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AMPK Activation of PGC-1α/NRF-1-Dependent SELENOT Gene Transcription Promotes PACAP-Induced Neuroendocrine Cell Differentiation Through Tolerance to Oxidative Stress

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Abstract

Several cues including pituitary adenylate cyclase-activating polypeptide (PACAP), which acts through cAMP stimulation, specify the conversion of sympathoadrenal (SA) precursors toward different cell phenotypes by promoting their survival and differentiation. Selenoprotein T (SELENOT) is a PACAP-stimulated ER oxidoreductase that exerts an essential antioxidant activity and whose up-regulation is associated with SA cell differentiation. In the present study, we investigated the transcriptional cascade elicited by PACAP/cAMP to trigger SELENOT gene transcription during the conversion of PC12 cells from SA progenitor-like cells toward a neuroendocrine phenotype. Unexpectedly, we found that PACAP/cAMP recruits the canonical pathway that regulates mitochondrial function in order to elicit SELENOT gene transcription and the consequent antioxidant response during PC12 cell differentiation. This cascade involves LKB1-mediated AMPK activation in order to stimulate SELENOT gene transcription through the PGC1-α/NRF-1 complex, thus allowing SELENOT to promote PACAP-stimulated neuroendocrine cell survival and differentiation. Our data reveal that a PACAP and cAMP-activated AMPK-PGC-1α/NRF-1 cascade is critical for the coupling of oxidative stress tolerance, via SELENOT gene expression, and mitochondrial biogenesis in order to achieve PC12 cell differentiation. The data further highlight the essential role of SELENOT in cell metabolism during differentiation.

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References

  1. Francis NJ, Landis SC (1999) Cellular and molecular determinants of sympathetic neuron development. Annu Rev Neurosci 22:541–566. https://doi.org/10.1146/annurev.neuro.22.1.541

    Article  CAS  PubMed  Google Scholar 

  2. Anderson DJ (1993) Molecular control of cell fate in the neural crest: the sympathoadrenal lineage. Annu Rev Neurosci 16:129–158. https://doi.org/10.1146/annurev.ne.16.030193.001021

    Article  CAS  PubMed  Google Scholar 

  3. Huber K (2006) The sympathoadrenal cell lineage: specification, diversification, and new perspectives. Dev Biol 298:335–343. https://doi.org/10.1016/j.ydbio.2006.07.010

    Article  CAS  PubMed  Google Scholar 

  4. Emery AC, Eiden MV, Eiden LE (2014) Separate cyclic AMP sensors for neuritogenesis, growth arrest, and survival of neuroendocrine cells. J Biol Chem 289:10126–10139. https://doi.org/10.1074/jbc.M113.529321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Ravni A, Bourgault S, Lebon A, Chan P, Galas L, Fournier A, Vaudry H, Gonzalez B et al (2006) The neurotrophic effects of PACAP in PC12 cells: control by multiple transduction pathways. J Neurochem 98:321–329. https://doi.org/10.1111/j.1471-4159.2006.03884.x

    Article  CAS  PubMed  Google Scholar 

  6. Grumolato L, Louiset E, Alexandre D, Ait-Ali D, Turquier V, Fournier A, Fasolo A, Vaudry H et al (2003) PACAP and NGF regulate common and distinct traits of the sympathoadrenal lineage: effects on electrical properties, gene markers and transcription factors in differentiating PC12 cells. Eur J Neurosci 17:71–82

    Article  PubMed  Google Scholar 

  7. Ghzili H, Grumolato L, Thouennon E, Vaudry H, Anouar Y (2006) Possible implication of the transcriptional regulator Id3 in PACAP-induced pro-survival signaling during PC12 cell differentiation. Regul Pept 137:89–94. https://doi.org/10.1016/j.regpep.2006.06.015

    Article  CAS  PubMed  Google Scholar 

  8. Hamelink C, Tjurmina O, Damadzic R, Young WS, Weihe E, Lee HW, Eiden LE (2002) Pituitary adenylate cyclase-activating polypeptide is a sympathoadrenal neurotransmitter involved in catecholamine regulation and glucohomeostasis. Proc Natl Acad Sci U S A 99:461–466. https://doi.org/10.1073/pnas.012608999

    Article  CAS  PubMed  Google Scholar 

  9. Deutsch PJ, Sun Y (1992) The 38-amino acid form of pituitary adenylate cyclase-activating polypeptide stimulates dual signaling cascades in PC12 cells and promotes neurite outgrowth. J Biol Chem 267:5108–5113

    CAS  PubMed  Google Scholar 

  10. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Kim T, Tao-Cheng JH, Eiden LE, Loh YP (2001) Chromogranin A, an “on/off” switch controlling dense-core secretory granule biogenesis. Cell 106:499–509

    Article  CAS  PubMed  Google Scholar 

  12. Montero-Hadjadje M, Vaingankar S, Elias S, Tostivint H, Mahata SK, Anouar Y (2008) Chromogranins A and B and secretogranin II: evolutionary and functional aspects. Acta Physiol (Oxf) 192:309–324. https://doi.org/10.1111/j.1748-1716.2007.01806.x

    Article  CAS  Google Scholar 

  13. Grumolato L, Ghzili H, Montero-Hadjadje M, Gasman S, Lesage J, Tanguy Y, Galas L, Ait-Ali D et al (2008) Selenoprotein T is a PACAP-regulated gene involved in intracellular Ca2+ mobilization and neuroendocrine secretion. FASEB J 22:1756–1768. https://doi.org/10.1096/fj.06-075820

    Article  CAS  PubMed  Google Scholar 

  14. Hamieh A, Cartier D, Abid H, Calas A, Burel C, Bucharles C, Jehan C, Grumolato L et al (2017) Selenoprotein T is a novel OST subunit that regulates UPR signaling and hormone secretion. EMBO Rep 18:1935–1946. https://doi.org/10.15252/embr.201643504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Boukhzar L, Hamieh A, Cartier D, Tanguy Y, Alsharif I, Castex M, Arabo A, El Hajji S et al (2016) Selenoprotein T exerts an essential oxidoreductase activity that protects dopaminergic neurons in mouse models of Parkinson’s disease. Antioxid Redox Signal 24:557–574. https://doi.org/10.1089/ars.2015.6478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Castex MT, Arabo A, Benard M, Roy V, Le Joncour V, Prevost G, Bonnet JJ, Anouar Y et al (2016) Selenoprotein T deficiency leads to neurodevelopmental abnormalities and hyperactive behavior in mice. Mol Neurobiol 53:5818–5832. https://doi.org/10.1007/s12035-015-9505-7

    Article  CAS  PubMed  Google Scholar 

  17. Tanguy Y, Falluel-Morel A, Arthaud S, Boukhzar L, Manecka DL, Chagraoui A, Prevost G, Elias S et al (2011) The PACAP-regulated gene selenoprotein T is highly induced in nervous, endocrine, and metabolic tissues during ontogenetic and regenerative processes. Endocrinology 152:4322–4335. https://doi.org/10.1210/en.2011-1246

    Article  CAS  PubMed  Google Scholar 

  18. Anouar Y, Lihrmann I, Falluel-Morel A, Boukhzar L (2018) Selenoprotein T is a key player in ER proteostasis, endocrine homeostasis and neuroprotection. Free Radic Biol Med. https://doi.org/10.1016/j.freeradbiomed.2018.05.076

    Article  CAS  PubMed  Google Scholar 

  19. Prevost G, Arabo A, Jian L, Quelennec E, Cartier D, Hassan S, Falluel-Morel A, Tanguy Y et al (2013) The PACAP-regulated gene selenoprotein T is abundantly expressed in mouse and human beta-cells and its targeted inactivation impairs glucose tolerance. Endocrinology 154:3796–3806. https://doi.org/10.1210/en.2013-1167

    Article  CAS  PubMed  Google Scholar 

  20. Rabinovitch RC, Samborska B, Faubert B, Ma EH, Gravel SP, Andrzejewski S, Raissi TC, Pause A et al (2017) AMPK maintains cellular metabolic homeostasis through regulation of mitochondrial reactive oxygen species. Cell Rep 21:1–9. https://doi.org/10.1016/j.celrep.2017.09.026

    Article  CAS  PubMed  Google Scholar 

  21. Botia B, Seyer D, Ravni A, Benard M, Falluel-Morel A, Cosette P, Jouenne T, Fournier A et al (2008) Peroxiredoxin 2 is involved in the neuroprotective effects of PACAP in cultured cerebellar granule neurons. J Mol Neurosci 36:61–72. https://doi.org/10.1007/s12031-008-9075-5

    Article  CAS  PubMed  Google Scholar 

  22. Grumolato L, Elkahloun AG, Ghzili H, Alexandre D, Coulouarn C, Yon L, Salier JP, Eiden LE et al (2003) Microarray and suppression subtractive hybridization analyses of gene expression in pheochromocytoma cells reveal pleiotropic effects of pituitary adenylate cyclase-activating polypeptide on cell proliferation, survival, and adhesion. Endocrinology 144:2368–2379. https://doi.org/10.1210/en.2002-0106

    Article  CAS  PubMed  Google Scholar 

  23. Miyamoto K, Tsumuraya T, Ohtaki H, Dohi K, Satoh K, Xu Z, Tanaka S, Murai N et al (2014) PACAP38 suppresses cortical damage in mice with traumatic brain injury by enhancing antioxidant activity. J Mol Neurosci 54:370–379. https://doi.org/10.1007/s12031-014-0309-4

    Article  CAS  PubMed  Google Scholar 

  24. Ohtaki H, Satoh A, Nakamachi T, Yofu S, Dohi K, Mori H, Ohara K, Miyamoto K et al (2010) Regulation of oxidative stress by pituitary adenylate cyclase-activating polypeptide (PACAP) mediated by PACAP receptor. J Mol Neurosci 42:397–403. https://doi.org/10.1007/s12031-010-9350-0

    Article  CAS  PubMed  Google Scholar 

  25. Satoh J, Kawana N, Yamamoto Y (2013) Pathway analysis of ChIP-Seq-based NRF1 target genes suggests a logical hypothesis of their involvement in the pathogenesis of neurodegenerative diseases. Gene Regul Syst Bio 7:139–152. https://doi.org/10.4137/GRSB.S13204

    Article  PubMed  PubMed Central  Google Scholar 

  26. Scarpulla RC, Vega RB, Kelly DP (2012) Transcriptional integration of mitochondrial biogenesis. Trends Endocrinol Metab 23:459–466. https://doi.org/10.1016/j.tem.2012.06.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Virbasius CA, Virbasius JV, Scarpulla RC (1993) NRF-1, an activator involved in nuclear-mitochondrial interactions, utilizes a new DNA-binding domain conserved in a family of developmental regulators. Genes Dev 7:2431–2445

    Article  CAS  PubMed  Google Scholar 

  28. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S et al (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98:115–124. https://doi.org/10.1016/S0092-8674(00)80611-X

    Article  CAS  PubMed  Google Scholar 

  29. Knutti D, Kralli A (2001) PGC-1, a versatile coactivator. Trends Endocrinol Metab 12:360–365

    Article  CAS  PubMed  Google Scholar 

  30. St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, Jager S, Handschin C, Zheng K et al (2006) Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127:397–408. https://doi.org/10.1016/j.cell.2006.09.024

    Article  CAS  PubMed  Google Scholar 

  31. Wright DC, Han DH, Garcia-Roves PM, Geiger PC, Jones TE, Holloszy JO (2007) Exercise-induced mitochondrial biogenesis begins before the increase in muscle PGC-1alpha expression. J Biol Chem 282:194–199. https://doi.org/10.1074/jbc.M606116200

    Article  CAS  PubMed  Google Scholar 

  32. Fernandez-Marcos PJ, Auwerx J (2011) Regulation of PGC-1alpha, a nodal regulator of mitochondrial biogenesis. Am J Clin Nutr 93:884S–8890S. https://doi.org/10.3945/ajcn.110.001917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Austin S, St-Pierre J (2012) PGC1alpha and mitochondrial metabolism—emerging concepts and relevance in ageing and neurodegenerative disorders. J Cell Sci 125:4963–4971. https://doi.org/10.1242/jcs.113662

    Article  CAS  PubMed  Google Scholar 

  34. Kahn BB, Alquier T, Carling D, Hardie DG (2005) AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab 1:15–25. https://doi.org/10.1016/j.cmet.2004.12.003

    Article  CAS  PubMed  Google Scholar 

  35. Hardie DG (2011) AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev 25:1895–1908. https://doi.org/10.1101/gad.17420111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Hardie DG (2014) AMPK—sensing energy while talking to other signaling pathways. Cell Metab 20:939–952. https://doi.org/10.1016/j.cmet.2014.09.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Bergeron R, Ren JM, Cadman KS, Moore IK, Perret P, Pypaert M, Young LH, Semenkovich CF et al (2001) Chronic activation of AMP kinase results in NRF-1 activation and mitochondrial biogenesis. Am J Physiol Endocrinol Metab 281:E1340–E1346

    Article  CAS  PubMed  Google Scholar 

  38. Hutchinson DS, Summers RJ, Bengtsson T (2008) Regulation of AMP-activated protein kinase activity by G-protein coupled receptors: potential utility in treatment of diabetes and heart disease. Pharmacol Ther 119:291–310. https://doi.org/10.1016/j.pharmthera.2008.05.008

    Article  CAS  PubMed  Google Scholar 

  39. Gascon S, Murenu E, Masserdotti G, Ortega F, Russo GL, Petrik D, Deshpande A, Heinrich C et al (2016) Identification and successful negotiation of a metabolic checkpoint in direct neuronal reprogramming. Cell Stem Cell 18:396–409. https://doi.org/10.1016/j.stem.2015.12.003

    Article  CAS  PubMed  Google Scholar 

  40. Ravni A, Eiden LE, Vaudry H, Gonzalez BJ, Vaudry D (2006) Cycloheximide treatment to identify components of the transitional transcriptome in PACAP-induced PC12 cell differentiation. J Neurochem 98:1229–1241. https://doi.org/10.1111/j.1471-4159.2006.03962.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Seaborn T, Ravni A, Au R, Chow BK, Fournier A, Wurtz O, Vaudry H, Eiden LE et al (2014) Induction of Serpinb1a by PACAP or NGF is required for PC12 cells survival after serum withdrawal. J Neurochem. https://doi.org/10.1111/jnc.12780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Manecka DL, Lelievre V, Anouar Y (2014) Inhibition of constitutive TNF production is associated with PACAP-mediated differentiation in PC12 cells. FEBS Lett 588:3008–3014. https://doi.org/10.1016/j.febslet.2014.06.009

    Article  CAS  PubMed  Google Scholar 

  43. Manecka DL, Mahmood SF, Grumolato L, Lihrmann I, Anouar Y (2013) Pituitary adenylate cyclase-activating polypeptide (PACAP) promotes both survival and neuritogenesis in PC12 cells through activation of nuclear factor kappaB (NF-kappaB) pathway: involvement of extracellular signal-regulated kinase (ERK), calcium, and c-REL. J Biol Chem 288:14936–14948. https://doi.org/10.1074/jbc.M112.434597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Kienlen Campard P, Crochemore C, Rene F, Monnier D, Koch B, Loeffler JP (1997) PACAP type I receptor activation promotes cerebellar neuron survival through the cAMP/PKA signaling pathway. DNA Cell Biol 16:323–333

    Article  CAS  PubMed  Google Scholar 

  45. Vaudry D, Falluel-Morel A, Bourgault S, Basille M, Burel D, Wurtz O, Fournier A, Chow BK et al (2009) Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacol Rev 61:283–357. https://doi.org/10.1124/pr.109.001370

    Article  CAS  PubMed  Google Scholar 

  46. Scarpulla RC (2006) Nuclear control of respiratory gene expression in mammalian cells. J Cell Biochem 97:673–683. https://doi.org/10.1002/jcb.20743

    Article  CAS  PubMed  Google Scholar 

  47. Hardie DG (2011) Sensing of energy and nutrients by AMP-activated protein kinase. Am J Clin Nutr 93:891S–8896S. https://doi.org/10.3945/ajcn.110.001925

    Article  CAS  PubMed  Google Scholar 

  48. Vazquez-Manrique RP, Farina F, Cambon K, Dolores Sequedo M, Parker AJ, Millan JM, Weiss A, Deglon N et al (2016) AMPK activation protects from neuronal dysfunction and vulnerability across nematode, cellular and mouse models of Huntington’s disease. Hum Mol Genet 25:1043–1058. https://doi.org/10.1093/hmg/ddv513

    Article  CAS  PubMed  Google Scholar 

  49. Williams T, Courchet J, Viollet B, Brenman JE, Polleux F (2011) AMP-activated protein kinase (AMPK) activity is not required for neuronal development but regulates axogenesis during metabolic stress. Proc Natl Acad Sci U S A 108:5849–5854. https://doi.org/10.1073/pnas.1013660108

    Article  PubMed  PubMed Central  Google Scholar 

  50. Dulovic M, Jovanovic M, Xilouri M, Stefanis L, Harhaji-Trajkovic L, Kravic-Stevovic T, Paunovic V, Ardah MT et al (2014) The protective role of AMP-activated protein kinase in alpha-synuclein neurotoxicity in vitro. Neurobiol Dis 63:1–11. https://doi.org/10.1016/j.nbd.2013.11.002

    Article  CAS  PubMed  Google Scholar 

  51. Dasgupta B, Milbrandt J (2007) Resveratrol stimulates AMP kinase activity in neurons. Proc Natl Acad Sci U S A 104:7217–7222. https://doi.org/10.1073/pnas.0610068104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Dasgupta B, Milbrandt J (2009) AMP-activated protein kinase phosphorylates retinoblastoma protein to control mammalian brain development. Dev Cell 16:256–270. https://doi.org/10.1016/j.devcel.2009.01.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Stetler RA, Leak RK, Yin W, Zhang L, Wang S, Gao Y, Chen J (2012) Mitochondrial biogenesis contributes to ischemic neuroprotection afforded by LPS pre-conditioning. J Neurochem 123(Suppl 2):125–137. https://doi.org/10.1111/j.1471-4159.2012.07951.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Salminen A, Kaarniranta K, Haapasalo A, Soininen H, Hiltunen M (2011) AMP-activated protein kinase: a potential player in Alzheimer’s disease. J Neurochem 118:460–474. https://doi.org/10.1111/j.1471-4159.2011.07331.x

    Article  CAS  PubMed  Google Scholar 

  55. Ma TC, Buescher JL, Oatis B, Funk JA, Nash AJ, Carrier RL, Hoyt KR (2007) Metformin therapy in a transgenic mouse model of Huntington’s disease. Neurosci Lett 411:98–103. https://doi.org/10.1016/j.neulet.2006.10.039

    Article  CAS  PubMed  Google Scholar 

  56. Shaw MM, Gurr WK, McCrimmon RJ, Schorderet DF, Sherwin RS (2007) 5′AMP-activated protein kinase alpha deficiency enhances stress-induced apoptosis in BHK and PC12 cells. J Cell Mol Med 11:286–298. https://doi.org/10.1111/j.1582-4934.2007.00023.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Scarpulla RC (2002) Transcriptional activators and coactivators in the nuclear control of mitochondrial function in mammalian cells. Gene 286:81–89

    Article  CAS  PubMed  Google Scholar 

  58. Cam H, Balciunaite E, Blais A, Spektor A, Scarpulla RC, Young R, Kluger Y, Dynlacht BD (2004) A common set of gene regulatory networks links metabolism and growth inhibition. Mol Cell 16:399–411. https://doi.org/10.1016/j.molcel.2004.09.037

    Article  CAS  PubMed  Google Scholar 

  59. Kobayashi M, Yamamoto M (2006) Nrf2-Keap1 regulation of cellular defense mechanisms against electrophiles and reactive oxygen species. Adv Enzym Regul 46:113–140. https://doi.org/10.1016/j.advenzreg.2006.01.007

    Article  CAS  Google Scholar 

  60. Miyamoto N, Izumi H, Miyamoto R, Kondo H, Tawara A, Sasaguri Y, Kohno K (2011) Quercetin induces the expression of peroxiredoxins 3 and 5 via the Nrf2/NRF1 transcription pathway. Invest Ophthalmol Vis Sci 52:1055–1063. https://doi.org/10.1167/iovs.10-5777

    Article  CAS  PubMed  Google Scholar 

  61. Chang C, Wu G, Gao P, Yang L, Liu W, Zuo J (2014) Upregulated Parkin expression protects mitochondrial homeostasis in DJ-1 knockdown cells and cells overexpressing the DJ-1 L166P mutation. Mol Cell Biochem 387:187–195. https://doi.org/10.1007/s11010-013-1884-3

    Article  CAS  PubMed  Google Scholar 

  62. Huo L, Scarpulla RC (2001) Mitochondrial DNA instability and peri-implantation lethality associated with targeted disruption of nuclear respiratory factor 1 in mice. Mol Cell Biol 21:644–654. https://doi.org/10.1128/MCB.21.2.644-654.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Larsson NG, Wang J, Wilhelmsson H, Oldfors A, Rustin P, Lewandoski M, Barsh GS, Clayton DA (1998) Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat Genet 18:231–236. https://doi.org/10.1038/ng0398-231

    Article  CAS  PubMed  Google Scholar 

  64. Becker TS, Burgess SM, Amsterdam AH, Allende ML, Hopkins N (1998) Not really finished is crucial for development of the zebrafish outer retina and encodes a transcription factor highly homologous to human Nuclear Respiratory Factor-1 and avian Initiation Binding Repressor. Development 125:4369–4378

    CAS  PubMed  Google Scholar 

  65. DeSimone SM, White K (1993) The Drosophila erect wing gene, which is important for both neuronal and muscle development, encodes a protein which is similar to the sea urchin P3A2 DNA binding protein. Mol Cell Biol 13:3641–3649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Chang WT, Chen HI, Chiou RJ, Chen CY, Huang AM (2005) A novel function of transcription factor alpha-Pal/NRF-1: increasing neurite outgrowth. Biochem Biophys Res Commun 334:199–206. https://doi.org/10.1016/j.bbrc.2005.06.079

    Article  CAS  PubMed  Google Scholar 

  67. Evans MJ, Scarpulla RC (1990) NRF-1: a trans-activator of nuclear-encoded respiratory genes in animal cells. Genes Dev 4:1023–1034

    Article  CAS  PubMed  Google Scholar 

  68. Hawley SA, Pan DA, Mustard KJ, Ross L, Bain J, Edelman AM, Frenguelli BG, Hardie DG (2005) Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab 2:9–19. https://doi.org/10.1016/j.cmet.2005.05.009

    Article  CAS  PubMed  Google Scholar 

  69. Collins SP, Reoma JL, Gamm DM, Uhler MD (2000) LKB1, a novel serine/threonine protein kinase and potential tumour suppressor, is phosphorylated by cAMP-dependent protein kinase (PKA) and prenylated in vivo. Biochem J 345(Pt 3):673–680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Vaudry D, Gonzalez BJ, Basille M, Anouar Y, Fournier A, Vaudry H (1998) Pituitary adenylate cyclase-activating polypeptide stimulates both c-fos gene expression and cell survival in rat cerebellar granule neurons through activation of the protein kinase A pathway. Neuroscience 84:801–812

    Article  CAS  PubMed  Google Scholar 

  71. Onoue S, Endo K, Ohshima K, Yajima T, Kashimoto K (2002) The neuropeptide PACAP attenuates beta-amyloid (1-42)-induced toxicity in PC12 cells. Peptides 23:1471–1478

    Article  CAS  PubMed  Google Scholar 

  72. Frodin M, Peraldi P, Van Obberghen E (1994) Cyclic AMP activates the mitogen-activated protein kinase cascade in PC12 cells. J Biol Chem 269:6207–6214

  73. Villalba M, Bockaert J, Journot L (1997) Pituitary adenylate cyclase-activating polypeptide (PACAP-38) protects cerebellar granule neurons from apoptosis by activating the mitogen-activated protein kinase (MAP kinase) pathway. J Neurosci 17:83–90

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Emery AC, Eiden LE (2012) Signaling through the neuropeptide GPCR PAC(1) induces neuritogenesis via a single linear cAMP- and ERK-dependent pathway using a novel cAMP sensor. FASEB J 26:3199–3211. https://doi.org/10.1096/fj.11-203042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Grumolato L, Liu G, Mong P, Mudbhary R, Biswas R, Arroyave R, Vijayakumar S, Economides AN et al (2010) Canonical and noncanonical Wnts use a common mechanism to activate completely unrelated coreceptors. Genes Dev 24:2517–2530. https://doi.org/10.1101/gad.1957710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Spencer VA, Sun JM, Li L, Davie JR (2003) Chromatin immunoprecipitation: a tool for studying histone acetylation and transcription factor binding. Methods 31:67–75

    Article  CAS  PubMed  Google Scholar 

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Funding

This work was supported by Inserm (U1239), the Conseil Régional de Normandie, the University of Rouen Normandie and the European Union. Europe is involved in Normandie with European Regional Development Fund (ERDF).

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Author notes

  1. Houssni Abid, Dorthe Cartier, Youssef Anouar, and Isabelle Lihrmann equally contributed to this work.

Authors and Affiliations

  1. UNIROUEN, Inserm U1239, Neuronal and Neuroendocrine Differentiation and Communication Laboratory, Rouen-Normandie University, 76821, Mont-Saint-Aignan, France

    Houssni Abid, Dorthe Cartier, Abdallah Hamieh, Christine Bucharles, Hugo Pothion, Destiny-Love Manecka, Jérôme Leprince, Youssef Anouar & Isabelle Lihrmann

  2. Institute for Research and Innovation in Biomedicine, 76000, Rouen, France

    Houssni Abid, Dorthe Cartier, Abdallah Hamieh, Christine Bucharles, Hugo Pothion, Destiny-Love Manecka, Jérôme Leprince, Sahil Adriouch, Olivier Boyer, Youssef Anouar & Isabelle Lihrmann

  3. CNRS UMR 7051, Neurophysiopathol Inst, Aix-Marseille University, 13015 Marseille, France

    Anne-Marie François-Bellan

  4. UNIROUEN, Inserm U1234, Pathophysiology and Biotherapy of Inflammatory and Autoimmune Diseases, Rouen-Normandie University, 76000, Rouen, France

    Sahil Adriouch & Olivier Boyer

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  1. Houssni Abid
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I.L. and Y.A. designed the experiments. H.A., D.C, A.H., A-M.F-B., C.B., H.P., D-L.M. and A.S. performed the experiments; J.L. and O.B. helped to analyze the data, I.L. and Y.A. wrote the manuscript.

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Correspondence to Isabelle Lihrmann.

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The authors declare they have no competing interest.

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Abid, H., Cartier, D., Hamieh, A. et al. AMPK Activation of PGC-1α/NRF-1-Dependent SELENOT Gene Transcription Promotes PACAP-Induced Neuroendocrine Cell Differentiation Through Tolerance to Oxidative Stress. Mol Neurobiol 56, 4086–4101 (2019). https://doi.org/10.1007/s12035-018-1352-x

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