Metabolic Enzymes Enjoying New Partnerships as RNA-Binding Proteins

Trends in Endocrinology and Metabolism

Volumn 26, Issue 12, 2015, Pages 746-757

  Castello, Alfredo ^a   Hentze, Matthias W ^b   Preiss, Thomas ^c,d  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c Australian National University   (Australia)

^d VICTOR CHANG CARDIAC RESEARCH INSTITUTE   (Australia)

Author keywords

Metabolic enzymes; Metabolon; Post transcriptional regulation; Post translational modifications; RNA; RNA binding proteins

Indexed keywords

ACONITATE HYDRATASE; ENZYME; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; IRON REGULATORY PROTEIN 1; METABOLIC ENZYME; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ENZYME ACTIVITY; ENZYME REGULATION; GENE CONTROL; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; REVIEW; RNA BINDING; GENE EXPRESSION REGULATION; METABOLISM;

ENZYMES; GENE EXPRESSION REGULATION; HUMANS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA-BINDING PROTEINS;

EID: 84949547310     PISSN: 10432760     EISSN: 18793061     Source Type: Journal    
DOI: 10.1016/j.tem.2015.09.012     Document Type: Review

References (89)

1. Hong S.H., et al. Nuclear receptors and metabolism: from feast to famine. Diabetologia 2014, 57:860-867.
2. Zhao X., et al. Nuclear receptors rock around the clock. EMBO Rep. 2014, 15:518-528.
3. Privalsky M.L. The role of corepressors in transcriptional regulation by nuclear hormone receptors. Annu. Rev. Physiol. 2004, 66:315-360.
4. Liu Y., et al. Reduction of hepatic glucocorticoid receptor and hexose-6-phosphate dehydrogenase expression ameliorates diet-induced obesity and insulin resistance in mice. J. Mol. Endocrinol. 2008, 41:53-64.
5. Laffitte B.A., et al. Activation of liver X receptor improves glucose tolerance through coordinate regulation of glucose metabolism in liver and adipose tissue. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:5419-5424.
6. Renga B., et al. Glucocorticoid receptor mediates the gluconeogenic activity of the farnesoid X receptor in the fasting condition. FASEB J. 2012, 26:3021-3031.
7. Zhang Y., et al. Activation of the nuclear receptor FXR improves hyperglycemia and hyperlipidemia in diabetic mice. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:1006-1011.
8. Grefhorst A., et al. Stimulation of lipogenesis by pharmacological activation of the liver X receptor leads to production of large, triglyceride-rich very low density lipoprotein particles. J. Biol. Chem. 2002, 277:34182-34190.
9. Mangelsdorf D.J., et al. The nuclear receptor superfamily: the second decade. Cell 1995, 83:835-839.
10. Yang X., et al. Nuclear receptor expression links the circadian clock to metabolism. Cell 2006, 126:801-810.
11. Schwanhausser B., et al. Global quantification of mammalian gene expression control. Nature 2011, 473:337-342.
12. Ciesla J. Metabolic enzymes that bind RNA: yet another level of cellular regulatory network?. Acta Biochim. Pol. 2006, 53:11-32.
13. Chu E., et al. Autoregulation of human thymidylate synthase messenger RNA translation by thymidylate synthase. Proc. Natl. Acad. Sci. U.S.A. 1991, 88:8977-8981.
14. Chu E., et al. Regulation of thymidylate synthase in human colon cancer cells treated with 5-fluorouracil and interferon-gamma. Mol. Pharmacol. 1993, 43:527-533.
15. Chu E., et al. Identification of a thymidylate synthase ribonucleoprotein complex in human colon cancer cells. Mol. Cell. Biol. 1994, 14:207-213.
16. Hentze M.W. Enzymes as RNA-binding proteins: a role for (di)nucleotide-binding domains?. Trends Biochem. Sci. 1994, 19:101-103.
17. Hentze M.W., Preiss T. The REM phase of gene regulation. Trends Biochem. Sci. 2010, 35:423-426.
18. Chu E., et al. Identification of an RNA binding site for human thymidylate synthase. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:517-521.
19. +-binding fold of glyceraldehyde-3-phosphate dehydrogenase as a novel RNA-binding domain. Biochem. Biophys. Res. Commun. 2000, 275:253-260.
20. +-binding region (Rossmann fold). J. Biol. Chem. 1995, 270:2755-2763.
21. Walden W.E., et al. Structure of dual function iron regulatory protein 1 complexed with ferritin IRE-RNA. Science 2006, 314:1903-1908.
22. Zhang Y., et al. Interaction between thymidylate synthase and its cognate mRNA in zebrafish embryos. PLoS ONE 2010, 5:e10618.
23. Galy B., et al. Iron regulatory proteins are essential for intestinal function and control key iron absorption molecules in the duodenum. Cell Metab. 2008, 7:79-85.
24. Galy B., et al. Iron homeostasis in the brain: complete iron regulatory protein 2 deficiency without symptomatic neurodegeneration in the mouse. Nat. Genet. 2006, 38:967-969. discussion 969-970.
25. Chang C.H., et al. Posttranscriptional control of T cell effector function by aerobic glycolysis. Cell 2013, 153:1239-1251.
26. Scherrer T., et al. A screen for RNA-binding proteins in yeast indicates dual functions for many enzymes. PLoS ONE 2010, 5:e15499.
27. Tsvetanova N.G., et al. Proteome-wide search reveals unexpected RNA-binding proteins in Saccharomyces cerevisiae. PLoS ONE 2010, 5:e12671.
28. Baltz A.G., et al. The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts. Mol. Cell 2012, 46:674-690.
29. Castello A., et al. Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell 2012, 149:1393-1406.
30. Castello A., et al. System-wide identification of RNA-binding proteins by interactome capture. Nat. Protoc. 2013, 8:491-500.
31. Kwon S.C., et al. The RNA-binding protein repertoire of embryonic stem cells. Nat. Struct. Mol. Biol. 2013, 20:1122-1130.
32. Ait-Bara S., Carpousis A.J. RNA degradosomes in bacteria and chloroplasts: classification, distribution and evolution of RNase E homologs. Mol. Microbiol. 2015, 97:1021-1035.
33. McLean J.E., et al. Inosine 5'-monophosphate dehydrogenase binds nucleic acids in vitro and in vivo. Biochem. J. 2004, 379:243-251.
34. Hedstrom L. IMP dehydrogenase-linked retinitis pigmentosa. Nucleosides Nucleotides Nucleic Acids 2008, 27:839-849.
35. Busskamp V., et al. Genetic reactivation of cone photoreceptors restores visual responses in retinitis pigmentosa. Science 2010, 329:413-417.
36. Mortimer S.E., Hedstrom L. Autosomal dominant retinitis pigmentosa mutations in inosine 5'-monophosphate dehydrogenase type I disrupt nucleic acid binding. Biochem. J. 2005, 390:41-47.
37. McGrew D.A., Hedstrom L. Towards a pathological mechanism for IMPDH1-linked retinitis pigmentosa. Adv. Exp. Med. Biol. 2012, 723:539-545.
38. Castello A., et al. RNA-binding proteins in Mendelian disease. Trends Genet. 2013, 29:318-327.
39. Holzmann J., et al. RNase P without RNA: identification and functional reconstitution of the human mitochondrial tRNA processing enzyme. Cell 2008, 135:462-474.
40. Rauschenberger K., et al. A non-enzymatic function of 17beta-hydroxysteroid dehydrogenase type 10 is required for mitochondrial integrity and cell survival. EMBO Mol. Med. 2010, 2:51-62.
41. Deutschmann A.J., et al. Mutation or knock-down of 17beta-hydroxysteroid dehydrogenase type 10 cause loss of MRPP1 and impaired processing of mitochondrial heavy strand transcripts. Hum. Mol. Genet. 2014, 23:3618-3628.
42. Constable A., et al. Modulation of the RNA-binding activity of a regulatory protein by iron in vitro: switching between enzymatic and genetic function?. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:4554-4558.
43. Hentze M.W., Argos P. Homology between IRE-BP, a regulatory RNA-binding protein, aconitase, and isopropylmalate isomerase. Nucleic Acids Res. 1991, 19:1739-1740.
44. Kennedy M.C., et al. Purification and characterization of cytosolic aconitase from beef liver and its relationship to the iron-responsive element binding protein. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:11730-11734.
45. Rouault T.A., et al. Structural relationship between an iron-regulated RNA-binding protein (IRE-BP) and aconitase: functional implications. Cell 1991, 64:881-883.
46. Hentze M.W., et al. Identification of the iron-responsive element for the translational regulation of human ferritin mRNA. Science 1987, 238:1570-1573.
47. Casey J.L., et al. Iron-responsive elements: regulatory RNA sequences that control mRNA levels and translation. Science 1988, 240:924-928.
48. Mullner E.W., Kuhn L.C. A stem-loop in the 3' untranslated region mediates iron-dependent regulation of transferrin receptor mRNA stability in the cytoplasm. Cell 1988, 53:815-825.
49. Leibold E.A., Munro H.N. Cytoplasmic protein binds in vitro to a highly conserved sequence in the 5' untranslated region of ferritin heavy- and light-subunit mRNAs. Proc. Natl. Acad. Sci. U.S.A. 1988, 85:2171-2175.
50. Rouault T.A., et al. Binding of a cytosolic protein to the iron-responsive element of human ferritin messenger RNA. Science 1988, 241:1207-1210.
51. Rouault T.A., et al. Cloning of the cDNA encoding an RNA regulatory protein - the human iron-responsive element-binding protein. Proc. Natl. Acad. Sci. U.S.A. 1990, 87:7958-7962.
52. Guo B., et al. Iron regulates cytoplasmic levels of a novel iron-responsive element-binding protein without aconitase activity. J. Biol. Chem. 1994, 269:24252-24260.
53. Samaniego F., et al. Molecular characterization of a second iron-responsive element binding protein, iron regulatory protein 2. Structure, function, and post-translational regulation. J. Biol. Chem. 1994, 269:30904-30910.
54. Hentze M.W., et al. Two to tango: regulation of Mammalian iron metabolism. Cell 2010, 142:24-38.
55. Anderson C.P., et al. Mammalian iron metabolism and its control by iron regulatory proteins. Biochim. Biophys. Acta 2012, 1823:1468-1483.
56. Wilkinson N., Pantopoulos K. The IRP/IRE system in vivo: insights from mouse models. Front. Pharmacol. 2014, 5:176.
57. Zhang D.L., et al. The physiological functions of iron regulatory proteins in iron homeostasis - an update. Front. Pharmacol. 2014, 5:124.
58. Luscieti S., et al. Novel mutations in the ferritin-L iron-responsive element that only mildly impair IRP binding cause hereditary hyperferritinaemia cataract syndrome. Orphanet J. Rare Dis. 2013, 8:30.
59. Meyron-Holtz E.G., et al. Genetic ablations of iron regulatory proteins 1 and 2 reveal why iron regulatory protein 2 dominates iron homeostasis. EMBO J. 2004, 23:386-395.
60. Tristan C., et al. The diverse functions of GAPDH: views from different subcellular compartments. Cell Signal. 2011, 23:317-323.
61. Mukhopadhyay R., et al. The GAIT system: a gatekeeper of inflammatory gene expression. Trends Biochem. Sci. 2009, 34:324-331.
62. Dollenmaier G., Weitz M. Interaction of glyceraldehyde-3-phosphate dehydrogenase with secondary and tertiary RNA structural elements of the hepatitis A virus 3' translated and non-translated regions. J. Gen. Virol. 2003, 84:403-414.
63. Ryazanov A.G. Glyceraldehyde-3-phosphate dehydrogenase is one of the three major RNA-binding proteins of rabbit reticulocytes. FEBS Lett. 1985, 192:131-134.
64. Singh R., Green M.R. Sequence-specific binding of transfer RNA by glyceraldehyde-3-phosphate dehydrogenase. Science 1993, 259:365-368.
65. Rodriguez-Pascual F., et al. Glyceraldehyde-3-phosphate dehydrogenase regulates endothelin-1 expression by a novel, redox-sensitive mechanism involving mRNA stability. Mol. Cell. Biol. 2008, 28:7139-7155.
66. Zhou Y., et al. The multifunctional protein glyceraldehyde-3-phosphate dehydrogenase is both regulated and controls colony-stimulating factor-1 messenger RNA stability in ovarian cancer. Mol. Cancer Res. 2008, 6:1375-1384.
67. Bonafe N., et al. Glyceraldehyde-3-phosphate dehydrogenase binds to the AU-Rich 3' untranslated region of colony-stimulating factor-1 (CSF-1) messenger RNA in human ovarian cancer cells: possible role in CSF-1 posttranscriptional regulation and tumor phenotype. Cancer Res. 2005, 65:3762-3771.
68. Perucho M., et al. Identification of the mammalian DNA-binding protein P8 as glyceraldehyde-3-phosphate dehydrogenase. Eur. J. Biochem. 1977, 81:557-562.
69. Ryazanov A.G., et al. Association of glyceraldehyde-3-phosphate dehydrogenase with mono- and polyribosomes of rabbit reticulocytes. Eur. J. Biochem. 1988, 171:301-305.
70. Devalaraja-Narashimha K., Padanilam B.J. PARP-1 inhibits glycolysis in ischemic kidneys. J. Am. Soc. Nephrol. 2009, 20:95-103.
71. Du X., et al. Inhibition of GAPDH activity by poly(ADP-ribose) polymerase activates three major pathways of hyperglycemic damage in endothelial cells. J. Clin. Invest. 2003, 112:1049-1057.
72. Ralser M., et al. Dynamic rerouting of the carbohydrate flux is key to counteracting oxidative stress. J. Biol. 2007, 6:10.
73. Ravichandran V., et al. S-Thiolation of glyceraldehyde-3-phosphate dehydrogenase induced by the phagocytosis-associated respiratory burst in blood monocytes. J. Biol. Chem. 1994, 269:25010-25015.
74. Kondo S., et al. Binding of glyceraldehyde-3-phosphate dehydrogenase to the cis-acting element of structure-anchored repression in ccn2 mRNA. Biochem. Biophys. Res. Commun. 2011, 405:382-387.
75. Robinson J.B., Srere P.A. Organization of Krebs tricarboxylic acid cycle enzymes in mitochondria. J. Biol. Chem. 1985, 260:10800-10805.
76. Robinson J.B., et al. Further characterization of the Krebs tricarboxylic acid cycle metabolon. J. Biol. Chem. 1987, 262:1786-1790.
77. Ovadi J., Srere P.A. Macromolecular compartmentation and channeling. Int. Rev. Cytol. 2000, 192:255-280.
78. Mazurek S., et al. Studies on associations of glycolytic and glutaminolytic enzymes in MCF-7 cells: role of P36. J. Cell. Physiol. 1996, 167:238-250.
79. Wu F., Minteer S. Krebs cycle metabolon: structural evidence of substrate channeling revealed by cross-linking and mass spectrometry. Angew. Chem. Int. Ed. Engl. 2015, 54:1851-1854.
80. An S., et al. Reversible compartmentalization of de novo purine biosynthetic complexes in living cells. Science 2008, 320:103-106.
81. Delebecque C.J., et al. Organization of intracellular reactions with rationally designed RNA assemblies. Science 2011, 333:470-474.
82. Clingman C.C., et al. Allosteric inhibition of a stem cell RNA-binding protein by an intermediary metabolite. Elife 2014, 3:e02848.
83. Xing S., Poirier Y. The protein acetylome and the regulation of metabolism. Trends Plant Sci. 2012, 17:423-430.
84. Dabo S., Meurs E.F. dsRNA-dependent protein kinase PKR and its role in stress, signaling and HCV infection. Viruses 2012, 4:2598-2635.
85. Balachandran S., Barber G.N. PKR in innate immunity, cancer, and viral oncolysis. Methods Mol. Biol. 2007, 383:277-301.
86. Donnelly N., et al. The eIF2alpha kinases: their structures and functions. Cell. Mol. Life Sci. 2013, 70:3493-3511.
87. Szabo A., Rajnavolgyi E. Collaboration of Toll-like and RIG-I-like receptors in human dendritic cells: tRIGgering antiviral innate immune responses. Am. J. Clin. Exp. Immunol. 2013, 2:195-207.
88. Habjan M., Pichlmair A. Cytoplasmic sensing of viral nucleic acids. Curr. Opin. Virol. 2015, 11:31-37.
89. Rigby R.E., Rehwinkel J. RNA degradation in antiviral immunity and autoimmunity. Trends Immunol. 2015, 36:179-188.