Role of AUF1 and HuR in the pH-responsive stabilization of phosphoenolpyruvate carboxykinase mRNA in LLC-PK1-F+ cells

American Journal of Physiology - Renal Physiology

Volumn 301, Issue 5, 2011, Pages

  Mufti, Judy ^a   Hajarnis, Sachin ^a   Shepardson, Kelly ^a   Gummadi, Lakshmi ^a   Taylor, Lynn ^a   Curthoys, Norman P ^a  

^a Veterinary Dentistry and Oral Surgery   (United States)

Author keywords

Electrophoretic mobility shift assay; Metabolic acidosis; Proximal tubule; SiRNA knockdown

Indexed keywords

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

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; GEL MOBILITY SHIFT ASSAY; HALF LIFE TIME; KIDNEY PROXIMAL TUBULE; METABOLIC ACIDOSIS; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STABILITY; RAT; WESTERN BLOTTING;

EID: 80055068790     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00303.2011     Document Type: Article

References (44)

1. Abe R, Sakashita E, Yamamoto K, Sakamoto H. Two different RNA binding activities for the AU-rich element and the poly(A) sequence of the mouse neuronal protein mHuC. Nucleic Acids Res 24: 4895-4901, 1996.
2. Beale EG, Chrapkiewicz NB, Scoble HA, Metz RJ, Quick DP, Noble RL, Donelson JE, Biemann K, Granner DK. Rat hepatic cytosolic phosphoenolpyruvate carboxykinase (GTP). Structures of the protein, messenger RNA, and gene. J Biol Chem 260: 10748-10760, 1985.
3. 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.
4. Burd CG, Dreyfuss G. Conserved structures and diversity of functions of RNA-binding proteins. Science 265: 615-621, 1994.
5. Buzby JS, Brewer G, Nugent DJ. Developmental regulation of RNA transcript destabilization by A + U-rich elements is AUF1-dependent. J Biol Chem 274: 33973-33978, 1999.
6. Buzby JS, Lee SM, Van Winkle P, DeMaria CT, Brewer G, Cairo MS. Increased granulocyte-macrophage colony-stimulating factor mRNA instability in cord versus adult mononuclear cells is translation-dependent and associated with increased levels of A + U-rich element binding factor. Blood 88: 2889-2897, 1996.
7. Curthoys NP. Renal ammonium ion production and excretion. In: The Kidney: Physiology and Pathophysiology, 4th Edition, edited by Alpern RJ and Hebert SC. San Diego, CA: Elsevier, 2007, p. 1601-1619.
8. 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.
9. Fan XC, Steitz JA. HNS, a nuclear-cytoplasmic shuttling sequence in HuR. Proc Natl Acad Sci USA 95: 15293-15298, 1998.
10. 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.
11. + cells. Am J Physiol Renal Physiol 283: F678-F688, 2002.
12. 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.
13. Gstraunthaler G, Handler JS. Isolation, growth, and characterization of a gluconeogenic strain of renal cells. Am J Physiol Cell Physiol 252: C232-C238, 1987.
14. Gstraunthaler G, Holcomb T, Feifel E, Liu W, Spitaler N, Curthoys NP. Differential expression and acid-base regulation of glutaminase mRNAs in gluconeogenic LLC-PK1-FBPase_ cells. Am J Physiol Renal Physiol 278: F227-F237, 2000.
15. Gstraunthaler G, Pfaller W, Kotanko P. Lack of fructose-1,6-bisphosphatase activity in LLC-PK1 cells. Am J Physiol Cell Physiol 248: C181-C183, 1985.
16. Gstraunthaler GJ. Epithelial cells in tissue culture. Renal Physiol Biochem 11: 1-42, 1988.
17. 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.
18. Hansen WR, Barsic-Tress N, Taylor L, Curthoys NP. The 3'-nontranslated region of rat renal glutaminase mRNA contains a pH-responsive stability element. Am J Physiol Renal Fluid Electrolyte Physiol 271: F126-F131, 1996.
19. Holcomb T, Curthoys NP, Gstraunthaler G. Supcellular localization of PEPCK and metabolism of gluconeogenic supstrains of renal cell lines. Am J Physiol Cell Physiol 268: C449-C457, 1995.
20. + cells. Am J Physiol Renal Fluid Electrolyte Physiol 271: F340-F346, 1996.
21. 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.
22. 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.
23. +-translocating ATPase mRNA during cellular energy depletion. J Biol Chem 280: 37957-37964, 2005.
24. 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.
25. 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.
26. Laterza OF, Curthoys NP. Specificity and functional analysis of the pH-responsive element within renal glutaminase mRNA. Am J Physiol Renal Physiol 278: F970-F977, 2000.
27. Laterza OF, Hansen WR, Taylor L, Curthoys NP. Identification of an mRNA-binding protein and the specific elements that may mediate the pH-responsive induction of renal glutaminase mRNA. J Biol Chem 272: 22481-22488, 1997.
28. Laterza OF, Taylor L, Unnithan S, Nguyen L, Curthoys NP. Mapping and functional analysis of an instability element in phosphoenolpyruvate carboxykinase mRNA. Am J Physiol Renal Physiol 279: F866-F873, 2000.
29. 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.
30. 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.
31. Ma WJ, Chung S, Furneaux H. The Elav-like proteins bind to AU-rich elements and to the poly(A) tail of mRNA. Nucleic Acids Res 25: 3564-3569, 1997.
32. 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.
33. 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.
34. Nowik M, Lecca MR, Velic A, Rehrauer H, Brandli AW, Wagner CA. Genome-wide gene expression profiling reveals renal genes regulated during metabolic acidosis. Physiol Genomics 32: 322-334, 2008.
35. O'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.
36. Pan YX, Chen H, Kilberg MS. Interaction of RNA-binding proteins HuR and AUF1 with the human ATF3 mRNA 3'-untranslated region regulates its amino acid limitation-induced stabilization. J Biol Chem 280: 34609-34616, 2005.
37. Ray D, Kazan H, Chan ET, Castillo LP, Chaudhry S, Talukder S, Blencowe BJ, Morris Q, Hughes TR. Rapid and systematic analysis of the RNA recognition specificities of RNA-binding proteins. Nat Biotechnol 27: 667-670, 2009.
38. deBoer PA, Moorman AF, Lamers WH. Changes in mRNAs for enzymes of glutamine metabolism in kidney and liver during ammonium chloride acidosis. Am J Physiol Renal Fluid Electrolyte Physiol 267: F400-F406, 1994.
39. 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.
40. + cells. Am J Physiol Renal Physiol 285: F258-F265, 2003.
41. Taylor L, Curthoys NP. Glutamine metabolism: role in acid-base balance. Biochem Molec Biol Ed 32: 291-304, 2004.
42. Tran H, Maurer F, Nagamine Y. Stabilization of urokinase and urokinase receptor mRNAs by HuR is linked to its cytoplasmic accumulation induced by activated mitogen-activated protein kinase-activated protein kinase 2. Mol Cell Biol 23: 7177-7188, 2003.
43. 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.
44. 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.