PHLIP peptide interaction with a membrane monitored by SAXS

Journal of Physical Chemistry B

Volumn 120, Issue 44, 2016, Pages 11484-11491

  Narayanan, Theyencheri ^a,c   Weerakkody, Dhammika ^b   Karabadzhak, Alexander G ^b   Anderson, Michael ^b   Andreev, Oleg A ^b   Reshetnyak, Yana K ^b  

^a EUROPEAN SYNCHROTRON RADIATION FACILITY   (France)

^b UNIVERSITY OF RHODE ISLAND   (United States)

^c YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD; LIPID BILAYERS; LIPOSOMES; MEDICAL APPLICATIONS; OLIGOMERS; X RAY SCATTERING;

BLOOD CIRCULATION; CONCENTRATION-DEPENDENT; KINETIC PROCESS; LIPOSOME STRUCTURES; OLIGOMERIC STATE; PEPTIDE ADSORPTION; TIME-RESOLVED SAXS; UNILAMELLAR VESICLE;

PEPTIDES;

LIPOSOME; MEMBRANE PROTEIN; PHLIP PROTEIN;

ADSORPTION; CHEMISTRY; LIPID BILAYER; PH; SMALL ANGLE SCATTERING; SYNTHESIS; X RAY DIFFRACTION;

ADSORPTION; HYDROGEN-ION CONCENTRATION; LIPID BILAYERS; LIPOSOMES; MEMBRANE PROTEINS; SCATTERING, SMALL ANGLE; X-RAY DIFFRACTION;

EID: 85019961991     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/acs.jpcb.6b06643     Document Type: Article

References (45)

1. Van den Berg, B.; Clemons, W. M., Jr.; Collinson, I.; Modis, Y.; Hartmann, E.; Harrison, S. C.; Rapoport, T. A. X-ray structure of a protein-conducting channel Nature 2004, 427, 36-44 10.1038/nature02218
2. Osborne, A. R.; Rapoport, T. A.; van den Berg, B. Protein translocation by the Sec61/SecY channel Annu. Rev. Cell Dev. Biol. 2005, 21, 529-550 10.1146/annurev.cellbio.21.012704.133214
3. White, S. H.; von Heijne, G. The machinery of membrane protein assembly Curr. Opin. Struct. Biol. 2004, 14, 397-404 10.1016/j.sbi.2004.07.003
4. Simpson, P. J.; Schwappach, B.; Dohlman, H. G.; Isaacson, R. L. Structures of Get3, Get4, and Get5 provide new models for TA membrane protein targeting Structure 2010, 18, 897-902 10.1016/j.str.2010.07.003
5. Brambillasca, S.; Yabal, M.; Makarow, M.; Borgese, N. Unassisted translocation of large polypeptide domains across phospholipid bilayers J. Cell Biol. 2006, 175, 767-777 10.1083/jcb.200608101
6. Renthal, R. Helix insertion into bilayers and the evolution of membrane proteins Cell. Mol. Life Sci. 2010, 67, 1077-1088 10.1007/s00018-009-0234-9
7. Ladokhin, A. S.; White, S. H. Interfacial folding and membrane insertion of a designed helical peptide Biochemistry 2004, 43, 5782-5791 10.1021/bi0361259
8. Hunt, J. F.; Earnest, T. N.; Bousche, O.; Kalghatgi, K.; Reilly, K.; Horvath, C.; Rothschild, K. J.; Engelman, D. M. A biophysical study of integral membrane protein folding Biochemistry 1997, 36, 15156-15176 10.1021/bi970146j
9. Reshetnyak, Y. K.; Andreev, O. A.; Lehnert, U.; Engelman, D. M. Translocation of molecules into cells by pH-dependent insertion of a transmembrane helix Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 6460-6465 10.1073/pnas.0601463103
10. Weerakkody, D.; Moshnikova, A.; Thakur, M. S.; Moshnikova, V.; Daniels, J.; Engelman, D. M.; Andreev, O. A.; Reshetnyak, Y. K. Family of pH (low) insertion peptides for tumor targeting Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 5834-5839 10.1073/pnas.1303708110
11. Musial-Siwek, M.; Karabadzhak, A.; Andreev, O. A.; Reshetnyak, Y. K.; Engelman, D. M. Tuning the insertion properties of pHLIP Biochim. Biophys. Acta, Biomembr. 2010, 1798, 1041-1046 10.1016/j.bbamem.2009.08.023
12. Karabadzhak, A. G.; Weerakkody, D.; Wijesinghe, D.; Thakur, M. S.; Engelman, D. M.; Andreev, O. A.; Markin, V. S.; Reshetnyak, Y. K. Modulation of the pHLIP transmembrane helix insertion pathway Biophys. J. 2012, 102, 1846-1855 10.1016/j.bpj.2012.03.021
13. Barrera, F. N.; Weerakkody, D.; Anderson, M.; Andreev, O. A.; Reshetnyak, Y. K.; Engelman, D. M. Roles of carboxyl groups in the transmembrane insertion of peptides J. Mol. Biol. 2011, 413, 359-371 10.1016/j.jmb.2011.08.010
14. Onyango, J. O.; Chung, M. S.; Eng, C. H.; Klees, L. M.; Langenbacher, R.; Yao, L.; An, M. Noncanonical amino acids to improve the pH response of pHLIP insertion at tumor acidity Angew. Chem., Int. Ed. 2015, 54, 3658-3663 10.1002/anie.201409770
15. Nguyen, V. P.; Alves, D. S.; Scott, H. L.; Davis, F. L.; Barrera, F. N. A Novel Soluble Peptide with pH-Responsive Membrane Insertion Biochemistry 2015, 54, 6567-6575 10.1021/acs.biochem.5b00856
16. Tapmeier, T. T.; Moshnikova, A.; Beech, J.; Allen, D.; Kinchesh, P.; Smart, S.; Harris, A.; McIntyre, A.; Engelman, D. M.; Andreev, O. A. The pH low insertion peptide pHLIP Variant 3 as a novel marker of acidic malignant lesions Proc. Natl. Acad. Sci. U.S.A. 2015, 112, 9710-9715 10.1073/pnas.1509488112
17. Viola-Villegas, N. T.; Carlin, S. D.; Ackerstaff, E.; Sevak, K. K.; Divilov, V.; Serganova, I.; Kruchevsky, N.; Anderson, M.; Blasberg, R. G.; Andreev, O. A. Understanding the pharmacological properties of a metabolic PET tracer in prostate cancer Proc. Natl. Acad. Sci. U.S.A. 2014, 111, 7254-7259 10.1073/pnas.1405240111
18. Cruz-Monserrate, Z.; Roland, C. L.; Deng, D.; Arumugam, T.; Moshnikova, A.; Andreev, O. A.; Reshetnyak, Y. K.; Logsdon, C. D. Targeting pancreatic ductal adenocarcinoma acidic microenvironment Sci. Rep. 2014, 4 4410 10.1038/srep04410
19. Sosunov, E. A.; Anyukhovsky, E. P.; Sosunov, A. A.; Moshnikova, A.; Wijesinghe, D.; Engelman, D. M.; Reshetnyak, Y. K.; Andreev, O. A. pH (low) insertion peptide (pHLIP) targets ischemic myocardium Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 82-86 10.1073/pnas.1220038110
20. Demoin, D. W.; Wyatt, L. C.; Edwards, K. J.; Abdel-Atti, D.; Sarparanta, M.; Pourat, J.; Longo, V. A.; Carlin, S. D.; Engelman, D. M.; Andreev, O. A.; Reshetnyak, Y. K.; Viola-Villegas, N.; Lewis, J. S. PET Imaging of Extracellular pH in Tumors with (64)Cu-and (18)F-Labeled pHLIP Peptides: A Structure-Activity Optimization Study Bioconjugate Chem. 2016, 27, 2014-2023 10.1021/acs.bioconjchem.6b00306
21. Reshetnyak, Y. K.; Yao, L.; Zheng, S.; Kuznetsov, S.; Engelman, D. M.; Andreev, O. A. Measuring tumor aggressiveness and targeting metastatic lesions with fluorescent pHLIP Mol. Imaging Biol. 2011, 13, 1146-1156 10.1007/s11307-010-0457-z
22. Antosh, M. P.; Wijesinghe, D. D.; Shrestha, S.; Lanou, R.; Huang, Y. H.; Hasselbacher, T.; Fox, D.; Neretti, N.; Sun, S.; Katenka, N. Enhancement of radiation effect on cancer cells by gold-pHLIP Proc. Natl. Acad. Sci. U.S.A. 2015, 112, 5372-5376 10.1073/pnas.1501628112
23. An, M.; Wijesinghe, D.; Andreev, O. A.; Reshetnyak, Y. K.; Engelman, D. M. pH-(low)-insertion-peptide (pHLIP) translocation of membrane impermeable phalloidin toxin inhibits cancer cell proliferation Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 20246-20250 10.1073/pnas.1014403107
24. Moshnikova, A.; Moshnikova, V.; Andreev, O. A.; Reshetnyak, Y. K. Antiproliferative effect of pHLIP-amanitin Biochemistry 2013, 52, 1171-1178 10.1021/bi301647y
25. Cheng, C. J.; Bahal, R.; Babar, I. A.; Pincus, Z.; Barrera, F.; Liu, C.; Svoronos, A.; Braddock, D. T.; Glazer, P. M.; Engelman, D. M. MicroRNA silencing for cancer therapy targeted to the tumour microenvironment Nature 2014, 518, 107-110 10.1038/nature13905
26. Burns, K. E.; Thevenin, D. Down-regulation of PAR1 activity with a pHLIP-based allosteric antagonist induces cancer cell death Biochem. J. 2015, 472, 287-295 10.1042/BJ20150876
27. Burns, K. E.; Robinson, M. K.; Thevenin, D. Inhibition of cancer cell proliferation and breast tumor targeting of pHLIP-monomethyl auristatin E conjugates Mol. Pharmaceutics 2015, 12, 1250-1258 10.1021/mp500779k
28. Reshetnyak, Y. K.; Andreev, O. A.; Segala, M.; Markin, V. S.; Engelman, D. M. Energetics of peptide (pHLIP) binding to and folding across a lipid bilayer membrane Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 15340-15345 10.1073/pnas.0804746105
29. Andreev, O. A.; Karabadzhak, A. G.; Weerakkody, D.; Andreev, G. O.; Engelman, D. M.; Reshetnyak, Y. K. pH (low) insertion peptide (pHLIP) inserts across a lipid bilayer as a helix and exits by a different path Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 4081-4086 10.1073/pnas.0914330107
30. Sharma, G. P.; Reshetnyak, Y. K.; Andreev, O. A.; Karbach, M.; Muller, G. Coil-helix transition of polypeptide at water-lipid interface J. Stat. Mech. 2015, 2015 P01034 10.1088/1742-5468/2015/01/P01034
31. Kučerka, N.; Nieh, M.-P.; Katsaras, J. Small-Angle Scattering from Homogenous and Heterogeneous Lipid Bilayers. In Advances in Planar Lipid Bilayers and Liposomes; Iglic, A.; Tien, H. T., Eds.; Academic Press: Burlington, 2010; Vol. 12, pp 201-235.
32. Kučerka, N.; Liu, Y.; Chu, N.; Petrache, H. I.; Tristram-Nagle, S.; Nagle, J. F. Structure of fully hydrated fluid phase DMPC and DLPC lipid bilayers using X-ray scattering from oriented multilamellar arrays and from unilamellar vesicles Biophys. J. 2005, 88, 2626-2637 10.1529/biophysj.104.056606
33. Narayanan, T.; Gummel, J.; Gradzielski, M. Probing the Self-Assembly of Unilamellar Vesicles Using Time-Resolved SAXS. In Advances in Planar Lipid Bilayers and Liposomes; Iglic, A.; Kulkarni, C. V., Eds.; Academic Press: Burlington, 2014; Vol. 20, pp 171-196.
34. Marquardt, D.; Heberle, F. A.; Nickels, J. D.; Pabst, G.; Katsaras, J. On scattered waves and lipid domains: detecting membrane rafts with X-rays and neutrons Soft Matter 2015, 11, 9055-9072 10.1039/C5SM01807B
35. Kiselev, M. A.; Zemlyanaya, E. V.; Aswal, V. K.; Neubert, R. H. What can we learn about the lipid vesicle structure from the small-angle neutron scattering experiment? Eur. Biophys. J. 2006, 35, 477-493 10.1007/s00249-006-0055-9
36. Pencer, J.; Krueger, S.; Adams, C. P.; Katsaras, J. Method of separated form factors for polydisperse vesicles J. Appl. Crystallogr. 2006, 39, 293 10.1107/S0021889806005255
37. Reshetnyak, Y. K.; Segala, M.; Andreev, O. A.; Engelman, D. M. A monomeric membrane peptide that lives in three worlds: in solution, attached to, and inserted across lipid bilayers Biophys. J. 2007, 93, 2363-2372 10.1529/biophysj.107.109967
38. Roy, R. S.; Gopi, H. N.; Raghothama, S.; Gilardi, R. D.; Karle, I. L.; Balaram, P. Peptide hairpins with strand segments containing alpha-and beta-amino acid residues: cross-strand aromatic interactions of facing Phe residues Biopolymers 2005, 80, 787-799 10.1002/bip.20294
39. Dietz, H.; Rief, M. Protein structure by mechanical triangulation Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 1244-1247 10.1073/pnas.0509217103
40. Carrion-Vazquez, M.; Li, H.; Lu, H.; Marszalek, P. E.; Oberhauser, A. F.; Fernandez, J. M. The mechanical stability of ubiquitin is linkage dependent Nat. Struct. Biol. 2003, 10, 738-743 10.1038/nsb965
41. Oesterhelt, F.; Oesterhelt, D.; Pfeiffer, M.; Engel, A.; Gaub, H. E.; Muller, D. J. Unfolding pathways of individual bacteriorhodopsins Science 2000, 288, 143-146 10.1126/science.288.5463.143
42. Pabst, G.; Rappolt, M.; Amenitsch, H.; Laggner, P. Structural information from multilamellar liposomes at full hydration: Full q-range fitting with high quality x-ray data Phys. Rev. E 2000, 62, 4000-4009 10.1103/PhysRevE.62.4000
43. Adochite, R. C.; Moshnikova, A.; Golijanin, J.; Andreev, O. A.; Katenka, N.; Reshetnyak, Y. K. Comparative study of tumor targeting and biodistribution of pH (Low) Insertion Peptides (pHLIP® peptides) conjugated with different fluorescent dyes Mol. Imaging Biol. 2016, 18, 686-696 10.1007/s11307-016-0949-6
44. Cheng, C. J.; Bahal, R.; Babar, I. A.; Pincus, Z.; Barrera, F.; Liu, C.; Svoronos, A.; Braddock, D. T.; Glazer, P. M.; Engelman, D. M. MicroRNA silencing for cancer therapy targeted to the tumour microenvironment Nature 2015, 518, 107-110 10.1038/nature13905
45. Zoonens, M.; Reshetnyak, Y. K.; Engelman, D. M. Bilayer interactions of pHLIP, a peptide that can deliver drugs and target tumors Biophys. J. 2008, 95, 225-235 10.1529/biophysj.107.124156