NMR spectroscopy inside prokaryotic and eukaryotic cells

Advances in Biomedical Spectroscopy

Volumn 3, Issue , 2011, Pages 162-184

  Bertrand, Karl ^a   Burz, David S ^a   Shekhtman, Alexander ^a   Dutta, Kaushi ^b  

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b NEW YORK STRUCTURAL BIOLOGY CENTER   (United States)

Author keywords

In cell NMR; protein structure; protein nucleic acid interactions; protein protein interactions

Indexed keywords

EID: 84865473801     PISSN: 18750656     EISSN: None     Source Type: Book Series    
DOI: 10.3233/978-1-60750-695-9-162     Document Type: Article

References (100)

1. Z. Serber, V. Dotsch, In-cell NMR spectroscopy, Biochemistry 40(2001), 14317-14323.
2. D. S. Waugh, Genetic tools for selective labeling of proteins with alpha-15N-amino acids, J. Biomol. NMR 8(1996), 184-192.
3. L. P. McIntosh, F. W. Dahlquist, Biosynthetic incorporation of 15N and 13C for assignment and interpretation of nuclear magnetic resonance spectra of proteins, Q. Rev. Biophys. 23(1990), 1-38.
4. Z. Serber, W. Straub, L. Corsini, A. M. Nomura, N. Shimba, C. S. Craik, P. Ortiz de Montellano, V. Dotsch, Methyl groups as probes for proteins and complexes in in-cell NMR experiments, J. Am. Chem. Soc. 126(2004), 7119-7125.
5. M. K. Rosen, K. H. Gardner, R. C. Willis, W. E. Parris, T. Pawson, L. E. Kay, Selective methyl protonation of perdeuterated proteins, J. Mol. Biol. 263(1996), 627-636.
6. H. Cheng, W. M. Westler, B. Xie, B. H. Oh, J. L. Markley, Protein expression selective isotopic labeling, and analysis of hyperfine-shifted NMR signals of Anabaena 7120 vegetative [2Fe-2S]ferredoxin, Arch Biochem. Biophys. 316(1995), 619-634.
7. D. S. Burz, K. Dutta, D. Cowburn, A. Shekhtman, Mapping structural interactions using in-cell NMR spectroscopy (STINT-NMR), Nat. Methods 3(2006), 91-93.
8. D. S. Burz, K. Dutta, D. Cowburn, A. Shekhtman, In-cell NMR for protein-protein interactions (STINT-NMR), Nat. Protoc. 1(2006), 146-152.
9. R. Lutz, H. Bujard, Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements, Nucleic Acids Res. 25(1997), 1203-1210.
10. P. P. Di Fiore, S. Polo, K. Hofmann, When ubiquitin meets ubiquitin receptors: a signalling connection, Nat. Rev. Mol. Cell Biol. 4(2003), 491-497.
11. K. G. Bache, C. Raiborg, A. Mehlum, H. Stenmark, STAM and Hrs are subunits of a multivalent ubiquitin-binding complex on early endosomes, J. Biol. Chem. 278(2003), 12513-12521.
12. A. Shekhtman, D. Cowburn, A ubiquitin-interacting motif from Hrs binds to and occludes the ubiquitin surface necessary for polyubiquitination in monoubiquitinated proteins, Biochemical and Biophysical Research Communications 296(2002), 1222-1227.
13. E. Mizuno, K. Kawahata, M. Kato, N. Kitamura, M. Komada, STAM proteins bind ubiquitinated proteins on the early endosome via the VHS domain and ubiquitin-interacting motif, Mol. Biol. Cell 14(2003), 3675-3689.
14. M. Groll, M. Bochtler, H. Brandstetter, T. Clausen, R. Huber, Molecular machines for protein degradation, Chembiochem 6(2005), 222-256.
15. D. Sakakibara, A. Sasaki, T. Ikeya, J. Hamatsu, T. Hanashima, M. Mishima, M. Yoshimasu, N. Hayashi, T. Mikawa, M. Walchli, B. O. Smith, M. Shirakawa, P. Guntert, Y. Ito, Protein structure determination in living cells by in-cell NMR spectroscopy, Nature 458(2009), 102-105.
16. P. Guntert, C. Mumenthaler, K. Wuthrich, Torsion angle dynamics for NMR structure calculation with the new program DYANA, J. Mol. Biol. 273(1997), 283-298.
17. D. J. Livingston, G. N. L. Mar, W. D. Brown, Myoglobin diffusion in bovine heart muscle, Science 220(1983), 71-73.
18. P. Schmieder, A. S. Stern, G Wagner, J. C. Hoch, Improved resolution in triple-resonance spectra by nonlinear sampling in the constant-time domain, J. Biomol. NMR 4(1994), 483-490.
19. D. Rovnyak, D. P. Frueh, M. Sastry, Z. Y. Sun, A. S. Stern, J. C. Hoch, G Wagner, Accelerated acquisition of high resolution triple-resonance spectra using non-uniform sampling and maximum entropy reconstruction, J. Magn. Reson. 170(2004), 15-21.
20. J. C. J. Barna, E. D. Laue, M. R. Mayger, J. Skilling, S. J. P. Worrall, Exponential sampling, an alternative method for sampling in two-dimensional NMR experiments, J. Magn. Reson. 73(1987), 69-77.
21. E. D. Laue, M. R. Mayger, J. Skilling, J. Staunton, Reconstruction of phase sensitive 2D NMR spectra by maximum entropy, J. Magn. Reson. 68(1986), 14-29.
22. D. S. Burz, A. Shekhtman, In-cell biochemistry using NMR spectroscopy, PLoS ONE 3(2008), e2571.
23. S. Polo, S. Sigismund, M. Faretta, M. Guidi, M. R. Capua, G. Bossi, H. Chen, P. De Camilli, P. P. Di Fiore, A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins, Nature 416(2002), 451-455.
24. L. Hicke, H. Riezman, Ubiquitination of a yeast plasma membrane receptor signals its ligandstimulated endocytosis, Cell 84(1996), 277-287.
25. A. Pandey, M. M. Fernandez, H. Steen, B. Blagoev, M. M. Nielsen, S. Roche, M. Mann, H. F. Lodish, Identification of a novel immunoreceptor tyrosine-based activation motif-containing molecule, STAM2, by mass spectrometry and its involvement in growth factor and cytokine receptor signaling pathways, J. Biol. Chem. 275(2000), 38633-38639.
26. I. G Old, S. E. Phillips, P. G Stockley, I. Saint Girons, Regulation of methionine biosynthesis in the Enterobacteriaceae, Prog. Biophys. Mol. Biol. 56(1991), 145-185.
27. J. Gal, A. Szvetnik, R. Schnell, M. Kalman, The metD D-methionine transporter locus of Escherichia coli is an ABC transporter gene cluster, J. Bacteriol. 184(2002), 4930-4932.
28. J. Belfaiza, C. Parsot, A. Martel, C. B. de la Tour, D. Margarita, G. N. Cohen, I. Saint-Girons, Evolution in biosynthetic pathways: two enzymes catalyzing consecutive steps in methionine biosynthesis originate from a common ancestor and possess a similar regulatory region, Proc. Natl. Acad. Sci. U. S. A. 83(1986), 867-871.
29. I. Saint-Girons, J. Belfaiza, Y. Guillou, D. Perrin, N. Guiso, O. Barzu, G. N. Cohen, Interactions of the Escherichia coli methionine repressor with the metF operator and with its corepressor, S-adenosylmethionine, J. Biol. Chem. 261(1986), 10936-10940.
30. R. Shoeman, B. Redfield, T. Coleman, R. C. Greene, A. A. Smith, N Brot, H. Weissbach, Regulation of methionine synthesis in Escherichia coli: Effect of metJ gene product and S-adenosylmethionine on the expression of the metF gene, Proc. Natl. Acad. Sci. U. S. A. 82(1985), 3601-3605.
31. M. R. Emmett, J. R. Johnson, Control of metF gene expression in maxicell preparations of Escherichia coli K-12: reversible action of the metJ protein and effect of vitamin B12, J. Bacteriol. 168(1986), 1491-1494.
32. C. D. Collier, J. R. Johnson, The Escherichia coli K-12 metJ193 allele contains a point mutation which alters the hydrophobic pocket responsible for in vitro binding of S-adenosylmethionine: effects on cell growth and induction of met regulon expression, J. Bacteriol. 172(1990), 3918-3924.
33. A. M. Augustus, P. N. Reardon, L. D. Spicer, MetJ repressor interactions with DNA probed by in-cell NMR, Proc. Natl. Acad. Sci. U. S. A. 106(2009), 5065-5069.
34. I. D. Lawrenson, P. G. Stockley, Kinetic analysis of operator binding by the E. coli methionine repressor highlights the role (s) of electrostatic interactions, FEBS Lett. 564(2004), 136-142.
35. J. Xie, R. Thapa, S. Reverdatto, D. S. Burz, A. Shekhtman, Screening of small molecule interactor library by using in-cell NMR spectroscopy (SMILI-NMR), J. Med. Chem. 52(2009), 3516-3522.
36. M. W. Harding, A. Galat, D. E. Uehling, S. L. Schreiber, A receptor for the immunosuppressant FK506 is a cis-trans peptidyl-prolyl isomerase, Nature 341(1989), 758-760.
37. L. Dudkin, M. B. Dilling, P. J. Cheshire, F. C. Harwood, M. Hollingshead, S. G Arbuck, R. Travis, E. A. Sausville, P. J. Houghton, Biochemical correlates of mTOR inhibition by the rapamycin ester CCI-779 and tumor growth inhibition, Clin. Cancer Res. 7(2001), 1758-1764.
38. P. K Vogt, PI 3-kinase, mTOR, protein synthesis and cancer, Trends Mol. Med. 7(2001), 482-484.
39. D. C. Horwell, W. Howson, G. S. Ratcliffe, D. C. Rees, The design of a dipeptide library for screening at peptide receptor sites, Bioorg. Med. Chem. Lett. 3(1993), 799-702.
40. D. C. Horwell, J. Hughes, J. C. Hunter, M. C. Pritchard, R. S. Richardson, E. Roberts, G. N. Woodruff, Rationally designed " dipeptoid" analogues of CCK alpha-Methyltryptophan derivatives as highly selective and orally active gastrin and CCK-B antagonists with potent anxiolytic properties, J. Med. Chem. 34(1991), 404-414.
41. P. Boden, J. M. Eden, J. Hodgson, D. C. Horwell, J. Hughes, A. T. McKnight, R. A. Lewthwaite, M. C. Pritchard, J. Raphy, K Meecham, G. S. Ratcliffe, N. Suman-Chauhan, G. N. Woodruff, Use of a dipeptide chemical library in the development of non-peptide tachykinin NK3 receptor selective antagonists, J. Med. Chem. 39(1996), 1664-1675.
42. M. A. Ondetti, B. Rubin, D. W. Cushman, Design of specific inhibitors of angiotensin-converting enzyme: new class of orally active antihypertensive agents, Science 196(1977), 441-444.
43. E. R. Olson, D. S. Dunyak, L. M. Jurss, R. A. Poorman, Identification and characterization of dppA, an Escherichia coli gene encoding a periplasmic dipeptide transport protein, J. Bacteriol. 173(1991), 234-244.
44. H. Saito, K Inui, Dipeptide transporters in apical and basolateral membranes of the human intestinal cell line Caco-2, Am. J. Physiol. 265(1993), G289-294.
45. P. Selenko, Z. Serber, B. Gadea, J. Ruderman, G. Wagner, Quantitative NMR analysis of the protein G B1 domain in Xenopus laevis egg extracts and intact oocytes, Proc. Natl. Acad. Sci. U. S. A. 103(2006), 11904-11909.
46. A. M. Gronenborn, D. R. Filpula, N. Z. Essig, A. Achari, M. Whitlow, P. T. Wingfield, G. M. Clore, A novel, highly stable fold of the immunoglobulin binding domain of streptococcal protein G, Science 253(1991), 657-661.
47. K. Schnizler, M. Kuster, C. Methfessel, M. Fejtl, The Roboocyte: Automated cDNA/mRNA injection and subsequent TEVC recording on Xenopus Oocytes in 96-well microtiter plates., Receptors Channels 9(2003), 41-48.
48. K. Inomata, A. Ohno, H. Tochio, S. Isogai, T. Tenno, I. Nakase, T. Takeuchi, S. Futaki, Y. Ito, H. Hiroaki, M. Shirakawa, High-resolution multi-dimensional NMR spectroscopy of proteins in human cells, Nature 458(2009), 106-109.
49. S. Futaki, Oligoarginine vectors for intracellular delivery: design and cellular-uptake mechanisms, Biopolymers 84(2006), 241-249.
50. I. Nakase, T. Takeuchi, G Tanaka, S. Futaki, Methodological and cellular aspects that govern the internalization mechanisms of arginine-rich cell-penetrating peptides, Adv. Drug Deliv. Rev. 60(2008), 598-607.
51. P. A. Wender, W. C. Galliher, E. A. Goun, L. R. Jones, T. H. Pillow, The design of guanidinium-rich transporters and their internalization mechanisms, Adv. Drug Deliv. Rev. 60(2008), 452-472.
52. S. R. Schwarze, A. Ho, A. Vocero-Akbani, S. F. Dowdy, In vivo protein transduction: delivery of a biologically active protein into the mouse, Science 285(1999), 1569-1572.
53. T. Takeuchi, M. Kosuge, A. Tadokoro, Y. Sugiura, M. Nishi, M. Kawata, N. Sakai, S. Matile, S. Futaki, Direct and rapid cytosolic delivery using cell-penetrating peptides mediated by pyrenebutyrate, ACS Chem. Biol. 1(2006), 299-303.
54. L. Hicke, H. L. Schubert, C. P. Hill, Ubiquitin-binding domains, Nat. Rev. Mol. Cell Biol. 6(2005), 610-621.
55. F. Loison, P. Nizard, T. Sourisseau, P. Le Goff, L. Debure, Y. Le Drean, D. Michel, A ubiquitin-based assay for the cytosolic uptake of protein transduction domains, Mol. Ther. 11(2005), 205-214.
56. T. Sakai, H. Tochio, T. Tenno, Y. Ito, T. Kokubo, H. Hiroaki, M. Shirakawa, In-cell NMR spectroscopy of proteins inside Xenopus laevis oocytes, J. Biomol. NMR 36(2006), 179-188.
57. I. Giriat, T. W. Muir, Protein semi-synthesis in living cells, J. Am. Chem. Soc. 125(2003), 7180-7181.
58. T. Tenno, K. Fujiwara, H. Tochio, K. Iwai, E. H. Morita, H. Hayashi, S. Murata, H. Hiroaki, M. Sato, K. Tanaka, M. Shirakawa, Structural basis for distinct roles of Lys63-and Lys48-linked polyubiquitin chains, Genes Cells 9(2004), 865-875.
59. S. C. Johnston, S. M. Riddle, R. E. Cohen, C. P. Hill, Structural basis for the specificity of ubiquitin C-terminal hydrolases, EMBO J. 18(1999), 3877-3887.
60. M. Zhang, T. Yuan, Molecular mechanisms of calmodulin's functional versatility., Biochem. Cell. Biol. 76(1998), 313-323.
61. J. F. Bodart, J. M. Wieruszeski, L. Amniai, A. Leroy, I. Landrieu, A. Rousseau-Lescuyer, J. P. Vilain, G Lippens, NMR observation of Tau in Xenopus oocytes, J. Magn. Reson. 192(2008), 252-257.
62. D. L. Gard, M. W. Kirschner, Microtubule assembly in cytoplasmic extracts of Xenopus oocytes and eggs, J. Cell Biol. 105(1987), 2191-2201.
63. G Lippens, J. M. Wieruszeski, A. Leroy, C. Smet, A. Sillen, L. Buee, I. Landrieu, Proline-directed random-coil chemical shift values as a tool for the NMR assignment of the tau phosphorylation sites, Chembiochem 5(2004), 73-78.
64. C. Smet, A. Leroy, A. Sillen, J. M. Wieruszeski, I. Landrieu, G Lippens, Accepting its random coil nature allows a partial NMR assignment of the neuronal Tau protein, Chembiochem 5(2004), 1639-1646.
65. A. Sillen, P. Barbier, I. Landrieu, S. Lefebvre, J. M. Wieruszeski, A. Leroy, V. Peyrot, G Lippens, NMR investigation of the interaction between the neuronal protein tau and the microtubules, Biochemistry 46(2007), 3055-3064.
66. H. P. Richter, C. Hoock, B. Neumcke, Morphological and electrophysiological properties of centrifuged stratified Xenopus oocytes, Biol. Cell 84(1995), 129-138.
67. P. Delobel, S. Flament, M. Hamdane, A. Delacourte, J. P. Vilain, L. Buee, Modelling Alzheimerspecific abnormal Tau phosphorylation independently of GSK3beta and PKA kinase activities, FEBS Lett. 516(2002), 151-155.
68. I. Landrieu, L. Lacosse, A. Leroy, J. M. Wieruszeski, X. Trivelli, A. Sillen, N. Sibille, H. Schwalbe, K. Saxena, T. Langer, G Lippens, NMR analysis of a Tau phosphorylation pattern, J. Am. Chem. Soc. 128(2006), 3575-3583.
69. M. Sarkissian, R. Mendez, J. D. Richter, Progesterone and insulin stimulation of CPEB-dependent polyadenylation is regulated by Aurora A and glycogen synthase kinase-3, Genes Dev. 18(2004), 48-61.
70. P. Selenko, D. P. Frueh, S. J. Elsaesser, W. Haas, S. P. Gygi, G. Wagner, In situ observation of protein phosphorylation by high-resolution NMR spectroscopy, Nat. Struct. Mol. Biol. 15(2008), 321-329.
71. P. Zhou, A. A. Lugovsky, A solubility-enhancement tag (SET) fir NMR studies of poorly behaving proteins, J. Biomol. NMR 20(2001), 11-14.
72. S. Hubner, C. Y. Xiao, D. A. Jans, The protein kinase CK2 site (Ser111/112) enhances recognition of the simian virus 40 large T-antigen nuclear localization sequence by importin, J. Biol. Chem. 272(1997), 17191-17195.
73. H. P. Rihs, D. A. Jans, H. Fan, R. Peters, The rate of nuclear cytoplasmic protein transport is determined by the casein kinase II site flanking the nuclear localization sequence of the SV40 T-antigen, EMBO J. 10(1991), 633-639.
74. E. A. Bienkiewicz, K. J. Lumb, Random-coil chemical shifts of phosphorylated amino acids, J. Biomol. NMR 15(1999), 203-206.
75. A. W. Murray, Cell cycle extracts, Methods Cell. Biol. 36(1991), 581-605.
76. V. Wilhelm, P. Rojas, M. Gatica, C. C. Allende, J. E. Allende, Expression of the subunits of protein kinase CK2 during oogenesis in Xenopus laevis, Eur. J. Biochem. 232(1995), 671-676.
77. R. Hansel, S. Foldynova-Trantirkova, F. Lohr, J. Buck, E. Bongartz, E. Bamberg, H. Schwalbe, V. Dotsch, L. Trantirek, Evaluation of parameters critical for observing nucleic acids inside living Xenopus laevis oocytes by in-cell NMR spectroscopy, J. Am. Chem. Soc. 131(2009), 15761-15768.
78. E. Duchardt, H. Schwalbe, Residue specific ribose and nucleobase dynamics of the cUUCGg RNA tetraloop motif by MNMR 13C relaxation., J. Biomol. NMR 32(2005), 295-308.
79. J. Ferner, A. Villa, E. Duchardt, E. Widjajakusuma, J. Wohnert, G Stock, H. Schwalbe, NMR and MD studies of the temperature-dependent dynamics of RNA YNMG-tetraloops, Nucleic Acids Res. 36(2008), 1928-1940.
80. V. L. Makarov, Y. Hirose, J. P. Langmore, Long G tails at both ends of human chromosomes suggest a C strand degradation mechanism for telomere shortening, Cell 88(1997), 657-666.
81. A. M. Zahler, J. R. Williamson, T. R. Cech, D. M. Prescott, Inhibition of telomerase by G-quartet DNA structures, Nature 350(1991), 718-720.
82. Y. Qin, L. H. Hurley, Structures, folding patterns, and functions of intramolecular DNA G-quadruplexes found in eukaryotic promoter regions, Biochimie 90(2008), 1149-1171.
83. J. Dai, M. Carver, D. Yang, Polymorphism of human telomeric quadruplex structures, Biochimie 90(2008), 1172-1183.
84. M. Inoue, D. Miyoshi, N. Sugimoto, Structural switch of telomere DNA by pH and monovalent cation, Nucleic Acids Symp. Ser. (Oxf) (2005), 243-244.
85. J. Kypr, I. Kejnovska, D. Renciuk, M. Vorlickova, Circular dichroism and conformational polymorphism of DNA, Nucleic Acids Res. 37(2009), 1713-1725.
86. D. Miyoshi, S. Matsumura, W. Li, N. Sugimoto, Structural polymorphism of telomeric DNA regulated by pH and divalent cation, Nucleos. Nucleot. Nucl. 22(2003), 203-221.
87. D. Miyoshi, A. Nakao, N. Sugimoto, Structural transition of d (G4T4G4) from antiparallel to parallel G-quartet induced by divalent cations, Nucleic Acids Res. Suppl. (2001), 259-260.
88. D. Miyoshi, A. Nakao, N. Sugimoto, Molecular crowding regulates the structural switch of the DNA G-quadruplex, Biochemistry 41(2002), 15017-15024.
89. D. Miyoshi, A. Nakao, N. Sugimoto, Structural transition from antiparallel to parallel G-quadruplex of d (G4T4G4) induced by Ca2+, Nucleic Acids Res. 31(2003), 1156-1163.
90. B. Gatto, M. Palumbo, C. Sissi, Nucleic acid aptamers based on the G-quadruplex structure: therapeutic and diagnostic potential, Curr. Med. Chem. 16(2009), 1248-1265.
91. J. L. Huppert, Four-stranded nucleic acids: structure, function and targeting of G-quadruplexes, Chem. Soc. Rev. 37(2008), 1375-1384.
92. J. L. Huppert, Hunting G-quadruplexes, Biochimie 90(2008), 1140-1148.
93. J. L. Huppert, S. Balasubramanian, Prevalence of quadruplexes in the human genome, Nucleic Acids Res. 33(2005), 2908-2916.
94. J. L. Huppert, S. Balasubramanian, G-quadruplexes in promoters throughout the human genome, Nucleic Acids Res. 35(2007), 406-413.
95. H. J. Lipps, D. Rhodes, G-quadruplex structures: in vivo evidence and function, Trends Cell Biol. 19(2009), 414-422.
96. S. Neidle, G. N. Parkinson, Quadruplex DNA crystal structures and drug design, Biochimie 90(2008), 1184-1196.
97. T. M. Ou, Y. J. Lu, J. H. Tan, Z. S. Huang, K. Y. Wong, L. Q. Gu, G-quadruplexes: targets in anticancer drug design, ChemMedChem 3(2008), 690-713.
98. A. T. Phan, V. Kuryavyi, D. J. Patel, DNA architecture: from G to Z, Curr. Opin. Struct. Biol. 16(2006), 288-298.
99. H. M. Wong, L. Payet, J. L. Huppert, Function and targeting of G-quadruplexes, Curr. Opin. Mol. Ther. 11(2009), 146-155.
100. K. W. Lim, S. Amrane, S. Bouaziz, W. Xu, Y. Mu, D. J. Patel, K. N. Luu, A. T. Phan, Structure of the human telomere in K+ solution: a stable basket-type G-quadruplex with only two G-tetrad layers, J. Am. Chem. Soc. 131(2009), 4301-4309.