Skip to main content

Advertisement

SpringerLink
Log in

Differentiation of Neuroblastoma Cell Line N1E-115 Involves Several Signaling Cascades

  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

No systematic searches for differential expression of signaling proteins (SP) in undifferentiated vs. differentiated cell lineages were published and herein we used protein profiling for this purpose. The N1E-115 cell line was cultivated and an aliquot was differentiated with dimethylsulfoxide (DMSO), that is known to lead to a neuronal phenotype. Cell lysates were prepared, run on two-dimensional gel electrophoresis followed by MALDI-TOF-TOF identification of proteins and maps of identified SPs were generated. Seven SPs were comparable, 27 SPs: GTP-binding/Ras-related proteins, kinases, growth factors, calcium binding proteins, phosphatase-related proteins were observed in differentiated N1E-115 cells and eight SPs of the groups mentioned above were observed in undifferentiated cells only. Switching-on/off of several individual SPs from different signaling cascades during the differentiation process is a key to understand mechanisms involved. The findings reported herein are challenging in vitro and in vivo studies to confirm a functional role for deranged SPs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. K. L. Ferguson R. S. Slack (2003) ArticleTitleGrowth factors: can they promote neurogenesis? Trends Neurosci 26 283–285 Occurrence Handle1:CAS:528:DC%2BD3sXksVyqtbc%3D Occurrence Handle12798593

    CAS  PubMed  Google Scholar 

  2. S. Fagerstrom S. Pahlman C. Gestblom E. Nanberg (1996) ArticleTitleProtein kinase C-epsilon is implicated in neurite outgrowth in differentiating human neuroblastoma cells Cell Growth Differ 7 775–785 Occurrence Handle1:STN:280:BymA2svms1A%3D Occurrence Handle8780891

    CAS  PubMed  Google Scholar 

  3. S. Fagerstrom S. Pahlman E. Nanberg (1998) ArticleTitleProtein kinase C-dependent tyrosine phosphorylation of p130cas in differentiating neuroblastoma cells J. Biol. Chem 273 2336–2343 Occurrence Handle1:CAS:528:DyaK1cXnsVOrtQ%3D%3D Occurrence Handle9442079

    CAS  PubMed  Google Scholar 

  4. G. Kim Y. Choe J. Park S. Cho K. Kim (2002) ArticleTitleActivation of protein kinase A induces neuronal differentiation of HiB5 hippocampal progenitor cells Brain Res. Mol. Brain Res 109 134–145 Occurrence Handle1:CAS:528:DC%2BD3sXivVCgsg%3D%3D Occurrence Handle12531523

    CAS  PubMed  Google Scholar 

  5. S. O. Yoon S. P. Soltoff M. V. Chao (1997) ArticleTitleA dominant role of the juxtamembrane region of the TrkA nerve growth factor receptor during neuronal cell differentiation J. Biol. Chem 272 23231–23238 Occurrence Handle1:CAS:528:DyaK2sXmt1Wisr8%3D Occurrence Handle9287331

    CAS  PubMed  Google Scholar 

  6. A. Shimada C. A. Mason M. E. Morrison (1998) ArticleTitleTrkB signaling modulates spine density and morphology independent of dendrite structure in cultured neonatal Purkinje cells J. Neurosci 18 8559–8570 Occurrence Handle1:CAS:528:DyaK1cXntFOltLg%3D Occurrence Handle9786964

    CAS  PubMed  Google Scholar 

  7. E. A. Gryz S. O. Meakin (2000) ArticleTitleAcidic substitution of the activation loop tyrosines in TrkA supports nerve growth factor-independent cell survival and neuronal differentiation Oncogene 19 417–430 Occurrence Handle1:CAS:528:DC%2BD3cXpvVSmtA%3D%3D Occurrence Handle10656690

    CAS  PubMed  Google Scholar 

  8. A. Eggert N. Ikegaki X. Liu T. T. Chou V. M. Lee J. Q. Trojanowski G.M. Brodeur (2000) ArticleTitleMolecular dissection of TrkA signal transduction pathways mediating differentiation in human neuroblastoma cells Oncogene 19 2043–2051 Occurrence Handle1:CAS:528:DC%2BD3cXjtF2jsbk%3D Occurrence Handle10803465

    CAS  PubMed  Google Scholar 

  9. S. Peterson E. Bogenmann (2004) ArticleTitleThe RET and TRKA pathways collaborate to regulate neuroblastoma differentiation Oncogene 23 213–225 Occurrence Handle1:CAS:528:DC%2BD2cXovVKhtg%3D%3D Occurrence Handle14712226

    CAS  PubMed  Google Scholar 

  10. K. Fukunaga E. Miyamoto (1998) ArticleTitleRole of MAP kinase in neurons Mol. Neurobiol 16 79–95 Occurrence Handle1:CAS:528:DyaK1cXis1Oit7o%3D Occurrence Handle9554703

    CAS  PubMed  Google Scholar 

  11. T. Morooka E. Nishida (1998) ArticleTitleRequirement of p38 mitogen-activated protein kinase for neuronal differentiation in PC12 cells J. Biol. Chem 273 24285–24288 Occurrence Handle1:CAS:528:DyaK1cXmtlyru7Y%3D Occurrence Handle9733710

    CAS  PubMed  Google Scholar 

  12. T. O. Hansen J. F. Rehfeld F. C. Nielsen (2000) ArticleTitleCyclic AMP-induced neuronal differentiation via activation of p38 mitogen-activated protein kinase J. Neurochem 75 1870–1877 Occurrence Handle1:CAS:528:DC%2BD3cXns1ejtb4%3D Occurrence Handle11032876

    CAS  PubMed  Google Scholar 

  13. S. V. Kyosseva (2004) ArticleTitleMitogen-activated protein kinase signaling Int. Rev. Neurobiol 59 201–220 Occurrence Handle1:CAS:528:DC%2BD2cXktVertLw%3D Occurrence Handle15006489

    CAS  PubMed  Google Scholar 

  14. K. F. Jensen C. A. Ohmstede R. S. Fisher J. K. Olin N. Sahyoun (1991) ArticleTitleAcquisition and loss of a neuronal Ca2+/calmodulin-dependent protein kinase during neuronal differentiation Proc. Natl. Acad. Sci. USA 88 4050–4053 Occurrence Handle1:CAS:528:DyaK3MXisVCqtL0%3D Occurrence Handle2023954

    CAS  PubMed  Google Scholar 

  15. L. W. Kutcher S. R. Beauman E. I. Gruenstein M. A. Kaetzel J. R. Dedman (2003) ArticleTitleNuclear CaMKII inhibits neuronal differentiation of PC12 cells without affecting MAPK or CREB activation Am. J. Physiol. Cell Physiol 284 C1334–C1345 Occurrence Handle1:CAS:528:DC%2BD3sXltVegsro%3D Occurrence Handle12570987

    CAS  PubMed  Google Scholar 

  16. K. W. Wood H. Qi G. D’Arcangelo R. C. Armstrong T. M. Roberts S. Halegoua (1993) ArticleTitleThe cytoplasmic raf oncogene induces a neuronal phenotype in PC12 cells: a potential role for cellular raf kinases in neuronal growth factor signal transduction Proc. Natl. Acad. Sci. USA 11 5016–5020

    Google Scholar 

  17. W. L. Kuo M. Abe J. Rhee E. M. Eves S. A. McCarthy M. Yan D. J. Templeton M. McMahon M. R. Rosner (1996) ArticleTitleRaf, but not MEK or ERK, is sufficient for differentiation of hippocampal neuronal cells Mol. Cell. Biol 16 1458–1470 Occurrence Handle1:CAS:528:DyaK28XhvVahurs%3D Occurrence Handle8657119

    CAS  PubMed  Google Scholar 

  18. K. Takeda T. Hatai T. S. Hamazaki H. Nishitoh M. Saitoh H. Ichijo (2000) ArticleTitleApoptosis signal-regulating kinase 1 (ASK1) induces neuronal differentiation and survival of PC12 cells J. Biol. Chem 275 9805–9813 Occurrence Handle1:CAS:528:DC%2BD3cXitlCqsbw%3D Occurrence Handle10734135

    CAS  PubMed  Google Scholar 

  19. C. Anneren K. A. Reedquist J. L. Bos M. Welsh (2000) ArticleTitleGTK, a Src-related tyrosine kinase, induces nerve growth factor-independent neurite outgrowth in PC12 cells through activation of the Rap1 pathway. Relationship to Shb tyrosine phosphorylation and elevated levels of focal adhesion kinase J. Biol. Chem 275 29153–29161 Occurrence Handle10878015

    PubMed  Google Scholar 

  20. H. Jornvall A. Blokzijl P. ten Dijke C.F. Ibanez (2001) ArticleTitleThe orphan receptor serine/threonine kinase ALK7 signals arrest of proliferation and morphological differentiation in a neuronal cell line J. Biol. Chem 276 5140–5146 Occurrence Handle1:CAS:528:DC%2BD3MXhtlyjsrs%3D Occurrence Handle11084022

    CAS  PubMed  Google Scholar 

  21. K. Mielke T. Herdegen (2002) ArticleTitleFatal shift of signal transduction is an integral part of neuronal differentiation: JNKs realize TNFalpha-mediated apoptosis in neuronlike, but not naive, PC12 cells Mol. Cell. Neurosci 20 211–224 Occurrence Handle1:CAS:528:DC%2BD38XkvFKku70%3D Occurrence Handle12093155

    CAS  PubMed  Google Scholar 

  22. V. Waetzig T. Herdegen (2003) ArticleTitleA single c-Jun N-terminal kinase isoform (JNK3-p54) is an effector in both neuronal differentiation and cell death J. Biol. Chem 278 567–572 Occurrence Handle1:CAS:528:DC%2BD38XpvVWnsrs%3D Occurrence Handle12401814

    CAS  PubMed  Google Scholar 

  23. Y. M. Yu P. L. Han J. K. Lee (2003) ArticleTitleJNK pathway is required for retinoic acid-induced neurite outgrowth of human neuroblastoma, SH-SY5Y Neuroreport 14 941–945 Occurrence Handle1:CAS:528:DC%2BD3sXks1yqu7s%3D Occurrence Handle12802179

    CAS  PubMed  Google Scholar 

  24. P. Coulombe G. Rodier S. Pelletier J. Pellerin S Meloche (2003) ArticleTitleRapid turnover of extracellular signal-regulated kinase 3 by the ubiquitin-proteasome pathway defines a novel paradigm of mitogen-activated protein kinase regulation during cellular differentiation Mol. Cell. Biol 23 4542–4558 Occurrence Handle1:CAS:528:DC%2BD3sXltVSit70%3D Occurrence Handle12808096

    CAS  PubMed  Google Scholar 

  25. E. J. Yang J. H. Yoon D. S. Min K. C. Chung (2004) ArticleTitleLIM kinase 1 activates cAMP-responsive element-binding protein during the neuronal differentiation of immortalized hippocampal progenitor cells J. Biol. Chem 279 8903–8910 Occurrence Handle1:CAS:528:DC%2BD2cXhs1Onur0%3D Occurrence Handle14684741

    CAS  PubMed  Google Scholar 

  26. S. Leppa M. Eriksson R. Saffrich W. Ansorge D. Bohmann (2001) ArticleTitleComplex functions of AP-1 transcription factors in differentiation and survival of PC12 cells Mol. Cell. Biol 21 4369–4378 Occurrence Handle1:CAS:528:DC%2BD3MXksVOrtLo%3D Occurrence Handle11390664

    CAS  PubMed  Google Scholar 

  27. J. H. Wright P. Drueckes J. Bartoe Z. Zhao S. H. Shen E. G. Krebs (1997) ArticleTitleA role for the SHP-2 tyrosine phosphatase in nerve growth-induced PC12 cell differentiation Mol. Biol. Cell 8 1575–1585 Occurrence Handle1:CAS:528:DyaK2sXlvVWgu7o%3D Occurrence Handle9285826

    CAS  PubMed  Google Scholar 

  28. A. Okamura S. Goto T. Nishi T. Hamasaki Y. Ushio (1999) ArticleTitleOverexpression of striatal enriched phosphatase (STEP) promotes the neurite outgrowth induced by a cAMP analogue in PC12 cells Brain Res. Mol. Brain Res 67 1–9 Occurrence Handle1:CAS:528:DyaK1MXhvFGiu7g%3D Occurrence Handle10101226

    CAS  PubMed  Google Scholar 

  29. S. Strack (2002) ArticleTitleOverexpression of the protein phosphatase 2A regulatory subunit Bgamma promotes neuronal differentiation by activating the MAP kinase (MAPK) cascade J. Biol. Chem 277 41525–41532 Occurrence Handle1:CAS:528:DC%2BD38XotF2hurc%3D Occurrence Handle12191994

    CAS  PubMed  Google Scholar 

  30. I. A. Graef F. Wang F. Charron L. Chen J. Neilson M. Tessier-Lavigne G. R. Crabtree (2003) ArticleTitleNeurotrophins and netrins require calcineurin/NFAT signaling to stimulate outgrowth of embryonic axons Cell 113 657–670 Occurrence Handle1:CAS:528:DC%2BD3sXksFehurw%3D Occurrence Handle12787506

    CAS  PubMed  Google Scholar 

  31. D. Kramer L. Fresu D. S. Ashby T. C. Freeman A. A. Genazzani (2003) ArticleTitleCalcineurin controls the expression of numerous genes in cerebellar granule cells Mol. Cell. Neurosci 23 325–330 Occurrence Handle1:CAS:528:DC%2BD3sXksF2ht7k%3D Occurrence Handle12812763

    CAS  PubMed  Google Scholar 

  32. N. Jimenez A. Hernandez-Cruz (2001) ArticleTitleModifications of intracellular Ca2+ signalling during nerve growth factor-induced neuronal differentiation of rat adrenal chromaffin cells Eur. J. Neurosci 13 1487–1500 Occurrence Handle1:STN:280:DC%2BD3MzpsFyjtQ%3D%3D Occurrence Handle11328344

    CAS  PubMed  Google Scholar 

  33. D. Zechner Y. Fujita J. Hulsken T. Muller I. Walther M. M. Taketo E. B. Chrenshaw Suffix3rd W. Birchmeier C. Birchmeier (2003) ArticleTitlebeta-Catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system Dev. Biol 258 406–418 Occurrence Handle1:CAS:528:DC%2BD3sXksVyrsL8%3D Occurrence Handle12798297

    CAS  PubMed  Google Scholar 

  34. J. J. Otero W. Fu L. Kan A. E. Cuadra J. A. Kessler (2004) ArticleTitleBeta-catenin signaling is required for neural differentiation of embryonic stem cells Development 131 3545–3557 Occurrence Handle1:CAS:528:DC%2BD2cXnt1eltr0%3D Occurrence Handle15262888

    CAS  PubMed  Google Scholar 

  35. G. J. Ramakers B. Avci P. van Hulten A. Ooyen Particlevan J. Pelt Particlevan C. W. Pool M. B. Lequin (2001) ArticleTitleThe role of calcium signaling in early axonal and dendritic morphogenesis of rat cerebral cortex neurons under non-stimulated growth conditions Brain Res. Dev. Brain Res 126 163–172 Occurrence Handle1:CAS:528:DC%2BD3MXhvVahurg%3D Occurrence Handle11248350

    CAS  PubMed  Google Scholar 

  36. S. Mukobata T. Hibino A. Sugiyama Y. Urano A. Inatomi Y. Kanai H. Endo F. Tashiro (2002) ArticleTitleM6a acts as a nerve growth factor-gated Ca(2+) channel in neuronal differentiation Biochem. Biophys. Res. Commun 297 722–728 Occurrence Handle1:CAS:528:DC%2BD38XntlSitL8%3D Occurrence Handle12359212

    CAS  PubMed  Google Scholar 

  37. B. Honore H. Vorum (2000) ArticleTitleThe CREC family, a novel family of multiple EF-hand, low-affinity Ca(2+)-binding proteins localised to the secretory pathway of mammalian cells FEBS Lett 466 11–18 Occurrence Handle1:CAS:528:DC%2BD3cXltVCktg%3D%3D Occurrence Handle10648803

    CAS  PubMed  Google Scholar 

  38. W. S. Choi S. Y. Chun G. J. Markelonis T. H. Oh Y. J. Oh (2001) ArticleTitleOverexpression of calbindin-D28K induces neurite outgrowth in dopaminergic neuronal cells via activation of p38 MAPK Biochem. Biophys. Res. Commun 287 656–661 Occurrence Handle1:CAS:528:DC%2BD3MXmvV2jt7w%3D Occurrence Handle11563845

    CAS  PubMed  Google Scholar 

  39. M. Ozawa T. Muramatsu (1993) ArticleTitleReticulocalbin, a novel endoplasmic reticulum resident Ca(2+)-binding protein with multiple EF-hand motifs and a carboxyl-terminal HDEL sequence J. Biol. Chem 268 699–705 Occurrence Handle1:CAS:528:DyaK3sXks1Grurc%3D Occurrence Handle8416973

    CAS  PubMed  Google Scholar 

  40. F. N. Leeuwen H. E. Kain R. A. Kammen F. Michiels O. W. Kranenburg J. G. Collard (1997) ArticleTitleThe guanine nucleotide exchange factor Tiam1 affects neuronal morphology; opposing roles for the small GTPases Rac and Rho J. Cell. Biol 139 797–807 Occurrence Handle1:STN:280:DyaK1c%2Fht1aisw%3D%3D Occurrence Handle9348295

    CAS  PubMed  Google Scholar 

  41. T. Goi G. Rusanescu T. Urano L. A. Feig (1999) ArticleTitleRal-specific guanine nucleotide exchange factor activity opposes other Ras effectors in PC12 cells by inhibiting neurite outgrowth Mol. Cell. Biol 19 1731–1741 Occurrence Handle1:CAS:528:DyaK1MXhsFeqt74%3D Occurrence Handle10022860

    CAS  PubMed  Google Scholar 

  42. C. Menager K. Kaibuchi (2003) ArticleTitleRho proteins: their function in neurons Med. Sci. (Paris) 19 358–363

    Google Scholar 

  43. S. Estrach S. Schmidt S. Diriong A. Penna A. Blangy P. Fort A. Debant (2002) ArticleTitleThe Human Rho-GEF trio and its target GTPase RhoG are involved in the NGF pathway, leading to neurite outgrowth Curr. Biol 12 307–312 Occurrence Handle1:CAS:528:DC%2BD38XhslWgt7c%3D Occurrence Handle11864571

    CAS  PubMed  Google Scholar 

  44. A. Sebok N. Nusser B. Debreceni Z. Guo M. F. Santos J. Szeberenyi G. Tigyi (1999) ArticleTitleDifferent roles for RhoA during neurite initiation, elongation, regeneration in PC12 cells J. Neurochem 73 949–960 Occurrence Handle1:CAS:528:DyaK1MXlsVOitr4%3D Occurrence Handle10461884

    CAS  PubMed  Google Scholar 

  45. B. Furuta A. Harada Y. Kobayashi K. Takeuchi T. Kobayashi M. Umeda (2002) ArticleTitleIdentification and functional characterization of nadrin variants, a novel family of GTPase activating protein for rho GTPases J. Neurochem 82 1018–1028 Occurrence Handle1:CAS:528:DC%2BD38XmvVert7s%3D Occurrence Handle12358749

    CAS  PubMed  Google Scholar 

  46. M. L. Spencer H. Shao D. A. Andres (2002) ArticleTitleInduction of neurite extension and survival in pheochromocytoma cells by the Rit GTPase J. Biol. Chem 277 20160–20168 Occurrence Handle1:CAS:528:DC%2BD38XkslWgsLk%3D Occurrence Handle11914372

    CAS  PubMed  Google Scholar 

  47. D. L. Hynds M. L. Spencer D. A. Andres D. M. Snow (2003) ArticleTitleRit promotes MEK-independent neurite branching in human neuroblastoma cells J. Cell Sci 116 1925–1935 Occurrence Handle1:CAS:528:DC%2BD3sXkt1Olt78%3D Occurrence Handle12668729

    CAS  PubMed  Google Scholar 

  48. Z. Liu T. K. Chatterjee R. A. Fisher (2002) ArticleTitleRGS6 interacts with SCG10 and promotes neuronal differentiation. Role of the G gamma subunit-like (GGL) domain of RGS6 J. Biol. Chem 277 37832–37839 Occurrence Handle1:CAS:528:DC%2BD38XnsVejt7c%3D Occurrence Handle12140291

    CAS  PubMed  Google Scholar 

  49. J. Meng P. J. Casey (2002) ArticleTitleActivation of Gz attenuates Rap1-mediated differentiation of PC12 cells J. Biol. Chem 277 43417–43424 Occurrence Handle1:CAS:528:DC%2BD38Xos1emsbg%3D Occurrence Handle12198116

    CAS  PubMed  Google Scholar 

  50. B. G. Novitch H. Wichterle T. M. Jessell S. Sockanathan (2003) ArticleTitleA requirement for retinoic acid-mediated transcriptional activation in ventral neural patterning and motor neuron specification Neuron 40 81–95 Occurrence Handle1:CAS:528:DC%2BD3sXnvVygsbk%3D Occurrence Handle14527435

    CAS  PubMed  Google Scholar 

  51. B. Blumberg (1997) ArticleTitleAn essential role for retinoid signaling in anteroposterior neural specification and neuronal differentiation Semin. Cell Dev. Biol 8 417–428 Occurrence Handle1:CAS:528:DyaK2sXmt1Orur8%3D Occurrence Handle15001080

    CAS  PubMed  Google Scholar 

  52. T. Luo E. Wagner F. Grun U. C. Drager (2004) ArticleTitleRetinoic acid signaling in the brain marks formation of optic projections, maturation of the dorsal telencephalon, function of limbic sites J. Comp. Neurol 470 297–316 Occurrence Handle1:CAS:528:DC%2BD2cXitVyqtLg%3D Occurrence Handle14755518

    CAS  PubMed  Google Scholar 

  53. M. Schubert N. D. Holland H. Escriva L. Z. Holland V. Laudet (2004) ArticleTitleRetinoic acid influences anteroposterior positioning of epidermal sensory neurons and their gene expression in a developing chordate (amphioxus) Proc. Natl. Acad. Sci. USA 101 10320–10325 Occurrence Handle1:CAS:528:DC%2BD2cXmtVyrsr8%3D Occurrence Handle15226493

    CAS  PubMed  Google Scholar 

  54. M. Maden (2001) ArticleTitleRole and distribution of retinoic acid during CNS development Int. Rev. Cytol 209 1–77 Occurrence Handle1:CAS:528:DC%2BD38XhvVelur0%3D Occurrence Handle11580199

    CAS  PubMed  Google Scholar 

  55. R. Gallo F. Zazzeroni E. Alesse C. Mincione U. Borello P. Buanne R. D’Eugenio A. R. Mackay B. Argenti R. Gradini M. A. Russo M. Maroder G. Cossu L. Frati I. Screpanti A. Gulino (2002) ArticleTitleREN: a novel, developmentally regulated gene that promotes neural cell differentiation J. Cell Biol 158 731–740 Occurrence Handle1:CAS:528:DC%2BD38XmsVSnuro%3D Occurrence Handle12186855

    CAS  PubMed  Google Scholar 

  56. U. S. Singh J. Pan Y. L. Kao S. Joshi K. L. Young K. M. Baker (2003) ArticleTitleTissue transglutaminase mediates activation of RhoA and MAP kinase pathways during retinoic acid-induced neuronal differentiation of SH-SY5Y cells J. Biol. Chem 278 391–399 Occurrence Handle1:CAS:528:DC%2BD38XpvVWgur8%3D Occurrence Handle12401808

    CAS  PubMed  Google Scholar 

  57. G. Lopez-Carballo L. Moreno S. Masia P. Perez D. Barettino (2002) ArticleTitleActivation of the phosphatidylinositol 3-kinase/Akt signaling pathway by retinoic acid is required for neural differentiation of SH-SY5Y human neuroblastoma cells J. Biol. Chem 277 25297–25304 Occurrence Handle1:CAS:528:DC%2BD38XlsVWiu7c%3D Occurrence Handle12000752

    CAS  PubMed  Google Scholar 

  58. A. Contestabile E. Ciani (2004) ArticleTitleRole of nitric oxide in the regulation of neuronal proliferation, survival and differentiation Neurochem. Int 45 903–914 Occurrence Handle1:CAS:528:DC%2BD2cXmslOiu7s%3D Occurrence Handle15312985

    CAS  PubMed  Google Scholar 

  59. A. Cheng S. Wang J. Cai M. S. Rao M. P. Mattson (2003) ArticleTitleNitric oxide acts in a positive feedback loop with BDNF to regulate neural progenitor cell proliferation and differentiation in the mammalian brain Dev. Biol 258 319–333 Occurrence Handle1:CAS:528:DC%2BD3sXksVyrs7s%3D Occurrence Handle12798291

    CAS  PubMed  Google Scholar 

  60. S. Arnhold A. Fassbender F. J. Klinz K. Kruttwig B. Lohnig C. Andressen K. Addicks (2002) ArticleTitleNOS-II is involved in early differentiation of murine cortical, retinal and ES cell-derived neurons—an immunocytochemical and functional approach Int. J. Dev. Neurosci 20 83–92 Occurrence Handle1:CAS:528:DC%2BD38XktVaqtb0%3D Occurrence Handle12034139

    CAS  PubMed  Google Scholar 

  61. G. Cappelletti M. G. Maggioni G. Tedeschi R. Maci (2003) ArticleTitleProtein tyrosine nitration is triggered by nerve growth factor during neuronal differentiation of PC12 cells Exp. Cell Res 288 9–20 Occurrence Handle1:CAS:528:DC%2BD3sXls1Ojt7w%3D Occurrence Handle12878155

    CAS  PubMed  Google Scholar 

  62. X. Guo W. Ying J. Wan Z. Hu X. Qian H. Zhang F. He (2001) ArticleTitleProteomic characterization of early-stage differentiation of mouse embryonic stem cells into neural cells induced by all-trans retinoic acid in vitro Electrophoresis 22 3067–3075 Occurrence Handle1:CAS:528:DC%2BD3MXmvV2nsb8%3D Occurrence Handle11565801

    CAS  PubMed  Google Scholar 

  63. M. H. Maurer R. E. Feldmann SuffixJr. C. D. Futterer J. Butlin W. Kuschinsky (2004) ArticleTitleComprehensive proteome expression profiling of undifferentiated versus differentiated neural stem cells from adult rat hippocampus Neurochem. Res 29 1129–1144 Occurrence Handle1:CAS:528:DC%2BD2cXjtVWmurk%3D Occurrence Handle15176470

    CAS  PubMed  Google Scholar 

  64. M. M. Bradford (1976) ArticleTitleA rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem 72 248–254 Occurrence Handle1:CAS:528:DyaE28XksVehtrY%3D Occurrence Handle942051

    CAS  PubMed  Google Scholar 

  65. H. Langen P. Berndt D. Roder N. Cairns G. Lubec M. Fountoulakis (1999) ArticleTitleTwo-dimensional map of human brain proteins Electrophoresis 20 907–916 Occurrence Handle1:CAS:528:DyaK1MXjsVakt7k%3D Occurrence Handle10344266

    CAS  PubMed  Google Scholar 

  66. A. Peyrl K. Krapfenbauer I. Slavc J. W. Yang T. Strobel G. Lubec (2003) ArticleTitleProtein profiles of medulloblastoma cell lines DAOY and D283. Identification of tumor-related proteins and principles Proteomics 3 1781–1800 Occurrence Handle1:CAS:528:DC%2BD3sXnsFKks70%3D Occurrence Handle12973738

    CAS  PubMed  Google Scholar 

  67. M. C. Fishman P. R. Dragsten I. Spector (1981) ArticleTitleImmobilization of concanavalin A receptors during differentiation of neuroblastoma cells Nature 290 781–783 Occurrence Handle1:CAS:528:DyaL3MXkslOktL8%3D Occurrence Handle6261153

    CAS  PubMed  Google Scholar 

  68. C. Cosgrove P. Cobbett (1991) ArticleTitleInduction of temporally dissociated morphological and physiological differentiation of N1E-115 cells Brain Res. Bull 27 53–58 Occurrence Handle1:STN:280:By2D3svhsFA%3D Occurrence Handle1933436

    CAS  PubMed  Google Scholar 

  69. R. R. Rao W. S. Kisaalita (2002) ArticleTitleBiochemical and electrophysiological differentiation profile of a human neuroblastoma (IMR-32) cell line In Vitro Cell. Dev. Biol. Anim 38 450–456 Occurrence Handle12605539

    PubMed  Google Scholar 

  70. R. P. de Groot W. Kruijer (1991) ArticleTitleUp-regulation of Jun/AP-1 during differentiation of N1E-115 neuroblastoma cells Cell Growth Differ 2 631–636 Occurrence Handle1:CAS:528:DyaK38XhslWisb4%3D Occurrence Handle1809375

    CAS  PubMed  Google Scholar 

  71. A. Methner F. Leypoldt P. Joost J. Lewerenz (2001) ArticleTitleHuman septin 3 on chromosome 22q13.2 is upregulated by neuronal differentiation Biochem. Biophys. Res. Commun 283 48–56 Occurrence Handle1:CAS:528:DC%2BD3MXivFGhtbo%3D Occurrence Handle11322766

    CAS  PubMed  Google Scholar 

  72. I. E. Vega S. C. Hsu (2003) ArticleTitleThe septin protein Nedd5 associates with both the exocyst complex and microtubules and disruption of its GTPase activity promotes aberrant neurite sprouting in PC12 cells Neuroreport 14 31–37 Occurrence Handle1:CAS:528:DC%2BD3sXmsVSitA%3D%3D Occurrence Handle12544826

    CAS  PubMed  Google Scholar 

  73. H. Takano I. Komuro T. Oka I. Shiojima Y. Hiroi T. Mizuno Y. Yazaki (1998) ArticleTitleThe Rho family G proteins play a critical role in muscle differentiation Mol. Cell. Biol 18 1580–1589 Occurrence Handle1:CAS:528:DyaK1cXhtlehs78%3D Occurrence Handle9488475

    CAS  PubMed  Google Scholar 

  74. N. Vanegas A. Garcia-Sacristan L. A. Lopez-Fernandez M. Parraga J. del Mazo P. Hernandez J. B. Schvartzman D. B. Krimer (2003) ArticleTitleDifferential expression of Ran GTPase during HMBA-induced differentiation in murine erythroleukemia cells Leuk. Res 27 607–615 Occurrence Handle1:CAS:528:DC%2BD3sXis12htbw%3D Occurrence Handle12681360

    CAS  PubMed  Google Scholar 

  75. R. Daniel S. W. Chung T. K. Eisenstein B. M. Sultzer P. M. Wong (2001) ArticleTitleSpecific association of Type I c-Abl with Ran GTPase in lipopolysaccharide-mediated differentiation Oncogene 20 2618–2625 Occurrence Handle1:CAS:528:DC%2BD3MXktVWnurs%3D Occurrence Handle11420673

    CAS  PubMed  Google Scholar 

  76. E. Rydell K. E. Magnusson A. Sjo K. Axelsson (1990) ArticleTitleProtein kinase C and casein kinase II activities in two human colon carcinoma cell lines, HT-29 and CaCo-2: possible correlation with differentiation Biosci. Rep 10 293–299 Occurrence Handle1:CAS:528:DyaK3cXls12lt74%3D Occurrence Handle2224065

    CAS  PubMed  Google Scholar 

  77. J. Okabe-Kado T. Kasukabe M. Hozumi Y. Honma N. Kimura H. Baba T. Urano H. Shiku (1995) ArticleTitleA new function of Nm23/NDP kinase as a differentiation inhibitory factor, which does not require it’s kinase activity FEBS Lett 363 311–315 Occurrence Handle1:CAS:528:DyaK2MXlsFCmsbc%3D Occurrence Handle7737424

    CAS  PubMed  Google Scholar 

  78. D. Lombardi A. Sacchi G. D’Agostino G. Tibursi (1995) ArticleTitleThe association of the Nm23-M1 protein and beta-tubulin correlates with cell differentiation Exp. Cell Res 217 267–271 Occurrence Handle1:CAS:528:DyaK2MXkslyrsbw%3D Occurrence Handle7698225

    CAS  PubMed  Google Scholar 

  79. D. Lombardi M. L. Lacombe M. G. Paggi (2000) ArticleTitlenm23: unraveling its biological function in cell differentiation J. Cell. Physiol 182 144–149 Occurrence Handle1:CAS:528:DC%2BD3cXjtVGqsw%3D%3D Occurrence Handle10623877

    CAS  PubMed  Google Scholar 

  80. S. Hsu F. Huang L. Wang S. Banerjee S. Winawer E. Friedman (1994) ArticleTitleThe role of nm23 in transforming growth factor beta 1-mediated adherence and growth arrest Cell Growth Differ 5 909–917 Occurrence Handle1:CAS:528:DyaK2cXmt1arsL4%3D Occurrence Handle7819128

    CAS  PubMed  Google Scholar 

  81. F. Gervasi I. D’Agnano S. Vossio G. Zupi A. Sacchi D. Lombardi (1996) ArticleTitlenm23 influences proliferation and differentiation of PC12 cells in response to nerve growth factor Cell Growth Differ 7 1689–1695 Occurrence Handle1:CAS:528:DyaK28XnsVOhtbc%3D Occurrence Handle8959337

    CAS  PubMed  Google Scholar 

  82. S. E. Egan B. W. Giddings M. W. Brooks L. Buday A. M. Sizeland R. A. Weinberg (1993) ArticleTitleAssociation of Sos Ras exchange protein with Grb2 is implicated in tyrosine kinase signal transduction and transformation Nature 363 45–51 Occurrence Handle1:CAS:528:DyaK3sXkt1Ggurw%3D Occurrence Handle8479536

    CAS  PubMed  Google Scholar 

  83. K. Kageyama Y. Ihara S. Goto Y. Urata G. Toda K. Yano T. Kondo (2002) ArticleTitleOverexpression of calreticulin modulates protein kinase B/Akt signaling to promote apoptosis during cardiac differentiation of cardiomyoblast H9c2 cells J. Biol. Chem 277 19255–19264 Occurrence Handle1:CAS:528:DC%2BD38XksVWlt7g%3D Occurrence Handle11907032

    CAS  PubMed  Google Scholar 

  84. T. Nishiyama H. Sakemi H. Sumi S. Tokunaga K. Doi S. Ogata (2000) ArticleTitleA chromosomal locus encoding a phosphoserine phosphatase- and a truncated MinD-like protein affects differentiation in Streptomyces azureus ATCC14921 FEMS Microbiol. Lett 190 133–139 Occurrence Handle1:CAS:528:DC%2BD3cXlvV2lsbc%3D Occurrence Handle10981703

    CAS  PubMed  Google Scholar 

  85. L. Lucentini S. Fulle C. Riccioloni H. Pancioni F. Panara (2003) ArticleTitleLow molecular weight phosphotyrosine protein phosphatase from PC12 cells. Purification, some properties and expression during neurogenesis in vitro and in vivo Int. J. Biochem. Cell Biol 35 1378–1387 Occurrence Handle1:CAS:528:DC%2BD3sXksValt7k%3D Occurrence Handle12798350

    CAS  PubMed  Google Scholar 

  86. T. Fiaschi P. Chiarugi F. Buricchi E. Giannoni M. L. Taddei D. Talini G. Cozzi S. Zecchi-Orlandini G. Raugei G. Ramponi (2001) ArticleTitleLow molecular weight protein-tyrosine phosphatase is involved in growth inhibition during cell differentiation J. Biol. Chem 276 49156–49163 Occurrence Handle1:CAS:528:DC%2BD38XktlemtA%3D%3D Occurrence Handle11595742

    CAS  PubMed  Google Scholar 

  87. T. Yamazaki H. Nakano M. Hayakari M. Tanaka J. Mayama S. Tsuchida (2004) ArticleTitleDifferentiation induction of human keratinocytes by phosphatidylethanolamine-binding protein J. Biol. Chem 279 32191–32195 Occurrence Handle1:CAS:528:DC%2BD2cXmtVChsrw%3D Occurrence Handle15155742

    CAS  PubMed  Google Scholar 

  88. G. Di Paolo V. Pellier M. Catsicas B. Antonsson S. Catsicas G. Grenningloh (1996) ArticleTitleThe phosphoprotein stathmin is essential for nerve growth factor-stimulated differentiation J. Cell Biol 133 1383–1390 Occurrence Handle1:CAS:528:DyaK28XjslKjtrY%3D Occurrence Handle8682872

    CAS  PubMed  Google Scholar 

  89. C. Sorg E. Michels U. Malorny C. Neumann (1984) ArticleTitleMigration inhibitory factors and macrophage differentiation Springer Semin. Immunopathol 7 311–320 Occurrence Handle1:STN:280:BiqC3MrptlM%3D Occurrence Handle6395408

    CAS  PubMed  Google Scholar 

  90. S. A. Sarkar R. P. Sharma (2002) ArticleTitleExpression of selected apoptosis related genes, MIF, IGIF and TNF alpha, during retinoic acid-induced neural differentiation in murine embryonic stem cells Cell Struct. Funct 27 99–107 Occurrence Handle1:CAS:528:DC%2BD38Xls1Cqsr8%3D Occurrence Handle12207051

    CAS  PubMed  Google Scholar 

  91. C. Busch G. Siegenthaler A. Vahlquist J. P. Sundelin Saksena U. Eriksson (1992) ArticleTitleExpression of cellular retinoid-binding proteins during normal and abnormal epidermal differentiation J. Invest. Dermatol 99 795–802 Occurrence Handle1:CAS:528:DyaK3sXlslWhtQ%3D%3D Occurrence Handle1335015

    CAS  PubMed  Google Scholar 

  92. A. V. Perez-Castro V. T. Tran M. C. Nguyen-Huu (1993) ArticleTitleDefective lens fiber differentiation and pancreatic tumorigenesis caused by ectopic expression of the cellular retinoic acid-binding protein I Development 119 363–375 Occurrence Handle1:CAS:528:DyaK2cXhvVyiurY%3D Occurrence Handle8287793

    CAS  PubMed  Google Scholar 

  93. P. Brabet C. Pantaloni J. Bockaert V Homburger (1991) ArticleTitleMetabolism of two Go alpha isoforms in neuronal cells during differentiation J. Biol. Chem 266 12825–12828 Occurrence Handle1:CAS:528:DyaK3MXks12gsbs%3D Occurrence Handle1906458

    CAS  PubMed  Google Scholar 

  94. B. Rouot N. Charpentier C. Chabbert J. Carrette R. Zumbihl J. Bockaert V. Homburger (1992) ArticleTitleSpecific antibodies against Go isoforms reveal the early expression of the Go2 alpha subunit and appearance of Go1 alpha during neuronal differentiation Mol. Pharmacol 41 273–280 Occurrence Handle1:CAS:528:DyaK38Xls1ygs70%3D Occurrence Handle1538708

    CAS  PubMed  Google Scholar 

  95. T. Abe M. Kato H. Miki T. Takenawa T Endo (2003) ArticleTitleSmall GTPase Tc10 and its homologue RhoT induce N-WASP-mediated long process formation and neurite outgrowth J. Cell Sci 116 155–168 Occurrence Handle1:CAS:528:DC%2BD3sXmtF2luw%3D%3D Occurrence Handle12456725

    CAS  PubMed  Google Scholar 

  96. C. Hall G. J. Michael N. Cann G. Ferrari M. Teo T. Jacobs C. Monfires L. Lim (2001) ArticleTitlealpha2-chimaerin, a Cdc42/Rac1 regulator, is selectively expressed in the rat embryonic nervous system and is involved in neuritogenesis in N1E-115 neuroblastoma cells J. Neurosci 21 5191–5202 Occurrence Handle1:CAS:528:DC%2BD3MXkvFSrs78%3D Occurrence Handle11438594

    CAS  PubMed  Google Scholar 

  97. R. Amendola R. Martinez A. Neuroni D. Venturelli B. Tanno B. Callabretta G. Raschella (1995) ArticleTitleDR-nm23 gene expression in neuroblastoma cells: relationship to integrin expression, adhesion characteristics, differentiation J. Natl. Cancer Inst 89 1300–1310

    Google Scholar 

  98. B. R. Chakravarthy J. Wong J. P. Durkin (1995) ArticleTitleEvidence that the modulation of membrane-associated protein kinase C activity by an endogenous inhibitor plays a role in N1E-115 murine neuroblastoma cell differentiation J. Neurochem 65 1569–1579 Occurrence Handle1:CAS:528:DyaK2MXotFOlu7c%3D Occurrence Handle7561851

    CAS  PubMed  Google Scholar 

  99. O. Kranenburg V. Scharnhorst A. J. Van der Eb A. Zantema (1995) ArticleTitleInhibition of cyclin-dependent kinase activity triggers neuronal differentiation of mouse neuroblastoma cells J. Cell Biol 131 227–234 Occurrence Handle1:CAS:528:DyaK2MXot1Oku7Y%3D Occurrence Handle7559779

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. CChem, FRSC (UK), Department of Pediatrics, Medical University of Vienna, Währinger Gürtel 18, A 1090, Vienna, Austria

    Ji-eun Oh, Karlin Raja Karlmark, Joo-ho Shin, Arnold Pollak & Gert Lubec

  2. Obstetrics and Gynecology, Prenatal Diagnosis and Therapy, Medical University of Vienna, Vienna, Austria

    Karlin Raja Karlmark, Angelika Freilinger & Markus Hengstschläger

Authors
  1. Ji-eun Oh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karlin Raja Karlmark
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joo-ho Shin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Arnold Pollak
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Angelika Freilinger
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Markus Hengstschläger
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gert Lubec
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gert Lubec.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Oh, Je., Karlmark, K.R., Shin, Jh. et al. Differentiation of Neuroblastoma Cell Line N1E-115 Involves Several Signaling Cascades. Neurochem Res 30, 333–348 (2005). https://doi.org/10.1007/s11064-005-2607-2

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-005-2607-2

Keywords

Search

Navigation