Polyribosome and ribonucleoprotein complex redistribution of mRNA induced by GnRH involves both EIF2AK3 and MAPK signaling

Molecular and Cellular Endocrinology

Volumn 382, Issue 1, 2014, Pages 346-357

  Do, Minh Ha T ^a   Kim, Taeshin ^a   He, Feng ^a   Dave, Hiral ^a   Intriago, Rachel E ^a   Astorga, Uriah A ^a   Jain, Sonia ^a   Lawson, Mark A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dusp1; Gonadotropins; Luteinizing hormone; Pituitary; Translation; Unfolded protein response

Indexed keywords

DUAL SPECIFICITY PHOSPHATASE; GONADORELIN; GONADOTROPIN; INITIATION FACTOR 2ALPHA KINASE 3; INITIATION FACTOR 4E; LUTEINIZING HORMONE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN SERINE THREONINE KINASE; RIBONUCLEOPROTEIN; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; FRACTIONATION; GENE EXPRESSION REGULATION; HORMONE SYNTHESIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYSOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSLATION REGULATION; UNFOLDED PROTEIN RESPONSE;

DUSP1; GONADOTROPINS; LUTEINIZING HORMONE; PITUITARY; TRANSLATION; UNFOLDED PROTEIN RESPONSE;

3' UNTRANSLATED REGIONS; ANIMALS; CELL LINE; DUAL SPECIFICITY PHOSPHATASE 1; EIF-2 KINASE; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GONADOTROPIN-RELEASING HORMONE; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; MAP KINASE SIGNALING SYSTEM; MICE; POLYRIBOSOMES; PROTEIN BIOSYNTHESIS; PROTEIN KINASE C; RIBONUCLEOPROTEINS; RNA, MESSENGER; SIROLIMUS; TETRADECANOYLPHORBOL ACETATE; UNFOLDED PROTEIN RESPONSE;

EID: 84887550637     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2013.10.007     Document Type: Article

References (52)

1. Alarid E.T., Windle J.J., Whyte D.B., Mellon P.L. Immortalization of pituitary cells at discrete stages of development by directed oncogenesis in transgenic mice. Development 1996, 122:3319-3329.
2. 2+/NFAT signaling pathway decode GnRH pulse frequency?. J. Biol. Chem. 2009, 284:35746-35757.
3. Armstrong S.P., Caunt C.J., Fowkes R.C., Tsaneva-Atanasova K., McArdle C.A. Pulsatile and sustained gonadotropin-releasing hormone (GnRH) receptor signaling: does the ERK signaling pathway decode GnRH pulse frequency?. J. Biol. Chem. 2010, 285:24360-24371.
4. Beretta L., Gingras A.C., Svitkin Y.V., Hall M.N., Sonenberg N. Rapamycin blocks the phosphorylation of 4E-BP1 and inhibits cap-dependent initiation of translation. EMBO J. 1996, 15:658-664.
5. Bhalla U.S., Ram P.T., Iyengar R. MAP kinase phosphatase as a locus of flexibility in a mitogen-activated protein kinase signaling network. Science 2002, 297:1018-1023.
6. Brondello J.M., Pouyssegur J., McKenzie F.R. Reduced MAP kinase phosphatase-1 degradation after p42/p44MAPK-dependent phosphorylation. Science 1999, 286:2514-2517.
7. Burger L.L., Dalkin A.C., Aylor K.W., Haisenleder D.J., Marshall J.C. GnRH pulse frequency modulation of gonadotropin subunit gene transcription in normal gonadotropes-assessment by primary transcript assay provides evidence for roles of GnRH and follistatin. Endocrinology 2002, 143:3243-3249.
8. Burger L.L., Haisenleder D.J., Dalkin A.C., Marshall J.C. Regulation of gonadotropin subunit gene transcription. J. Mol. Endocrinol. 2004, 33:559-584.
9. Burger L.L., Haisenleder D.J., Marshall J.C. GnRH pulse frequency differentially regulates steroidogenic factor 1 (SF1), dosage-sensitive sex reversal-AHC critical region on the X chromosome gene 1 (DAX1), and serum response factor (SRF): potential mechanism for GnRH pulse frequency regulation of LH beta transcription in the rat. Endocrine 2011, 39:212-219.
10. Caunt C.J., Armstrong S.P., Rivers C.A., Norman M.R., McArdle C.A. Spatiotemporal regulation of ERK2 by dual specificity phosphatases. J. Biol. Chem. 2008, 283:26612-26623.
11. Clement S.L., Scheckel C., Stoecklin G., Lykke-Andersen J. Phosphorylation of tristetraprolin by MK2 impairs AU-rich element mRNA decay by preventing deadenylase recruitment. Mol. Cell. Biol. 2011, 31:256-266.
12. Dang Do A.N., Kimball S.R., Cavener D.R., Jefferson L.S. EIF2alpha kinases GCN2 and PERK modulate transcription and translation of distinct sets of mRNAs in mouse liver. Physiol. Genom. 2009, 38:328-341.
13. Deglincerti A., Jaffrey S.R. Insights into the roles of local translation from the axonal transcriptome. Open Biol. 2012, 2:120079.
14. Do M.H., Santos S.J., Lawson M.A. GnRH induces the unfolded protein response in the LbetaT2 pituitary gonadotrope cell line. Mol. Endocrinol. 2009, 23:100-112.
15. Dobkin-Bekman M., Rahamin-Ben Navi L., Shterntal B., Sviridonov L., Przedecki F., Naidich-Exler M., Brodie C., Seger R., Naor Z. Differential role of PKC isoforms in GnRH and phorbol 12-myristate 13-acetate activation of extracellular signal-regulated kinase and Jun N-terminal kinase. Endocrinology 2010, 151:4894-4907.
16. Eisen M.B., Spellman P.T., Brown P.O., Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA 1998, 95:14863-14868.
17. Emmons J., Townley-Tilson W.H., Deleault K.M., Skinner S.J., Gross R.H., Whitfield M.L., Brooks S.A. Identification of TTP mRNA targets in human dendritic cells reveals TTP as a critical regulator of dendritic cell maturation. RNA 2008, 14:888-902.
18. Feng D., Wei J., Gupta S., McGrath B.C., Cavener D.R. Acute ablation of PERK results in ER dysfunctions followed by reduced insulin secretion and cell proliferation. BMC Cell Biol. 2009, 10:61.
19. Ferris H.A., Shupnik M.A. Mechanisms for pulsatile regulation of the gonadotropin subunit genes by GNRH1. Biol. Reprod. 2006, 74:993-998.
20. Fribley A., Zhang K., Kaufman R.J. Regulation of apoptosis by the unfolded protein response. Methods Mol. Biol. 2009, 559:191-204.
21. Gentleman R., Carey V., Huber W., Irizarry R., Dudoit S. Bioinformatics and Computational Biology Solutions Using R and Bioconductor 2005, Springer, New York.
22. Irizarry R.A., Bolstad B.M., Collin F., Cope L.M., Hobbs B., Speed T.P. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 2003, 31:e15.
23. Jain R., Devine T., George A.D., Chittur S.V., Baroni T.E., Penalva L.O., Tenenbaum S.A. RIP-Chip analysis: RNA-binding protein immunoprecipitation-microarray (chip) profiling. Methods Mol. Biol. 2011, 703:247-263.
24. Jeffrey K.L., Brummer T., Rolph M.S., Liu S.M., Callejas N.A., Grumont R.J., Gillieron C., Mackay F., Grey S., Camps M., Rommel C., Gerondakis S.D., Mackay C.R. Positive regulation of immune cell function and inflammatory responses by phosphatase PAC-1. Nat. Immunol. 2006, 7:274-283.
25. Kakar S.S., Winters S.J., Zacharias W., Miller D.M., Flynn S. Identification of distinct gene expression profiles associated with treatment of LbetaT2 cells with gonadotropin-releasing hormone agonist using microarray analysis. Gene 2003, 308:67-77.
26. Kondratyev M., Avezov E., Shenkman M., Groisman B., Lederkremer G.Z. PERK-dependent compartmentalization of ERAD and unfolded protein response machineries during ER stress. Exp. Cell Res. 2007, 313:3395-3407.
27. Kuhn K.M., DeRisi J.L., Brown P.O., Sarnow P. Global and specific translational regulation in the genomic response of Saccharomyces cerevisiae to a rapid transfer from a fermentable to a nonfermentable carbon source. Mol. Cell. Biol. 2001, 21:916-927.
28. Kuwano Y., Kim H.H., Abdelmohsen K., Pullmann R., Martindale J.L., Yang X., Gorospe M. MKP-1 mRNA stabilization and translational control by RNA-binding proteins HuR and NF90. Mol. Cell. Biol. 2008, 28:4562-4575.
29. Lawson M.A., Tsutsumi R., Zhang H., Talukdar I., Butler B.K., Santos S.J., Mellon P.L., Webster N.J. Pulse sensitivity of the luteinizing hormone beta promoter is determined by a negative feedback loop involving early growth response-1 and Ngfi-A binding protein 1 and 2. Mol. Endocrinol. 2007, 21:1175-1191.
30. Leclerc G.M., Boockfor F.R., Faught W.J., Frawley L.S. Development of a destabilized firefly luciferase enzyme for measurement of gene expression. Biotechniques 2000, 29. 590-591, 594-596, 598 passim.
31. Li S., Zhu F., Zykova T., Kim M.O., Cho Y.Y., Bode A.M., Peng C., Ma W., Carper A., Langfald A., Dong Z. T-LAK cell-originated protein kinase (TOPK) phosphorylation of MKP1 protein prevents solar ultraviolet light-induced inflammation through inhibition of the p38 protein signaling pathway. J. Biol. Chem. 2011, 286:29601-29609.
32. Lim S., Pnueli L., Tan J.H., Naor Z., Rajagopal G., Melamed P. Negative feedback governs gonadotrope frequency-decoding of gonadotropin releasing hormone pulse-frequency. PLoS One 2009, 4:e7244.
33. Lin N.Y., Lin C.T., Chang C.J. Modulation of immediate early gene expression by tristetraprolin in the differentiation of 3T3-L1 cells. Biochem. Biophys. Res. Commun. 2008, 365:69-74.
34. Mathews M.B., Sonenberg N., Hershey J.W.B. Origins and principles of translational control. Translational Control of Gene Expression 2000, 1-31. Cold Spring Harbor Laboratory Press, Cold Spring Harbor. second ed. N. Sonenberg, J.W.B. Hershey, M.B. Mathews (Eds.).
35. Nanbru C., Lafon I., Audigier S., Gensac M.C., Vagner S., Huez G., Prats A.C. Alternative translation of the proto-oncogene c-myc by an internal ribosome entry site. J. Biol. Chem. 1997, 272:32061-32066.
36. Nguyen K.A., Intriago R.E., Upadhyay H.C., Santos S.J., Webster N.J., Lawson M.A. Modulation of gonadotropin-releasing hormone-induced extracellular signal-regulated kinase activation by dual-specificity protein phosphatase 1 in LbetaT2 gonadotropes. Endocrinology 2010, 151:4882-4893.
37. Nguyen K.A., Santos S.J., Kreidel M.K., Diaz A.L., Rey R., Lawson M.A. Acute regulation of translation initiation by gonadotropin-releasing hormone in the gonadotrope cell line LbetaT2. Mol. Endocrinol. 2004, 18:1301-1312.
38. Rosenfeld S., Wang T., Kim Y., Milner J. Numerical deconvolution of cDNA microarray signal: simulation study. Ann. NY Acad. Sci. 2004, 1020:110-123.
39. Ruf F., Sealfon S.C. Genomics view of gonadotrope signaling circuits. Trends Endocrinol. Metab. 2004, 15:331-338.
40. Saito A., Ochiai K., Kondo S., Tsumagari K., Murakami T., Cavener D.R., Imaizumi K. Endoplasmic reticulum stress response mediated by the PERK-eIF2(alpha)-ATF4 pathway is involved in osteoblast differentiation induced by BMP2. J. Biol. Chem. 2011, 286:4809-4818.
41. Scheuner D., Kaufman R.J. The unfolded protein response: a pathway that links insulin demand with beta-cell failure and diabetes. Endocr. Rev. 2008, 29:317-333.
42. Storey J.D. A direct approach to false discovery rates. J. R. Stat. Soc. Ser. B 2002, 479-498.
43. Tsaneva-Atanasova K., Caunt C.J., Armstrong S.P., Perrett R.M., McArdle C.A. Decoding neurohormone pulse frequency by convergent signalling modules. Biochem. Soc. Trans. 2012, 40:273-278.
44. Tusher V.G., Tibshirani R., Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA 2001, 98:5116-5121.
45. Vasilyev V.V., Lawson M.A., Dipaolo D., Webster N.J., Mellon P.L. Different signaling pathways control acute induction versus long-term repression of LHbeta transcription by GnRH. Endocrinology 2002, 143:3414-3426.
46. Verfaillie T., Rubio N., Garg A.D., Bultynck G., Rizzuto R., Decuypere J.P., Piette J., Linehan C., Gupta S., Samali A., Agostinis P. PERK is required at the ER-mitochondrial contact sites to convey apoptosis after ROS-based ER stress. Cell Death Differ. 2012.
47. Walter P., Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science 2011, 334:1081-1086.
48. Wei J., Sheng X., Feng D., McGrath B., Cavener D.R. PERK is essential for neonatal skeletal development to regulate osteoblast proliferation and differentiation. J. Cell Physiol. 2008, 217:693-707.
49. Wurmbach E., Yuen T., Ebersole B.J., Sealfon S.C. Gonadotropin-releasing hormone receptor-coupled gene network organization. J. Biol. Chem. 2001, 276:47195-47201.
50. Zhang K., Kaufman R.J. Protein folding in the endoplasmic reticulum and the unfolded protein response. Handb. Exp. Pharmacol. 2006, 69-91.
51. Zhang P., McGrath B., Li S., Frank A., Zambito F., Reinert J., Gannon M., Ma K., McNaughton K., Cavener D.R. The PERK eukaryotic initiation factor 2 alpha kinase is required for the development of the skeletal system, postnatal growth, and the function and viability of the pancreas. Mol. Cell. Biol. 2002, 22:3864-3874.
52. Zhang T., Roberson M.S. Role of MAP kinase phosphatases in GnRH-dependent activation of MAP kinases. J. Mol. Endocrinol. 2006, 36:41-50.