Skip to main content

Advertisement

SpringerLink
Log in

Impact of Reck expression and promoter activity in neuronal in vitro differentiation

  • Short Communication
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Reck (REversion-inducing Cysteine-rich protein with Kazal motifs) tumor suppressor gene encodes a multifunctional glycoprotein which inhibits the activity of several matrix metalloproteinases (MMPs), and has the ability to modulate the Notch and canonical Wnt pathways. Reck-deficient neuro-progenitor cells undergo precocious differentiation; however, modulation of Reck expression during progression of the neuronal differentiation process is yet to be characterized. In the present study, we demonstrate that Reck expression levels are increased during in vitro neuronal differentiation of PC12 pheochromocytoma cells and P19 murine teratocarcinoma cells and characterize mouse Reck promoter activity during this process. Increased Reck promoter activity was found upon induction of differentiation in PC12 cells, in accordance with its increased mRNA expression levels in mouse in vitro models. Interestingly, Reck overexpression, prior to the beginning of the differentiation protocol, led to diminished efficiency of the neuronal differentiation process. Taken together, our findings suggest that increased Reck expression at early stages of differentiation diminishes the number of neuron-like cells, which are positive for the beta-3 tubulin marker. Our data highlight the importance of Reck expression evaluation to optimize in vitro neuronal differentiation protocols.

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

References

  1. Assis-Ribas T, Forni MF, Winnischofer SMB, Sogayar MC, Trombetta-Lima M (2018) Extracellular matrix dynamics during mesenchymal stem cells differentiation. Dev Biol 437(2):63–74. https://doi.org/10.1016/j.ydbio.2018.03.002

    Article  CAS  PubMed  Google Scholar 

  2. Ferrer-Ferrer M, Dityatev A (2018) Shaping synapses by the neural extracellular matrix. Front Neuroanat 12:40. https://doi.org/10.3389/fnana.2018.00040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Su W, Matsumoto S, Sorg B, Sherman LS (2019) Distinct roles for hyaluronan in neural stem cell niches and perineuronal nets. Matrix Biol 78–79:272–283. https://doi.org/10.1016/j.matbio.2018.01.022

    Article  CAS  PubMed  Google Scholar 

  4. Itoh Y, Nagase H (2002) Matrix metalloproteinases in cancer. Essays Biochem 38:21–36

    Article  CAS  PubMed  Google Scholar 

  5. Bijata M, Labus J, Guseva D, Stawarski M, Butzlaff M, Dzwonek J, Schneeberg J, Böhm K, Michaluk P, Rusakov DA, Dityatev A, Wilczyński G, Wlodarczyk J, Ponimaskin E (2017) Synaptic remodeling depends on signaling between serotonin receptors and the extracellular matrix. Cell Rep 19(9):1767–1782. https://doi.org/10.1016/j.celrep.2017.05.023

    Article  CAS  PubMed  Google Scholar 

  6. Ali SA, Pappas IS, Parnavelas JG (1998) Collagen type IV promotes the differentiation of neuronal progenitors and inhibits astroglial differentiation in cortical cell cultures. Brain Res Dev Brain Res 110(1):31–38

    Article  CAS  PubMed  Google Scholar 

  7. Tonti GA, Mannello F, Cacci E, Biagioni S (2009) Neural stem cells at the crossroads: MMPs may tell the way. Int J Dev Biol 53(1):1–17. https://doi.org/10.1387/ijdb.082573gt

    Article  CAS  PubMed  Google Scholar 

  8. Lemmens K, Bollaerts I, Bhumika S, de Groef L, Van Houcke J, Darras VM, Van Hove I, Moons L (2016) Matrix metalloproteinases as promising regulators of axonal regrowth in the injured adult zebrafish retinotectal system: MMP in regenerative zebrafish retina. J Comp Neurol 524(7):1472–1493. https://doi.org/10.1002/cne.23920

    Article  CAS  PubMed  Google Scholar 

  9. Miyata S, Kitagawa H (2017) Formation and remodeling of the brain extracellular matrix in neural plasticity: roles of chondroitin sulfate and hyaluronan. Biochim Biophys Acta Gen Subj 1861(10):2420–2434. https://doi.org/10.1016/j.bbagen.2017.06.010

    Article  CAS  PubMed  Google Scholar 

  10. Shu T, Liu C, Pang M, Wang J, Liu B, Zhou W, Wang X, Wu T, Wang Q, Rong L (2018) Effects and mechanisms of matrix metalloproteinase 2 on neural differentiation of induced pluripotent stem cells. Brain Res 1678:407–418. https://doi.org/10.1016/j.brainres.2017.11.006

    Article  CAS  PubMed  Google Scholar 

  11. Takahashi C, Sheng Z, Horan TP, Kitayama H, Maki M, Hitomi K, Kitaura Y, Takai S, Sasahara RM, Horimoto A, Ikawa Y, Ratzkin BJ, Arakawa T, Noda M (1998) Regulation of matrix metalloproteinase-9 and inhibition of tumor invasion by the membrane-anchored glycoprotein RECK. Proc Natl Acad Sci U S A 95(22):13221–13226. https://doi.org/10.1073/pnas.95.22.13221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Oh J, Takahashi R, Kondo S, Mizoguchi A, Adachi E, Sasahara RM, Nishimura S, Imamura Y, Kitayama H, Alexander DB, Ide C, Horan TP, Arakawa T, Yoshida H, Nishikawa S, Itoh Y, Seiki M, Itohara S, Takahashi C, Noda M (2001) The membrane-anchored MMP inhibitor RECK is a key regulator of extracellular matrix integrity and angiogenesis. Cell 107(6):789–800

    Article  CAS  PubMed  Google Scholar 

  13. Omura A, Matsuzaki T, Mio K, Ogura T, Yamamoto M, Fujita A, Okawa K, Kitayama H, Takahashi C, Sato C, Noda M (2009) RECK forms cowbell-shaped dimers and inhibits matrix metalloproteinase-catalyzed cleavage of fibronectin. J Biol Chem 284(6):3461–3469. https://doi.org/10.1074/jbc.M806212200

    Article  CAS  PubMed  Google Scholar 

  14. Miki T, Takegami Y, Okawa K, Muraguchi T, Noda M, Takahashi C (2007) The reversion-inducing cysteine-rich protein with Kazal motifs (RECK) interacts with membrane type 1 matrix metalloproteinase and CD13/aminopeptidase N and modulates their endocytic pathways. J Biol Chem 282(16):12341–12352. https://doi.org/10.1074/jbc.M610948200

    Article  CAS  PubMed  Google Scholar 

  15. Muraguchi T, Takegami Y, Ohtsuka T, Kitajima S, Chandana EPS, Omura A, Miki T, Takahashi R, Matsumoto N, Ludwig A, Noda M, Takahashi C (2007) RECK modulates Notch signaling during cortical neurogenesis by regulating ADAM10 activity. Nat Neurosci 10(7):838–845. https://doi.org/10.1038/nn1922

    Article  CAS  PubMed  Google Scholar 

  16. Ulrich F, Carretero-Ortega J, Menéndez J, Narvaez C, Sun B, Lancaster E, Pershad V, Trzaska S, Véliz E, Kamei M, Prendergast A, Kidd KR, Shaw KM, Castranova DA, Pham VN, Lo BD, Martin BL, Raible DW, Weinstein BM, Torres-Vázquez J (2016) Reck enables cerebrovascular development by promoting canonical Wnt signaling. Development 143(1):147–159. https://doi.org/10.1242/dev.123059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Cho C, Smallwood PM, Nathans J (2017) Reck and Gpr124 are essential receptor cofactors for Wnt7a/Wnt7b-specific signaling in mammalian CNS angiogenesis and blood-brain barrier regulation. Neuron 95(5):1056–1073.e5. https://doi.org/10.1016/j.neuron.2017.07.031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Vallon M, Yuki K, Nguyen TD, Chang J, Yuan J, Siepe D, Miao Y, Essler M, Noda M, Garcia KC, Kuo CJ (2018) A RECK-WNT7 receptor-ligand interaction enables isoform-specific regulation of Wnt bioavailability. Cell Rep 25(2):339–349.e9. https://doi.org/10.1016/j.celrep.2018.09.045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Echizenya M, Kondo S, Takahashi R, Oh J, Kawashima S, Kitayama H, Takahashi C, Noda M (2005) The membrane-anchored MMP-regulator RECK is a target of myogenic regulatory factors. Oncogene 24(38):5850–5857. https://doi.org/10.1038/sj.onc.1208733

    Article  CAS  PubMed  Google Scholar 

  20. Kondo S, Shukunami C, Morioka Y, Matsumoto N, Takahashi R, Oh J, Atsumi T, Umezawa A, Kudo A, Kitayama H, Hiraki Y, Noda M (2007) Dual effects of the membrane-anchored MMP regulator RECK on chondrogenic differentiation of ATDC5 cells. J Cell Sci 120(5):849–857. https://doi.org/10.1242/jcs.03388

    Article  CAS  PubMed  Google Scholar 

  21. Zambuzzi WF, Yano CL, Cavagis ADM, Peppelenbosch MP, Granjeiro JM, Ferreira CV (2009) Ascorbate-induced osteoblast differentiation recruits distinct MMP-inhibitors: RECK and TIMP-2. Mol Cell Biochem 322(1–2):143–150. https://doi.org/10.1007/s11010-008-9951-x

    Article  CAS  PubMed  Google Scholar 

  22. Mahl C, Egea V, Megens RTA, Pitsch T, Santovito D, Weber C, Ries C (2016) RECK (reversion-inducing cysteine-rich protein with Kazal motifs) regulates migration, differentiation and Wnt/β-catenin signaling in human mesenchymal stem cells. Cell Mol Life Sci 73(7):1489–1501. https://doi.org/10.1007/s00018-015-2054-4

    Article  CAS  PubMed  Google Scholar 

  23. Hayashi MAF, Guerreiro JR, Cassola AC, Lizier NF, Kerkis A, Camargo ACM, Kerkis I (2010) Long-term culture of mouse embryonic stem cell-derived adherent neurospheres and functional neurons. Tissue Eng Part C Methods 16(6):1493–1502. https://doi.org/10.1089/ten.TEC.2009.0788

    Article  CAS  PubMed  Google Scholar 

  24. Sukoyan MA, Kerkis AY, Mello MRB, Kerkis IE, Visintin JA, Pereira LV (2002) Establishment of new murine embryonic stem cell lines for the generation of mouse models of human genetic diseases. Braz J Med Biol Res 35(5):535–542. https://doi.org/10.1590/S0100-879X2002000500004

    Article  CAS  PubMed  Google Scholar 

  25. Leszczyński P, Śmiech M, Teeli AS, Zołocińska A, Słysz A, Pojda Z, Pierzchała M, Taniguchi H (2019) Neurogenesis using P19 embryonal carcinoma cells. J Vis Exp 146:58225. https://doi.org/10.3791/58225

    Article  CAS  Google Scholar 

  26. Hayashi MAF, Guerreiro JR, Charych E, Kamiya A, Barbosa RL, Machado MF, Campeiro JD, Oliveira V, Sawa A, Camargo ACM, Brandon NJ (2010) Assessing the role of endooligopeptidase activity of Ndel1 (nuclear-distribution gene E homolog like-1) in neurite outgrowth. Mol Cell Neurosci 44(4):353–361. https://doi.org/10.1016/j.mcn.2010.04.006

    Article  CAS  PubMed  Google Scholar 

  27. Santiago MF, Liour SS, Mendez-Otero R, Yu RK (2005) Glial-guided neuronal migration in P19 embryonal carcinoma stem cell aggregates. J Neurosci Res 81(1):9–20. https://doi.org/10.1002/jnr.20532

    Article  CAS  PubMed  Google Scholar 

  28. Sasahara RM, Takahashi C, Noda M (1999) Involvement of the Sp1 site in ras-mediated downregulation of the RECK metastasis suppressor gene. Biochem Biophys Res Commun 264(3):668–675. https://doi.org/10.1006/bbrc.1999.1552

    Article  CAS  PubMed  Google Scholar 

  29. Guerreiro JR, Winnischofer SMB, Bastos MF, Portaro FCV, Sogayar MC, de Camargo ACM, Hayashi MAF (2005) Cloning and characterization of the human and rabbit NUDEL-oligopeptidase promoters and their negative regulation. Biochim Biophys Acta 1730(1):77–84

    Article  CAS  PubMed  Google Scholar 

  30. Ausubel FM (ed) (1987) Current protocols in molecular biology. Wiley, New York

    Google Scholar 

  31. Messeguer X, Escudero R, Farré D, Núñez O, Martínez J, Albà MM (2002) PROMO: Detection of known transcription regulatory elements using species-tailored searches. Bioinformatics (Oxford, England) 18(2):333–334. https://doi.org/10.1093/bioinformatics/18.2.333

    Article  CAS  Google Scholar 

  32. Farré D, Roset R, Huerta M, Adsuara JE, Roselló L, Albà MM, Messeguer X (2003) Identification of patterns in biological sequences at the ALGGEN server: PROMO and MALGEN. Nucleic Acids Res 31(13):3651–3653. https://doi.org/10.1093/nar/gkg605

    Article  PubMed  PubMed Central  Google Scholar 

  33. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9):e45. https://doi.org/10.1093/nar/29.9.e45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3(7):research0034.1. https://doi.org/10.1186/gb-2002-3-7-research0034

    Article  Google Scholar 

  35. 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(7):2424–2428. https://doi.org/10.1073/pnas.73.7.2424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Liu C, Zhong Y, Apostolou A, Fang S (2013) Neural differentiation of human embryonic stem cells as an in vitro tool for the study of the expression patterns of the neuronal cytoskeleton during neurogenesis. Biochem Biophys Res Commun 439(1):154–159. https://doi.org/10.1016/j.bbrc.2013.07.130

    Article  CAS  PubMed  Google Scholar 

  37. Ito K, Sanosaka T, Igarashi K, Ideta-Otsuka M, Aizawa A, Uosaki Y, Noguchi A, Arakawa H, Nakashima K, Takizawa T (2016) Identification of genes associated with the astrocyte-specific gene Gfap during astrocyte differentiation. Sci Rep 6(1):23903. https://doi.org/10.1038/srep23903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Iso T, Kedes L, Hamamori Y (2003) HES and HERP families: multiple effectors of the notch signaling pathway. J Cell Phys 194(3):237–255. https://doi.org/10.1002/jcp.10208

    Article  CAS  Google Scholar 

  39. Lee JB, Werbowetski-Ogilvie TE, Lee J-H, McIntyre BAS, Schnerch A, Hong S-H, Park I-H, Daley GQ, Bernstein ID, Bhatia M (2013) Notch-HES1 signaling axis controls hemato-endothelial fate decisions of human embryonic and induced pluripotent stem cells. Blood 122(7):1162–1173. https://doi.org/10.1182/blood-2012-12-471649

    Article  CAS  PubMed  Google Scholar 

  40. Kobayashi T, Kageyama R (2010) Hes1 regulates embryonic stem cell differentiation by suppressing Notch signaling: regulation of ES cell differentiation. Genes Cells 15(7):689–698. https://doi.org/10.1111/j.1365-2443.2010.01413.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Naranjo JR, Mellström B, Auwerx J, Mollinedo F, Sassone-Corsi P (1990) Unusual c- fos induction upon chromaffin PC12 differentiation by sodium butyrate: loss of fos autoregulatory function. Nucleic Acids Res 18:3605–3610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Eriksson M, Taskinen M, Leppä S (2007) Mitogen activated protein kinase-dependent activation of c-Jun and c-Fos is required for neuronal differentiation but not for growth and stress response in PC12 cells. J Cell Physiol 210:538–548

    Article  CAS  PubMed  Google Scholar 

  43. Velazquez FN, Prucca CG, Etienne O, D’Astolfo DS, Silvestre DC, Boussin FD, Caputto BL (2015) Brain development is impaired in c-fos -/- mice. Oncotarget 6:16883

    Article  PubMed  PubMed Central  Google Scholar 

  44. Ishibashi M, Moriyoshi K, Sasai Y, Shiota K, Nakanishi S, Kageyama R (1994) Persistent expression of helix-loop-helix factor HES-1 prevents mammalian neural differentiation in the central nervous system. EMBO J 13:1799–1805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Ishibashi M, Ang SL, Shiota K, Nakanishi S, Kageyama R, Guillemot F (1995) Targeted disruption of mammalian hairy and Enhancer of split homolog-1 (HES-1) leads to up-regulation of neural helix-loop-helix factors, premature neurogenesis, and severe neural tube defects. Genes Dev 9:3136–3148

    Article  CAS  PubMed  Google Scholar 

  46. Cortés-Canteli M, Pignatelli M, Santos A, Perez-Castillo A (2002) CCAAT/enhancer-binding protein β plays a regulatory role in differentiation and apoptosis of neuroblastoma cells. J Biol Chem 277:5460–5467

    Article  PubMed  Google Scholar 

  47. Cortes-Canteli M, Aguilar-Morante D, Sanz-SanCristobal M, Megias D, Santos A, Perez-Castillo A (2011) Role of C/EBPβ transcription factor in adult hippocampal neurogenesis. PLoS ONE 6:e24842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Domizi P, Aoyama C, Banchio C (1841) Choline kinase alpha expression during RA-induced neuronal differentiation: Role of C/EBPβ. Biochim Biophys Acta BBA 2014:544–551

    Google Scholar 

  49. Groot de RP, Kruijer W (1991) Up-regulation of Jun/AP-1 during differentiation of N1E–115 neuroblastoma cells. Cell Growth Differ 2:631–636

    PubMed  Google Scholar 

  50. Leppa S (1998) Differential regulation of c-Jun by ERK and JNK during PC12 cell differentiation. EMBO J 17:4404–4413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Vaque JP, Fernandez-Garcia B, Garcia-Sanz P, Ferrandiz N, Bretones G, Calvo F, Crespo P, Marin MC, Leon J (2008) c-Myc inhibits Ras-mediated differentiation of pheochromocytoma cells by blocking c-jun up-regulation. Mol Cancer Res 6:325–339

    Article  CAS  PubMed  Google Scholar 

  52. Lu L, Zhou H, Pan B, Li X, Fu Z, Liu J, Shi Z, Chu T, Wei Z, Ning G, Feng S (2017) c-Jun amino-terminal kinase is involved in valproic acid-mediated neuronal differentiation of mouse embryonic NSCs and neurite outgrowth of NSC-derived neurons. Neurochem Res 42:1254–1266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Yang H, Xia Y, Lu SQ, Soong TW, Feng ZW (2008) Basic fibroblast growth factor-induced neuronal differentiation of mouse bone marrow stromal cells requires FGFR-1, MAPK/ERK, and transcription factor AP-1. J Biol Chem 283:5287–5295

    Article  CAS  PubMed  Google Scholar 

  54. Benkoussa M, Brand C, Delmotte M-H, Formstecher P, Lefebvre P (2002) Retinoic acid receptors inhibit AP1 activation by regulating extracellular signal-regulated kinase and CBP recruitment to an AP1-responsive promoter. Mol Cell Biol 22:4522–4534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Abbott MA, Joksimovic M, Tuggle CK (2005) Ectopic HOXA5 expression results in abnormal differentiation, migration and p53-independent cell death of superficial dorsal horn neurons. Dev Brain Res 159:87–97

    Article  CAS  Google Scholar 

  56. Joksimovic M, Jeannotte L, Tuggle CK (2005) Dynamic expression of murine HOXA5 protein in the central nervous system. Gene Expr Patterns 5:792–800

    Article  CAS  PubMed  Google Scholar 

  57. Hegedus B, Dasgupta B, Shin JE, Emnett RJ, Hart-Mahon EK, Elghazi L, Bernal-Mizrachi E, Gutmann DH (2007) Neurofibromatosis-1 regulates neuronal and glial cell differentiation from neuroglial progenitors in vivo by both cAMP- and Ras-dependent mechanisms. Cell Stem Cell 1:443–457

    Article  CAS  PubMed  Google Scholar 

  58. Patrakitkomjorn S, Kobayashi D, Morikawa T, Wilson MM, Tsubota N, Irie A, Ozawa T, Aoki M, Arimura N, Kaibuchi K, Saya H, Araki N (2008) Neurofibromatosis type 1 (NF1) tumor suppressor, neurofibromin, regulates the neuronal differentiation of PC12 cells via its associating protein, CRMP-2. J Biol Chem 283:9399–9413

    Article  CAS  PubMed  Google Scholar 

  59. Anastasaki C, Gutmann DH (2014) Neuronal NF1/RAS regulation of cyclic AMP requires atypical PKC activation. Hum Mol Genet 23:6712–6721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Son GH, Geum D, Jung H, Kim K (2008) Glucocorticoid inhibits growth factor-induced differentiation of hippocampal progenitor HiB5 cells: effects of glucocorticoid on neuronal differentiation. J Neurochem 79:1013–1021

    Article  Google Scholar 

  61. Terada K, Kojima Y, Watanabe T, Izumo N, Chiba K, Karube Y (2014) Inhibition of nerve growth factor-induced neurite outgrowth from PC12 Cells by dexamethasone: signaling pathways through the glucocorticoid receptor and phosphorylated Akt and ERK1/2. PLoS ONE 9:e93223

    Article  PubMed  PubMed Central  Google Scholar 

  62. Nürnberg E, Horschitz S, Schloss P, Meyer-Lindenberg A (2018) Basal glucocorticoid receptor activation induces proliferation and inhibits neuronal differentiation of human induced pluripotent stem cell-derived neuronal precursor cells. J Steroid Biochem Mol Biol 182:119–126

    Article  PubMed  Google Scholar 

  63. Delfini M-C (2004) Ectopic Myf5 or MyoD prevents the neuronal differentiation program in addition to inducing skeletal muscle differentiation, in the chick neural tube. Development 131:713–723

    Article  CAS  PubMed  Google Scholar 

  64. Fong AP, Yao Z, Zhong JW, Johnson NM, Farr GH, Maves L, Tapscott SJ (2015) Conversion of MyoD to a neurogenic factor: binding site specificity determines lineage. Cell Rep 10:1937–1946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Bai R-Y, Staedtke V, Lidov HG, Eberhart CG, Riggins GJ (2012) OTX2 represses myogenic and neuronal differentiation in medulloblastoma cells. Cancer Res 72:5988–6001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Nardelli J, Thiesson D, Fujiwara Y, Tsai F-Y, Orkin SH (1999) Expression and genetic interaction of transcription factors GATA-2 and GATA-3 during development of the mouse central nervous system. Dev Biol 210:305–321

    Article  CAS  PubMed  Google Scholar 

  67. Herberth B, Minkó K, Csillag A, Jaffredo T, Madarász E (2005) SCL, GATA-2 and Lmo2 expression in neurogenesis. Int J Dev Neurosci 23:449–463

    Article  CAS  PubMed  Google Scholar 

  68. He Y, Dupree J, Wang J, Sandoval J, Li J, Liu H, Shi Y, Nave KA, Casaccia-Bonnefil P (2007) The transcription factor Yin Yang 1 is essential for oligodendrocyte progenitor differentiation. Neuron 55:217–230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Knauss JL, Miao N, Kim S-N, Nie Y, Shi Y, Wu T, Pinto HB, Donohoe ME, Sun T (2018) Long noncoding RNA Sox2ot and transcription factor YY1 co-regulate the differentiation of cortical neural progenitors by repressing Sox2. Cell Death Dis 9:799

    Article  PubMed  PubMed Central  Google Scholar 

  70. Pan HC, Yang CN, Hung YW, Lee WJ, Tien HR, Shen CC, Sheehan J, Chou CT, Sheu ML (2013) Reciprocal modulation of C/EBP-α and C/EBP-β by IL-13 in activated microglia prevents neuronal death. Eur J Immunol 43:2854–2865

    Article  CAS  PubMed  Google Scholar 

  71. Huang T-C, Chang H-Y, Chen C-Y, Wu P-Y, Lee H, Liao Y-F, Hsu W-M, Huang H-C, Juan H-F (2011) Silencing of miR-124 induces neuroblastoma SK-N-SH cell differentiation, cell cycle arrest and apoptosis through promoting AHR. FEBS Lett 585:3582–3586

    Article  CAS  PubMed  Google Scholar 

  72. Dever DP, Adham ZO, Thompson B, Genestine M, Cherry J, Olschowka JA, DiCicco-Bloom E, Opanashuk LA (2016) Aryl hydrocarbon receptor deletion in cerebellar granule neuron precursors impairs neurogenesis: AhR deletion in cerebellar granule neurons. Dev Neurobiol 76:533–550

    Article  CAS  PubMed  Google Scholar 

  73. Kimura E, Tohyama C (2017) Embryonic and postnatal expression of aryl hydrocarbon receptor mrna in mouse brain. Front Neuroanat. https://doi.org/10.3389/fnana.2017.00004

    Article  PubMed  PubMed Central  Google Scholar 

  74. Harris G, Masgutova A, Collin M, Toch M, Hidalgo-Figueroa B, Jacob LM, Corcoran C, Francius F (2018) Clotman, Onecut factors and Pou2f2 regulate the distribution of V2 interneurons in the mouse developing spinal cord. Dev Biol 56:15968

    Google Scholar 

  75. Guerrini L, Blasi F, Denis-Donini S (1995) Synaptic activation of NF-kappa B by glutamate in cerebellar granule neurons in vitro. Proc Natl Acad Sci 92:9077–9081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Gutierrez H, O’Keeffe GW, Gavalda N, Gallagher D, Davies AM (2008) Nuclear factor B signaling either stimulates or inhibits neurite growth depending on the phosphorylation status of p65/RelA. J Neurosci 28:8246–8256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Pozniak PD, Darbinyan A, Khalili K (2016) TNF-α/TNFR2 regulatory axis stimulates EphB2-mediated neuroregeneration via activation of NF-κB: TNF-α activation of EphB2-mediated regeneration. J Cell Physiol 231:1237–1248

    Article  CAS  PubMed  Google Scholar 

  78. i-Altaba R, Prezioso VR, Darnell JE, Jessell TM (1993) Sequential expression of HNF-3β and HNF-3α by embryonic organizing centers: the dorsal lip/node, notochord and floor plate. Mech Dev 44:91–108

    Article  Google Scholar 

  79. Rao MS, Yukawa M, Omori M, Thorgeirsson SS, Reddy JK (1996) Expression of transcription factors and stem cell factor precedes hepatocyte differentiation in rat pancreas. Gene Exp 6:15–22

    CAS  Google Scholar 

  80. Jacob A, Budhiraja S, Reichel RR (1997) Differential induction of HNF-3 transcription factors during neuronal differentiation. Exp Cell Res 234:277–284

    Article  CAS  PubMed  Google Scholar 

  81. Callaghan DA, Dong L, Callaghan SM, Hou YX, Dagnino L, Slack RS (1999) Neural precursor cells differentiating in the absence of Rb exhibit delayed terminal mitosis and deregulated E2F 1 and 3 activity. Dev Biol 207:257–270

    Article  CAS  PubMed  Google Scholar 

  82. Jin Z, Liu L, Bian W, Chen Y, Xu G, Cheng L, Jing N (2009) Different transcription factors regulate nestin gene expression during P19 cell neural differentiation and central nervous system development. J Biol Chem 284:8160–8173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Moasser MM, Reuter VE, Dmitrovsky E (1995) Overexpression of the retinoic acid receptor gamma directly induces terminal differentiation of human embryonal carcinoma cells. Oncogene 10:1537–1543

    CAS  PubMed  Google Scholar 

  84. Calderon F, Kim H-Y (2007) Role of RXR in neurite outgrowth induced by docosahexaenoic acid. Prostaglandins Leukot Essen Fatty Acids 77:227–232

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to Professor Makoto Noda for kindly providing the Reck promoter constructs and to Dr. Irene Yan for kindly providing the rat pheochromocytoma PC12 cells. We also wish to thank Rosemary Oliveira and Michely Reis for secretarial assistance and Ms. Zizi de Mendonça, Dr. Marluce da Cunha Mantovani and Mr. Alan Pereira dos Santos for the excellent technical assistance. We acknowledge the invaluable financial support provided by the following agencies: Brazilian Federal Bank for Social and Economical Development (BNDES) grant number 09.2.1066.1; Federal Agency for Higher Education Training (CAPES/PVE) grant number 88881.068070/2014-01, and CAPES Finance Code 001; Brazilian National Council for Research and Development (CNPq) grant numbers 401430/2013-8, 457601/2013-2, 409960/2013-6, 426896/2016-5, 465656/2014-5, 454234/2014-7 and 455953/2014-7; MCS, MAF and HU are recipients of CNPq Productivity Award (number 3118/2015-6, 304566/2019-5 and 306392/2017-8, respectively; São Paulo Research State Foundation (FAPESP) grant numbers 2016/05311-2, 2016/18277-7; 2015/26328-8, 2014/50891-1, 2017/02413-1, 2018/20014-0, 2012/50880-4, 2018/07366-4, 2017/02413-1 and 2019/13112-8; Brazilian Federal Agency for Studies and Projects (FINEP) grants 01.08.0622.05, 51634-1 AD and 01.08.0484.00); Brazilian Science and Technology Ministry (MCTI) and the Health Ministry (MS-DECIT).

Author information

Authors and Affiliations

  1. Núcleo de Terapia Celular e Molecular (NUCEL), Faculdade de Medicina, Universidade de São Paulo (USP), Rua Pangaré, 100 (Cidade Universitária), São Paulo, SP, 05360-130, Brazil

    Marina Trombetta-Lima, Thais Assis-Ribas & Mari C. Sogayar

  2. Departamento de Bioquímica, Instituto de Química, Universidade de São Paulo (USP), São Paulo, SP, 05508-000, Brazil

    Ricardo C. Cintra, Isis C. C. Nascimento, Henning Ulrich & Mari C. Sogayar

  3. Departamento de Farmacologia, Escola Paulista de Medicina (EPM), Universidade Federal de São Paulo (UNIFESP), Rua 3 de Maio 100, Ed INFAR, 3º andar, São Paulo, SP, 04044-020, Brazil

    Joana D. Campeiro & Mirian A. F. Hayashi

  4. Faculdade de Farmácia, Universidade Paulista (UNIP), São Paulo, SP, 05347-020, Brazil

    Juliano R. Guerreiro

  5. Departamento de Bioquímica e Biologia Molecular, Universidade Federal do Paraná (UFPR), Curitiba, PR, 81531-990, Brazil

    Sheila M. B. Winnischofer

  6. Departamento de Biologia Celular, Universidade Federal do Paraná (UFPR), Curitiba, PR, 81531-990, Brazil

    Sheila M. B. Winnischofer

Authors
  1. Marina Trombetta-Lima
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thais Assis-Ribas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ricardo C. Cintra
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joana D. Campeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Juliano R. Guerreiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sheila M. B. Winnischofer
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Isis C. C. Nascimento
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Henning Ulrich
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Mirian A. F. Hayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Mari C. Sogayar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Mirian A. F. Hayashi or Mari C. Sogayar.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The present study followed the principles of ethical and professional conduct. No human material or animal subjects were used.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

11033_2021_6175_MOESM1_ESM.docx

Electronic supplementary material 1 (DOCX 188 kb) Reck mRNA expression during the different stages of the neuronal differentiation protocol of USP-4 murine embryonic cells. EB stands for embryoid bodies or spheroids; and DIF for the final differentiation stage. * represents p < 0.05, and ** p < 0.01 (DOCX 187 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Trombetta-Lima, M., Assis-Ribas, T., Cintra, R.C. et al. Impact of Reck expression and promoter activity in neuronal in vitro differentiation. Mol Biol Rep 48, 1985–1994 (2021). https://doi.org/10.1007/s11033-021-06175-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-021-06175-6

Keywords

Search

Navigation