This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Nielsen, J.
Right arrow Articles by Nielsen, F. C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Nielsen, J.
Right arrow Articles by Nielsen, F. C.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, February 1999, p. 1262-1270, Vol. 19, No. 2
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.

A Family of Insulin-Like Growth Factor II mRNA-Binding Proteins Represses Translation in Late Development

Jacob Nielsen,1 Jan Christiansen,1,* Jens Lykke-Andersen,1 Anders H. Johnsen,3 Ulla M. Wewer,2 and Finn C. Nielsen3

RNA Regulation Centre, Institute of Molecular Biology,1 and Institute of Molecular Pathology,2 University of Copenhagen, and Department of Clinical Biochemistry, Rigshospitalet,3 Copenhagen, Denmark

Received 28 September 1998/Returned for modification 27 October 1998/Accepted 9 November 1998

Insulin-like growth factor II (IGF-II) is a major fetal growth factor. The IGF-II gene generates multiple mRNAs with different 5' untranslated regions (5' UTRs) that are translated in a differential manner during development. We have identified a human family of three IGF-II mRNA-binding proteins (IMPs) that exhibit multiple attachments to the 5' UTR from the translationally regulated IGF-II leader 3 mRNA but are unable to bind to the 5' UTR from the constitutively translated IGF-II leader 4 mRNA. IMPs contain the unique combination of two RNA recognition motifs and four hnRNP K homology domains and are homologous to the Xenopus Vera and chicken zipcode-binding proteins. IMP localizes to subcytoplasmic domains in a growth-dependent and cell-specific manner and causes a dose-dependent translational repression of IGF-II leader 3 -luciferase mRNA. Mouse IMPs are produced in a burst at embryonic day 12.5 followed by a decline towards birth, and, similar to IGF-II, IMPs are especially expressed in developing epithelia, muscle, and placenta in both mouse and human embryos. The results imply that cytoplasmic 5' UTR-binding proteins control IGF-II biosynthesis during late mammalian development.

* Corresponding author. Mailing address: Institute of Molecular Biology, University of Copenhagen, Sølvgade 83 H, DK-1307 Copenhagen K, Denmark. Phone: 45 35 32 20 08. Fax: 45 35 32 20 40. E-mail: janchr{at}mermaid.molbio.ku.dk.

Molecular and Cellular Biology, February 1999, p. 1262-1270, Vol. 19, No. 2
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Christiansen, J., Kolte, A. M, Hansen, T. v O, Nielsen, F. C (2009). IGF2 mRNA-binding protein 2: biological function and putative role in type 2 diabetes. J Mol Endocrinol 43: 187-195 [Abstract] [Full Text]  
  • Weinlich, S., Huttelmaier, S., Schierhorn, A., Behrens, S.-E., Ostareck-Lederer, A., Ostareck, D. H. (2009). IGF2BP1 enhances HCV IRES-mediated translation initiation via the 3'UTR. RNA 15: 1528-1542 [Abstract] [Full Text]  
  • Cornu, M., Yang, J.-Y., Jaccard, E., Poussin, C., Widmann, C., Thorens, B. (2009). Glucagon-Like Peptide-1 Protects {beta}-Cells Against Apoptosis by Increasing the Activity of an Igf-2/Igf-1 Receptor Autocrine Loop. Diabetes 58: 1816-1825 [Abstract] [Full Text]  
  • Gu, W., Pan, F., Singer, R. H. (2009). Blocking {beta}-catenin binding to the ZBP1 promoter represses ZBP1 expression, leading to increased proliferation and migration of metastatic breast-cancer cells. J. Cell Sci. 122: 1895-1905 [Abstract] [Full Text]  
  • van Hoek, M., Langendonk, J. G., de Rooij, S. R., Sijbrands, E. J.G., Roseboom, T. J. (2009). Genetic Variant in the IGF2BP2 Gene May Interact With Fetal Malnutrition to Affect Glucose Metabolism. Diabetes 58: 1440-1444 [Abstract] [Full Text]  
  • Duan, H., Cherradi, N., Feige, J.-J., Jefcoate, C. (2009). cAMP-Dependent Posttranscriptional Regulation of Steroidogenic Acute Regulatory (STAR) Protein by the Zinc Finger Protein ZFP36L1/TIS11b. Mol. Endocrinol. 23: 497-509 [Abstract] [Full Text]  
  • Tanaka, M., Sasaki, K., Kamata, R., Hoshino, Y., Yanagihara, K., Sakai, R. (2009). A Novel RNA-Binding Protein, Ossa/C9orf10, Regulates Activity of Src Kinases To Protect Cells from Oxidative Stress-Induced Apoptosis. Mol. Cell. Biol. 29: 402-413 [Abstract] [Full Text]  
  • Weidensdorfer, D., Stohr, N., Baude, A., Lederer, M., Kohn, M., Schierhorn, A., Buchmeier, S., Wahle, E., Huttelmaier, S. (2009). Control of c-myc mRNA stability by IGF2BP1-associated cytoplasmic RNPs. RNA 15: 104-115 [Abstract] [Full Text]  
  • Murphy, R., Baptista, J., Holly, J., Umpleby, A. M., Ellard, S., Harries, L. W., Crolla, J., Cundy, T., Hattersley, A. T. (2008). Severe Intrauterine Growth Retardation and Atypical Diabetes Associated with a Translocation Breakpoint Disrupting Regulation of the Insulin-Like Growth Factor 2 Gene. J. Clin. Endocrinol. Metab. 93: 4373-4380 [Abstract] [Full Text]  
  • Gu, W., Wells, A. L., Pan, F., Singer, R. H. (2008). Feedback Regulation between Zipcode Binding Protein 1 and {beta}-Catenin mRNAs in Breast Cancer Cells. Mol. Cell. Biol. 28: 4963-4974 [Abstract] [Full Text]  
  • Zhou, Y., Rong, L., Lu, J., Pan, Q., Liang, C. (2008). Insulin-Like Growth Factor II mRNA Binding Protein 1 Associates with Gag Protein of Human Immunodeficiency Virus Type 1, and Its Overexpression Affects Virus Assembly. J. Virol. 82: 5683-5692 [Abstract] [Full Text]  
  • Boyerinas, B., Park, S.-M., Shomron, N., Hedegaard, M. M., Vinther, J., Andersen, J. S., Feig, C., Xu, J., Burge, C. B., Peter, M. E. (2008). Identification of Let-7-Regulated Oncofetal Genes. Cancer Res. 68: 2587-2591 [Abstract] [Full Text]  
  • Sitnikova, L., Mendese, G., Liu, Q., Woda, B. A., Lu, D., Dresser, K., Mohanty, S., Rock, K. L., Jiang, Z. (2008). IMP3 Predicts Aggressive Superficial Urothelial Carcinoma of the Bladder. Clin. Cancer Res. 14: 1701-1706 [Abstract] [Full Text]  
  • Oberman, F., Rand, K., Maizels, Y., Rubinstein, A. M., Yisraeli, J. K. (2007). VICKZ proteins mediate cell migration via their RNA binding activity. RNA 13: 1558-1569 [Abstract] [Full Text]  
  • Scott, L. J., Mohlke, K. L., Bonnycastle, L. L., Willer, C. J., Li, Y., Duren, W. L., Erdos, M. R., Stringham, H. M., Chines, P. S., Jackson, A. U., Prokunina-Olsson, L., Ding, C.-J., Swift, A. J., Narisu, N., Hu, T., Pruim, R., Xiao, R., Li, X.-Y., Conneely, K. N., Riebow, N. L., Sprau, A. G., Tong, M., White, P. P., Hetrick, K. N., Barnhart, M. W., Bark, C. W., Goldstein, J. L., Watkins, L., Xiang, F., Saramies, J., Buchanan, T. A., Watanabe, R. M., Valle, T. T., Kinnunen, L., Abecasis, G. R., Pugh, E. W., Doheny, K. F., Bergman, R. N., Tuomilehto, J., Collins, F. S., Boehnke, M. (2007). A Genome-Wide Association Study of Type 2 Diabetes in Finns Detects Multiple Susceptibility Variants. Science 316: 1341-1345 [Abstract] [Full Text]  
  • Jonson, L., Vikesaa, J., Krogh, A., Nielsen, L. K., Hansen, T. vO., Borup, R., Johnsen, A. H., Christiansen, J., Nielsen, F. C. (2007). Molecular Composition of IMP1 Ribonucleoprotein Granules. Mol. Cell. Proteomics 6: 798-811 [Abstract] [Full Text]  
  • Polesskaya, A., Cuvellier, S., Naguibneva, I., Duquet, A., Moss, E. G., Harel-Bellan, A. (2007). Lin-28 binds IGF-2 mRNA and participates in skeletal myogenesis by increasing translation efficiency. Genes Dev. 21: 1125-1138 [Abstract] [Full Text]  
  • Cleynen, I., Brants, J. R., Peeters, K., Deckers, R., Debiec-Rychter, M., Sciot, R., Van de Ven, W. J.M., Petit, M. M.R. (2007). HMGA2 Regulates Transcription of the Imp2 Gene via an Intronic Regulatory Element in Cooperation with Nuclear Factor-{kappa}B. Mol Cancer Res 5: 363-372 [Abstract] [Full Text]  
  • Sparanese, D., Lee, C. H. (2007). CRD-BP shields c-myc and MDR-1 RNA from endonucleolytic attack by a mammalian endoribonuclease. Nucleic Acids Res 35: 1209-1221 [Abstract] [Full Text]  
  • Natkunam, Y., Vainer, G., Chen, J., Zhao, S., Marinelli, R. J., Hammer, A. S., Hamilton-Dutoit, S., Pikarsky, E., Amir, G., Levy, R., Yisraeli, J. K., Lossos, I. S. (2007). Expression of the RNA-binding protein VICKZ in normal hematopoietic tissues and neoplasms. haematol 92: 176-183 [Abstract] [Full Text]  
  • Kato, T., Hayama, S., Yamabuki, T., Ishikawa, N., Miyamoto, M., Ito, T., Tsuchiya, E., Kondo, S., Nakamura, Y., Daigo, Y. (2007). Increased Expression of Insulin-like Growth Factor-II Messenger RNA-Binding Protein 1 Is Associated with Tumor Progression in Patients with Lung Cancer. Clin. Cancer Res. 13: 434-442 [Abstract] [Full Text]  
  • Geng, C., Macdonald, P. M. (2006). Imp Associates with Squid and Hrp48 and Contributes to Localized Expression of gurken in the Oocyte. Mol. Cell. Biol. 26: 9508-9516 [Abstract] [Full Text]  
  • Stohr, N., Lederer, M., Reinke, C., Meyer, S., Hatzfeld, M., Singer, R. H., Huttelmaier, S. (2006). ZBP1 regulates mRNA stability during cellular stress. JCB 175: 527-534 [Abstract] [Full Text]  
  • Nie, M., Htun, H. (2006). Different modes and potencies of translational repression by sequence-specific RNA-protein interaction at the 5'-UTR. Nucleic Acids Res 34: 5528-5540 [Abstract] [Full Text]  
  • Patel, G. P., Ma, S., Bag, J. (2005). The autoregulatory translational control element of poly(A)-binding protein mRNA forms a heteromeric ribonucleoprotein complex. Nucleic Acids Res 33: 7074-7089 [Abstract] [Full Text]  
  • Islam, S., Montgomery, R. K., Fialkovich, J. J., Grand, R. J. (2005). Developmental and Regional Expression and Localization of mRNAs Encoding Proteins Involved in RNA Translocation. J. Histochem. Cytochem. 53: 1501-1509 [Abstract] [Full Text]  
  • Zekri, L., Chebli, K., Tourriere, H., Nielsen, F. C., Hansen, T. V. O., Rami, A., Tazi, J. (2005). Control of Fetal Growth and Neonatal Survival by the RasGAP-Associated Endoribonuclease G3BP. Mol. Cell. Biol. 25: 8703-8716 [Abstract] [Full Text]  
  • Hammer, N. A, Hansen, T. v O, Byskov, A. G., Rajpert-De Meyts, E., Grondahl, M. L., Bredkjaer, H. E, Wewer, U. M, Christiansen, J., Nielsen, F. C (2005). Expression of IGF-II mRNA-binding proteins (IMPs) in gonads and testicular cancer. Reproduction 130: 203-212 [Abstract] [Full Text]  
  • Meng, Z., King, P. H., Nabors, L. B., Jackson, N. L., Chen, C.-Y., Emanuel, P. D., Blume, S. W. (2005). The ELAV RNA-stability factor HuR binds the 5'-untranslated region of the human IGF-IR transcript and differentially represses cap-dependent and IRES-mediated translation. Nucleic Acids Res 33: 2962-2979 [Abstract] [Full Text]  
  • Ioannidis, P., Mahaira, L. G., Perez, S. A., Gritzapis, A. D., Sotiropoulou, P. A., Kavalakis, G. J., Antsaklis, A. I., Baxevanis, C. N., Papamichail, M. (2005). CRD-BP/IMP1 Expression Characterizes Cord Blood CD34+ Stem Cells and Affects c-myc and IGF-II Expression in MCF-7 Cancer Cells. J. Biol. Chem. 280: 20086-20093 [Abstract] [Full Text]  
  • Liao, B., Hu, Y., Herrick, D. J., Brewer, G. (2005). The RNA-binding Protein IMP-3 Is a Translational Activator of Insulin-like Growth Factor II Leader-3 mRNA during Proliferation of Human K562 Leukemia Cells. J. Biol. Chem. 280: 18517-18524 [Abstract] [Full Text]  
  • Woods, A. J., Kantidakis, T., Sabe, H., Critchley, D. R., Norman, J. C. (2005). Interaction of Paxillin with Poly(A)-Binding Protein 1 and Its Role in Focal Adhesion Turnover and Cell Migration. Mol. Cell. Biol. 25: 3763-3773 [Abstract] [Full Text]  
  • Lindegaard, M. L. S., Nielsen, J. E., Hannibal, J., Nielsen, L. B. (2005). Expression of the endothelial lipase gene in murine embryos and reproductive organs. J. Lipid Res. 46: 439-444 [Abstract] [Full Text]  
  • Liao, B., Patel, M., Hu, Y., Charles, S., Herrick, D. J., Brewer, G. (2004). Targeted Knockdown of the RNA-binding Protein CRD-BP Promotes Cell Proliferation via an Insulin-like Growth Factor II-dependent Pathway in Human K562 Leukemia Cells. J. Biol. Chem. 279: 48716-48724 [Abstract] [Full Text]  
  • Nielsen, J., Kristensen, M. A., Willemoes, M., Nielsen, F. C., Christiansen, J. (2004). Sequential dimerization of human zipcode-binding protein IMP1 on RNA: a cooperative mechanism providing RNP stability. Nucleic Acids Res 32: 4368-4376 [Abstract] [Full Text]  
  • Faber, K., Axler, O., Dahlback, B., Nielsen, L. B. (2004). Characterization of apoM in normal and genetically modified mice. J. Lipid Res. 45: 1272-1278 [Abstract] [Full Text]  
  • Otulakowski, G., Rafii, B., O'Brodovich, H. (2004). Differential Translational Efficiency of ENaC Subunits During Lung Development. Am. J. Respir. Cell Mol. Bio. 30: 862-870 [Abstract] [Full Text]  
  • Hansen, T. V. O., Hammer, N. A., Nielsen, J., Madsen, M., Dalbaeck, C., Wewer, U. M., Christiansen, J., Nielsen, F. C. (2004). Dwarfism and Impaired Gut Development in Insulin-Like Growth Factor II mRNA-Binding Protein 1-Deficient Mice. Mol. Cell. Biol. 24: 4448-4464 [Abstract] [Full Text]  
  • Tessier, C. R., Doyle, G. A., Clark, B. A., Pitot, H. C., Ross, J. (2004). Mammary Tumor Induction in Transgenic Mice Expressing an RNA-Binding Protein. Cancer Res. 64: 209-214 [Abstract] [Full Text]  
  • Yaniv, K., Fainsod, A., Kalcheim, C., Yisraeli, J. K. (2003). The RNA-binding protein Vg1 RBP is required for cell migration during early neural development. Development 130: 5649-5661 [Abstract] [Full Text]  
  • Eom, T., Antar, L. N., Singer, R. H., Bassell, G. J. (2003). Localization of a {beta}-Actin Messenger Ribonucleoprotein Complex with Zipcode-Binding Protein Modulates the Density of Dendritic Filopodia and Filopodial Synapses. J. Neurosci. 23: 10433-10444 [Abstract] [Full Text]  
  • Koziol, J. A., Zhang, J.-Y., Casiano, C. A., Peng, X.-X., Shi, F.-D., Feng, A. C., Chan, E. K. L., Tan, E. M. (2003). Recursive Partitioning as an Approach to Selection of Immune Markers for Tumor Diagnosis. Clin. Cancer Res. 9: 5120-5126 [Abstract] [Full Text]  
  • Hayano, T., Yanagida, M., Yamauchi, Y., Shinkawa, T., Isobe, T., Takahashi, N. (2003). Proteomic Analysis of Human Nop56p-associated Pre-ribosomal Ribonucleoprotein Complexes: POSSIBLE LINK BETWEEN Nop56p AND THE NUCLEOLAR PROTEIN TREACLE RESPONSIBLE FOR TREACHER COLLINS SYNDROME. J. Biol. Chem. 278: 34309-34319 [Abstract] [Full Text]  
  • Zhang, J.-Y., Casiano, C. A., Peng, X.-X., Koziol, J. A., Chan, E. K. L., Tan, E. M. (2003). Enhancement of Antibody Detection in Cancer Using Panel of Recombinant Tumor-associated Antigens. Cancer Epidemiol. Biomarkers Prev. 12: 136-143 [Abstract] [Full Text]  
  • Farina, K. L., Huttelmaier, S., Musunuru, K., Darnell, R., Singer, R. H. (2003). Two ZBP1 KH domains facilitate {beta}-actin mRNA localization, granule formation, and cytoskeletal attachment. JCB 160: 77-87 [Abstract] [Full Text]  
  • Monk, D, Bentley, L, Beechey, C, Hitchins, M, Peters, J, Preece, M A, Stanier, P, Moore, G E (2002). Characterisation of the growth regulating gene IMP3, a candidate for Silver-Russell syndrome. J. Med. Genet. 39: 575-581 [Full Text]  
  • O'Sullivan, D. C., Szestak, T. A. M., Pell, J. M. (2002). Regulation of IGF-I mRNA by GH: putative functions for class 1 and 2 message. Am. J. Physiol. Endocrinol. Metab. 283: E251-E258 [Abstract] [Full Text]  
  • Nielsen, F. C., Nielsen, J., Kristensen, M. A., Koch, G., Christiansen, J. (2002). Cytoplasmic trafficking of IGF-II mRNA-binding protein by conserved KH domains. J. Cell Sci. 115: 2087-2097 [Abstract] [Full Text]  
  • Goya, L., de la Puente, A., Ramos, S., Martin, M. A., Escriva, F., Alvarez, C., Pascual-Leone, A. M. (2001). Regulation of IGF-I and -II by Insulin in Primary Cultures of Fetal Rat Hepatocytes. Endocrinology 142: 5089-5096 [Abstract] [Full Text]  
  • Burns, J. L., Hassan, A. B. (2001). Cell survival and proliferation are modified by insulin-like growth factor 2 between days 9 and 10 of mouse gestation. Development 128: 3819-3830 [Abstract] [Full Text]  
  • Lu, M., Nakamura, R. M., Dent, E. D., Zhang, J.-Y., Nielsen, F. C., Christiansen, J., Chan, E. K. L., Tan, E. M. (2001). Aberrant Expression of Fetal RNA-Binding Protein p62 in Liver Cancer and Liver Cirrhosis. Am. J. Pathol. 159: 945-953 [Abstract] [Full Text]  
  • DAS, M., HARVEY, I., CHU, L. L., SINHA, M., PELLETIER, J. (2001). Full-length cDNAs: more than just reaching the ends. Physiol. Genomics 6: 57-80 [Abstract] [Full Text]  
  • Gingras, A.-C., Raught, B., Sonenberg, N. (2001). Regulation of translation initiation by FRAP/mTOR. Genes Dev. 15: 807-826 [Full Text]  
  • Doyle, G. A., Bourdeau-Heller, J. M., Coulthard, S., Meisner, L. F., Ross, J. (2000). Amplification in Human Breast Cancer of a Gene Encoding a c-myc mRNA-binding Protein. Cancer Res. 60: 2756-2759 [Abstract] [Full Text]  
  • Cazzola, M., Skoda, R. C. (2000). Translational pathophysiology: a novel molecular mechanism of human disease. Blood 95: 3280-3288 [Abstract] [Full Text]  
  • Coulis, C. M., Lee, C., Nardone, V., Prokipcak, R. D. (2000). Inhibition of c-myc Expression in Cells by Targeting an RNA-Protein Interaction Using Antisense Oligonucleotides. Mol. Pharmacol. 57: 485-494 [Abstract] [Full Text]  
  • Runge, S., Nielsen, F. C., Nielsen, J., Lykke-Andersen, J., Wewer, U. M., Christiansen, J. (2000). H19 RNA Binds Four Molecules of Insulin-like Growth Factor II mRNA-binding Protein. J. Biol. Chem. 275: 29562-29569 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»