Ascl1‐induced neuronal differentiation of P19 cells requires expression of a specific inhibitor protein of cyclic AMP‐dependent protein kinase
dc.contributor.author | Huang, Holly S. | en_US |
dc.contributor.author | Turner, David L. | en_US |
dc.contributor.author | Thompson, Robert C. | en_US |
dc.contributor.author | Uhler, Michael D. | en_US |
dc.date.accessioned | 2012-03-16T15:59:20Z | |
dc.date.available | 2013-05-01T17:24:41Z | en_US |
dc.date.issued | 2012-03 | en_US |
dc.identifier.citation | Huang, Holly S.; Turner, David L.; Thompson, Robert C.; Uhler, Michael D. (2012). "Ascl1‐induced neuronal differentiation of P19 cells requires expression of a specific inhibitor protein of cyclic AMP‐dependent protein kinase." Journal of Neurochemistry 120(5). <http://hdl.handle.net/2027.42/90302> | en_US |
dc.identifier.issn | 0022-3042 | en_US |
dc.identifier.issn | 1471-4159 | en_US |
dc.identifier.uri | https://hdl.handle.net/2027.42/90302 | |
dc.description.abstract | cAMP‐dependent protein kinase (PKA) plays a critical role in nervous system development by modulating sonic hedgehog and bone morphogenetic protein signaling. In the current studies, P19 embryonic carcinoma cells were neuronally differentiated by expression of the proneural basic helix‐loop‐helix transcription factor Ascl1. After expression of Ascl1, but prior to expression of neuronal markers such as microtubule associated protein 2 and neuronal β‐tubulin, P19 cells demonstrated a large, transient increase in both mRNA and protein for the endogenous protein kinase inhibitor (PKI)β. PKIβ‐targeted shRNA constructs both reduced the levels of PKIβ expression and blocked the neuronal differentiation of P19 cells. This inhibition of differentiation was rescued by transfection of a shRNA‐resistant expression vector for the PKIβ protein, and this rescue required the PKA‐specific inhibitory sequence of the PKIβ protein. PKIβ played a very specific role in the Ascl1‐mediated differentiation process as other PKI isoforms were unable to rescue the deficit conferred by shRNA‐mediated knockdown of PKIβ. Our results define a novel requirement for PKIβ and its inhibition of PKA during neuronal differentiation of P19 cells. | en_US |
dc.publisher | Blackwell Publishing Ltd | en_US |
dc.publisher | Wiley Periodicals, Inc. | en_US |
dc.subject.other | ShRNA | en_US |
dc.subject.other | Cyclic AMP | en_US |
dc.subject.other | Differentiation | en_US |
dc.title | Ascl1‐induced neuronal differentiation of P19 cells requires expression of a specific inhibitor protein of cyclic AMP‐dependent protein kinase | en_US |
dc.type | Article | en_US |
dc.rights.robots | IndexNoFollow | en_US |
dc.subject.hlbsecondlevel | Neurosciences | en_US |
dc.subject.hlbtoplevel | Health Sciences | en_US |
dc.description.peerreviewed | Peer Reviewed | en_US |
dc.contributor.affiliationum | Neuroscience Graduate Program, University of Michigan, Ann Arbor, Michigan, USA | en_US |
dc.contributor.affiliationum | Molecular and Behavioral Neuroscience Institute, University of Michigan, Ann Arbor, Michigan, USA | en_US |
dc.contributor.affiliationum | Department of Biological Chemistry, University of Michigan, Ann Arbor, Michigan, USA | en_US |
dc.contributor.affiliationum | Department of Psychiatry, University of Michigan, Ann Arbor, Michigan, USA | en_US |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/90302/1/j.1471-4159.2011.07332.x.pdf | |
dc.identifier.doi | 10.1111/j.1471-4159.2011.07332.x | en_US |
dc.identifier.source | Journal of Neurochemistry | en_US |
dc.identifier.citedreference | Scarpetta M. A. and Uhler M. D. ( 1993 ) Evidence for two additional isoforms of the endogenous protein kinase inhibitor of cAMP‐dependent protein kinase in mouse. J. Biol. Chem. 268, 10927 – 10931. | en_US |
dc.identifier.citedreference | Papadopoulou N., Chen J., Randeva H. S., Levine M. A., Hillhouse E. W. and Grammatopoulos D. K. ( 2004 ) Protein kinase A‐induced negative regulation of the corticotropin‐releasing hormone R1alpha receptor‐extracellularly regulated kinase signal transduction pathway: the critical role of Ser301 for signaling switch and selectivity. Mol. Endocrinol. 18, 624 – 639. | en_US |
dc.identifier.citedreference | Parras C. M., Galli R., Britz O., Soares S., Galichet C., Battiste J., Johnson J. E., Nakafuku M., Vescovi A. and Guillemot F. ( 2004 ) Mash1 specifies neurons and oligodendrocytes in the postnatal brain. EMBO J. 23, 4495 – 4505. | en_US |
dc.identifier.citedreference | Pittman R. H., Clay C. M., Farmerie T. A. and Nilson J. H. ( 1994 ) Functional analysis of the placenta‐specific enhancer of the human glycoprotein hormone alpha subunit gene. Emergence of a new element. J. Biol. Chem. 269, 19360 – 19368. | en_US |
dc.identifier.citedreference | Roche K. W., O’Brien R. J., Mammen A. L., Bernhardt J. and Huganir R. L. ( 1996 ) Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit. Neuron 16, 1179 – 1188. | en_US |
dc.identifier.citedreference | Rosen O. M. and Erlichman J. ( 1975 ) Reversible autophosphorylation of a cyclic 3’:5’‐AMP‐dependent protein kinase from bovine cardiac muscle. J. Biol. Chem. 250, 7788 – 7794. | en_US |
dc.identifier.citedreference | Sanchez S., Jimenez C., Carrera A. C., Diaz‐Nido J., Avila J. and Wandosell F. ( 2004 ) A cAMP‐activated pathway, including PKA and PI3K, regulates neuronal differentiation. Neurochem. Int. 44, 231 – 242. | en_US |
dc.identifier.citedreference | Scott J. D., Glaccum M. B., Fischer E. H. and Krebs E. G. ( 1986 ) Primary‐structure requirements for inhibition by the heat‐stable inhibitor of the cAMP‐dependent protein kinase. Proc. Natl Acad. Sci. USA 83, 1613 – 1616. | en_US |
dc.identifier.citedreference | Strickland S. and Mahdavi V. ( 1978 ) The induction of differentiation in teratocarcinoma stem cells by retinoic acid. Cell 15, 393 – 403. | en_US |
dc.identifier.citedreference | Strickland S., Smith K. K. and Marotti K. R. ( 1980 ) Hormonal induction of differentiation in teratocarcinoma stem cells: generation of parietal endoderm by retinoic acid and dibutyryl cAMP. Cell 21, 347 – 355. | en_US |
dc.identifier.citedreference | Sun T., Echelard Y., Lu R., Yuk D. I., Kaing S., Stiles C. D. and Rowitch D. H. ( 2001 ) Olig bHLH proteins interact with homeodomain proteins to regulate cell fate acquisition in progenitors of the ventral neural tube. Curr. Biol. 11, 1413 – 1420. | en_US |
dc.identifier.citedreference | Takahashi H. and Liu F. C. ( 2006 ) Genetic patterning of the mammalian telencephalon by morphogenetic molecules and transcription factors. Birth Defects Res. C Embryo Today 78, 256 – 266. | en_US |
dc.identifier.citedreference | Taylor S. S., Buechler J. A. and Yonemoto W. ( 1990 ) cAMP‐dependent protein kinase: framework for a diverse family of regulatory enzymes. Annu. Rev. Biochem. 59, 971 – 1005. | en_US |
dc.identifier.citedreference | Thomson J. A. and Marshall V. S. ( 1998 ) Primate embryonic stem cells. Curr. Top. Dev. Biol. 38, 133 – 165. | en_US |
dc.identifier.citedreference | Tiecke E., Turner R., Sanz‐Ezquerro J. J., Warner A. and Tickle C. ( 2007 ) Manipulations of PKA in chick limb development reveal roles in digit patterning including a positive role in Sonic Hedgehog signaling. Dev. Biol. 305, 312 – 324. | en_US |
dc.identifier.citedreference | Tojima T., Kobayashi S. and Ito E. ( 2003 ) Dual role of cyclic AMP‐dependent protein kinase in neuritogenesis and synaptogenesis during neuronal differentiation. J. Neurosci. Res. 74, 829 – 837. | en_US |
dc.identifier.citedreference | Uhler M. D. and Abou‐Chebl A. ( 1992 ) Cellular concentrations of protein kinase A modulate prostaglandin and cAMP induction of alkaline phosphatase. J. Biol. Chem. 267, 8658 – 8665. | en_US |
dc.identifier.citedreference | Uhler M. D., Carmichael D. F., Lee D. C., Chrivia J. C., Krebs E. G. and McKnight G. S. ( 1986 ) Isolation of cDNA clones coding for the catalytic subunit of mouse cAMP‐dependent protein kinase. Proc. Natl Acad. Sci. USA 83, 1300 – 1304. | en_US |
dc.identifier.citedreference | Van Patten S. M., Ng D. C., Th’ng J. P., Angelos K. L., Smith A. J. and Walsh D. A. ( 1991 ) Molecular cloning of a rat testis form of the inhibitor protein of cAMP‐dependent protein kinase. Proc. Natl Acad. Sci. USA 88, 5383 – 5387. | en_US |
dc.identifier.citedreference | Van Patten S. M., Donaldson L. F., McGuinness M. P., Kumar P., Alizadeh A., Griswold M. D. and Walsh D. A. ( 1997 ) Specific testicular cellular localization and hormonal regulation of the PKIalpha and PKIbeta isoforms of the inhibitor protein of the cAMP‐dependent protein kinase. J. Biol. Chem. 272, 20021 – 20029. | en_US |
dc.identifier.citedreference | Vojtek A. B., Taylor J., DeRuiter S. L., Yu J. Y., Figueroa C., Kwok R. P. and Turner D. L. ( 2003 ) Akt regulates basic helix‐loop‐helix transcription factor‐coactivator complex formation and activity during neuronal differentiation. Mol. Cell. Biol. 23, 4417 – 4427. | en_US |
dc.identifier.citedreference | Wadzinski B. E., Wheat W. H., Jaspers S., Peruski Jr L. F., Lickteig R. L., Johnson G. L. and Klemm D. J. ( 1993 ) Nuclear protein phosphatase 2A dephosphorylates protein kinase A‐phosphorylated CREB and regulates CREB transcriptional stimulation. Mol. Cell. Biol. 13, 2822 – 2834. | en_US |
dc.identifier.citedreference | Wen W., Harootunian A. T., Adams S. R., Feramisco J., Tsien R. Y., Meinkoth J. L. and Taylor S. S. ( 1994 ) Heat‐stable inhibitors of cAMP‐dependent protein kinase carry a nuclear export signal. J. Biol. Chem. 269, 32214 – 32220. | en_US |
dc.identifier.citedreference | Zheng L., Yu L., Tu Q., Zhang M., He H., Chen W., Gao J., Yu J., Wu Q. and Zhao S. ( 2000 ) Cloning and mapping of human PKIB and PKIG, and comparison of tissue expression patterns of three members of the protein kinase inhibitor family, including PKIA. Biochem. J. 349, 403 – 407. | en_US |
dc.identifier.citedreference | Zoller M. J., Nelson N. C. and Taylor S. S. ( 1981 ) Affinity labeling of cAMP‐dependent protein kinase with p‐fluorosulfonylbenzoyl adenosine. Covalent modification of lysine 71. J. Biol. Chem. 256, 10837 – 10842. | en_US |
dc.identifier.citedreference | Ahn S., Olive M., Aggarwal S., Krylov D., Ginty D. D. and Vinson C. ( 1998 ) A dominant‐negative inhibitor of CREB reveals that it is a general mediator of stimulus‐dependent transcription of c‐fos. Mol. Cell. Biol. 18, 967 – 977. | en_US |
dc.identifier.citedreference | Ashby C. D. and Walsh D. A. ( 1972 ) Characterization of the interaction of a protein kinase inhibitor with adenosine 3′,5′‐monophosphate‐dependent protein kinases. J. Biol. Chem. 247, 6637 – 6642. | en_US |
dc.identifier.citedreference | Banky P., Huang L. J. and Taylor S. S. ( 1998 ) Dimerization/docking domain of the type Ialpha regulatory subunit of cAMP‐dependent protein kinase. Requirements for dimerization and docking are distinct but overlapping. J. Biol. Chem. 273, 35048 – 35055. | en_US |
dc.identifier.citedreference | Baude E. J., Dignam S. S., Reimann E. M. and Uhler M. D. ( 1994 ) Evidence for the importance of hydrophobic residues in the interactions between the cAMP‐dependent protein kinase catalytic subunit and the protein kinase inhibitors. J. Biol. Chem. 269, 18128 – 18133. | en_US |
dc.identifier.citedreference | Belyamani M., Gangolli E. A. and Idzerda R. L. ( 2001 ) Reproductive function in protein kinase inhibitor‐deficient mice. Mol. Cell. Biol. 21, 3959 – 3963. | en_US |
dc.identifier.citedreference | Bertrand N., Castro D. S. and Guillemot F. ( 2002 ) Proneural genes and the specification of neural cell types. Nat. Rev. Neurosci. 3, 517 – 530. | en_US |
dc.identifier.citedreference | Brown N. A., Stofko R. E. and Uhler M. D. ( 1990 ) Induction of alkaline phosphatase in mouse L cells by overexpression of the catalytic subunit of cAMP‐dependent protein kinase. J. Biol. Chem. 265, 13181 – 13189. | en_US |
dc.identifier.citedreference | Canals M., Angulo E., Casado V. et al. ( 2005 ) Molecular mechanisms involved in the adenosine A and A receptor‐induced neuronal differentiation in neuroblastoma cells and striatal primary cultures. J. Neurochem. 92, 337 – 348. | en_US |
dc.identifier.citedreference | Casarosa S., Fode C. and Guillemot F. ( 1999 ) Mash1 regulates neurogenesis in the ventral telencephalon. Development 126, 525 – 534. | en_US |
dc.identifier.citedreference | Chen S., Ji M., Paris M., Hullinger R. L. and Andrisani O. M. ( 2005 ) The cAMP pathway regulates both transcription and activity of the paired homeobox transcription factor Phox2a required for development of neural crest‐derived and central nervous system‐derived catecholaminergic neurons. J. Biol. Chem. 280, 41025 – 41036. | en_US |
dc.identifier.citedreference | Chow Y. W. and Wang H. L. ( 1998 ) Functional modulation of P2X2 receptors by cyclic AMP‐dependent protein kinase. J. Neurochem. 70, 2606 – 2612. | en_US |
dc.identifier.citedreference | Chung K. H., Hart C. C., Al‐Bassam S., Avery A., Taylor J., Patel P. D., Vojtek A. B. and Turner D. L. ( 2006 ) Polycistronic RNA polymerase II expression vectors for RNA interference based on BIC/miR‐155. Nucleic Acids Res. 34, e53. | en_US |
dc.identifier.citedreference | Collins S. P. and Uhler M. D. ( 1997 ) Characterization of PKIγ, a novel isoform of the protein kinase inhibitor of cAMP‐dependent protein kinase. J. Biol. Chem. 272, 18169 – 18178. | en_US |
dc.identifier.citedreference | Corbin J. D., Cobb C. E., Beebe S. J., Granner D. K., Koch S. R., Gettys T. W., Blackmore P. F., Francis S. H. and Wells J. N. ( 1988 ) Mechanism and function of cAMP‐ and cGMP‐dependent protein kinases. Adv. Second Messenger Phosphoprotein Res. 21, 75 – 86. | en_US |
dc.identifier.citedreference | Dalton G. D. and Dewey W. L. ( 2006 ) Protein kinase inhibitor peptide (PKI): a family of endogenous neuropeptides that modulate neuronal cAMP‐dependent protein kinase function. Neuropeptides 40, 23 – 34. | en_US |
dc.identifier.citedreference | Delegeane A. M., Ferland L. H. and Mellon P. L. ( 1987 ) Tissue‐specific enhancer of the human glycoprotein hormone alpha‐subunit gene: dependence on cyclic AMP‐inducible elements. Mol. Cell. Biol. 7, 3994 – 4002. | en_US |
dc.identifier.citedreference | Farah M. H., Olson J. M., Sucic H. B., Hume R. I., Tapscott S. J. and Turner D. L. ( 2000 ) Generation of neurons by transient expression of neural bHLH proteins in mammalian cells. Development 127, 693 – 702. | en_US |
dc.identifier.citedreference | Gangolli E. A., Belyamani M., Muchinsky S., Narula A., Burton K. A., McKnight G. S., Uhler M. D. and Idzerda R. L. ( 2000 ) Deficient gene expression in protein kinase inhibitor alpha Null mutant mice. Mol. Cell. Biol. 20, 3442 – 3448. | en_US |
dc.identifier.citedreference | Ghayor C., Ehrbar M., San Miguel B., Gratz K. W. and Weber F. E. ( 2009 ) cAMP enhances BMP2‐signaling through PKA and MKP1‐dependent mechanisms. Biochem. Biophys. Res. Commun. 381, 247 – 252. | en_US |
dc.identifier.citedreference | Glass D. B., Lundquist L. J., Katz B. M. and Walsh D. A. ( 1989 ) Protein kinase inhibitor‐(6‐22)‐amide peptide analogs with standard and nonstandard amino acid substitutions for phenylalanine 10. Inhibition of cAMP‐dependent protein kinase. J. Biol. Chem. 264, 14579 – 14584. | en_US |
dc.identifier.citedreference | Gowan K., Helms A. W., Hunsaker T. L., Collisson T., Ebert P. J., Odom R. and Johnson J. E. ( 2001 ) Crossinhibitory activities of Ngn1 and Math1 allow specification of distinct dorsal interneurons. Neuron 31, 219 – 232. | en_US |
dc.identifier.citedreference | Hagiwara M., Alberts A., Brindle P., Meinkoth J., Feramisco J., Deng T., Karin M., Shenolikar S. and Montminy M. ( 1992 ) Transcriptional attenuation following cAMP induction requires PP‐1‐mediated dephosphorylation of CREB. Cell 70, 105 – 113. | en_US |
dc.identifier.citedreference | Hedin L., McKnight G. S., Lifka J., Durica J. M. and Richards J. S. ( 1987 ) Tissue distribution and hormonal regulation of messenger ribonucleic acid for regulatory and catalytic subunits of adenosine 3’,5’‐monophosphate‐dependent protein kinases during ovarian follicular development and luteinization in the rat. Endocrinology 120, 1928 – 1935. | en_US |
dc.identifier.citedreference | Hofmann F., Beavo J. A., Bechtel P. J. and Krebs E. G. ( 1975 ) Comparison of adenosine 3’:5’‐monophosphate‐dependent protein kinases from rabbit skeletal and bovine heart muscle. J. Biol. Chem. 250, 7795 – 7801. | en_US |
dc.identifier.citedreference | Huang H. S., Kubish G. M., Redmond T. M., Turner D. L., Thompson R. C., Murphy G. G. and Uhler M. D. ( 2010 ) Direct transcriptional induction of Gadd45gamma by Ascl1 during neuronal differentiation. Mol. Cell. Neurosci. 44, 282 – 296. | en_US |
dc.identifier.citedreference | Huggenvik J. I., Collard M. W., Stofko R. E., Seasholtz A. F. and Uhler M. D. ( 1991 ) Regulation of the human enkephalin promoter by two isoforms of the catalytic subunit of cyclic adenosine 3′,5′‐monophosphate‐dependent protein kinase. Mol. Endocrinol. 5, 921 – 930. | en_US |
dc.identifier.citedreference | Iyer G. H., Garrod S., Woods Jr V. L. and Taylor S. S. ( 2005 ) Catalytic independent functions of a protein kinase as revealed by a kinase‐dead mutant: study of the Lys72His mutant of cAMP‐dependent kinase. J. Mol. Biol. 351, 1110 – 1122. | en_US |
dc.identifier.citedreference | Jameson J. L., Albanese C. and Habener J. F. ( 1989 ) Distinct adjacent protein‐binding domains in the glycoprotein hormone alpha gene interact independently with a cAMP‐responsive enhancer. J. Biol. Chem. 264, 16190 – 16196. | en_US |
dc.identifier.citedreference | Kawakami M. and Nakanishi N. ( 2001 ) The role of an endogenous PKA inhibitor, PKIalpha, in organizing left‐right axis formation. Development 128, 2509 – 2515. | en_US |
dc.identifier.citedreference | Kim G., Choe Y., Park J., Cho S. and Kim K. ( 2002 ) Activation of protein kinase A induces neuronal differentiation of HiB5 hippocampal progenitor cells. Brain Res. Mol. Brain Res. 109, 134 – 145. | en_US |
dc.identifier.citedreference | Kumar P. and Walsh D. A. ( 2002 ) A dual‐specificity isoform of the protein kinase inhibitor PKI produced by alternate gene splicing. Biochem. J. 362, 533 – 537. | en_US |
dc.identifier.citedreference | Kumar P., Van Patten S. M. and Walsh D. A. ( 1997 ) Multiplicity of the beta form of the cAMP‐dependent protein kinase inhibitor protein generated by post‐translational modification and alternate translational initiation. J. Biol. Chem. 272, 20011 – 20020. | en_US |
dc.identifier.citedreference | Lee D. C., Carmichael D. F., Krebs E. G. and McKnight G. S. ( 1983 ) Isolation of a cDNA clone for the type I regulatory subunit of bovine cAMP‐dependent protein kinase. Proc. Natl Acad. Sci. USA 80, 3608 – 3612. | en_US |
dc.identifier.citedreference | Lo L. C., Johnson J. E., Wuenschell C. W., Saito T. and Anderson D. J. ( 1991 ) Mammalian achaete‐scute homolog 1 is transiently expressed by spatially restricted subsets of early neuroepithelial and neural crest cells. Genes Dev. 5, 1524 – 1537. | en_US |
dc.identifier.citedreference | Masai I., Yamaguchi M., Tonou‐Fujimori N., Komori A. and Okamoto H. ( 2005 ) The hedgehog‐PKA pathway regulates two distinct steps of the differentiation of retinal ganglion cells: the cell‐cycle exit of retinoblasts and their neuronal maturation. Development 132, 1539 – 1553. | en_US |
dc.identifier.citedreference | Mellon P. L., Clegg C. H., Correll L. A. and McKnight G. S. ( 1989 ) Regulation of transcription by cyclic AMP‐dependent protein kinase. Proc. Natl Acad. Sci. USA 86, 4887 – 4891. | en_US |
dc.identifier.citedreference | Newlon M. G., Roy M., Morikis D., Hausken Z. E., Coghlan V., Scott J. D. and Jennings P. A. ( 1999 ) The molecular basis for protein kinase A anchoring revealed by solution NMR. Nat. Struct. Biol. 6, 222 – 227. | en_US |
dc.identifier.citedreference | Nguyen P. V. and Woo N. H. ( 2003 ) Regulation of hippocampal synaptic plasticity by cyclic AMP‐dependent protein kinases. Prog. Neurobiol. 71, 401 – 437. | en_US |
dc.identifier.citedreference | Nieto M., Schuurmans C., Britz O. and Guillemot F. ( 2001 ) Neural bHLH genes control the neuronal versus glial fate decision in cortical progenitors. Neuron 29, 401 – 413. | en_US |
dc.identifier.citedreference | Ohta Y., Nakagawa K., Imai Y., Katagiri T., Koike T. and Takaoka K. ( 2008 ) Cyclic AMP enhances Smad‐mediated BMP signaling through PKA‐CREB pathway. J. Bone Miner. Metab. 26, 478 – 484. | en_US |
dc.identifier.citedreference | Pan Y., Wang C. and Wang B. ( 2009 ) Phosphorylation of Gli2 by protein kinase A is required for Gli2 processing and degradation and the Sonic Hedgehog‐regulated mouse development. Dev. Biol. 326, 177 – 189. | en_US |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
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