The Fanconi Anemia Protein FANCC Binds to and Facilitates the Activation of STAT1 by Gamma Interferon and Hematopoietic Growth Factors

REFERENCES

• Avalos, B. R., Parker, J. M., Ware, D. A., Hunter, M. G., Sibert, K. A., and Druker, B. J.. 1997. Dissociation of the Jak kinase pathway from G-CSF receptor signaling in neutrophils. Exp. Hematol. 25:160–168
   PubMed Web of Science ®Google Scholar
• Bach, E. A., Aguet, M., and Schreiber, R. D.. 1997. The IFN gamma receptor: a paradigm for cytokine receptor signaling. Annu. Rev. Immunol. 15:563–591
   PubMed Web of Science ®Google Scholar
• Bagnara, G. P., Strippoli, P., Bonsi, L., Brizzi, M. F., Avanzi, G. C., Timeus, F., Ramenghi, U., Piaggio, G., Tong, J., Podesta, M. et al. 1992. Effect of stem cell factor on colony growth from acquired and constitutional (Fanconi) aplastic anemia. Blood 80:382–387
   PubMedGoogle Scholar
• Bradford, M. M.. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248–254
   PubMed Web of Science ®Google Scholar
• Brizzi, M. F., Dentelli, P., Rosso, A., Yarden, Y., and Pegoraro, L.. 1999. STAT protein recruitment and activation in c-Kit deletion mutants. J. Biol. Chem. 274:16965–16972
   PubMedGoogle Scholar
• Darnell, J. E.Jr.. 1997. STATs and gene regulation. Science 277:1630–1635
   PubMed Web of Science ®Google Scholar
• DeBerry, C., Mou, S., and Linnekin, D.. 1997. STAT1 associates with c-kit and is activated in response to stem cell factor. Biochem. J. 327:73–80
   PubMed Web of Science ®Google Scholar
• Dignam, J. D., Lebovitz, R. M., and Roeder, R. G.. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475–1489
   PubMed Web of Science ®Google Scholar
• Durbin, J. E., Hackenmiller, R., Simon, M. C., and Levy, D. E.. 1996. Targeted disruption of the mouse Stat1 gene results in compromised innate immunity to viral disease. Cell 84:443–450
   PubMed Web of Science ®Google Scholar
• Fagerlie, S., Diaz, J., Faulkner, G., Grompe, M., Keeble, W., Tower, P., Christianson, T., and Bagby, G. C.. 1997. The Fanconi anemia group C gene product is necessary for normal Stat1 phosphorylation. Blood 90 (Suppl. 1): 571a
   PubMedGoogle Scholar
• Garcia-Higuera, I., Kuang, Y., Naf, D., Wasik, J., and D'Andrea, A. D.. 1999. Fanconi anemia proteins FANCA, FANCC, and FANCG/XRCC9 interact in a functional nuclear complex. Mol. Cell. Biol. 19:4866–4873
   PubMed Web of Science ®Google Scholar
• Greenlund, A. C., Farrar, M. A., Viviano, B. L., and Schreiber, R. D.. 1994. Ligand-induced IFN gamma receptor tyrosine phosphorylation couples the receptor to its signal transduction system (p91). EMBO J. 13:1591–1600
   PubMed Web of Science ®Google Scholar
• Greenlund, A. C., Morales, M. O., Viviano, B. L., Yan, H., Krolewski, J., and Schreiber, R. D.. 1995. Stat recruitment by tyrosine-phosphorylated cytokine receptors: an ordered reversible affinity-driven process. Immunity 2:677–687
   PubMed Web of Science ®Google Scholar
• Haneline, L. S., Broxmeyer, H. E., Cooper, S., Hangoc, G., Carreau, M., Buchwald, M., and Clapp, D. W.. 1998. Multiple inhibitory cytokines induce deregulated progenitor growth and apoptosis in hematopoietic cells from Fac−/− mice. Blood 91:4092–4098
   PubMed Web of Science ®Google Scholar
• Hilton, D. J., Richardson, R. T., Alexander, W. S., Viney, E. M., Willson, T. A., Sprigg, N. S., Starr, R., Nicholson, S. E., Metcalf, D., and Nicola, N. A.. 1998. Twenty proteins containing a C-terminal SOCS box form five structural classes. Proc. Natl. Acad. Sci. USA 95:114–119
   PubMed Web of Science ®Google Scholar
• Hoatlin, M. E., Christianson, T. A., Keeble, W. W., Hammond, A. T., Zhi, Y., Heinrich, M. C., Tower, P. A., Bagby, G. C.Jr.. 1998. The Fanconi anemia group C gene product is located in both the nucleus and cytoplasm of human cells. Blood 91:1418–1425
   PubMed Web of Science ®Google Scholar
• Hoatlin, M. E., Zhi, Y., Ball, H., Silvey, K., Melnick, A., Stone, S., Arai, S., Hawe, N., Owen, G., Zelent, A., and Licht, J. D.. 1999. A novel BTB/POZ transcriptional repressor protein interacts with the Fanconi anemia group C protein and PLZF. Blood 94:3737–3747
   PubMedGoogle Scholar
• Horvath, C. M., and Darnell, J. E.. 1997. The state of the STATs: recent developments in the study of signal transduction to the nucleus. Curr. Opin. Cell Biol. 9:233–239
   PubMed Web of Science ®Google Scholar
• Hovland, P., Flick, J., Johnston, M., and Sclafani, R. A.. 1989. Galactose as a gratuitous inducer of GAL gene expression in yeasts growing on glucose. Gene 83:57–64
   PubMed Web of Science ®Google Scholar
• Ihle, J. N.. 1995. Cytokine receptor signalling. Nature 377:591–594
   PubMed Web of Science ®Google Scholar
• Ihle, J. N.. 1996. STATs: signal transducers and activators of transcription. Cell 84:331–334
   PubMed Web of Science ®Google Scholar
• Ihle, J. N., and Kerr, I. M.. 1995. Jaks and Stats in signaling by the cytokine receptor superfamily. Trends Genet. 11:69–74
   PubMed Web of Science ®Google Scholar
• Ihle, J. N., Nosaka, T., Thierfelder, W., Quelle, F. W., and Shimoda, K.. 1997. Jaks and Stats in cytokine signaling. Stem Cells 15 (Suppl 1):105–111
   PubMedGoogle Scholar
• Kirito, K., Uchida, M., Takatoku, M., Nakajima, K., Hirano, T., Miura, Y., and Komatsu, N.. 1998. A novel function of STAT1 and Stat3 proteins in erythropoietin-induced erythroid differentiation of a human leukemia cell line. Blood 92:462–471
   PubMed Web of Science ®Google Scholar
• Kohlhuber, F., Rogers, N. C., Watling, D., Feng, J., Guschin, D., Briscoe, J., Witthuhn, B. A., Kotenko, S. V., Pestka, S., Stark, G. R., Ihle, J. N., and Kerr, I. M.. 1997. A JAK1/JAK2 chimera can sustain alpha and gamma interferon responses. Mol. Cell. Biol. 17:695–706
   PubMed Web of Science ®Google Scholar
• Kozak, S. L., and Kabat, D.. 1990. Ping-pong amplification of a retroviral vector achieves high-level gene expression: human growth hormone production. J. Virol. 64:3500–3508
   PubMed Web of Science ®Google Scholar
• Li, Y., and Youssoufian, H.. 1997. MxA overexpression reveals a common genetic link in four Fanconi anemia complementation groups. J. Clin. Investig. 100:2873–2880
   PubMed Web of Science ®Google Scholar
• Meraz, M. A., White, J. M., Sheehan, K. C., Bach, E. A., Rodig, S. J., Dighe, A. S., Kaplan, D. H., Riley, J. K., Greenlund, A. C., Campbell, D., Carver-Moore, K., DuBois, R. N., Clark, R., Aguet, M., and Schreiber, R. D.. 1996. Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell 84:431–442
   PubMed Web of Science ®Google Scholar
• Metcalf, D., Alexander, W. S., Elefanty, A. G., Nicola, N. A., Hilton, D. J., Starr, R., Mifsud, S., and DiRago, L.. 1999. Aberrant hematopoiesis in mice with inactivation of the gene encoding SOCS-1. Leukemia 13:926–934
   PubMed Web of Science ®Google Scholar
• Muller, M., Briscoe, J., Laxton, C., Guschin, D., Ziemiecki, A., Silvennoinen, O., Harpur, A. G., Barbieri, G., Witthuhn, B. A., and Schindler, C.. 1993. The protein tyrosine kinase JAK1 complements defects in interferon-alpha/beta and -gamma signal transduction. Nature 366:129–135
   PubMed Web of Science ®Google Scholar
• Nelson, J. R., Lawrence, C. W., and Hinkle, D. C.. 1996. Thymine-thymine dimer bypass by yeast DNA polymerase zeta. Science 272:1646–1649
   PubMed Web of Science ®Google Scholar
• Nelson, J. R., Lawrence, C. W., and Hinkle, D. C.. 1996. Deoxycytidyl transferase activity of yeast REV1 protein. Nature 382:729–731
   PubMed Web of Science ®Google Scholar
• Neubauer, H., Cumano, A., Muller, M., Wu, H., Huffstadt, U., and Pfeffer, K.. 1998. Jak2 deficiency defines an essential developmental checkpoint in definitive hematopoiesis. Cell 93:397–409
   PubMed Web of Science ®Google Scholar
• Pallard, C., Gouilleux, F., Benit, L., Cocault, L., Souyri, M., Levy, D., Groner, B., Gisselbrecht, S., and Dusanter-Fourt, I.. 1995. Thrombopoietin activates a STAT5-like factor in hematopoietic cells. EMBO J. 14:2847–2856
   PubMed Web of Science ®Google Scholar
• Parganas, E., Wang, D., Stravopodis, D., Topham, D. J., Marine, J.-C., Teglund, S., Vanin, E. F., Bodner, S., Colamonici, O. R., van Deusen, J. M., Grosveld, G., and Ihle, J. N.. 1998. Jak2 is essential for signaling through a variety of cytokine receptors. Cell 93:385–395
   PubMed Web of Science ®Google Scholar
• Penta, K., and Sawyer, S. T.. 1995. Erythropoietin induces the tyrosine phosphorylation, nuclear translocation, and DNA binding of STAT1 and STAT5 in erythroid cells. J. Biol. Chem. 270:31282–31287
   PubMed Web of Science ®Google Scholar
• Rajotte, D., Sadowski, H. B., Haman, A., Gopalbhai, K., Meloche, S., Liu, L., Krystal, G., and Hoang, T.. 1996. Contribution of both STAT and SRF/TCF to c-fos promoter activation by granulocyte-macrophage colony-stimulating factor. Blood 88:2906–2916
   PubMed Web of Science ®Google Scholar
• Rathbun, R. K., Faulkner, G. R., Ostroski, M. H., Christianson, T. A., Hughes, G., Jones, G., Cahn, R., Maziarz, R., Royle, G., Keeble, W., Heinrich, M. C., Grompe, M., Tower, P. A., and Bagby, G. C.. 1997. Inactivation of the Fanconi anemia group C gene augments interferon-gamma-induced apoptotic responses in hematopoietic cells. Blood 90:974–985
   PubMed Web of Science ®Google Scholar
• Rodig, S. J., Meraz, M. A., White, J. M., Lampe, P. A., Riley, J. K., Arthur, C. D., King, K. L., Sheehan, K. C. F., Yin, L., Pennica, D., Johnson, E. M., and Schreiber, R. D.. 1998. Disruption of the Jak1 gene demonstrates obligatory and nonredundant roles of the Jaks in cytokine-induced biologic responses. Cell 93:373–383
   PubMed Web of Science ®Google Scholar
• Ronni, T., Sareneva, T., Pirhonen, J., and Julkunen, I.. 1995. Activation of IFN-alpha, IFN-gamma, MxA, and IFN regulatory factor 1 genes in influenza A virus-infected human peripheral blood mononuclear cells. J. Immunol. 154:2764–2774
   PubMedGoogle Scholar
• Sakamoto, H., Yasukawa, H., Masuhara, M., Tanimura, S., Sasaki, A., Yuge, K., Ohtsubo, M., Ohtsuka, A., Fujita, T., Ohta, T., Furukawa, Y., Iwase, S., Yamada, H., and Yoshimura, A.. 1998. A Janus kinase inhibitor, JAB, is an interferon-gamma-inducible gene and confers resistance to interferons. Blood 92:1668–1676
   PubMed Web of Science ®Google Scholar
• Sakatsume, M., Igarashi, K., Winestock, K. D., Garotta, G., Larner, A. C., and Finbloom, D. S.. 1995. The Jak kinases differentially associate with the alpha and beta (accessory factor) chains of the interferon gamma receptor to form a functional receptor unit capable of activating STAT transcription factors. J. Biol. Chem. 270:17528–17534
   PubMed Web of Science ®Google Scholar
• Sato, T., Selleri, C., Young, N. S., and Maciejewski, J. P.. 1997. Inhibition of interferon regulatory factor-1 expression results in predominance of cell growth stimulatory effects of interferon-gamma due to phosphorylation of Stat1 and Stat3. Blood 90:4749–4758
   PubMedGoogle Scholar
• Schindler, C., Darnell, J. E.Jr.. 1995. Transcriptional responses to polypeptide ligands: the JAK-STAT pathway. Annu. Rev. Biochem. 64:621–651
   PubMed Web of Science ®Google Scholar
• Schindler, C., Shuai, K., Prezioso, V. R., Darnell, J. E.Jr.. 1992. Interferon-dependent tyrosine phosphorylation of a latent cytoplasmic transcription factor. Science 257:809–813
   PubMed Web of Science ®Google Scholar
• Segal, G. M., Smith, T. D., Heinrich, M. C., Ey, F. S., Bagby, G. C.Jr.. 1992. Specific repression of granulocyte-macrophage and granulocyte colony-stimulating factor gene expression in interleukin-1-stimulated endothelial cells with antisense oligodeoxynucleotides. Blood 80:609–616
   PubMedGoogle Scholar
• Shimoda, K., Feng, J., Murakami, H., Nagata, S., Watling, D., Rogers, N. C., Stark, G. R., Kerr, I. M., and Ihle, J. N.. 1997. Jak1 plays an essential role for receptor phosphorylation and Stat activation in response to granulocyte colony-stimulating factor. Blood 90:597–604
   PubMed Web of Science ®Google Scholar
• Shuai, K., Stark, G. R., Kerr, I. M., Darnell, J. E.Jr.. 1993. A single phosphotyrosine residue of Stat91 required for gene activation by interferon-gamma. Science 261:1744–1746
   PubMed Web of Science ®Google Scholar
• Staeheli, P., and Sutcliffe, J. G.. 1988. Identification of a second interferon-regulated murine Mx gene. Mol. Cell. Biol. 8:4524–4528
   PubMedGoogle Scholar
• Strathdee, C. A., Gavish, H., Shannon, W. R., and Buchwald, M.. 1992. Cloning of cDNAs for Fanconi's anaemia by functional complementation. Nature 356:763–767
   PubMed Web of Science ®Google Scholar
• Tauchi, T., Feng, G. S., Shen, R., Hoatlin, M., Bagby, G. C.Jr., Kabat, D., Lu, L., and Broxmeyer, H. E.. 1995. Involvement of SH2-containing phosphotyrosine phosphatase Syp in erythropoietin receptor signal transduction pathways. J. Biol. Chem. 270:5631–5635
   PubMed Web of Science ®Google Scholar
• Tower, P. A., Christianson, T. A., Peters, S. T., Ostroski, M. L., Hoatlin, M. E., Zigler, A. J., Heinrich, M. C., Rathbun, R. K., Keeble, W., Faulkner, G. R., Bagby, G. C.Jr.. 1998. Expression of the Fanconi anemia group C gene in hematopoietic cells is not influenced by oxidative stress, cross-linking agents, radiation, heat, or mitotic inhibitory factors. Exp. Hematol. 26:19–26
   PubMed Web of Science ®Google Scholar
• Waisfisz, Q., de Winter, J. P., Kruyt, F. A., de Groot, J., van der Weel, L., Dijkmans, L. M., Zhi, Y., Arwert, F., Scheper, R. J., Youssoufian, H., Hoatlin, M. E., and Joenje, H.. 1999. A physical complex of the Fanconi anemia proteins FANCG/XRCC9 and FANCA. Proc. Natl. Acad. Sci. USA 96:10320–10325
   PubMed Web of Science ®Google Scholar
• Watling, D., Guschin, D., Muller, M., Silvennoinen, O., Witthuhn, B. A., Quelle, F. W., Rogers, N. C., Schindler, C., Stark, G. R., Ihle, J. N. et al. 1993. Complementation by the protein tyrosine kinase JAK2 of a mutant cell line defective in the interferon-gamma signal transduction pathway. Nature 366:166–170
   PubMed Web of Science ®Google Scholar
• Whitney, M. A., Royle, G., Low, M. J., Kelly, M. A., Axthelm, M. K., Reifsteck, C., Olson, S., Braun, R. E., Heinrich, M. C., Rathbun, R. K., Bagby, G. C., and Grompe, M.. 1996. Germ cell defects and hematopoietic hypersensitivity to gamma-interferon in mice with a targeted disruption of the Fanconi anemia C gene. Blood 88:49–58
   PubMed Web of Science ®Google Scholar
• Yamashita, T., Barber, D. L., Zhu, Y., Wu, N., and D'Andrea, A. D.. 1994. The Fanconi anemia polypeptide FACC is localized to the cytoplasm. Proc. Natl. Acad. Sci. USA 91:6712–6716
   PubMed Web of Science ®Google Scholar
• Youssoufian, H.. 1994. Localization of Fanconi anemia C protein to the cytoplasm of mammalian cells. Proc. Natl. Acad. Sci. USA 91:7975–7979
   PubMed Web of Science ®Google Scholar
• Zhu, X., Wen, Z., Xu, L. Z., Darnell, J. E.Jr.. 1997. STAT1 serine phosphorylation occurs independently of tyrosine phosphorylation and requires an activated Jak2 kinase. Mol. Cell. Biol. 17:6618–6623
   PubMedGoogle Scholar