Concurrent binding and modifications of AUF1 and HuR mediate the pH-responsive stabilization of phosphoenolpyruvate carboxykinase mRNA in kidney cells

American Journal of Physiology - Renal Physiology

Volumn 303, Issue 11, 2012, Pages

  Gummadi, Lakshmi ^a   Taylor, Lynn ^a   Curthoys, Norman P ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

2 D gels; Metabolic acidosis; mRNA stabilization; MS2 recruitment; siRNA knockdown

Indexed keywords

COMPLEMENTARY DNA; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN D; HUR PROTEIN; MESSENGER RNA; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); SMALL INTERFERING RNA;

3' UNTRANSLATED REGION; ARTICLE; IN VITRO STUDY; KIDNEY CELL; METABOLIC ACIDOSIS; PH; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TWO DIMENSIONAL GEL ELECTROPHORESIS; WESTERN BLOTTING;

EID: 84870498865     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00400.2012     Document Type: Article

References (52)

1. Abdelmohsen K, Gorospe M. Posttranscriptional regulation of cancer traits by HuR. WIRE RNA 1: 214-229, 2010.
2. Abdelmohsen K, Pullmann R Jr, Lal A, Kim HH, Galban S, Yang X, Blethrow JD, Walker M, Shubert J, Gillespie DA, Furneaux H, Gorospe M. Phosphorylation of HuR by Chk2 regulates SIRT1 expression. Mol Cell 25: 543-557, 2007.
3. Barker A, Epis MR, Porter CJ, Hopkins BR, Wilce MC, Wilce JA, Giles KM, Leedman PJ. Sequence requirements for RNA binding by HuR and AUF1. J Biochem 151: 423-437, 2012.
4. Baron-Benhamou J, Gehring NH, Kulozik AE, Hentze MW. Using the lambdaN peptide to tether proteins to RNAs. Methods Mol Biol 257: 135-154, 2004.
5. Bell O, Gaberman E, Kilav R, Levi R, Cox KB, Molkentin JD, Silver J, Naveh-Many T. The protein phosphatase calcineurin determines basal parathyroid hormone gene expression. Mol Endocrinol 19: 516-526, 2005.
6. Bradford MM. 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, 1976.
7. Brennan CM, Steitz JA. HuR and mRNA stability. Cell Mol Life Sci 58: 266-277, 2001.
8. Burd CG, Dreyfuss G. Conserved structures and diversity of functions of RNA-binding proteins. Science 265: 615-621, 1994.
9. Cok SJ, Acton SJ, Sexton AE, Morrison AR. Identification of RNAbinding proteins in RAW 264.7 cells that recognize a lipopolysaccharideresponsive element in the 3-untranslated region of the murine cyclooxygenase-2 mRNA. J Biol Chem 279: 8196-8205, 2004.
10. Coller J, Wickens M. Tethered function assays using 3' untranslated regions. Methods 26: 142-150, 2002.
11. Curthoys NP. Renal ammonium ion production and excretion. In: The Kidney: Physiology and Pathophysiology, 4th Edition, edited by Alpern RJ and Hebert SC. New York: Elsevier, 2007, p. 1601-1619.
12. Curthoys NP, Gstraunthaler G. Mechanism of increased renal gene expression during metabolic acidosis. Am J Physiol Renal Physiol 281: F381-F390, 2001.
13. Curthoys NP, Taylor L, Hoffert JD, Knepper MA. Proteomic analysis of the adaptive response of rat renal proximal tubules to metabolic acidosis. Am J Physiol Renal Physiol 292: F140-F147, 2007.
14. DeMaria CT, Brewer G. AUF1 binding affinity to A+U-rich elements correlates with rapid mRNA degradation. J Biol Chem 271: 12179-12184, 1996.
15. Doller A, Akool el S, Huwiler A, Muller R, Radeke HH, Pfeilschifter J, Eberhardt W. Posttranslational modification of the AU-rich element binding protein HuR by protein kinase Cdelta elicits angiotensin IIinduced stabilization and nuclear export of cyclooxygenase 2 mRNA. Mol Cell Biol 28: 2608-2625, 2008.
16. Doller A, Huwiler A, Muller R, Radeke HH, Pfeilschifter J, Eberhardt W. Protein kinase C alpha-dependent phosphorylation of the mRNAstabilizing factor HuR: implications for posttranscriptional regulation of cyclooxygenase-2. Mol Biol Cell 18: 2137-2148, 2007.
17. Ehrenman K, Long L, Wagner BJ, Brewer G. Characterization of cDNAs encoding the murine A+U-rich RNA-binding protein AUF1. Gene 149: 315-319, 1994.
18. Fan XC, Steitz JA. HNS, a nuclear-cytoplasmic shuttling sequence in HuR. Proc Natl Acad Sci USA 95: 15293-15298, 1998.
19. Fan XC, Steitz JA. Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J 17: 3448-3460, 1998.
20. + cells. Am J Physiol Renal Physiol 283: F678-F688, 2002.
21. Gallouzi IE, Brennan CM, Stenberg MG, Swanson MS, Eversole A, Maizels N, Steitz JA. HuR binding to cytoplasmic mRNA is perturbed by heat shock. Proc Natl Acad Sci USA 97: 3073-3078, 2000.
22. + cells. Am J Physiol Renal Physiol 278: F227-F237, 2000.
23. Hajarnis S, Schroeder JM, Curthoys NP. 3'-Untranslated region of phosphoenolpyruvate carboxykinase mRNA contains multiple instability elements that bind AUF1. J Biol Chem 280: 28272-28280, 2005.
24. Halperin ML. Metabolic aspects of metabolic acidosis. Clin Invest Med 16: 294-305, 1993.
25. Hwang JJ, Curthoys NP. Effect of acute alterations in acid-base balance on rat renal glutaminase and phosphoenolpyruvate carboxykinase gene expression. J Biol Chem 266: 9392-9396, 1991.
26. Hwang JJ, Perera S, Shapiro RA, Curthoys NP. Mechanism of altered renal glutaminase gene expression in response to chronic acidosis. Biochemistry 30: 7522-7526, 1991.
27. Jeyaraj SC, Dakhlallah D, Hill SR, Lee BS. Expression and distribution of HuR during ATP depletion and recovery in proximal tubule cells. Am J Physiol Renal Physiol 291: F1255-F1263, 2006
28. Keene JD. Why is Hu where? Shuttling of early-response-gene messenger RNA subsets. Proc Natl Acad Sci USA 96: 5-7, 1999.
29. Lafarga V, Cuadrado A, Lopez de Silanes I, Bengoechea R, Fernandez-Capetillo O, Nebreda AR. p38 Mitogen-activated protein kinaseand HuR-dependent stabilization of p21(Cip1) mRNA mediates the G(1)/S checkpoint. Mol Cell Biol 29: 4341-4351, 2009.
30. Lal A, Mazan-Mamczarz K, Kawai T, Yang X, Martindale JL, Gorospe M. Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J 23: 3092-3102, 2004.
31. Laroia G, Schneider RJ. Alternate exon insertion controls selective ubiquitination and degradation of different AUF1 protein isoforms. Nucleic Acids Res 30: 3052-3058, 2002.
32. LeCuyer KA, Behlen LS, Uhlenbeck OC. Mutants of the bacteriophage MS2 coat protein that alter its cooperative binding to RNA. Biochemistry 34: 10600-10606, 1995.
33. Levy NS, Chung S, Furneaux H, Levy AP. Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J Biol Chem 273: 6417-6423, 1998.
34. Lopez de Silanes I, Gorospe M, Taniguchi H, Abdelmohsen K, Srikantan S, Alaminos M, Berdasco M, Urdinguio RG, Fraga MF, Jacinto FV, Esteller M. The RNA-binding protein HuR regulates DNA methylation through stabilization of DNMT3b mRNA. Nucleic Acids Res 37: 2658-2671, 2009.
35. Lopez de Silanes I, Zhan M, Lal A, Yang X, Gorospe M. Identification of a target RNA motif for RNA-binding protein HuR. Proc Natl Acad Sci USA 101: 2987-2992, 2004.
36. Lykke-Andersen J, Shu MD, Steitz JA. Human Upf proteins target an mRNA for nonsense-mediated decay when bound downstream of a termination codon. Cell 103: 1121-1131, 2000.
37. Masuda K, Abdelmohsen K, Kim MM, Srikantan S, Lee EK, Tominaga K, Selimyan R, Martindale JL, Yang X, Lehrmann E, Zhang Y, Becker KG, Wang JY, Kim HH, Gorospe M. Global dissociation of HuR-mRNA complexes promotes cell survival after ionizing radiation. EMBO J 30: 1040-1053, 2011.
38. McMullen MR, Cocuzzi E, Hatzoglou M, Nagy LE. Chronic ethanol exposure increases the binding of HuR to the TNFalpha 3'-untranslated region in macrophages. J Biol Chem 278: 38333-38341, 2003.
39. Mufti J, Hajarnis S, Shepardson K, Gummadi L, Taylor L, Curthoys NP. Role of AUF1 and HuR in the pH-responsive stabilization of phosphoenolpyruvate carboxykinase mRNA in LLC-PK-F cells. Am J Physiol Renal Physiol 301: F1066-F1077, 2011.
40. Hayre M, Taylor L, Andratsch M, Feifel E, Gstraunthaler G, Curthoys NP. Effects of constitutively active and dominant negative MAPK kinase (MKK) 3 and MKK6 on the pH-responsive increase in phosphoenolpyruvate carboxykinase mRNA. J Biol Chem 281: 2982-2988, 2006.
41. Palanisamy V, Park NJ, Wang J, Wong DT. AUF1 and HuR proteins stabilize interleukin-8 mRNA in human saliva. J Dental Res 87: 772-776, 2008.
42. Pont AR, Sadri N, Hsiao SJ, Smith S, Schneider RJ. mRNA decay factor AUF1 maintains normal aging, telomere maintenance, and suppression of senescence by activation of telomerase transcription. Mol Cell 47: 5-15, 2012.
43. Raineri I, Wegmueller D, Gross B, Certa U, Moroni C. Roles of AUF1 isoforms, HuR and BRF1 in ARE-dependent mRNA turnover studied by RNA interference. Nucleic Acids Res 32: 1279-1288, 2004.
44. Schroeder JM, Ibrahim H, Taylor L, Curthoys NP. Role of deadenylation and AUF1 binding in the pH-responsive stabilization of glutaminase mRNA. Am J Physiol Renal Physiol 290: F733-F740, 2006.
45. Stern R. Fluid, electrolytes and acid-base disturbances. NephSAPTM 3: 192-231, 2004.
46. Tannen RL, Sahai A. Biochemical pathways and modulators of renal ammoniagenesis. Miner Electrolyte Metab 16: 249-258, 1990.
47. Wagner BJ, DeMaria CT, Sun Y, Wilson GM, Brewer G. Structure and genomic organization of the human AUF1 gene: alternative pre-mRNA splicing generates four protein isoforms. Genomics 48: 195-202, 1998.
48. Wagner CA. Metabolic acidosis: new insights from mouse models. Curr Opin Nephrol Hypertens 16: 471-476, 2007.
49. Wang W, Furneaux H, Cheng H, Caldwell MC, Hutter D, Liu Y, Holbrook N, Gorospe M. HuR regulates p21 mRNA stabilization by UV light. Mol Cell Biol 20: 760-769, 2000.
50. Wilson GM, Lu J, Sutphen K, Suarez Y, Sinha S, Brewer B, Villanueva-Feliciano EC, Ysla RM, Charles S, Brewer G. Phosphorylation of p40AUF1 regulates binding to A + U-rich mRNA-destabilizing elements and protein-induced changes in ribonucleoprotein structure. J Biol Chem 278: 33039-33048, 2003.
51. Yaman I, Fernandez J, Sarkar B, Schneider RJ, Snider MD, Nagy LE, Hatzoglou M. 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, 2002.
52. Zhang W, Wagner BJ, Ehrenman K, Schaefer AW, DeMaria CT, Crater D, DeHaven K, Long L, Brewer G. Purification, characterization, and cDNA cloning of an AU-rich element RNA-binding protein, AUF1. Mol Cell Biol 13: 7652-7665, 1993.