Nerve growth factor induces cell cycle arrest of astrocytes

Developmental Neurobiology

Volumn 72, Issue 6, 2012, Pages 766-776

  Cragnolini, Andrea B ^a,b   Volosin, Marta ^a   Huang, Yangyang ^a,c   Friedman, Wilma J ^a  

^a RUTGERS UNIVERSITY   (United States)

^b UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

^c RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Astrocyte; Cell cycle; Nerve growth factor; P75 NTR; Proliferation

Indexed keywords

CYCLIN D1; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE 4; CYCLIN E; PILOCARPINE; PROTEIN P75; PROTEIN TYROSINE KINASE A; RECOMBINANT EPIDERMAL GROWTH FACTOR; RECOMBINANT NERVE GROWTH FACTOR; TYROSINE KINASE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; IMMUNOCYTOCHEMISTRY; MALE; NERVE CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; RAT; SEIZURE; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; ASTROCYTES; CELL CYCLE; CELL CYCLE CHECKPOINTS; CELLS, CULTURED; CYCLIN-DEPENDENT KINASES; EPIDERMAL GROWTH FACTOR; NERVE GROWTH FACTOR; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, NERVE GROWTH FACTOR;

EID: 84860898313     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.20981     Document Type: Article

References (68)

1. Aprelikova O, Xiong Y, Liu ET. 1995. Both p16 and p21 families of cyclin-dependent kinase (CDK) inhibitors block the phosphorylation of cyclin-dependent kinases by the CDK-activating kinase. J Biol Chem 270: 18195-18197.
2. Bai S, Datta J, Jacob ST, Ghoshal K. 2007. Treatment of PC12 cells with nerve growth factor induces proteasomal degradation of T-cadherin that requires tyrosine phosphorylation of its cadherin domain. J Biol Chem 282: 27171-27180.
3. Barker PA. 2004. p75NTR is positively promiscuous: Novel partners and new insights. Neuron 42: 529-533.
4. Berkemeier LR, Winslow JW, Kaplan DR, Nikolics K, Goeddel DV, Rosenthal A. 1991. Neurotrophin-5: A novel neurotrophic factor that activates trk and trkB. Neuron 7: 857-866.
5. Besson A, Dowdy SF, Roberts JM. 2008. CDK inhibitors: Cell cycle regulators and beyond. Dev Cell 14: 159-169.
6. Bramanti V, Campisi A, Tomassoni D, Costa A, Fisichella A, Mazzone V, Denaro L, Avitabile M, Amenta F, Avola R. 2007. Astroglial-conditioned media and growth factors modulate proliferation and differentiation of astrocytes in primary culture. Neurochem Res 32: 49-56.
7. Canepa ET, Scassa ME, Ceruti JM, Marazita MC, Carcagno AL, Sirkin PF, Ogara MF. 2007. INK4 proteins, a family of mammalian CDK inhibitors with novel biological functions. IUBMB Life 59: 419-426.
8. Chao MV. 1994. The p75 neurotrophin receptor. J Neurobiol 25: 1373-1385.
9. Chao MV. 2003. Neurotrophins and their receptors: A convergence point for many signalling pathways. Nat Rev Neurosci 4: 299-309.
10. Chittka A, Arevalo J, Rodriguez-Guzman M, Perez P, Chao M, Sendtner M. 2004. The p75NTR-interacting protein SC1 inhibits cell cycle progression by transcriptional repression of cyclin E. J Cell Biol 164: 985-996.
11. Chittka A, Chao MV. 1999. Identification of a zinc finger protein whose subcellular distribution is regulated by serum and nerve growth factor. Proc Natl Acad Sci U S A 96: 10705-10710.
12. Cirillo G, Cavaliere C, Bianco MR, De Simone A, Colangelo AM, Sellitti S, Alberghina L, Papa M. 2010. Intrathecal NGF administration reduces reactive astrocytosis and changes neurotrophin receptors expression pattern in a rat model of neuropathic pain. Cell Mol Neurobiol 30: 51-62.
13. Cirillo G, Colangelo AM, Bianco MR, Cavaliere C, Zaccaro L, Sarmientos P, Alberghina L, Papa M. 2011. BB14, a Nerve Growth Factor (NGF)-like peptide shown to be effective in reducing reactive astrogliosis and restoring synaptic homeostasis in a rat model of peripheral nerve injury. Biotechnol Adv.
14. Cragnolini AB, Huang Y, Gokina P, Friedman WJ. 2009. Nerve growth factor attenuates proliferation of astrocytes via the p75 neurotrophin receptor. Glia 57: 1386-1392.
15. Evangelopoulos ME, Weis J, Kruttgen A. 2004. Neurotrophin effects on neuroblastoma cells: Correlation with trk and p75NTR expression and influence of Trk receptor bodies. J Neurooncol 66: 101-110.
16. Friedman WJ. 2000. Neurotrophins induce death of hippocampal neurons via the p75 receptor. J Neurosci 20: 6340-6346.
17. Friedman WJ, Thakur S, Seidman L, Rabson AB. 1996. Regulation of nerve growth factor mRNA by interleukin-1 in rat hippocampal astrocytes is mediated by NFkB. J Biol Chem 271: 31115-31120.
18. Gigliozzi A, Alpini G, Baroni GS, Marucci L, Metalli VD, Glaser SS, Francis H, Mancino MG, Ueno Y, Barbaro B, Benedetti A, Attili AF, Alvaro D. 2004. Nerve growth factor modulates the proliferative capacity of the intrahepatic biliary epithelium in experimental cholestasis. Gastroenterology 127: 1198-1209.
19. Greene LA, Tischler AS. 1976. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci U S A 73: 2424-2428.
20. Hallböök F, Ibanez CF, Persson H. 1991. Evolutionary studies of the nerve growth factor family reveal a novel member abundantly expressed in Xenopus ovary. Neuron 6: 845-858.
21. Hanbury R, Charles V, Chen EY, Leventhal L, Rosenstein JM, Mufson EJ, Kordower JH. 2002. Excitotoxic and metabolic damage to the rodent striatum: Role of the P75 neurotrophin receptor and glial progenitors. J Comp Neurol 444: 291-305.
22. Hohn A, Leibrock J, Bailey K, Barde Y-A. 1990. Identification and characterization of a novel member of the nerve growth factor/brain-derived neurotrophic factor family. Nature 344: 339-341.
23. Huang EJ, Reichardt LF. 2003. Trk receptors: Roles in neuronal signal transduction. Annu Rev Biochem 72: 609-642.
24. Huff KR, Schreier W. 1989. Fibroblast growth factor pretreatment reduces epidermal growth factor-induced proliferation in rat astrocytes. Life Sci 45: 1515-1520.
25. Hutton LA, deVellis J, Perez-Polo JR. 1992. Expression of p75NGFR TrkA, and TrkB mRNA in rat C6 glioma and type I astrocyte cultures. J Neurosci Res 32: 375-383.
26. Ito H, Nomoto H, Furukawa S. 2003. Growth arrest of PC12 cells by nerve growth factor is dependent on the phosphatidylinositol 3-kinase/Akt pathway via p75 neurotrophin receptor. J Neurosci Res 72: 211-217.
27. Jin H, Pan Y, Zhao L, Zhai H, Li X, Sun L, He L, Chen Y, Hong L, Du Y, Fan D. 2007. p75 neurotrophin receptor suppresses the proliferation of human gastric cancer cells. Neoplasia 9: 471-478.
28. Khursigara G, Bertin J, Yano H, DiStefano PS, Chao MV. 2001. A pro-survival function for the p75 receptor death domain mediated through the CARD protein RIP2. J Neurosci 21: 5854-5863.
29. Khwaja F, Djakiew D. 2003. Inhibition of cell-cycle effectors of proliferation in bladder tumor epithelial cells by the p75NTR tumor suppressor. Mol Carcinog 36: 153-160.
30. Krygier S, Djakiew D. 2001. Molecular characterization of the loss of p75(NTR) expression in human prostate tumor cells. Mol Carcinog 31: 46-55.
31. Krygier S, Djakiew D. 2002. Neurotrophin receptor p75(NTR) suppresses growth and nerve growth factor-mediated metastasis of human prostate cancer cells. Int J Cancer 98: 1-7.
32. Lambert WS, Clark AF, Wordinger RJ. 2004. Effect of exogenous neurotrophins on Trk receptor phosphorylation, cell proliferation, and neurotrophin secretion by cells isolated from the human lamina cribrosa. Mol Vis 10: 289-296.
33. Leibrock J, Lottspeich F, Hohn A, Hofer M, Hengerer B, Masiakowski P, Thoenen H, Barde Y-A. 1989. Molecular cloning and expression of brain-derived neurotrophic factor. Nature 341: 149-152.
34. Levi-Montalcini R. 1987. The nerve growth factor 35 years later. Science 237: 1154-1162.
35. Levi-Montalcini R, Angeletti PU. 1968. The nerve growth factor. Physiol Rev 48: 534-569.
36. Maisonpierre PC, Belluscio L, Squinto S, Ip NY, Furth ME, Lindsay RM, Yancopoulos GD. 1990. Neurotrophin-3: A neurotrophic factor related to NGF and BDNF. Science 247: 1446-1451.
37. Mann GJ, Musgrove EA, Fox RM, Thelander L. 1988. Ribonucleotide reductase M1 subunit in cellular proliferation, quiescence, and differentiation. Cancer Res 48: 5151-5156.
38. McCarthy KD, DeVellis J. 1980. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85: 890-902.
39. Montagnoli A, Fiore F, Eytan E, Carrano AC, Draetta GF, Hershko A, Pagano M. 1999. Ubiquitination of p27 is regulated by Cdk-dependent phosphorylation and trimeric complex formation. Genes Dev 13: 1181-9.
40. Moser KV, Reindl M, Blasig I, Humpel C. 2004. Brain capillary endothelial cells proliferate in response to NGF, express NGF receptors and secrete NGF after inflammation. Brain Res 1017: 53-60.
41. Munz B, Hildt E, Springer ML, Blau HM. 2002. RIP2, a checkpoint in myogenic differentiation. Mol Cell Biol 22: 5879-5886.
42. O'Connor PM. 1997. Mammalian G1 and G2 phase checkpoints. Cancer Surv 29: 151-182.
43. Obaya AJ, Sedivy JM. 2002. Regulation of cyclin-Cdk activity in mammalian cells. Cell Mol Life Sci 59: 126-142.
44. Oderfeld-Nowak B, Bacia A. 1994. Expression of astroglial nerve growth factor in damaged brain. Acta Neurobiol Exp 54: 73-80.
45. Parkhurst CN, Zampieri N, Chao MV. 2010. Nuclear localization of the p75 neurotrophin receptor intracellular domain. J Biol Chem 285: 5361-5368.
46. Patapoutian A, Reichardt LF. 2001. Trk receptors: Mediators of neurotrophin action. Curr Opin Neurobiol 11: 272-280.
47. Pierchala BA, Tsui CC, Milbrandt J, Johnson EM. 2007. NGF augments the autophosphorylation of Ret via inhibition of ubiquitin-dependent degradation. J Neurochem 100: 1169-1176.
48. Pincheira R, Baerwald M, Dunbar JD, Donner DB. 2009. Sall2 is a novel p75NTR-interacting protein that links NGF signalling to cell cycle progression and neurite outgrowth. EMBO J 28: 261-273.
49. Ren QG, Yu Y, Luo X, Jie XM, Pan DJ, Wang W. 2009. Characterization of proteasome inhibition on astrocytes cell cycle. J Mol Neurosci 38: 57-66.
50. Rosenthal A, Goeddel DV, Nguyen T, Lewis M, Shih A, Laramee GR, Nikolics K, Winslow JW. 1990. Primary structure and biological activity of a novel human neurotrophic factor. Neuron 4: 767-773.
51. Rudge JS, Li Y, Pasnikowski EM, Mattson K, Pan L, Yancopoulos GD, Wiegand SJ, Lindsay RM, Ip NY. 1994. Neurotrophic factor receptors and their signal transduction capabilities in rat astrocytes. Eur J Neurosci 6: 693-705.
52. Satyanarayana A, Kaldis P. 2009. Mammalian cell-cycle regulation: Several Cdks, numerous cyclins and diverse compensatory mechanisms. Oncogene 28: 2925-2939.
53. Semkova I, Krieglstein J. 1999. Ciliary neurotrophic factor enhances the expression of NGF and p75 low-affinity NGF receptor in astrocytes. Brain Res 838: 184-192.
54. Serrano M, Hannon GJ, Beach D. 1993. A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature 366: 704-707.
55. Sherr CJ. 1993. Mammalian G1 cyclins. Cell 73: 1059-1065.
56. Sherr CJ. D-type cyclins. 1995. Trends Biochem Sci 20: 187-90.
57. Sherr CJ, Roberts JM. 1999. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 13: 1501-12.
58. Sherr CJ, Roberts JM. 1995. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev 9: 1149-1163.
59. Toyoshima H, Hunter T. 1994. p27, a novel inhibitor of G1 cyclin-Cdk protein kinase activity, is related to p21. Cell 78: 67-74.
60. Urdiales JL, Becker E, Andrieu M, Thomas A, Jullien J, van Grunsven LA, Menut S, Evan GI, Martin-Zanca D, Rudkin BB. 1998. Cell cycle phase-specific surface expression of nerve growth factor receptors TrkA and p75(NTR). J Neurosci 18: 6767-6775.
61. van Grunsven LA, Thomas A, Urdiales JL, Machenaud S, Choler P, Durand I, Rudkin BB. 1996. Nerve growth factor-induced accumulation of PC12 cells expressing cyclin D1: Evidence for a G1 phase block. Oncogene 12: 855-862.
62. Vervoorts J, Luscher B. 2008. Post-translational regulation of the tumor suppressor p27(KIP1). Cell Mol Life Sci 65: 3255-3264.
63. Vilar M, Murillo-Carretero M, Mira H, Magnusson K, Besset V, Ibanez CF. 2006. Bex1, a novel interactor of the p75 neurotrophin receptor, links neurotrophin signaling to the cell cycle. EMBO J 25: 1219-1230.
64. Watanabe T, Katayama Y, Kimura S, Yoshino A. 1999. Control of proliferation and survival of C6 glioma cells with modification of the nerve growth factor autocrine system. J Neurooncol 41: 121-128.
65. Woo CW, Lucarelli E, Thiele CJ. 2004. NGF activation of TrkA decreases N-myc expression via MAPK path leading to a decrease in neuroblastoma cell number. Oncogene 23: 1522-1530.
66. Wooten MW, Geetha T. 2006. The role of ubiquitin in neurotrophin receptor signalling and sorting. Biochem Soc Trans 34: 757-760.
67. Zhang J, Geula C, Lu C, Koziel H, Hatcher LM, Roisen FJ. 2003. Neurotrophins regulate proliferation and survival of two microglial cell lines in vitro. Exp Neurol 183: 469-481.
68. Zhu H, Dahlstrom A, Hansson HA. 2005. Characterization of cell proliferation in the adult dentate under normal conditions and after kainate induced seizures using ribonucleotide reductase and BrdU. Brain Res 1036: 7-17.