MR imaging of protein folding in vitro employing Nuclear-Overhauser-mediated saturation transfer

NMR in Biomedicine

Volumn 26, Issue 12, 2013, Pages 1815-1822

  Zaiss, Moritz ^a   Kunz, Patrick ^a   Goerke, Steffen ^a   Radbruch, Alexander ^a,b   Bachert, Peter ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Bovine serum albumin (BSA); Brain tumors; Cancer; Chemical exchange saturation transfer (CEST); MRI; Nuclear Overhauser effect (NOE); Protein folding

Indexed keywords

BOVINE SERUM ALBUMINS; BRAIN TUMORS; CANCER; CHEMICAL EXCHANGE SATURATION TRANSFER; NUCLEAR OVERHAUSER EFFECTS;

BODY FLUIDS; CHEMICAL COMPOUNDS; FLUORESCENCE SPECTROSCOPY; MAGNETIC RESONANCE IMAGING; MAMMALS; NUCLEAR MAGNETIC RESONANCE; PROTEIN FOLDING; PROTONS; SPIN-LATTICE RELAXATION; TUMORS;

PROTEINS;

BOVINE SERUM ALBUMIN; PROTON; WATER;

ARTICLE; BRAIN TUMOR; DIPOLE; FLUORESCENCE SPECTROSCOPY; HUMAN; METABOLITE; MICROENVIRONMENT; MOLECULE; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PH; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTEIN TRANSPORT; PROTEIN UNFOLDING; SIGNAL TRANSDUCTION; TEMPERATURE;

BOVINAE;

BOVINE SERUM ALBUMIN (BSA); BRAIN TUMORS; CANCER; CHEMICAL EXCHANGE SATURATION TRANSFER (CEST); MRI; NUCLEAR OVERHAUSER EFFECT (NOE); PROTEIN FOLDING;

ADULT; ANIMALS; BRAIN NEOPLASMS; CATTLE; FEMALE; FLUORESCENCE; HUMANS; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MIDDLE AGED; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN UNFOLDING; SERUM ALBUMIN, BOVINE; UREA;

EID: 84888021983     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.3021     Document Type: Article

References (52)

1. Hartl FU, Hayer-Hartl M. Converging concepts of protein folding in vitro and in vivo. Nat. Struct. Mol. Biol. 2009; 16: 574-581.
2. Fersht AR. From the first protein structures to our current knowledge of protein folding: delights and scepticisms. Nat. Rev. Mol. Cell Biol. 2008; 9: 650-654.
3. Dill KA, Ozkan SB, Shell MS, Weikl TR. The protein folding problem. Annu. Rev. Biophys. 2008; 37: 289-316.
4. Balch WE, Morimoto RI, Dillin A, Kelly JW. Adapting proteostasis for disease intervention. Science 2008; 319: 916-919.
5. Gregersen N, Bross P, Vang S, Christensen JH. Protein misfolding and human disease. Annu. Rev. Genom. Hum. Genet. 2006; 7: 103-124.
6. Dai C, Whitesell L, Rogers AB, Lindquist S. Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell 2007; 130: 1005-1018.
7. Wüthrich K. NMR of Proteins and Nucleic Acids, Vol. 292. John Wiley & Sons: New York; 1986.
8. Ling W, Regatte RR, Navon G, Jerschow A. Assessment of glycosaminoglycan concentration in vivo by chemical exchange-dependent saturation transfer (gagCEST). Proc. Natl. Acad. Sci. U. S. A. 2008; 105: 2266-2270.
9. Jones CK, Polders D, Hua J, Zhu H, Hoogduin HJ, Zhou J, Luijten P, van Zijl PCM. In vivo three-dimensional whole-brain pulsed steady-state chemical exchange saturation transfer at 7 T. Magn. Reson. Med. 2012; 67: 1579-1589.
10. Jones C, Huang A, van Zijl P. Exchange-relayed nuclear Overhauser effect MRI. Proceedings of the 19th ISMRM Annual Meeting, Montreal, QC, Canada, 2011; 2735.
11. Jin T, Wang P, Zong X, Kim S-G. MR imaging of the amide-proton transfer effect and the pH-insensitive nuclear Overhauser effect at 9.4 T. Magn. Reson. Med. 2013; 69: 760-770.
12. Liu D, Zhou J, Xue R, Zuo Z, An J, Wang DJJ. Quantitative characterization of nuclear Overhauser enhancement and amide proton transfer effects in the human brain at 7 tesla. Magn. Reson. Med. 2012; Epub, ahead of print.
13. Jones CK, Huang A, Xu J, Edden RAE, Schär M, Hua J, Oskolkov N, Zacà D, Zhou J, McMahon MT, Pillai JJ, van Zijl PCM. Nuclear Overhauser enhancement (NOE) imaging in the human brain at 7 T. Neuroimage 2013; 77: 114-124.
14. Zhou J, Payen J-F, Wilson DA, Traystman RJ, van Zijl PCM. Using the amide proton signals of intracellular proteins and peptides to detect pH effects in MRI. Nat. Med. 2003; 9: 1085-1090.
15. Zhou J, van Zijl PCM. Chemical exchange saturation transfer imaging and spectroscopy. Prog. Nucl. Magn. Reson. Spectrosc. 2006; 48: 109-136.
16. Van Zijl PCM, Yadav NN. Chemical exchange saturation transfer (CEST): what is in a name and what isn't? Magn. Reson. Med. 2011; 65: 927-948.
17. Vinogradov E, Sherry AD, Lenkinski RE. CEST: from basic principles to applications, challenges and opportunities. J. Magn. Reson. 2013; 229: 155-172.
18. Liu G, Song X, Chan KWY, McMahon MT. Nuts and bolts of chemical exchange saturation transfer MRI. NMR Biomed. 2013. doi: 10.1002/nbm.2899
19. Otting G, Liepinsh E. Protein hydration viewed by high-resolution NMR spectroscopy: implications for magnetic resonance image contrast. Acc. Chem. Res. 1995; 28: 171-177.
20. Mori S, Berg JM, van Zijl PC. Separation of intramolecular NOE and exchange peaks in water exchange spectroscopy using spin-echo filters. J. Biomol. NMR 1996; 7: 77-82.
21. Hwang T-L, Mori S, Shaka AJ, van Zijl PCM. Application of phase-modulated CLEAN chemical EXchange spectroscopy (CLEANEX-PM) to detect water-protein proton exchange and intermolecular NOEs. J. Am. Chem. Soc. 1997; 119: 6203-6204.
22. Wüthrich K, Otting G, Liepinsh E. Protein hydration in aqueous solution. Faraday Discuss. 1992; 93: 35-45.
23. Levy Y, Onuchic JN. Water mediation in protein folding and molecular recognition. Annu. Rev. Biophys. Biomol. Struct. 2006; 35: 389-415.
24. Woodward CK, Hilton BD. Hydrogen exchange kinetics and internal motions in proteins and nucleic acids. Annu. Rev. Biophys. Bioeng. 1979; 8: 99-127.
25. Bai Y, Milne JS, Mayne L, Englander SW. Primary structure effects on peptide group hydrogen exchange. Proteins: Struct. Funct. Bioinform. 1993; 17: 75-86.
26. Englander SW. Protein folding intermediates and pathways studied by hydrogen exchange. Annu. Rev. Biophys. Biomolec. Struct. 2000; 29: 213-238.
27. Pace CN. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol. 1986; 131: 266-280.
28. Jones C, Zacà D, Hua J, Zhou J, Van Zijl P, Pillai JJ. Brain tumor clean-APT and NOE-CEST imaging at 7T. Proceedings of the 21st Annual Meeting ISMRM, Salt Lake City, UT, USA, 2013; 3648.
29. Zhou J, Hong X. APT and NOE imaging contrasts of glioma with different RF saturation powers. Proceedings of the 21st Annual Meeting ISMRM, Salt Lake City, UT, USA, 2013; 2527.
30. Singh A, Haris M, Cai K, Kogan F, Witschey WR, Zsido GA, McGarvey J, Nanga RP, Contijoch F, Pilla JJ, Gorman JH, Ferrari VA, Hariharan H, Gorman RC, Reddy R. Z-spectrum fitting for CEST contrast computation in in vivo myocardium tissue. Proceedings of the 21st Annual Meeting ISMRM, Salt Lake City, UT, USA, 2013; 1438.
31. Schmitt B, Zaiss M, Zhou J, Bachert P. Optimization of pulse train presaturation for CEST imaging in clinical scanners. Magn. Reson. Med. 2011; 65: 1620-1629.
32. Kim M, Gillen J, Landman BA, Zhou J, van Zijl PCM. Water saturation shift referencing (WASSR) for chemical exchange saturation transfer (CEST) experiments. Magn. Reson. Med. 2009; 61: 1441-1450.
33. Jin T, Wang P, Zong X, Kim S-G. MR imaging of the amide-proton transfer effect and the pH-insensitive nuclear Overhauser effect at 9.4 T. Magn. Reson. Med. 2012; 69: 760-770.
34. Neuhaus D. The Nuclear Overhauser Effect. VCH Publishing: New York; 1992.
35. Solomon I. Relaxation processes in a system of two spins. Phys. Rev. 1955; 99: 559.
36. Henkelman RM, Stanisz GJ, Graham SJ. Magnetization transfer in MRI: a review. NMR Biomed. 2001; 14: 57-64.
37. Zhou J, Yan K, Zhu H. A simple model for understanding the origin of the amide proton transfer MRI signal in tissue. Appl. Magn. Reson. 2012; 42: 393-402.
38. Pekar J, Jezzard P, Roberts DA, Leigh, Jr. JS, Frank JA, McLaughlin AC. Perfusion imaging with compensation for asymmetric magnetization transfer effects. Magn. Reson. Med. 1996; 35: 70-79.
39. Hua J, Jones C, Van Zijl PCM. Human brain magnetization transfer (MT) asymmetry dependence on RF saturation power. Proceedings of the 13th Annual Meeting ISMRM, Miami, FL, USA, 2005; 416.
40. Zaiss M, Goerke S, Bachert P. MT and spillover correction for quantitative steady-state pulsed CEST-MRI at 3T using the reciprocal Z-spectrum. arXiv:13026605 2013.
41. Wu R, Liu C-M, Liu PK, Sun PZ. Improved measurement of labile proton concentration-weighted chemical exchange rate (k(ws)) with experimental factor-compensated and T(1)-normalized quantitative chemical exchange saturation transfer (CEST) MRI. Contrast Media Mol. Imaging 2012; 7: 384-389.
42. Zaiss M, Schmitt B, Bachert P. Quantitative separation of CEST effect from magnetization transfer and spillover effects by Lorentzian-line-fit analysis of z-spectra. J. Magn. Reson. 2011; 211: 149-155.
43. Zaiss M, Bachert P. Exchange-dependent relaxation in the rotating frame for slow and intermediate exchange - modeling off-resonant spin-lock and chemical exchange saturation transfer. NMR Biomed. 2013; 26: 507-518.
44. Aguzzi A, O'Connor T. Protein aggregation diseases: pathogenicity and therapeutic perspectives. Nat. Rev. Drug Discov. 2010; 9: 237-248.
45. Hetz C, Glimcher LH. Protein homeostasis networks in physiology and disease. Curr. Opin. Cell Biol. 2011; 23: 123-125.
46. Chen B, Retzlaff M, Roos T, Frydman J. Cellular strategies of protein quality control. Cold Spring Harb. Perspect. Biol. 2011; 3: a004374.
47. Bowler BE. Residual structure in unfolded proteins. Curr. Opin. Struct. Biol. 2012; 22: 4-13.
48. Mikaelsson T, Adén J, Johansson LB-Å, Wittung-Stafshede P. Direct observation of protein unfolded state compaction in the presence of macromolecular crowding. Biophys. J. 2013; 104: 694-704.
49. Engel R, Westphal AH, Huberts DHEW, Nabuurs SM, Lindhoud S, Visser AJWG, van Mierlo CPM. Macromolecular crowding compacts unfolded apoflavodoxin and causes severe aggregation of the off-pathway intermediate during apoflavodoxin folding. J. Biol. Chem. 2008; 283: 27 383-27 394.
50. Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH, Blagosklonny MV, El-Deiry WS, Golstein P, Green DR, Hengartner M, Knight RA, Kumar S, Lipton SA, Malorni W, Nuñez G, Peter ME, Tschopp J, Yuan J, Piacentini M, Zhivotovsky B, Melino G. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 2009; 16: 3-11.
51. Zhou J, Tryggestad E, Wen Z, Lal B, Zhou T, Grossman R, Wang S, Yan K, Fu D-X, Ford E, Tyler B, Blakeley J, Laterra J, van Zijl PCM. Differentiation between glioma and radiation necrosis using molecular magnetic resonance imaging of endogenous proteins and peptides. Nat. Med. 2011; 17: 130-134.
52. Gerigk L, Schmitt B, Stieltjes B, Röder F, Essig M, Bock M, Schlemmer H-P, Röthke M. 7 Tesla imaging of cerebral radiation necrosis after arteriovenous malformations treatment using amide proton transfer (APT) imaging. J. Magn. Reson. Imaging 2012; 35: 1207-1209.