Skip to main content
SpringerLink
Log in

Gene Expression Profile of NF-κB, Nrf2, Glycolytic, and p53 Pathways During the SH-SY5Y Neuronal Differentiation Mediated by Retinoic Acid

  • Published:
Molecular Neurobiology Aims and scope Submit manuscript

Abstract

SH-SY5Y cells, a neuroblastoma cell line that is a well-established model system to study the initial phases of neuronal differentiation, have been used in studies to elucidate the mechanisms of neuronal differentiation. In the present study, we investigated alterations of gene expression in SH-SY5Y cells during neuronal differentiation mediated by retinoic acid (RA) treatment. We evaluated important pathways involving nuclear factor kappa B (NF-κB), nuclear E2-related factor 2 (Nrf2), glycolytic, and p53 during neuronal differentiation. We also investigated the involvement of reactive oxygen species (ROS) in modulating the gene expression profile of those pathways by antioxidant co-treatment with Trolox®, a hydrophilic analogue of α-tocopherol. We found that RA treatment increases levels of gene expression of NF-κB, glycolytic, and antioxidant pathway genes during neuronal differentiation of SH-SY5Y cells. We also found that ROS production induced by RA treatment in SH-SY5Y cells is involved in gene expression profile alterations, chiefly in NF-κB, and glycolytic pathways. Antioxidant co-treatment with Trolox® reversed the effects mediated by RA NF-κB, and glycolytic pathways gene expression. Interestingly, co-treatment with Trolox® did not reverse the effects in antioxidant gene expression mediated by RA in SH-SY5Y. To confirm neuronal differentiation, we quantified endogenous levels of tyrosine hydroxylase, a recognized marker of neuronal differentiation. Our data suggest that during neuronal differentiation mediated by RA, changes in profile gene expression of important pathways occur. These alterations are in part mediated by ROS production. Therefore, our results reinforce the importance in understanding the mechanism by which RA induces neuronal differentiation in SH-SY5Y cells, principally due this model being commonly used as a neuronal cell model in studies of neuronal pathologies.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Fineberg SK, Kosik KS, Davidson BL (2009) MicroRNAs potentiate neural development. Neuron 64(3):303–309. doi:10.1016/j.neuron.2009.10.020

    Article  CAS  PubMed  Google Scholar 

  2. Chen X, Du Z, Shi W, Wang C, Yang Y, Wang F, Yao Y, He K, Hao A (2013) 2-Bromopalmitate modulates neuronal differentiation through the regulation of histone acetylation. Stem Cell Res 12(2):481–491. doi:10.1016/j.scr.2013.12.010

    Article  PubMed  Google Scholar 

  3. Hadjal Y, Hadadeh O, Yazidi CE, Barruet E, Binetruy B (2013) A p38MAPK-p53 cascade regulates mesodermal differentiation and neurogenesis of embryonic stem cells. Cell Death Dis 4:e737. doi:10.1038/cddis.2013.246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Zhao F, Wu T, Lau A, Jiang T, Huang Z, Wang XJ, Chen W, Wong PK, Zhang DD (2009) Nrf2 promotes neuronal cell differentiation. Free Radic Biol Med 47(6):867–879. doi:10.1016/j.freeradbiomed.2009.06.029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. de Bittencourt Pasquali MA, Gelain DP, Zeidan-Chulia F, Pires AS, Gasparotto J, Terra SR, Moreira JC (2013) Vitamin A (retinol) downregulates the receptor for advanced glycation endproducts (RAGE) by oxidant-dependent activation of p38 MAPK and NF-kB in human lung cancer A549 cells. Cell Signal 25(4):939–954. doi:10.1016/j.cellsig.2013.01.013

    Article  PubMed  Google Scholar 

  6. Salminen A, Kauppinen A, Kaarniranta K (2012) Phytochemicals suppress nuclear factor-kappaB signaling: impact on health span and the aging process. Curr Opin Clin Nutr Metab Care 15(1):23–28. doi:10.1097/MCO.0b013e32834d3ae7

    Article  CAS  PubMed  Google Scholar 

  7. Bhakar AL, Tannis LL, Zeindler C, Russo MP, Jobin C, Park DS, MacPherson S, Barker PA (2002) Constitutive nuclear factor-kappa B activity is required for central neuron survival. J Neurosci 22(19):8466–8475

    CAS  PubMed  Google Scholar 

  8. O'Neill LA, Kaltschmidt C (1997) NF-kappa B: a crucial transcription factor for glial and neuronal cell function. Trends Neurosci 20(6):252–258

    Article  PubMed  Google Scholar 

  9. Kaltschmidt B, Sparna T, Kaltschmidt C (1999) Activation of NF-kappa B by reactive oxygen intermediates in the nervous system. Antioxid Redox Signal 1(2):129–144

    Article  CAS  PubMed  Google Scholar 

  10. Lane DP (1992) Cancer. p53, guardian of the genome. Nature 358(6381):15–16. doi:10.1038/358015a0

    Article  CAS  PubMed  Google Scholar 

  11. Mukhopadhyay UK, Mak AS (2009) p53: is the guardian of the genome also a suppressor of cell invasion? Cell Cycle 8(16):2481

    Article  CAS  PubMed  Google Scholar 

  12. Gaub P, Tedeschi A, Puttagunta R, Nguyen T, Schmandke A, Di Giovanni S (2010) HDAC inhibition promotes neuronal outgrowth and counteracts growth cone collapse through CBP/p300 and P/CAF-dependent p53 acetylation. Cell Death Differ 17(9):1392–1408. doi:10.1038/cdd.2009.216

    Article  CAS  PubMed  Google Scholar 

  13. Harris JJ, Jolivet R, Attwell D (2012) Synaptic energy use and supply. Neuron 75(5):762–777. doi:10.1016/j.neuron.2012.08.019

    Article  CAS  PubMed  Google Scholar 

  14. Campanucci V, Krishnaswamy A, Cooper E (2010) Diabetes depresses synaptic transmission in sympathetic ganglia by inactivating nAChRs through a conserved intracellular cysteine residue. Neuron 66(6):827–834. doi:10.1016/j.neuron.2010.06.010

    Article  CAS  PubMed  Google Scholar 

  15. Gutteridge JM, Halliwell B (2000) Free radicals and antioxidants in the year 2000. A historical look to the future. Ann N Y Acad Sci 899:136–147

    Article  CAS  PubMed  Google Scholar 

  16. Wang B, Zhu X, Kim Y, Li J, Huang S, Saleem S, Li RC, Xu Y, Dore S, Cao W (2012) Histone deacetylase inhibition activates transcription factor Nrf2 and protects against cerebral ischemic damage. Free Radic Biol Med 52(5):928–936. doi:10.1016/j.freeradbiomed.2011.12.006

    Article  CAS  PubMed  Google Scholar 

  17. Yan W, Wang HD, Hu ZG, Wang QF, Yin HX (2008) Activation of Nrf2-ARE pathway in brain after traumatic brain injury. Neurosci Lett 431(2):150–154. doi:10.1016/j.neulet.2007.11.060

    Article  CAS  PubMed  Google Scholar 

  18. Ramsey CP, Glass CA, Montgomery MB, Lindl KA, Ritson GP, Chia LA, Hamilton RL, Chu CT, Jordan-Sciutto KL (2007) Expression of Nrf2 in neurodegenerative diseases. J Neuropathol Exp Neurol 66(1):75–85. doi:10.1097/nen.0b013e31802d6da9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. da Frota Junior ML, Pires AS, Zeidan-Chulia F, Bristot IJ, Lopes FM, de Bittencourt Pasquali MA, Zanotto-Filho A, Behr GA, Klamt F, Gelain DP, Moreira JC (2011) In vitro optimization of retinoic acid-induced neuritogenesis and TH endogenous expression in human SH-SY5Y neuroblastoma cells by the antioxidant Trolox. Mol Cell Biochem 358(1–2):325–334. doi:10.1007/s11010-011-0983-2

    Article  PubMed  Google Scholar 

  20. Albanus RD, Juliani Siqueira Dalmolin R, Alves Castro MA, Augusto de Bittencourt Pasquali M, de Miranda Ramos V, Pens Gelain D, Fonseca Moreira JC (2013) Reverse engineering the neuroblastoma regulatory network uncovers MAX as One of the master regulators of tumor progression. PLoS One 8(12):e82457

    Article  PubMed  PubMed Central  Google Scholar 

  21. Xun Z, Lee DY, Lim J, Canaria CA, Barnebey A, Yanonne SM, McMurray CT (2012) Retinoic acid-induced differentiation increases the rate of oxygen consumption and enhances the spare respiratory capacity of mitochondria in SH-SY5Y cells. Mech Ageing Dev 133(4):176–185. doi:10.1016/j.mad.2012.01.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Castro MA, Filho JL, Dalmolin RJ, Sinigaglia M, Moreira JC, Mombach JC, de Almeida RM (2009) ViaComplex: software for landscape analysis of gene expression networks in genomic context. Bioinformatics 25(11):1468–1469. doi:10.1093/bioinformatics/btp246

    Article  CAS  PubMed  Google Scholar 

  23. von Mering C, Jensen LJ, Snel B, Hooper SD, Krupp M, Foglierini M, Jouffre N, Huynen MA, Bork P (2005) STRING: known and predicted protein-protein associations, integrated and transferred across organisms. Nucleic Acids Res 33:D433–D437. doi:10.1093/nar/gki005, Database issue

    Article  Google Scholar 

  24. Birney E, Andrews D, Caccamo M, Chen Y, Clarke L, Coates G, Cox T, Cunningham F, Curwen V, Cutts T, Down T, Durbin R, Fernandez-Suarez XM, Flicek P, Graf S, Hammond M, Herrero J, Howe K, Iyer V, Jekosch K, Kahari A, Kasprzyk A, Keefe D, Kokocinski F, Kulesha E, London D, Longden I, Melsopp C, Meidl P, Overduin B, Parker A, Proctor G, Prlic A, Rae M, Rios D, Redmond S, Schuster M, Sealy I, Searle S, Severin J, Slater G, Smedley D, Smith J, Stabenau A, Stalker J, Trevanion S, Ureta-Vidal A, Vogel J, White S, Woodwark C, Hubbard TJ (2006) Ensembl. Nucleic Acids Res 34:D556–D561. doi:10.1093/nar/gkj133, Database issue

    Article  CAS  PubMed  Google Scholar 

  25. Hooper SD, Bork P (2005) Medusa: a simple tool for interaction graph analysis. Bioinformatics 21(24):4432–4433. doi:10.1093/bioinformatics/bti696

    Article  CAS  PubMed  Google Scholar 

  26. Iyengar BR, Choudhary A, Sarangdhar MA, Venkatesh KV, Gadgil CJ, Pillai B (2014) Non-coding RNA interact to regulate neuronal development and function. Front Cell Neurosci 8:47. doi:10.3389/fncel.2014.00047

    Article  PubMed  PubMed Central  Google Scholar 

  27. Biedler JL, Helson L, Spengler BA (1973) Morphology and growth, tumorigenicity, and cytogenetics of human neuroblastoma cells in continuous culture. Cancer Res 33(11):2643–2652

    CAS  PubMed  Google Scholar 

  28. Mattson MP (2005) NF-kappaB in the survival and plasticity of neurons. Neurochem Res 30(6–7):883–893. doi:10.1007/s11064-005-6961-x

    Article  CAS  PubMed  Google Scholar 

  29. Casaccia-Bonnefil P, Carter BD, Dobrowsky RT, Chao MV (1996) Death of oligodendrocytes mediated by the interaction of nerve growth factor with its receptor p75. Nature 383(6602):716–719. doi:10.1038/383716a0

    Article  CAS  PubMed  Google Scholar 

  30. Carter BD, Kaltschmidt C, Kaltschmidt B, Offenhauser N, Bohm-Matthaei R, Baeuerle PA, Barde YA (1996) Selective activation of NF-kappa B by nerve growth factor through the neurotrophin receptor p75. Science 272(5261):542–545

    Article  CAS  PubMed  Google Scholar 

  31. Burke MA, Bothwell M (2003) p75 neurotrophin receptor mediates neurotrophin activation of NF-kappa B and induction of iNOS expression in P19 neurons. J Neurobiol 55(2):191–203. doi:10.1002/neu.10174

    Article  CAS  PubMed  Google Scholar 

  32. Heissmeyer V, Krappmann D, Wulczyn FG, Scheidereit C (1999) NF-kappaB p105 is a target of IkappaB kinases and controls signal induction of Bcl-3-p50 complexes. EMBO J 18(17):4766–4778. doi:10.1093/emboj/18.17.4766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Dechend R, Hirano F, Lehmann K, Heissmeyer V, Ansieau S, Wulczyn FG, Scheidereit C, Leutz A (1999) The Bcl-3 oncoprotein acts as a bridging factor between NF-kappaB/Rel and nuclear co-regulators. Oncogene 18(22):3316–3323. doi:10.1038/sj.onc.1202717

    Article  CAS  PubMed  Google Scholar 

  34. Gallagher D, Gutierrez H, Gavalda N, O'Keeffe G, Hay R, Davies AM (2007) Nuclear factor-kappaB activation via tyrosine phosphorylation of inhibitor kappaB-alpha is crucial for ciliary neurotrophic factor-promoted neurite growth from developing neurons. J Neurosci 27(36):9664–9669. doi:10.1523/JNEUROSCI.0608-07.2007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Dienel GA (2012) Fueling and imaging brain activation. ASN Neuro 4 (5). doi:10.1042/AN20120021, e00093 [pii], AN20120021 [pii]

  36. Cabrera-Valladares G, German MS, Matschinsky FM, Wang J, Fernandez-Mejia C (1999) Effect of retinoic acid on glucokinase activity and gene expression and on insulin secretion in primary cultures of pancreatic islets. Endocrinology 140(7):3091–3096. doi:10.1210/endo.140.7.6765

    Article  CAS  PubMed  Google Scholar 

  37. Lin YW, Lien LM, Yeh TS, Wu HM, Liu YL, Hsieh RH (2008) 9-cis retinoic acid induces retinoid X receptor localized to the mitochondria for mediation of mitochondrial transcription. Biochem Biophys Res Commun 377(2):351–354. doi:10.1016/j.bbrc.2008.09.122

    Article  CAS  PubMed  Google Scholar 

  38. Truckenmiller ME, Vawter MP, Cheadle C, Coggiano M, Donovan DM, Freed WJ, Becker KG (2001) Gene expression profile in early stage of retinoic acid-induced differentiation of human SH-SY5Y neuroblastoma cells. Restor Neurol Neurosci 18(2–3):67–80

    CAS  PubMed  Google Scholar 

  39. Pasquali MA, Gelain DP, Zanotto-Filho A, de Souza LF, de Oliveira RB, Klamt F, Moreira JC (2008) Retinol and retinoic acid modulate catalase activity in Sertoli cells by distinct and gene expression-independent mechanisms. Toxicol In Vitro 22(5):1177–1183. doi:10.1016/j.tiv.2008.03.007

    Article  CAS  PubMed  Google Scholar 

  40. Gelain DP, de Bittencourt Pasquali MA, Caregnato FF, Zanotto-Filho A, Moreira JC (2008) Retinol up-regulates the receptor for advanced glycation endproducts (RAGE) by increasing intracellular reactive species. Toxicol In Vitro 22(5):1123–1127. doi:10.1016/j.tiv.2008.02.016

    Article  CAS  PubMed  Google Scholar 

  41. Gelain DP, de Bittencourt Pasquali MA, Zanotto-Filho A, de Souza LF, de Oliveira RB, Klamt F, Moreira JC (2008) Retinol increases catalase activity and protein content by a reactive species-dependent mechanism in Sertoli cells. Chem Biol Interact 174(1):38–43. doi:10.1016/j.cbi.2008.04.025

    Article  CAS  PubMed  Google Scholar 

  42. Zanotto-Filho A, Cammarota M, Gelain DP, Oliveira RB, Delgado-Canedo A, Dalmolin RJ, Pasquali MA, Moreira JC (2008) Retinoic acid induces apoptosis by a non-classical mechanism of ERK1/2 activation. Toxicol In Vitro 22(5):1205–1212. doi:10.1016/j.tiv.2008.04.001

    Article  CAS  PubMed  Google Scholar 

  43. Pasquali MA, Gelain DP, Oliveira MR, Behr GA, Motta LL, Rocha RF, Klamt F, Moreira JC (2009) Vitamin A supplementation induces oxidative stress and decreases the immunocontent of catalase and superoxide dismutase in rat lungs. Exp Lung Res 35(5):427–438. doi:10.1080/01902140902747436

    Article  CAS  PubMed  Google Scholar 

  44. Pasquali MA, Gelain DP, de Oliveira MR, Behr GA, da Motta LL, da Rocha RF, Klamt F, Moreira JC (2009) Vitamin A supplementation for different periods alters oxidative parameters in lungs of rats. J Med Food 12(6):1375–1380. doi:10.1089/jmf.2008.0298

    Article  CAS  PubMed  Google Scholar 

  45. Pasquali MA, Schnorr CE, Feistauer LB, Gelain DP, Moreira JC (2010) Vitamin A supplementation to pregnant and breastfeeding female rats induces oxidative stress in the neonatal lung. Reprod Toxicol 30(3):452–456. doi:10.1016/j.reprotox.2010.05.085

    Article  CAS  PubMed  Google Scholar 

  46. de Bittencourt Pasquali MA, Roberto de Oliveira M, De Bastiani MA, da Rocha RF, Schnorr CE, Gasparotto J, Gelain DP, Moreira JC (2012) k-NAME co-treatment prevent oxidative damage in the lung of adult Wistar rats treated with vitamin A supplementation. Cell Biochem Funct 30(3):256–263

    Article  PubMed  Google Scholar 

  47. Auten RL, O'Reilly MA, Oury TD, Nozik-Grayck E, Whorton MH (2006) Transgenic extracellular superoxide dismutase protects postnatal alveolar epithelial proliferation and development during hyperoxia. Am J Physiol Lung Cell Mol Physiol 290(1):L32–L40. doi:10.1152/ajplung.00133.2005

    Article  CAS  PubMed  Google Scholar 

  48. Dong A, Shen J, Krause M, Akiyama H, Hackett SF, Lai H, Campochiaro PA (2006) Superoxide dismutase 1 protects retinal cells from oxidative damage. J Cell Physiol 208(3):516–526. doi:10.1002/jcp.20683

    Article  CAS  PubMed  Google Scholar 

  49. Holtzclaw WD, Dinkova-Kostova AT, Talalay P (2004) Protection against electrophile and oxidative stress by induction of phase 2 genes: the quest for the elusive sensor that responds to inducers. Adv Enzyme Regul 44:335–367. doi:10.1016/j.advenzreg.2003.11.013

    Article  CAS  PubMed  Google Scholar 

  50. Nguyen T, Nioi P, Pickett CB (2009) The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J Biol Chem 284(20):13291–13295. doi:10.1074/jbc.R900010200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Miao W, Hu L, Scrivens PJ, Batist G (2005) Transcriptional regulation of NF-E2 p45-related factor (NRF2) expression by the aryl hydrocarbon receptor-xenobiotic response element signaling pathway: direct cross-talk between phase I and II drug-metabolizing enzymes. J Biol Chem 280(21):20340–20348. doi:10.1074/jbc.M412081200

    Article  CAS  PubMed  Google Scholar 

  52. Lau A, Villeneuve NF, Sun Z, Wong PK, Zhang DD (2008) Dual roles of Nrf2 in cancer. Pharmacol Res 58(5–6):262–270. doi:10.1016/j.phrs.2008.09.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Niture SK, Khatri R, Jaiswal AK (2014) Regulation of Nrf2-an update. Free Radic Biol Med 66:36–44. doi:10.1016/j.freeradbiomed.2013.02.008

    Article  CAS  PubMed  Google Scholar 

  54. Chen KF, Chen HL, Tai WT, Feng WC, Hsu CH, Chen PJ, Cheng AL (2011) Activation of phosphatidylinositol 3-kinase/Akt signaling pathway mediates acquired resistance to sorafenib in hepatocellular carcinoma cells. J Pharmacol Exp Ther 337(1):155–161. doi:10.1124/jpet.110.175786

    Article  CAS  PubMed  Google Scholar 

  55. Lopez-Carballo G, Moreno L, Masia S, Perez P, Barettino D (2002) Activation 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(28):25297–25304. doi:10.1074/jbc.M201869200

    Article  CAS  PubMed  Google Scholar 

  56. Vanlandingham JW, Tassabehji NM, Somers RC, Levenson CW (2005) Expression profiling of p53-target genes in copper-mediated neuronal apoptosis. Neuromolecular Med 7(4):311–324. doi:10.1385/NMM:7:4:311

    Article  CAS  PubMed  Google Scholar 

  57. Culmsee C, Mattson MP (2005) p53 in neuronal apoptosis. Biochem Biophys Res Commun 331(3):761–777. doi:10.1016/j.bbrc.2005.03.149

    Article  CAS  PubMed  Google Scholar 

  58. Nagao M, Campbell K, Burns K, Kuan CY, Trumpp A, Nakafuku M (2008) Coordinated control of self-renewal and differentiation of neural stem cells by Myc and the p19ARF-p53 pathway. J Cell Biol 183(7):1243–1257. doi:10.1083/jcb.200807130, jcb.200807130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Meletis K, Wirta V, Hede SM, Nister M, Lundeberg J, Frisen J (2006) p53 suppresses the self-renewal of adult neural stem cells. Development 133(2):363–369. doi:10.1242/dev.02208

    Article  CAS  PubMed  Google Scholar 

  60. Xavier JM, Morgado AL, Sola S, Rodrigues CM (2014) Mitochondrial translocation of p53 modulates neuronal fate by preventing differentiation-induced mitochondrial stress. Antioxid Redox Signal. doi:10.1089/ars.2013.5417

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was funded by the National Counsel of Technological and Scientific Development (CNPq) (grants: 560221/2010-0, and 470973/2012-9), and FAPERGS (grants: PG 12/1060-6, and IPG 0427-2551/14-0).

Conflict of Interest

The authors declare no conflict of interest

Author information

Authors and Affiliations

  1. Departamento de Bioquímica, Centro de Estudos em Estresse Oxidativo, Universidade Federal do Rio Grande do Sul—UFRGS, Rua Ramiro Barcelos 2600, Cep 90035-003, Porto Alegre, Rio Grande do Sul, Brazil

    Matheus Augusto de Bittencourt Pasquali, Vitor Miranda de Ramos, Ricardo D′Oliveira Albanus, Alice Kunzler, Luis Henrinque Trentin de Souza, Daniel Pens Gelain & José Cláudio Fonseca Moreira

  2. Departamento de Bioquímica, Instituto de Medicina Tropical, Universidade Federal do Rio Grande do Norte—UFRN, Avenida Senador Salgado Filho 3000, Cep 59078-900, Natal, Rio Grande do Norte, Brazil

    Matheus Augusto de Bittencourt Pasquali & Rodrigo Juliani Siqueira Dalmolin

  3. Departamento de Informática Aplicada, Universidade Federal do Rio Grande do Sul—UFRGS, Rua Bento Gonçalves 9500, Cep 91501-970, Porto Alegre, Rio Grande do Sul, Brazil

    Leila Ribeiro & Luigi Carro

Authors
  1. Matheus Augusto de Bittencourt Pasquali
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vitor Miranda de Ramos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ricardo D′Oliveira Albanus
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alice Kunzler
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Luis Henrinque Trentin de Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rodrigo Juliani Siqueira Dalmolin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Daniel Pens Gelain
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Leila Ribeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Luigi Carro
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. José Cláudio Fonseca Moreira
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matheus Augusto de Bittencourt Pasquali.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Bittencourt Pasquali, M.A., de Ramos, V.M., Albanus, R.D. et al. Gene Expression Profile of NF-κB, Nrf2, Glycolytic, and p53 Pathways During the SH-SY5Y Neuronal Differentiation Mediated by Retinoic Acid. Mol Neurobiol 53, 423–435 (2016). https://doi.org/10.1007/s12035-014-8998-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12035-014-8998-9

Keywords

Search

Navigation