RNA-Binding Protein HuR Is Required for Stabilization of SLC11A1 mRNA and SLC11A1 Protein Expression

REFERENCES

• Adams, D. J., D. J. Beveridge, L. van der Wyden, H. Mangs, P. J. Leedman, and B. J. Morris. 2003. HADHB, HuR, and CP1 bind to the distal 3′-untranslated region of human renin mRNA and differentially modulate renin expression. J. Biol. Chem. 278:44894–44903.
   PubMedGoogle Scholar
• Atasoy, U., S. L. Curry, I. Lopez de Silanes, A. B. Shyu, V. Casolaro, M. Gorospe, and C. Stellato. 2003. Regulation of eotaxin gene expression by TNF-alpha and IL-4 through mRNA stabilization: involvement of the RNA-binding protein HuR. J. Immunol. 171:4369–4378.
   PubMed Web of Science ®Google Scholar
• Atasoy, U., J. Watson, D. Patel, and J. D. Keene. 1998. ELAV protein HuA (HuR) can redistribute between nucleus and cytoplasm and is upregulated during serum stimulation and T cell activation. J. Cell Sci. 111:3145–3156.
   PubMed Web of Science ®Google Scholar
• Atkinson, P. G., and C. H. Barton. 1998. Ectopic expression of Nramp1 in COS-1 cells modulates iron accumulation. FEBS Lett. 425:239–242.
   PubMed Web of Science ®Google Scholar
• Bakheet, T., M. Frevel, B. R. Williams, W. Greer, and K. S. Khabar. 2001. ARED: human AU-rich element-containing mRNA database reveals an unexpectedly diverse functional repertoire of encoded proteins. Nucleic Acids Res. 29:246–254.
   PubMedGoogle Scholar
• Blackwell, J. M., C. H. Barton, J. K. White, T. I. Roach, M. A. Shaw, S. H. Whitehead, B. A. Mock, S. Searle, H. Williams, and A. M. Baker. 1994. Genetic regulation of leishmanial and mycobacterial infections: the Lsh/Ity/Bcg gene story continues. Immunol. Lett. 43:99–107.
   PubMed Web of Science ®Google Scholar
• Blackwell, J. M., T. Goswami, C. A. Evans, D. Sibthorpe, N. Papo, J. K. White, S. Searle, E. N. Miller, C. S. Peacock, H. Mohammed, and M. Ibrahim. 2001. SLC11A1 (formerly NRAMP1) and disease resistance. Cell. Microbiol. 3:773–784.
   PubMed Web of Science ®Google Scholar
• Bradley, D. J. 1977. Regulation of Leishmania populations within the host. II. Genetic control of acute susceptibility of mice to Leishmania donovani infection. Clin. Exp. Immunol. 30:130–140.
   PubMed Web of Science ®Google Scholar
• Brennan, C. M., and J. A. Steitz. 2001. HuR and mRNA stability. Cell. Mol. Life Sci. 58:266–277.
   PubMed Web of Science ®Google Scholar
• Brown, D. H., W. LaFuse, and B. S. Zwilling. 1995. Cytokine-mediated activation of macrophages from Mycobacterium bovis BCG-resistant and -susceptible mice: differential effects of corticosterone on antimycobacterial activity and expression of the Bcg gene (candidate Nramp). Infect. Immun. 63:2983–2988.
   PubMedGoogle Scholar
• Cellier, M., C. Shustik, W. Dalton, E. Rich, J. Hu, D. Malo, E. Schurr, and P. Gros. 1997. Expression of the human NRAMP1 gene in professional primary phagocytes: studies in blood cells and in HL-60 promyelocytic leukemia. J. Leukoc. Biol. 61:96–105.
   PubMedGoogle Scholar
• Chen, C. Y., and A. B. Shyu. 1995. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20:465–470.
   PubMed Web of Science ®Google Scholar
• Chen, C. Y., F. Gatto-Konczak, Z. Wu, and M. Karin. 1998. Stabilization of interleukin-2 mRNA by the c-Jun NH2-terminal kinase pathway. Science 280:1945–1949.
   PubMed Web of Science ®Google Scholar
• Dean, J. L., R. Wait, K. R. Mahtani, G. Sully, A. R. Clark, and J. Saklatvala. 2001. The 3′ untranslated region of tumor necrosis factor alpha mRNA is a target of the mRNA-stabilizing factor HuR. Mol. Cell. Biol. 21:721–730.
   PubMed Web of Science ®Google Scholar
• Denkert, C., W. Weichert, K. J. Winzer, B. M. Muller, A. Noske, S. Niesporek, G. Kristiansen, H. Guski, M. Dietel, and S. Hauptmann. 2004. Expression of the ELAV-like protein HuR is associated with higher tumor grade and increased cyclooxygenase-2 expression in human breast carcinoma. Clin. Cancer Res. 10:5580–5586.
   PubMed Web of Science ®Google Scholar
• Denkert, C., W. Weichert, S. Pest, I. Koch, D. Licht, M. Kobel, A. Reles, J. Sehouli, M. Dietel, and S. Hauptmann. 2004. Overexpression of the embryonic-lethal abnormal vision-like protein HuR in ovarian carcinoma is a prognostic factor and is associated with increased cyclooxygenase 2 expression. Cancer Res. 64:189–195.
   PubMed Web of Science ®Google Scholar
• Di Marco, S., Z. Hel, C. Lachance, H. Furneaux, and D. Radzioch. 2001. Polymorphism in the 3′-untranslated region of TNFalpha mRNA impairs binding of the post-transcriptional regulatory protein HuR to TNFalpha mRNA. Nucleic Acids Res. 29:863–871.
   PubMed Web of Science ®Google Scholar
• Dixon, D. A., N. D. Tolley, P. H. King, L. B. Nabors, T. M. McIntyre, G. A. Zimmerman, and S. M. Prescott. 2001. Altered expression of the mRNA stability factor HuR promotes cyclooxygenase-2 expression in colon cancer cells. J. Clin. Investig. 108:1657–1665.
   PubMed Web of Science ®Google Scholar
• Donninger, H., T. J. Cashmore, T. Scriba, D. C. Petersen, V. R. Janse, and V. M. Hayes. 2004. Functional analysis of novel SLC11A1 (NRAMP1) promoter variants in susceptibility to HIV-1. J. Med. Genet. 41:e49.
   PubMedGoogle Scholar
• Estrada-Chavez, C., A. L. Pereira-Suarez, M. A. Meraz, C. Arriaga, A. Garcia-Carranca, C. Sanchez-Rodriguez, and R. Mancilla. 2001. High-level expression of NRAMP1 in peripheral blood cells and tuberculous granulomas from Mycobacterium bovis-infected bovines. Infect. Immun. 69:7165–7168.
   PubMedGoogle Scholar
• Fan, X. C., and J. A. Steitz. 1998. Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J. 17:3448–3460.
   PubMed Web of Science ®Google Scholar
• Figueroa, A., A. Cuadrado, J. Fan, U. Atasoy, G. E. Muscat, P. Munoz-Canoves, M. Gorospe, and A. Munoz. 2003. Role of HuR in skeletal myogenesis through coordinate regulation of muscle differentiation genes. Mol. Cell. Biol. 23:4991–5004.
   PubMed Web of Science ®Google Scholar
• Gallouzi, I. E., C. M. Brennan, M. G. Stenberg, M. S. Swanson, A. Eversole, N. Maizels, and J. A. Steitz. 2000. HuR binding to cytoplasmic mRNA is perturbed by heat shock. Proc. Natl. Acad. Sci. USA 97:3073–3078.
   PubMedGoogle Scholar
• Gallouzi, I. E., and J. A. Steitz. 2001. Delineation of mRNA export pathways by the use of cell-permeable peptides. Science 294:1895–1901.
   PubMed Web of Science ®Google Scholar
• Garnon, J., C. Lachance, M. S. Di, Z. Hel, D. Marion, M. C. Ruiz, M. M. Newkirk, E. W. Khandjian, and D. Radzioch. 2005. Fragile X-related protein FXR1P regulates proinflammatory cytokine tumor necrosis factor expression at the post-transcriptional level. J. Biol. Chem. 280:5750–5763.
   PubMed Web of Science ®Google Scholar
• Good, P. J. 1995. A conserved family of elav-like genes in vertebrates. Proc. Natl. Acad. Sci. USA 92:4557–4561.
   PubMed Web of Science ®Google Scholar
• Govoni, G., and P. Gros. 1998. Macrophage NRAMP1 and its role in resistance to microbial infections. Inflamm. Res. 47:277–284.
   PubMedGoogle Scholar
• Govoni, G., S. Gauthier, F. Billia, N. N. Iscove, and P. Gros. 1997. Cell-specific and inducible Nramp1 gene expression in mouse macrophages in vitro and in vivo. J. Leukoc. Biol. 62:277–286.
   PubMed Web of Science ®Google Scholar
• Harris, P., and P. Ralph. 1985. Human leukemic models of myelomonocytic development: a review of the HL-60 and U937 cell lines. J. Leukoc. Biol. 37:407–422.
   PubMed Web of Science ®Google Scholar
• Holtmann, H., R. Winzen, P. Holland, S. Eickemeier, E. Hoffmann, D. Wallach, N. L. Malinin, J. A. Cooper, K. Resch, and M. Kracht. 1999. Induction of interleukin-8 synthesis integrates effects on transcription and mRNA degradation from at least three different cytokine- or stress-activated signal transduction pathways. Mol. Cell. Biol. 19:6742–6753.
   PubMed Web of Science ®Google Scholar
• Iwai, Y., K. Akahane, D. H. Pluznik, and R. B. Cohen. 1993. Ca2+ ionophore A23187-dependent stabilization of granulocyte-macrophage colony-stimulating factor messenger RNA in murine thymoma EL-4 cells is mediated through two distinct regions in the 3′-untranslated region. J. Immunol. 150:4386–4394.
   PubMedGoogle Scholar
• Keene, J. D. 1999. Why is Hu where? Shuttling of early-response-gene messenger RNA subsets. Proc. Natl. Acad. Sci. USA 96:5–7.
   PubMed Web of Science ®Google Scholar
• Lafuse, W. P., G. R. Alvarez, and B. S. Zwilling. 2000. Regulation of Nramp1 mRNA stability by oxidants and protein kinase C in RAW264.7 macrophages expressing Nramp1(Gly169). Biochem. J. 351:687–696.
   PubMedGoogle Scholar
• Lal, A., K. Mazan-Mamczarz, T. Kawai, X. Yang, J. L. Martindale, and M. Gorospe. 2004. Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J. 23:3092–3102.
   PubMed Web of Science ®Google Scholar
• Lasa, M., K. R. Mahtani, A. Finch, G. Brewer, J. Saklatvala, and A. R. Clark. 2000. Regulation of cyclooxygenase 2 mRNA stability by the mitogen-activated protein kinase p38 signaling cascade. Mol. Cell. Biol. 20:4265–4274.
   PubMed Web of Science ®Google Scholar
• Le, C., V, J. B. Cowland, J. Calafat, and N. Borregaard. 1996. Targeting of proteins to granule subsets is determined by timing and not by sorting: the specific granule protein NGAL is localized to azurophil granules when expressed in HL-60 cells. Proc. Natl. Acad. Sci. USA 93:6454–6457.
   PubMedGoogle Scholar
• Li, H., S. Park, B. Kilburn, M. A. Jelinek, A. Henschen-Edman, D. W. Aswad, M. R. Stallcup, and I. A. Laird-Offringa. 2002. Lipopolysaccharide-induced methylation of HuR, an mRNA-stabilizing protein, by CARM1. Coactivator-associated arginine methyltransferase. J. Biol. Chem. 277:44623–44630.
   PubMed Web of Science ®Google Scholar
• Lindstein, T., C. H. June, J. A. Ledbetter, G. Stella, and C. B. Thompson. 1989. Regulation of lymphokine messenger RNA stability by a surface-mediated T cell activation pathway. Science 244:339–343.
   PubMed Web of Science ®Google Scholar
• McMullen, M. R., E. Cocuzzi, M. Hatzoglou, and L. E. Nagy. 2003. Chronic ethanol exposure increases the binding of HuR to the TNFalpha 3′-untranslated region in macrophages. J. Biol. Chem. 278:38333–38341.
   PubMed Web of Science ®Google Scholar
• Mohamed, H. S., M. E. Ibrahim, E. N. Miller, J. K. White, H. J. Cordell, J. M. Howson, C. S. Peacock, E. A. Khalil, A. M. El Hassan, and J. M. Blackwell. 2004. SLC11A1 (formerly NRAMP1) and susceptibility to visceral leishmaniasis in The Sudan. Eur. J. Hum. Genet. 12:66–74.
   PubMedGoogle Scholar
• Pages, G., E. Berra, J. Milanini, A. P. Levy, and J. Pouyssegur. 2000. Stress-activated protein kinases (JNK and p38/HOG) are essential for vascular endothelial growth factor mRNA stability. J. Biol. Chem. 275:26484–26491.
   PubMed Web of Science ®Google Scholar
• Park, J. W., M. A. Jang, Y. H. Lee, A. Passaniti, and T. K. Kwon. 2001. p53-independent elevation of p21 expression by PMA results from PKC-mediated mRNA stabilization. Biochem. Biophys. Res. Commun. 280:244–248.
   PubMedGoogle Scholar
• Peng, S. S., C. Y. Chen, N. Xu, and A. B. Shyu. 1998. RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J. 17:3461–3470.
   PubMed Web of Science ®Google Scholar
• Plant, J., and A. A. Glynn. 1976. Genetics of resistance to infection with Salmonella typhimurium in mice. J. Infect. Dis. 133:72–78.
   PubMed Web of Science ®Google Scholar
• Roig, E. A., E. Richer, F. Canonne-Hergaux, P. Gros, and M. F. Cellier. 2002. Regulation of NRAMP1 gene expression by 1alpha,25-dihydroxy-vitamin D(3) in HL-60 phagocytes. J. Leukoc. Biol. 71:890–904.
   PubMedGoogle Scholar
• Ross, J. 1995. mRNA stability in mammalian cells. Microbiol. Rev. 59:423–450.
   PubMedGoogle Scholar
• Ross, J. 1996. Control of messenger RNA stability in higher eukaryotes. Trends Genet. 12:171–175.
   PubMed Web of Science ®Google Scholar
• Rousseau, S., N. Morrice, M. Peggie, D. G. Campbell, M. Gaestel, and P. Cohen. 2002. Inhibition of SAPK2a/p38 prevents hnRNP A0 phosphorylation by MAPKAP-K2 and its interaction with cytokine mRNAs. EMBO J. 21:6505–6514.
   PubMed Web of Science ®Google Scholar
• Searle, S., and J. M. Blackwell. 1999. Evidence for a functional repeat polymorphism in the promoter of the human NRAMP1 gene that correlates with autoimmune versus infectious disease susceptibility. J. Med. Genet. 36:295–299.
   PubMed Web of Science ®Google Scholar
• Seko, Y., H. Azmi, R. Fariss, and J. A. Ragheb. 2004. Selective cytoplasmic translocation of HuR and site-specific binding to the interleukin-2 mRNA are not sufficient for CD28-mediated stabilization of the mRNA. J. Biol. Chem. 279:33359–33367.
   PubMed Web of Science ®Google Scholar
• Shaw, G., and R. Kamen. 1986. A conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46:659–667.
   PubMed Web of Science ®Google Scholar
• Skamene, E., P. Gros, A. Forget, P. A. Kongshavn, C. St Charles, and B. A. Taylor. 1982. Genetic regulation of resistance to intracellular pathogens. Nature 297:506–509.
   PubMed Web of Science ®Google Scholar
• Takahashi, K., J. Satoh, Y. Kojima, K. Negoro, M. Hirai, Y. Hinokio, Y. Kinouchi, S. Suzuki, N. Matsuura, T. Shimosegawa, and Y. Oka. 2004. Promoter polymorphism of SLC11A1 (formerly NRAMP1) confers susceptibility to autoimmune type 1 diabetes mellitus in Japanese. Tissue Antigens 63:231–236.
   PubMedGoogle Scholar
• Tenenbaum, S. A., P. J. Lager, C. C. Carson, and J. D. Keene. 2002. Ribonomics: identifying mRNA subsets in mRNP complexes using antibodies to RNA-binding proteins and genomic arrays. Methods 26:191–198.
   PubMed Web of Science ®Google Scholar
• van der Giessen, K., S. Di Marco, E. Clair, and I. E. Gallouzi. 2003. RNAi-mediated HuR depletion leads to the inhibition of muscle cell differentiation. J. Biol. Chem. 278:47119–47128.
   PubMed Web of Science ®Google Scholar
• Vidal, S. M., D. Malo, K. Vogan, E. Skamene, and P. Gros. 1993. Natural resistance to infection with intracellular parasites: isolation of a candidate for Bcg. Cell 73:469–485.
   PubMed Web of Science ®Google Scholar
• Vidal, S. M., E. Pinner, P. Lepage, S. Gauthier, and P. Gros. 1996. Natural resistance to intracellular infections: Nramp1 encodes a membrane phosphoglycoprotein absent in macrophages from susceptible (Nramp1 D169) mouse strains. J. Immunol. 157:3559–3568.
   PubMed Web of Science ®Google Scholar
• Wang, W., J. Fan, X. Yang, S. Fürer-Galban, I. Lopez de Silanes, C. von Kobbe, J. Guo, S. N. Georas, F. Foufelle, D. G. Hardie, D. Carling, and M. Gorospe. 2002. AMP-activated kinase regulates cytoplasmic HuR. Mol. Cell. Biol. 22:3425–3436.
   PubMed Web of Science ®Google Scholar
• Wang, W., H. Furneaux, H. Cheng, M. C. Caldwell, D. Hutter, Y. Liu, N. Holbrook, and M. Gorospe. 2000. HuR regulates p21 mRNA stabilization by UV light. Mol. Cell. Biol. 20:760–769.
   PubMed Web of Science ®Google Scholar
• Westmark, C. J., and J. S. Malter. 2001. Up-regulation of nucleolin mRNA and protein in peripheral blood mononuclear cells by extracellular-regulated kinase. J. Biol. Chem. 276:1119–1126.
   PubMedGoogle Scholar
• Westmark, C. J., and J. S. Malter. 2001. Extracellular-regulated kinase controls beta-amyloid precursor protein mRNA decay. Brain Res. Mol. Brain Res. 90:193–201.
   PubMedGoogle Scholar
• Wilusz, C. J., M. Wormington, and S. W. Peltz. 2001. The cap-to-tail guide to mRNA turnover. Nat. Rev. Mol. Cell Biol. 2:237–246.
   PubMed Web of Science ®Google Scholar
• Winzen, R., M. Kracht, B. Ritter, A. Wilhelm, C. Y. Chen, A. B. Shyu, M. Muller, M. Gaestel, K. Resch, and H. Holtmann. 1999. The p38 MAP kinase pathway signals for cytokine-induced mRNA stabilization via MAP kinase-activated protein kinase 2 and an AU-rich region-targeted mechanism. EMBO J. 18:4969–4980.
   PubMed Web of Science ®Google Scholar
• Wodnar-Filipowicz, A., and C. Moroni. 1990. Regulation of interleukin 3 mRNA expression in mast cells occurs at the posttranscriptional level and is mediated by calcium ions. Proc. Natl. Acad. Sci. USA 87:777–781.
   PubMed Web of Science ®Google Scholar
• Yaman, I., J. Fernandez, B. Sarkar, R. J. Schneider, M. D. Snider, L. E. Nagy, and M. Hatzoglou. 2002. Nutritional control of mRNA stability is mediated by a conserved AU-rich element that binds the cytoplasmic shuttling protein HuR. J. Biol. Chem. 277:41539–41546.
   PubMedGoogle Scholar
• Zhao, K. W., X. Li, Q. Zhao, Y. Huang, D. Li, Z. G. Peng, W. Z. Shen, J. Zhao, Q. Zhou, Z. Chen, P. J. Sims, T. Wiedmer, and G. Q. Chen. 2004. Protein kinase Cdelta mediates retinoic acid and phorbol myristate acetate-induced phospholipid scramblase 1 gene expression: its role in leukemic cell differentiation. Blood 104:3731–3738.
   PubMed Web of Science ®Google Scholar