Solution NMR studies on the orientation of membrane-bound peptides and proteins by paramagnetic probes

Molecules

Volumn 18, Issue 7, 2013, Pages 7407-7435

  Schrank, Evelyne ^a   Wagner, Gabriel E ^a   Zangger, Klaus ^a  

^a UNIVERSITY OF GRAZ   (Austria)

Author keywords

Dodecylphosphocholine; Membrane bound peptides and proteins; Micelle; NMR spectroscopy; Paramagnetic relaxation

Indexed keywords

ANTIMICROBIAL CATIONIC PEPTIDE; BACTERIAL TOXIN; CALCIUM BINDING PROTEIN; CELL PENETRATING PEPTIDE; MEMBRANE PROTEIN; PEPTIDE; PHOSPHOLAMBAN;

CELL MEMBRANE; CHEMISTRY; MAGNETIC FIELD; NUCLEAR MAGNETIC RESONANCE; PROCEDURES; METHODOLOGY; REVIEW;

ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIAL TOXINS; CALCIUM-BINDING PROTEINS; CELL MEMBRANE; CELL-PENETRATING PEPTIDES; MAGNETIC FIELDS; MEMBRANE PROTEINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDES;

EID: 84880842684     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules18077407     Document Type: Review

References (129)

1. Lehnert, U.; Xia, Y.; Royce, T.E.; Goh, C.S.; Liu, Y.; Senes, A.; Yu, H.; Zhang, Z.L.; Engelman, D.M.; Gerstein, M. Computational analysis of membrane proteins: Genomic occurrence, Structure prediction and helix interactions. Q. Rev. Biophys. 2004, 37, 121-146.
2. Overington, J.P.; Al-Lazikani, B.; Hopkins, A.L. How many drug targets are there? Nat. Rev. Drug Discov. 2006, 5, 993-996.
3. Raman, P.; Cherezov, V.; Caffrey, M. The membrane proztein data bank. Cell. Mol. Life Sci. 2006, 63, 36-51.
4. Klammt, C.; Maslennikov, I.; Bayrhuber, M.; Eichmann, C.; Vajpai, N.; Chiu, E.J.; Blain, K.Y.; Esquivies, L.; Kwon, J.H.; Balana, B.; et al. Facile backbone structure determination of human membrane proteins by NMR spectroscopy. Nat. Methods 2012, 9, 834-839.
5. Hohlweg, W.; Kosol, S.; Zangger, K. Determining the orientation and localization of membrane-bound peptides. Curr. Protein Pept. Sci. 2012, 13, 267-279.
6. Pervushin, K.; Riek, R.; Wider, G.; Wüthrich, K. Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc. Natl. Acad. Sci. USA 1997, 94, 12366-12371.
7. Kainosho, M.; Torizawa, T.; Iwashita, Y.; Terauchi, T.; Mei Ono, A.; Güntert, P. Optimal isotope labelling for NMR protein structure determinations. Nature 2006, 440, 52-57.
8. Göbl, C.; Dulle, M.; Hohlweg, W.; Grossauer, J.; Falsone, S.F.; Glatter, O.; Zangger, K. Influence of phosphocholine alkyl chain length on peptide-micelle interactions and micellar size and shape. J. Phys. Chem. B 2010, 114, 4717-4724.
9. Kallick, D.A.; Tessmer, M.R.; Watts, C.R.; Li, C.Y. The use of dodecylphosphocholine micelles in solution NMR. J. Magn. Reson. B 1995, 109, 60-65.
10. Keifer, P.A.; Peterkofsky, A.; Wang, G. Effects of detergent alkyl chain length and chemical structure on the properties of a micelle-bound bacterial membrane targeting peptide. Anal. Biochem. 2004, 331, 33-39.
11. Dürr, U.H.; Gildenberg, M.; Ramamoorthy, A. The magic of bicelles lights up membrane protein structure. Chem. Rev. 2012, 112, 6054-6074.
12. Warschawski, D.E.; Arnold, A.A.; Beaugrand, M.; Gravel, A.; Chartrand, E.; Marcotte, I. Choosing membrane mimetics for NMR structural studies of transmembrane proteins. Biochim. Biophys. Acta 2011, 1808, 1957-1974.
13. Hagn, F.; Etzkorn, M.; Raschle, T.; Wagner, G. Optimized phospholipid bilayer nanodiscs facilitate high-resolution structure determination of membrane proteins. J. Am. Chem. Soc. 2013, 135, 1919-1925.
14. Puthenveetil, R.; Vinogradova, O. Optimization of the design and preparation of nanoscale phospholipid bilayers for its application to solution NMR. Proteins 2013, 81, 1222-1231.
15. Bertini, I.; Luchinat, C.; Parigi, G. Solution NMR of Paramagnetic Molecules; Elsevier: Amsterdam, The Netherlands, 2001.
16. Brown, L.R.; Bosch, C.; Wüthrich, K. Location and orientation relative to the micelle surface for glucagon in mixed micelles with dodecylphosphocholine: EPR and NMR studies. Biochim. Biophys. Acta 1981, 642, 296-312.
17. Respondek, M.; Madl, T.; Göbl, C.; Golser, R.; Zangger, K. Mapping the orientation of helices in micelle-bound peptides by paramagnetic relaxation waves. J. Am. Chem. Soc. 2007, 129, 5228-5234.
18. Fernandez, C.; Hilty, C.; Wider, G.; Wüthrich, K. Lipid-protein interactions in DHPC micelles containing the integral membrane protein OmpX investigated by NMR spectroscopy. Proc. Natl. Acad. Sci. USA 2002, 99, 13533-13537.
19. Hilty, C.; Wider, G.; Fernandez, C.; Wüthrich, K. Membrane protein - lipid interactions in mixed micelles studied by NMR spectroscopy with the use of paramagnetic reagents. ChemBioChem 2004, 5, 467-473.
20. Yamamoto, K.; Vivekanandan, S.; Ramamoorthy, A. Fast NMR data acquisition from bicelles containing a membrane-associated peptide at natural-abundance. J. Phys. Chem. B 2011, 115, 12448-12455.
21. Yamamoto, K.; Xu, J.; Kawulka, K.E.; Vederas, J.C.; Ramamoorthy, A. Use of a copper-chelated lipid speeds up NMR measurements from membrane proteins. J. Am. Chem. Soc. 2010, 132, 6929-6931.
22. Nielsen, R.D.; Che, K.; Gelb, M.H.; Robinson, B.H. A ruler for determining the position of proteins in membranes. J. Am. Chem. Soc. 2005, 127, 6430-6442.
23. Prosser, R.S.; Luchette, P.A. An NMR study of the origin of dioxygen-induced spin-lattice relaxation enhancement and chemical shift perturbation. J. Magn. Reson. 2004, 171, 225-232.
24. Prosser, R.S.; Luchette, P.A.; Westerman, P.W. Using O2 to probe membrane immersion depth by 19F NMR. Proc. Natl. Acad. Sci. USA 2000, 97, 9967-9971.
25. Luchette, P.A.; Prosser, R.S.; Sanders, C.R. Oxygen as a paramagnetic probe of membrane protein structure by cysteine mutagenesis and 19F NMR spectroscopy. J. Am. Chem. Soc. 2002, 124, 1778-1781.
26. Evanics, F.; Hwang, P.M.; Cheng, Y.; Kay, L.E.; Prosser, R.S. Topology of an outer-membrane enzyme: Measuring oxygen and water contacts in solution NMR studies of PagP. J. Am. Chem. Soc. 2006, 128, 8256-8264.
27. Fazal, M.A.; Roy, B.C.; Sun, S.; Mallik, S.; Rodgers, K.R. Surface recognition of a protein using designed transition metal complexes. J. Am. Chem. Soc. 2001, 123, 6283-6290.
28. Niccolai, N.; Spiga, O.; Bernini, A.; Scarselli, M.; Ciutti, A.; Fiaschi, I.; Chiellini, S.; Molinari, H.; Temussi, P.A. NMR studies of protein hydration and TEMPOL accessibility. J. Mol. Biol. 2003, 332, 437-447.
29. Pintacuda, G.; Otting, G. Identification of protein surfaces by NMR measurements with a pramagnetic Gd(III) chelate. J. Am. Chem. Soc. 2002, 124, 372-373.
30. Kosol, S.; Schrank, E.; Bukvic-Krajacic, M.; Wagner, G.E.; Meyer, H.; Göbl, C.; Zangger, K.; Novak, P. Probing the interactions of macrolide antibiotics with membrane-mimetics by NMR spectroscopy. J. Med. Chem. 2012, 55, 5632-5636.
31. Zangger, K.; Respondek, M.; Göbl, C.; Hohlweg, W.; Rasmussen, K.; Grampp, G.; Madl, T. Positioning of micelle-bound peptides by paramagnetic relaxation enhancements. J. Phys. Chem. B 2009, 113, 4400-4406.
32. Madl, T.; Bermel, W.; Zangger, K. Use of relaxation enhancements in a paramagnetic environment for the structure determination of proteins using NMR spectroscopy. Angew. Chem. Int. Ed. Engl. 2009, 48, 8259-8262.
33. Fröhlich, R.F.; Schrank, E.; Zangger, K. 2, 2, 2-Trifluoroethyl 6-thio-beta-D-glucopyranoside as a selective tag for cysteines in proteins. Carbohydr. Res. 2012, 361, 100-104.
34. Pintacuda, G.; Otting, G. Identification of Protein Surfaces by NMR Measurements with a Paramagnetic Gd(III) Chelate. J. Am. Chem. Soc. 2001, 124, 372-373.
35. Zangger, K.; Gossler, R.; Khatai, L.; Lohner, K.; Jilek, A. Structures of the glycine-rich diastereomeric peptides bombinin H2 and H4. Toxicon 2008, 52, 246-254.
36. Meyer, N.H.; Zangger, K. Simplifying Proton NMR Spectra by Instant Homonuclear Broadband Decoupling. Angew. Chem. Int. Ed. Engl. 2013, doi:10.1002/anie.201300129.
37. Kosol, S.; Zangger, K. Dynamics and orientation of a cationic antimicrobial peptide in two membrane-mimetic systems. J. Struct. Biol. 2010, 170, 172-179.
38. Grossauer, J.; Kosol, S.; Schrank, E.; Zangger, K. The peptide hormone ghrelin binds to membrane-mimetics via its octanoyl chain and an adjacent phenylalanine. Bioorg. Med. Chem. 2010, 18, 5483-5488.
39. Göbl, C.; Kosol, S.; Stockner, T.; Rückert, H.M.; Zangger, K. Solution structure and membrane binding of the toxin fst of the par addiction module. Biochemistry 2010, 49, 6567-6575.
40. Franzmann, M.; Otzen, D.; Wimmer, R. Quantitative use of paramagnetic relaxation enhancements for determining orientations and insertion depths of peptides in micelles. Chembiochem 2009, 10, 2339-2347.
41. Cohen, L.S.; Arshava, B.; Neumoin, A.; Becker, J.M.; Guntert, P.; Zerbe, O.; Naider, F. Comparative NMR analysis of an 80-residue G protein-coupled receptor fragment in two membrane mimetic environments. Biochim. Biophys. Acta 2011, 1808, 2674-2684.
42. Page, R.C.; Lee, S.; Moore, J.D.; Opella, S.J.; Cross, T.A. Backbone structure of a small helical integral membrane protein: A unique structural characterization. Protein Sci. 2009, 18, 134-146.
43. Shi, L.; Traaseth, N.J.; Verardi, R.; Gustavsson, M.; Gao, J.; Veglia, G. Paramagnetic-based NMR restraints lift residual dipolar coupling degeneracy in multidomain detergent-solubilized membrane proteins. J. Am. Chem. Soc. 2011, 133, 2232-2241.
44. MacLennan, D.H.; Kranias, E.G. Phospholamban: A crucial regulator of cardiac contractility. Nat. Rev. Mol. Cell. Biol. 2003, 4, 566-577.
45. Simmerman, H.K.; Kobayashi, Y.M.; Autry, J.M.; Jones, L.R. A leucine zipper stabilizes the pentameric membrane domain of phospholamban and forms a coiled-coil pore structure. J. Biol. Chem. 1996, 271, 5941-5946.
46. Karim, C.B.; Marquardt, C.G.; Stamm, J.D.; Barany, G.; Thomas, D.D. Synthetic null-cysteine phospholamban analogue and the corresponding transmembrane domain inhibit the Ca-ATPase. Biochemistry 2000, 39, 10892-10897.
47. Traaseth, N.J.; Shi, L.; Verardi, R.; Mullen, D.G.; Barany, G.; Veglia, G. Structure and topology of monomeric phospholamban in lipid membranes determined by a hybrid solution and solid-state NMR approach. Proc. Natl. Acad. Sci. USA 2009, 106, 10165-10170.
48. Traaseth, N.J.; Verardi, R.; Torgersen, K.D.; Karim, C.B.; Thomas, D.D.; Veglia, G. Spectroscopic validation of the pentameric structure of phospholamban. Proc. Natl. Acad. Sci. USA 2007, 104, 14676-14681.
49. Zamoon, J.; Mascioni, A.; Thomas, D.D.; Veglia, G. NMR solution structure and topological orientation of monomeric phospholamban in dodecylphosphocholine micelles. Biophys. J. 2003, 85, 2589-2598.
50. Al-Abdul-Wahid, M.S.; Verardi, R.; Veglia, G.; Prosser, R.S. Topology and immersion depth of an integral membrane protein by paramagnetic rates from dissolved oxygen. J. Biomol. NMR 2011, 51, 173-183.
51. Praekelt, U.M.; Meacock, P.A. HSP12, a new small heat shock gene of Saccharomyces cerevisiae: analysis of structure, regulation and function. Mol. Gen. Genet. 1990, 223, 97-106.
52. Singarapu, K.K.; Tonelli, M.; Chow, D.C.; Frederick, R.O.; Westler, W.M.; Markley, J.L. Structural characterization of Hsp12, the heat shock protein from Saccharomyces cerevisiae, in aqueous solution where it is intrinsically disordered and in detergent micelles where it is locally alpha-helical. J. Biol. Chem. 2011, 286, 43447-43453.
53. Welker, S.; Rudolph, B.; Frenzel, E.; Hagn, F.; Liebisch, G.; Schmitz, G.; Scheuring, J.; Kerth, A.; Blume, A.; Weinkauf, S.; Haslbeck, M.; Kessler, H.; Buchner, J. Hsp12 is an intrinsically unstructured stress protein that folds upon membrane association and modulates membrane function. Mol. Cell. 2010, 39, 507-520.
54. Zasloff, M. Antimicrobial peptides of multicellular organisms. Nature 2002, 415, 389-395.
55. Hancock, R.E. W.; Lehrer, R. Cationic peptides: A new source of antibiotics. Trends Biotech. 1998, 16, 82-88.
56. Abbassi, F.; Lequin, O.; Piesse, C.; Goasdoue, N.; Foulon, T.; Nicolas, P.; Ladram, A. Temporin-SHf, a new type of phe-rich and hydrophobic ultrashort antimicrobial peptide. J. Biol. Chem. 2010, 285, 16880-16892.
57. Tossi, A.; Sandri, L.; Giangaspero, A. Amphipathic, Alpha-helical antimicrobial peptides. Biopolymers 2000, 55, 4-30.
58. Hancock, R.E.; Sahl, H.G. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol. 2006, 24, 1551-1557.
59. Nicolas, P. Multifunctional host defense peptides: Intracellular- targeting antimicrobial peptides. FEBS J. 2009, 276, 6483-6496.
60. Oppenheim, J.J.; Yang, D. Alarmins: Chemotactic activators of immune responses. Curr. Opin. Immunol. 2005, 17, 359-365.
61. Seo, M.D.; Won, H.S.; Kim, J.H.; Mishig-Ochir, T.; Lee, B.J. Antimicrobial peptides for therapeutic applications: A review. Molecules 2012, 17, 12276-12286.
62. Li, Y.; Xiang, Q.; Zhang, Q.; Huang, Y.; Su, Z. Overview on the recent study of antimicrobial peptides: Origins, Functions, Relative mechanisms and application. Peptides 2012, 37, 207-215.
63. Matsuzaki, K. Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetype. Biochim. Biophys. Acta 1999, 1462, 1-10.
64. Dempsey, C.E. The actions of melittin on membranes. Biochim. Biophys. Acta 1990, 1031, 143-161.
65. Pistolesi, S.; Pogni, R.; Feix, J.B. Membrane insertion and bilayer perturbation by antimicrobial peptide CM15. Biophys. J. 2007, 93, 1651-1660.
66. Bhargava, K.; Feix, J.B. Membrane binding, Structure, and localization of cecropin-mellitin hybrid peptides: A site-directed spin-labeling study. Biophys. J. 2004, 86, 329-336.
67. Ramamoorthy, A.; Marassi, F.M.; Zasloff, M.; Opella, S.J. Three-dimensional solid-state NMR spectroscopy of a peptide oriented in membrane bilayers. J. Biomol. NMR 1995, 6, 329-334.
68. Porcelli, F.; Buck-Koehntop, B.A.; Thennarasu, S.; Ramamoorthy, A.; Veglia, G. Structures of the dimeric and monomeric variants of magainin antimicrobial peptides (MSI-78 and MSI-594) in micelles and bilayers, determined by NMR spectroscopy. Biochemistry 2006, 45, 5793-5799.
69. Lequin, O.; Bruston, F.; Convert, O.; Chassaing, G.; Nicolas, P. Helical structure of dermaseptin B2 in a membrane-mimetic environment. Biochemistry 2003, 42, 10311-10323.
70. Saravanan, R.; Bhattacharjya, S. Oligomeric structure of a cathelicidin antimicrobial peptide in dodecylphosphocholine micelle determined by NMR spectroscopy. Biochim. Biophys. Acta 2011, 1808, 369-381.
71. Van Den Hooven, H.W.; Spronk, C.A.; van de Kamp, M.; Konings, R.N.; Hilbers, C.W.; van de van, F.J. Surface location and orientation of the lantibiotic nisin bound to membranemimicking micelles of dodecylphosphocholine and of sodium dodecylsulphate. Eur. J. Biochem. 1996, 235, 394-403.
72. Simmaco, M.; Mignogna, G.; Canofeni, S.; Miele, R.; Mangoni, M.L.; Barra, D. Temporins, antimicrobial peptides from the European red frog Rana temporaria. Eur. J. Biochem. 1996, 242, 788-792.
73. Abbassi, F.; Galanth, C.; Amiche, M.; Saito, K.; Piesse, C.; Zargarian, L.; Hani, K.; Nicolas, P.; Lequin, O.; Ladram, A. Solution structure and model membrane interactions of temporins-SH, antimicrobial peptides from amphibian skin. A NMR spectroscopy and differential scanning calorimetry study. Biochemistry 2008, 47, 10513-10525.
74. Saravanan, R.; Bhunia, A.; Bhattacharjya, S. Micelle-bound structures and dynamics of the hinge deleted analog of melittin and its diastereomer: Implications in cell selective lysis by D-amino acid containing antimicrobial peptides. Biochim. Biophys. Acta 2010, 1798, 128-139.
75. Lee, D.K.; Brender, J.R.; Sciacca, M.F.; Krishnamoorthy, J.; Yu, C.; Ramamoorthy, A. Lipid composition-dependent membrane fragmentation and pore-forming mechanisms of membrane disruption by pexiganan (MSI-78). Biochemistry 2013, doi:10.1021/bi400087n.
76. Ovchinnikova, T.V.; Shenkarev, Z.O.; Balandin, S.V.; Nadezhdin, K.D.; Paramonov, A.S.; Kokryakov, V.N.; Arseniev, A.S. Molecular insight into mechanism of antimicrobial action of the β-hairpin peptide arenicin: Specific oligomerization in detergent micelles. Biopolymers 2008, 89, 455-464.
77. Shenkarev, Z.O.; Balandin, S.V.; Trunov, K.I.; Paramonov, A.S.; Sukhanov, S.V.; Barsukov, L.I.; Arseniev, A.S.; Ovchinnikova, T.V. Molecular mechanism of action of betahairpin antimicrobial peptide arenicin: Oligomeric structure in dodecylphosphocholine micelles and pore formation in planar lipid bilayers. Biochemistry 2011, 50, 6255-6265.
78. Garcia-Olmedo, F.; Molina, A.; Alamillo, J.M.; Rodriguez-Palenzuela, P. Plant defense peptides. Biopolymers 1998, 47, 479-491.
79. McDonald, N.Q.; Hendrickson, W.A. A structural superfamily of growth factors containing a cystine knot motif. Cell 1993, 73, 421-424.
80. Craik, D.J.; Cemazar, M.; Wang, C.K.; Daly, N.L. The cyclotide family of circular miniproteins: Nature's combinatorial peptide template. Biopolymers 2006, 84, 250-266.
81. Craik, D.J.; Daly, N.L.; Waine, C. The cystine knot motif in toxins and implications for drug design. Toxicon. 2001, 39, 43-60.
82. Craik, D.J.; Daly, N.L. NMR as a tool for elucidating the structures of circular and knotted proteins. Mol. Biosyst. 2007, 3, 257-265.
83. Rosengren, K.J.; Daly, N.L.; Plan, M.R.; Waine, C.; Craik, D.J. Twists, Knots, and rings in proteins. Structural definition of the cyclotide framework. J. Biol. Chem. 2003, 278, 8606-8616.
84. Felizmenio-Quimio, M.E.; Daly, N.L.; Craik, D.J. Circular proteins in plants: solution structure of a novel macrocyclic trypsin inhibitor from Momordica cochinchinensis. J. Biol. Chem. 2001, 276, 22875-22882.
85. Craik, D.J.; Daly, N.L.; Bond, T.; Waine, C. Plant cyclotides: A unique family of cyclic and knotted proteins that defines the cyclic cystine knot structural motif. J. Mol. Biol. 1999, 294, 1327-1336.
86. Shenkarev, Z.O.; Nadezhdin, K.D.; Lyukmanova, E.N.; Sobol, V.A.; Skjeldal, L.; Arseniev, A.S. Divalent cation coordination and mode of membrane interaction in cyclotides: NMR spatial structure of ternary complex Kalata B7/Mn2+/DPC micelle. J. Inorg. Biochem. 2008, 102, 1246-1256.
87. Goransson, U.; Sjogren, M.; Svangard, E.; Claeson, P.; Bohlin, L. Reversible antifouling effect of the cyclotide cycloviolacin O2 against barnacles. J. Nat. Prod. 2004, 67, 1287-1290.
88. Jennings, C.; West, J.; Waine, C.; Craik, D.; Anderson, M. Biosynthesis and insecticidal properties of plant cyclotides: The cyclic knotted proteins from Oldenlandia affinis. Proc. Natl. Acad. Sci. USA 2001, 98, 10614-10619.
89. Gran, L. On the effect of a polypeptide isolated from "Kalata-Kalata" (Oldenlandia affinis DC) on the oestrogen dominated uterus. Acta Pharmacol. Toxicol. (Copenh) 1973, 33, 400-408.
90. Witherup, K.M.; Bogusky, M.J.; Anderson, P.S.; Ramjit, H.; Ransom, R.W.; Wood, T.; Sardana, M. Cyclopsychotride A, a biologically active, 31-residue cyclic peptide isolated from Psychotria longipes. J. Nat. Prod. 1994, 57, 1619-1625.
91. Miljanich, G.P.; Ramachandran, J. Antagonists of neuronal calcium channels: Structure, Function, and therapeutic implications. Annu. Rev. Pharmacol. Toxicol. 1995, 35, 707-734.
92. Tam, J.P.; Lu, Y.A.; Yang, J.L.; Chiu, K.W. An unusual structural motif of antimicrobial peptides containing end-to-end macrocycle and cystine-knot disulfides. Proc. Natl. Acad. Sci. USA 1999, 96, 8913-8918.
93. Gustafson, K.R.; Sowder, R.C.; Henderson, L.E.; Parsons, I.C.; Kashman, Y.; Cardellina, J.H.; McMahon, J.B.; Buckheit, R.W.; Pannell, L.K.; Boyd, M.R. Circulins A and B. Novel human immunodeficiency virus (HIV)-inhibitory macrocyclic peptides from the tropical tree Chassalia parvifolia. J. Am. Chem. Soc. 1994, 116, 9337-9338.
94. Hallock, Y.F.; Sowder, R.C., 2nd; Pannell, L.K.; Hughes, C.B.; Johnson, D.G.; Gulakowski, R.; Cardellina, J.H., 2nd; Boyd, M.R. Cycloviolins A-D, anti-HIV macrocyclic peptides from Leonia cymosa. J. Org. Chem. 2000, 65, 124-128.
95. Daly, N.L.; Clark, R.J.; Plan, M.R.; Craik, D.J. Kalata B8, a novel antiviral circular protein, exhibits conformational flexibility in the cystine knot motif. Biochem. J. 2006, 393, 619-626.
96. Shenkarev, Z.O.; Nadezhdin, K.D.; Sobol, V.A.; Sobol, A.G.; Skjeldal, L.; Arseniev, A.S. Conformation and mode of membrane interaction in cyclotides. Spatial structure of kalata B1 bound to a dodecylphosphocholine micelle. FEBS J. 2006, 273, 2658-2672.
97. Daly, N.L.; Rosengren, K.J.; Craik, D.J. Discovery, structure and biological activities of cyclotides. Adv. Drug Deliv. Rev. 2009, 61, 918-930.
98. Simonsen, S.M.; Sando, L.; Rosengren, K.J.; Wang, C.K.; Colgrave, M.L.; Daly, N.L.; Craik, D.J. Alanine scanning mutagenesis of the prototypic cyclotide reveals a cluster of residues essential for bioactivity. J. Biol. Chem. 2008, 283, 9805-9813.
99. Lindholm, P.; Goransson, U.; Johansson, S.; Claeson, P.; Gullbo, J.; Larsson, R.; Bohlin, L.; Backlund, A. Cyclotides: A novel type of cytotoxic agents. Mol. Cancer Ther. 2002, 1, 365-369.
100. Wang, C.K.; Colgrave, M.L.; Ireland, D.C.; Kaas, Q.; Craik, D.J. Despite a conserved cystine knot motif, different cyclotides have different membrane binding modes. Biophys. J. 2009, 97, 1471-1481.
101. Tang, J.; Yin, H.; Qiu, J.; Tucker, M.J.; DeGrado, W.F.; Gai, F. Using two fluorescent probes to dissect the binding, insertion, and dimerization kinetics of a model membrane peptide. J. Am. Chem. Soc. 2009, 131, 3816-3817.
102. Bourbigot, S.; Dodd, E.; Horwood, C.; Cumby, N.; Fardy, L.; Welch, W.H.; Ramjan, Z.; Sharma, S.; Waring, A.J.; Yeaman, M.R.; Booth, V. Antimicrobial peptide RP-1 structure and interactions with anionic versus zwitterionic micelles. Biopolymers 2009, 91, 1-13.
103. Wang, Y.; Schlamadinger, D.E.; Kim, J.E.; McCammon, J.A. Comparative molecular dynamics simulations of the antimicrobial peptide CM15 in model lipid bilayers. Biochim. Biophys. Acta 2012, 1818, 1402-1409.
104. Dittmer, J.; Thogersen, L.; Underhaug, J.; Bertelsen, K.; Vosegaard, T.; Pedersen, J.M.; Schiott, B.; Tajkhorshid, E.; Skrydstrup, T.; Nielsen, N.C. Incorporation of antimicrobial peptides into membranes: A combined liquid-state NMR and molecular dynamics study of alamethicin in DMPC/DHPC bicelles. J. Phys. Chem. B 2009, 113, 6928-6937.
105. Sauve, S.; Buijs, D.; Gingras, G.; Aubin, Y. Interactions between the conserved hydrophobic region of the prion protein and dodecylphosphocholine micelles. J. Biol. Chem. 2012, 287, 1915-1922.
106. Liu, G.; Prabhakar, A.; Aucoin, D.; Simon, M.; Sparks, S.; Robbins, K.J.; Sheen, A.; Petty, S.A.; Lazo, N.D. Mechanistic studies of peptide self-assembly: Transient alpha-helices to stable beta-sheets. J. Am. Chem. Soc. 2010, 132, 18223-18232.
107. Jarvet, J.; Danielsson, J.; Damberg, P.; Oleszczuk, M.; Gräslund, A. Positioning of the Alzheimer Abeta(1-40) peptide in SDS micelles using NMR and paramagnetic probes. J. Biomol. NMR 2007, 39, 63-72.
108. Wahlstrom, A.; Hugonin, L.; Peralvarez-Marin, A.; Jarvet, J.; Graslund, A. Secondary structure conversions of Alzheimer's Abeta(1-40) peptide induced by membrane-mimicking detergents. FEBS J. 2008, 275, 5117-5128.
109. Yamaguchi, T.; Matsuzaki, K.; Hoshino, M. Interaction between soluble Abeta-(1-40) monomer and Abeta-(1-42) fibrils probed by paramagnetic relaxation enhancement. FEBS Lett. 2013, 587, 620-624.
110. Nanga, R.P.; Brender, J.R.; Xu, J.; Hartman, K.; Subramanian, V.; Ramamoorthy, A. Three-dimensional structure and orientation of rat islet amyloid polypeptide protein in a membrane environment by solution NMR spectroscopy. J. Am. Chem. Soc. 2009, 131, 8252-8261.
111. Patil, S.M.; Xu, S.; Sheftic, S.R.; Alexandrescu, A.T. Dynamic alpha-helix structure of micelle-bound human amylin. J. Biol. Chem. 2009, 284, 11982-11991.
112. Nanga, R.P.; Brender, J.R.; Vivekanandan, S.; Popovych, N.; Ramamoorthy, A. NMR structure in a membrane environment reveals putative amyloidogenic regions of the SEVI precursor peptide PAP(248-286). J. Am. Chem. Soc. 2009, 131, 17972-17979.
113. Mukherjee, S.; Ghosh, R.N.; Maxfield, F.R. Endocytosis. Physiol. Rev. 1997, 77, 759-803.
114. Lindgren, M.; Hallbrink, M.; Prochiantz, A.; Langel, U. Cell-penetrating peptides. Trends Pharmacol. Sci. 2000, 21, 99-103.
115. Lindberg, M.; Jarvet, J.; Langel, U.; Graslund, A. Secondary structure and position of the cell-penetrating peptide transportan in SDS micelles as determined by NMR. Biochemistry 2001, 40, 3141-3149.
116. Berlose, J.P.; Convert, O.; Derossi, D.; Brunissen, A.; Chassaing, G. Conformational and associative behaviours of the third helix of antennapedia homeodomain in membrane-mimetic environments. Eur. J. Biochem. 1996, 242, 372-386.
117. Drin, G.; Demene, H.; Temsamani, J.; Brasseur, R. Translocation of the pAntp peptide and its amphipathic analogue AP-2AL. Biochemistry 2001, 40, 1824-1834.
118. Lindberg, M.; Graslund, A. The position of the cell penetrating peptide penetratin in SDS micelles determined by NMR. FEBS Lett. 2001, 497, 39-44.
119. Lindberg, M.; Biverstahl, H.; Graslund, A.; Maler, L. Structure and positioning comparison of two variants of penetratin in two different membrane mimicking systems by NMR. Eur. J. Biochem. 2003, 270, 3055-3063.
120. Derossi, D.; Chassaing, G.; Prochiantz, A. Trojan peptides: the penetratin system for intracellular delivery. Trends Cell. Biol. 1998, 8, 84-87.
121. Ohman, A.; Lycksell, P.O.; Jureus, A.; Langel, U.; Bartfai, T.; Graslund, A. NMR study of the conformation and localization of porcine galanin in SDS micelles. Comparison with an inactive analog and a galanin receptor antagonist. Biochemistry 1998, 37, 9169-9178.
122. Barany-Wallje, E.; Andersson, A.; Graslund, A.; Maler, L. NMR solution structure and position of transportan in neutral phospholipid bicelles. FEBS Lett. 2004, 567, 265-269.
123. Lau, A.L.; Chan, S.I. Alamethicin-mediated fusion of lecithin vesicles. Proc. Natl. Acad. Sci. USA 1975, 72, 2170-2174.
124. Feigenson, G.W.; Meers, P.R.; Kingsley, P.B. NMR observation of gramicidin A' in phosphatidylcholine vesicles. Biochim. Biophys. Acta 1977, 471, 487-491.
125. Weinstein, S.; Wallace, B.A.; Blout, E.R.; Morrow, J.S.; Veatch, W. Conformation of gramicidin A channel in phospholipid vesicles: A 13C and 19F nuclear magnetic resonance study. Proc. Natl. Acad. Sci. USA 1979, 76, 4230-4234.
126. Glover, K.J.; Whiles, J.A.; Wu, G.; Yu, N.; Deems, R.; Struppe, J.O.; Stark, R.E.; Komives, E.A.; Vold, R.R. Structural evaluation of phospholipid bicelles for solution-state studies of membrane-associated biomolecules. Biophys. J. 2001, 81, 2163-2171.
127. Tjandra, N.; Bax, A. Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science 1997, 278, 1111-1114.
128. Matsumori, N.; Morooka, A.; Murata, M. Conformation and location of membrane-bound salinomycin-sodium complex deduced from NMR in isotropic bicelles. J. Am. Chem. Soc. 2007, 129, 14989-14995.
129. Morrison, E.A.; DeKoster, G.T.; Dutta, S.; Vafabakhsh, R.; Clarkson, M.W.; Bahl, A.; Kern, D.; Ha, T.; Henzler-Wildman, K.A. Antiparallel EmrE exports drugs by exchanging between asymmetric structures. Nature 2012, 481, 45-50.