neurosci. Lett. 2008, 447:20-25.
16. Fry D.W., Bridges A.J., Denny W.A., Doherty A., Greis K.D., Hicks J.L., Hook K.E., Keller P.R., Leopold W.R., Loo J.A., McNamara D.J., Nelson J.M., Sherwood V., Smaill J.B., Trumpp-Kallmeyer S., Dobrusin E.M. Specific, irreversible inactivation of the epidermal growth factor receptor and erbB2, by a new class of tyrosine kinase inhibitor. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:12022-12027.
17. Gao Y., Vasilyev D.V., Goncalves M.B., Howell F.V., Hobbs C., Reisenberg M., Shen R., Zhang M.Y., Strassle B.W., Lu P., Mark L., Piesla M.J., Deng K., Kouranova E.V., Ring R.H., Whiteside G.T., Bates B., Walsh F.S., Williams G., Pangalos M.N., Samad T.A., Doherty P. Loss of retrograde endocannabinoid signaling and reduced adult neurogenesis in diacylglycerol lipase knock-out mice. J. Neurosci. 2010, 30:2017-2024.
18. Gatley S.J., Gifford A.N., Volkow N.D., Lan R., Makriyannis A. 123I-labeled AM251: a radioiodinated ligand which binds in vivo to mouse brain cannabinoid CB1 receptors. Eur. J. Pharmacol. 1996, 307:331-338.
19. Gauthier L.R., Charrin B.C., Borrell-Pages M., Dompierre J.P., Rangone H., Cordelieres F.P., De Mey J., MacDonald M.E., Lessmann V., Humbert S., Saudou F. Huntingtin controls neurotrophic support and survival of neurons by enhancing BDNF vesicular transport along microtubules. Cell 2004, 118:127-138.
20. Glaser T., Pollard S.M., Smith A., Brustle O. Tripotential differentiation of adherently expandable neural stem (NS) cells. PLoS One 2007, 2:e298.
21. Gobert R.P., Joubert L., Curchod M.L., Salvat C., Foucault I., Jorand-Lebrun C., Lamarine M., Peixoto H., Vignaud C., Fremaux C., Jomotte T., Francon B., Alliod C., Bernasconi L., Abderrahim H., Perrin D., Bombrun A., Zanoguera F., Rommel C., Hooft van Huijsduijnen R. Convergent functional genomics of oligodendrocyte differentiation identifies multiple autoinhibitory signaling circuits. Mol. Cell. Biol. 2009, 29:1538-1553.
22. Goncalves M.B., Suetterlin P., Yip P., Molina-Holgado F., Walker D.J., Oudin M.J., Zentar M.P., Pollard S., Yanez-Munoz R.J., Williams G., Walsh F.S., Pangalos M.N., Doherty P. A diacylglycerol lipase-CB2 cannabinoid pathway regulates adult subventricular zone neurogenesis in an age-dependent manner. Mol. Cell. Neurosci. 2008, 38:526-536.
23. Howlett A.C., Barth F., Bonner T.I., Cabral G., Casellas P., Devane W.A., Felder C.C., Herkenham M., Mackie K., Martin B.R., Mechoulam R., Pertwee R.G. International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol. Rev. 2002, 54:161-202.
24. Huang H.C., Klein P.S. The Frizzled family: receptors for multiple signal transduction pathways. Genome Biol. 2004, 5:234.
25. Iwamura H., Suzuki H., Ueda Y., Kaya T., Inaba T. In vitro and in vivo pharmacological characterization of JTE-907, a novel selective ligand for cannabinoid CB2 receptor. J. Pharmacol. Exp. Ther. 2001, 296:420-425.
26. Jiang W., Zhang Y., Xiao L., Van Cleemput J., Ji S.P., Bai G., Zhang X. Cannabinoids promote embryonic and adult hippocampus neurogenesis and produce anxiolytic- and antidepressant-like effects. J. Clin. Investig. 2005, 115:3104-3116.
27. Jin K., Sun Y., Xie L., Batteur S., Mao X.O., Smelick C., Logvinova A., Greenberg D.A. Neurogenesis and aging: FGF-2 and HB-EGF restore neurogenesis in hippocampus and subventricular zone of aged mice. Aging Cell 2003, 2:175-183.
28. Jin Z., Luo R., Piao X. Chapter 1 GPR56 and its related diseases. Prog. Mol. Biol. Transl. Sci. 2009, 89C:1-13.
29. Jonsson M., Andersson T. Repression of Wnt-5a impairs DDR1 phosphorylation and modifies adhesion and migration of mammary cells. J. Cell Sci. 2001, 114:2043-2053.
30. Kriegstein A., Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells. Annu. Rev. Neurosci. 2009, 32:149-184.
31. Kuhn H.G., Winkler J., Kempermann G., Thal L.J., Gage F.H. Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J. Neurosci. 1997, 17:5820-5829.
32. Lamb J., Crawford E.D., Peck D., Modell J.W., Blat I.C., Wrobel M.J., Lerner J., Brunet J.P., Subramanian A., Ross K.N., Reich M., Hieronymus H., Wei G., Armstrong S.A., Haggarty S.J., Clemons P.A., Wei R., Carr S.A., Lander E.S., Golub T.R. The Connectivity Map: using gene-expression signatures to connect small molecules, genes, and disease. Science 2006, 313:1929-1935.
33. Learish R.D., Bruss M.D., Haak-Frendscho M. Inhibition of mitogen-activated protein kinase kinase blocks proliferation of neural progenitor cells. Brain Res. Dev. Brain Res. 2000, 122:97-109.
34. Levitzki A., Gazit A. Tyrosine kinase inhibition: an approach to drug development. Science 1995, 267:1782-1788.
35. Ma D.K., Ponnusamy K., Song M.R., Ming G.L., Song H. Molecular genetic analysis of FGFR1 signalling reveals distinct roles of MAPK and PLCgamma1 activation for self-renewal of adult neural stem cells. Mol. Brain 2009, 2:16.
36. Maison P., Walker D.J., Walsh F.S., Williams G., Doherty P. BDNF regulates neuronal sensitivity to endocannabinoids. Neurosci. Lett. 2009, 467:90-94.
37. McAllister S.D., Glass M. CB(1) and CB(2) receptor-mediated signalling: a focus on endocannabinoids. Prostaglandins Leukot. Essent. Fatty Acids 2002, 66:161-171.
38. Mercier F., Kitasako J.T., Hatton G.I. Anatomy of the brain neurogenic zones revisited: fractones and the fibroblast/macrophage network. J. Comp. Neurol. 2002, 451:170-188.
39. Mohammadi M., Froum S., Hamby J.M., Schroeder M.C., Panek R.L., Lu G.H., Eliseenkova A.V., Green D., Schlessinger J., Hubbard S.R. Crystal structure of an angiogenesis inhibitor bound to the FGF receptor tyrosine kinase domain. EMBO J. 1998, 17:5896-5904.
40. Molina-Holgado F., Rubio-Araiz A., Garcia-Ovejero D., Williams R.J., Moore J.D., Arevalo-Martin A., Gomez-Torres O., Molina-Holgado E. CB2 cannabinoid receptors promote mouse neural stem cell proliferation. Eur. J. Neurosci. 2007, 25:629-634.
41. Morshead C.M., Reynolds B.A., Craig C.G., McBurney M.W., Staines W.A., Morassutti D., Weiss S., van der Kooy D. Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 1994, 13:1071-1082.
42. Nusse R. Wnt signaling and stem cell control. Cell Res. 2008, 18:523-527.
43. Oudin M.J., Gajendra S., Williams G., Hobbs C., Lalli G., Doherty P. Endocannabinoids regulate the migration of subventricular zone-derived neuroblasts in the postnatal brain. J. Neurosci. 2011, 31:4000-4011.
44. Oudin M.J., Hobbs C., Doherty P. DAGL-dependent endocannabinoid signalling: roles in axonal pathfinding, synaptic plasticity and adult neurogenesis. Eur. J. Neurosci. 2011, 34:1634-1646.
45. Palazuelos J., Aguado T., Egia A., Mechoulam R., Guzman M., Galve-Roperh I. Non-psychoactive CB2 cannabinoid agonists stimulate neural progenitor proliferation. FASEB J. 2006, 20:2405-2407.
46. Palazuelos J., Ortega Z., Diaz-Alonso J., Guzman M., Galve-Roperh I. CB2 cannabinoid receptors promote neural progenitor cell proliferation via mTORC1 signaling. J. Biol. Chem. 2012, 287:1198-1209.
47. Pertwee R., Griffin G., Fernando S., Li X., Hill A., Makriyannis A. AM630, a competitive cannabinoid receptor antagonist. Life Sci. 1995, 56:1949-1955.
48. Pollard S., Conti L., Smith A. Exploitation of adherent neural stem cells in basic and applied neurobiology. Regen. Med. 2006, 1:111-118.
49. Pollard S.M., Conti L., Sun Y., Goffredo D., Smith A. Adherent neural stem (NS) cells from fetal and adult forebrain. Cereb. Cortex 2006, 16(Suppl. 1):i112-i120.
50. Riquelme P.A., Drapeau E., Doetsch F. Brain micro-ecologies: neural stem cell niches in the adult mammalian brain. Philosophical transactions of the Royal Society of London. Series B. Biol. Sci. 2008, 363:123-137.
51. Rozenfeld R., Bushlin I., Gomes I., Tzavaras N., Gupta A., Neves S., Battini L., Gusella G.L., Lachmann A., Ma'ayan A., Blitzer R.D., Devi L.A. Receptor heteromerization expands the repertoire of cannabinoid signaling in rodent neurons. PLoS One 2012, 7:e29239.
52. Samuels I.S., Karlo J.C., Faruzzi A.N., Pickering K., Herrup K., Sweatt J.D., Saitta S.C., Landreth G.E. Deletion of ERK2 mitogen-activated protein kinase identifies its key roles in cortical neurogenesis and cognitive function. J. Neurosci. 2008, 28:6983-6995.
53. Skaper S.D., Kee W.J., Facci L., Macdonald G., Doherty P., Walsh F.S. The FGFR1 inhibitor PD 173074 selectively and potently antagonizes FGF-2 neurotrophic and neurotropic effects. J. Neurochem. 2000, 75:1520-1527.
54. Sui X., Krantz S.B., You M., Zhao Z. Synergistic activation of MAP kinase (ERK1/2) by erythropoietin and stem cell factor is essential for expanded erythropoiesis. Blood 1998, 92:1142-1149.
55. Sun Y., Pollard S., Conti L., Toselli M., Biella G., Parkin G., Willatt L., Falk A., Cattaneo E., Smith A. Long-term tripotent differentiation capacity of human neural stem (NS) cells in adherent culture. Mol. Cell. Neurosci. 2008, 38:245-258.
56. Tropepe V., Craig C.G., Morshead C.M., van der Kooy D. Transforming growth factor-alpha null and senescent mice show decreased neural progenitor cell proliferation in the forebrain subependyma. J. Neurosci. 1997, 17:7850-7859.
57. Turner N., Grose R. Fibroblast growth factor signalling: from development to cancer. Nat. Rev. Cancer 2010, 10:116-129.
58. Williams, G., A searchable cross-platform gene expression database reveals connections between drug treatments and disease. BMC Genomics 13, 12.
59. Williams E.J., Doherty P. Evidence for and against a pivotal role of PI 3-kinase in a neuronal cell survival pathway [published erratum appears in Mol Cell Neurosci 2000 Mar;15(3):330]. Mol. Cell. Neurosci. 1999, 13:272-280.
60. Williams E.J., Walsh F.S., Doherty P. The FGF receptor uses the endocannabinoid signaling system to couple to an axonal growth response. J. Cell Biol. 2003, 160:481-486.
61. Wolfer, A., Wittner, B.S., Irimia, D., Flavin, R.J., Lupien, M., Gunawardane, R.N., Meyer, C.A., Lightcap, E.S., Tamayo, P., Mesirov, J.P., Liu, X.S., Shioda, T., Toner, M., Loda, M., Brown, M., Brugge, J.S., Ramaswamy, S., MYC regulation of a "poor-prognosis" metastatic cancer cell state. Proc. Natl. Acad. Sci. U. S. A. 107, 3698-3703.
62. Yamamoto T., Ebisuya M., Ashida F., Okamoto K., Yonehara S., Nishida E. Continuous ERK activation downregulates antiproliferative genes throughout G1 phase to allow cell-cycle progression. Curr. Biol. 2006, 16:1171-1182.
63. Zhao C., Deng W., Gage F.H. Mechanisms and functional implications of adult neurogenesis. Cell 2008, 132:645-660.
64. Zheng W., Nowakowski R.S., Vaccarino F.M. Fibroblast growth factor 2 is required for maintaining the neural stem cell pool in the mouse brain subventricular zone. Dev. Neurosci. 2004, 26:181-196.