Thermodynamic and structural determinants of differential pdx1 binding to elements from the insulin and IAPP promoters

Journal of Molecular Biology

Volumn 425, Issue 18, 2013, Pages 3360-3377

  Bastidas, Monique ^a   Showalter, Scott A ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

A box element; Diabetes; Homeodomain; Isothermal titration calorimetry; Nuclear magnetic resonance

Indexed keywords

AMYLIN; INSULIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PDX 1;

ARTICLE; CRYSTAL STRUCTURE; DNA BINDING; ISOTHERMAL TITRATION CALORIMETRY; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; THERMODYNAMICS;

MAMMALIA;

EID: 84883278371     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.06.011     Document Type: Article

References (61)

1. M. Sander, and M.S. German The β cell transcription factors and development of the pancreas J Mol Med 75 1997 327 340
2. J.C. Hutton, E.J. Penn, and M. Peshavaria Isolation and characterisation of insulin secretory granules from a rat islet cell tumour Diabetologia 23 1982 365 373
3. J. Suckale, and M. Solimena The insulin secretory granule as a signaling hub Trends Endocrinol Metab 21 2010 599 609
4. A. Ogawa, V. Harris, S.K. McCorkle, R.H. Unger, and K.L. Luskey Amylin secretion from the rat pancreas and its selective loss after streptozotocin treatment J Clin Invest 85 1990 973 976
5. P. Westermark, A. Andersson, and G.T. Westermark Islet amyloid polypeptide, islet amyloid, and diabetes mellitus Physiol Rev 91 2011 795 826
6. B. Akesson, G. Panagiotidis, P. Westermark, and I. Lundquist Islet amyloid polypeptide inhibits glucagon release and exerts a dual action on insulin release from isolated islets Regul Pept 111 2003 55 60
7. T.A. Lutz Control of energy homeostasis by amylin Cell Mol Life Sci 69 2012 1947 1965
8. P.A. Rushing, M.M. Hagan, R.J. Seeley, T.A. Lutz, and S.C. Woods Amylin: a novel action in the brain to reduce body weight Endocrinology 141 2000 850 853
9. T.A. Lutz Amylinergic control of food intake Physiol Behav 89 2006 465 471
10. H.J. Woerle, M. Albrecht, R. Linke, S. Zschau, C. Neumann, and M. Nicolaus Impaired hyperglycemia-induced delay in gastric emptying in patients with type 1 diabetes deficient for islet amyloid polypeptide Diabetes Care 31 2008 2325 2331
11. M.S. German, L.G. Moss, J. Wang, and W.J. Rutter The insulin and islet amyloid polypeptide genes contain similar cell-specific promoter elements that bind identical β-cell nuclear complexes Mol Cell Biol 12 1992 1777 1788
12. M. German, S. Ashcroft, K. Docherty, H. Edlund, T. Edlund, and S. Goodison The insulin gene promoter: a simplified nomenclature Diabetes 44 1995 1002 1004
13. A.S. Bernardo, C.W. Hay, and K. Docherty Pancreatic transcription factors and their role in the birth, life and survival of the pancreatic β cell Mol Cell Endocrinol 294 2008 1 9
14. E. Glick, D. Leshkowitz, and M.D. Walker Transcription factor BETA2 acts cooperatively with E2A and PDX1 to activate the insulin gene promoter J Biol Chem 275 2000 2199 2204
15. M.A. Cissell, L. Zhao, L. Sussel, E. Henderson, and R. Stein Transcription factor occupancy of the insulin gene in vivo. Evidence for direct regulation by Nkx2.2 J Biol Chem 278 2003 751 756
16. K. Ohneda, R.G. Mirmira, J. Wang, J.D. Johnson, and M.S. German The homeodomain of PDX-1 mediates multiple protein-protein interactions in the formation of a transcriptional activation complex on the insulin promoter Mol Cell Biol 20 2000 900 911
17. P. Serup, J. Jensen, F.G. Andersen, M.C. Jorgensen, N. Blume, and J.J. Holst Induction of insulin and islet amyloid polypeptide production in pancreatic islet glucagonoma cells by insulin promoter factor 1 Proc Natl Acad Sci USA 93 1996 9015 9020
18. S.K. Chakrabarti, J.C. James, and R.G. Mirmira Quantitative assessment of gene targeting in vitro and in vivo by the pancreatic transcription factor, Pdx1. Importance of chromatin structure in directing promoter binding J Biol Chem 277 2002 13286 13293
19. W.M. Macfarlane, S.C. Campbell, L.J. Elrick, V. Oates, G. Bermano, and K.J. Lindley Glucose regulates islet amyloid polypeptide gene transcription in a PDX1- and calcium-dependent manner J Biol Chem 275 2000 15330 15335
20. C.P. Miller, R.E. McGehee, and J.F. Habener IDX-1: a new homeodomain transcription factor expressed in rat pancreatic islets and duodenum that transactivates the somatostatin gene EMBO J 13 1994 1145 1156
21. A. Liberzon, G. Ridner, and M.D. Walker Role of intrinsic DNA binding specificity in defining target genes of the mammalian transcription factor PDX1 Nucleic Acids Res 32 2004 54 64
22. C.W. Hay, and K. Docherty Comparative analysis of insulin gene promoters: implications for diabetes research Diabetes 55 2006 3201 3213
23. D.A. Babu, T.G. Deering, and R.G. Mirmira A feat of metabolic proportions: Pdx1 orchestrates islet development and function in the maintenance of glucose homeostasis Mol Genet Metab 92 2007 43 55
24. A. Longo, G.P. Guanga, and R.B. Rose Structural basis for induced fit mechanisms in DNA recognition by the Pdx1 homeodomain Biochemistry 46 2007 2948 2957
25. M.S. German, and J. Wang The insulin gene contains multiple transcriptional elements that respond to glucose Mol Cell Biol 14 1994 4067 4075
26. W.M. MacFarlane, M.L. Read, M. Gilligan, I. Bujalska, and K. Docherty Glucose modulates the binding activity of the β-cell transcription factor IUF1 in a phosphorylation-dependent manner Biochem J 303 1994 625 631
27. D.G. Taylor, D. Babu, and R.G. Mirmira The C-terminal domain of the β cell homeodomain factor Nkx6.1 enhances sequence-selective DNA binding at the insulin promoter Biochemistry 44 2005 11269 11278
28. J. Francis, D.A. Babu, T.G. Deering, S.K. Chakrabarti, J.C. Garmey, and C. Evans-Molina Role of chromatin accessibility in the occupancy and transcription of the insulin gene by the pancreatic and duodenal homeobox factor 1 Mol Endocrinol 20 2006 3133 3145
29. S.E. Ades, and R.T. Sauer Specificity of minor-groove and major-groove interactions in a homeodomain-DNA complex Biochemistry 34 1995 14601 14608
30. J.L. Klepeis, K. Lindorff-Larsen, R.O. Dror, and D.E. Shaw Long-timescale molecular dynamics simulations of protein structure and function Curr Opin Struct Biol 19 2009 120 127
31. R.O. Dror, R.M. Dirks, J.P. Grossman, H. Xu, and D.E. Shaw Biomolecular simulation: a computational microscope for molecular biology Annu Rev Biophys 41 2012 429 452
32. D.E. Shaw, M.M. Deneroff, R.O. Dror, J.S. Kuskin, R.H. Larson, and J.K. Salmon Anton, a special-purpose machine for molecular dynamics simulation Commun ACM 51 2008 91 97
33. M. Billeter, Y.Q. Qian, G. Otting, M. Muller, W. Gehring, and K. Wuthrich Determination of the nuclear magnetic resonance solution structure of an Antennapedia homeodomain-DNA complex J Mol Biol 234 1993 1084 1093
34. J.A. Marsh, V.K. Singh, Z. Jia, and J.D. Forman-Kay Sensitivity of secondary structure propensities to sequence differences between α- and γ-synuclein: implications for fibrillation Protein Sci 15 2006 2795 2804
35. A.G. Palmer NMR characterization of the dynamics of biomacromolecules Chem Rev 104 2004 3623 3640
36. V.A. Jarymowycz, and M.J. Stone Fast time scale dynamics of protein backbones: NMR relaxation methods, applications, and functional consequences Chem Rev 106 2006 1624 1671
37. R. Bruschweiler New approaches to the dynamic interpretation and prediction of NMR relaxation data from proteins Curr Opin Struct Biol 13 2003 175 183
38. G. Lipari, and A. Szabo Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity J Am Chem Soc 104 1982 4546 4559
39. J.S. Anderson, M.D. Forman, S. Modleski, F.W. Dahlquist, and S.M. Baxter Cooperative ordering in homeodomain-DNA recognition: solution structure and dynamics of the MATa1 homeodomain Biochemistry 39 2000 10045 10054
40. S. Fausti, S. Weiler, C. Cuniberti, K.J. Hwang, K.T. No, and J.M. Gruschus Backbone dynamics for the wild type and a double H52R/T56W mutant of the vnd/NK-2 homeodomain from Drosophila melanogaster Biochemistry 40 2001 12004 12012
41. T. Doerdelmann, D.J. Kojetin, J.M. Baird-Titus, L.A. Solt, T.P. Burris, and M. Rance Structural and biophysical insights into the ligand-free Pitx2 homeodomain and a ring dermoid of the cornea inducing homeodomain mutant Biochemistry 51 2012 665 676
42. J.J. Prompers, and R. Brüschweiler General framework for studying the dynamics of folded and nonfolded proteins by NMR relaxation spectroscopy and MD simulation J Am Chem Soc 124 2002 4522 4534
43. M.W. Cluck, C.Y. Chan, and T.E. Adrian The regulation of amylin and insulin gene expression and secretion Pancreas 30 2005 1 14
44. M.S. German, M.A. Blanar, C. Nelson, L.G. Moss, and W.J. Rutter Two related helix-loop-helix proteins participate in separate cell-specific complexes that bind the insulin enhancer Mol Endocrinol 5 1991 292 299
45. H. Ohlsson, K. Karlsson, and T. Edlund IPF1, a homeodomain-containing transactivator of the insulin gene EMBO J 12 1993 4251 4259
46. N.J. Buurma, and I. Haq Advances in the analysis of isothermal titration calorimetry data for ligand-DNA interactions Methods 42 2007 162 172
47. D.A. Case, T.E. Cheatham, T. Darden, H. Gohlke, R. Luo, and K.M. Merz The Amber biomolecular simulation programs J Comput Chem 26 2005 1668 1688
48. V. Hornak, R. Abel, A. Okur, B. Strockbine, A. Roitberg, and C. Simmerling Comparison of multiple amber force fields and development of improved protein backbone parameters Proteins Struct Funct Bioinf 65 2006 712 725
49. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J Mol Graphics 14 1996 33 38
50. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, and E.C. Meng UCSF Chimera - a visualization system for exploratory research and analysis J Comput Chem 25 2004 1605 1612
51. S.A. Showalter, and R. Brüschweiler Validation of molecular dynamics simulations of biomolecules using NMR spin relaxation as benchmarks: application to the AMBER99SB force field J Chem Theory Comput 3 2007 961 975
52. 13C′ chemical shifts in proteins using a density functional database J Biomol NMR 21 2001 321 333
53. D.W. Li, and R. Brüschweiler Certification of molecular dynamics trajectories with NMR chemical shifts J Phys Chem Lett 1 2010 246 248
54. N.A. Baker, D. Sept, S. Joseph, M.J. Holst, and J.A. McCammon Electrostatics of nanosystems: application to microtubules and the ribosome Proc Natl Acad Sci USA 98 2001 10037 10041
55. Schrodinger, LLC. (2010). The PyMOL Molecular Graphics System, version 1.3r1.
56. N. Veeraraghavan, A. Ganguly, J.H. Chen, P.C. Bevilacqua, S. Hammes-Schiffer, and B.L. Golden Metal binding motif in the active site of the HDV ribozyme binds divalent and monovalent ions Biochemistry 50 2011 2672 2682
57. V. Kanelis, J.D. Forman-Kay, and L.E. Kay Multidimensional NMR methods for protein structure determination IUBMB Life 52 2001 291 302
58. A.M. Mandel, M. Akke, and A.G. Palmer Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme J Mol Biol 246 1995 144 163
59. R. Brüschweiler, X.B. Liao, and P.E. Wright Long-range motional restrictions in a multidomain zinc-finger protein from anisotropic tumbling Science 268 1995 886 889
60. α nuclear spin relaxation J Biomol NMR 9 1997 287 298
61. C. Wostenberg, K.A. Quarles, and S.A. Showalter Dynamic origins of differential RNA binding function in two dsRBDs from the miRNA "Microprocessor" complex Biochemistry 49 2010 10728 10736