Helix 8 of the angiotensin- II type 1A receptor interacts with phosphatidylinositol phosphates and modulates membrane insertion

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Hirst, Daniel J ^a   Lee, Tzong Hsien ^a   Pattenden, Leonard K ^a   Thomas, Walter G ^b   Aguilar, Marie Isabel ^a  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; LIPID BILAYER; PEPTIDE; POLYPHOSPHOINOSITIDE;

AMINO ACID SEQUENCE; ANIMAL; BIREFRINGENCE; CHEMICAL STRUCTURE; CHEMISTRY; INTERFEROMETRY; KINETICS; LIPID BILAYER; METABOLISM; MOLECULAR GENETICS; MOLECULAR WEIGHT; PIG; PROTEIN SECONDARY STRUCTURE; REGRESSION ANALYSIS; STRUCTURE ACTIVITY RELATION; TIME FACTOR;

AMINO ACID SEQUENCE; ANIMALS; BIREFRINGENCE; INTERFEROMETRY; KINETICS; LEAST-SQUARES ANALYSIS; LIPID BILAYERS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; PEPTIDES; PHOSPHATIDYLINOSITOL PHOSPHATES; PROTEIN STRUCTURE, SECONDARY; RECEPTOR, ANGIOTENSIN, TYPE 1; STRUCTURE-ACTIVITY RELATIONSHIP; SUS SCROFA; TIME FACTORS;

EID: 84934780278     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep09972     Document Type: Article

References (48)

1. Davies , M. , Secker , A. , Freitas , A. , Mendao , M. & Timmis , J. On the hierarchical classification of g protein-coupled receptors. Bioinformatics 23 , 3113-3118 (2007).
2. Eglen , R. , Bosse , R. & Reisine , T. Emerging concepts of guanin nucleotide-binding protein-coupled receptor (gpcr) function and implications for high throughput screening. Assay Drug Dev. Technol. 5 , 425-451 (2007).
3. Gasparo , M. d. , Catt , K. , Inagami , T. , Wright , J. & Unger , T. International union of pharmacology. XXIII. The angiotensin II receptors. Pharmacol. Rev. 52 , 415-472 (2000).
4. Venkatakrishnan , A. , Deupi , X. , Lebon , G. , Tate , C. , Schertler , G. & Babu , M. Molecular signatures of g-protein-coupled receptors. Nature 494 , 185-194 (2013).
5. Hunyady , L. & Catt , K. Pleiotropic at1 receptor signaling pathways mediating physiological and pathogenic actions of angiotensin II. Mol. Endocrinol. 20 , 953-970 (2006).
6. Vaughan , M. G. protein-coupled receptors minireview series. J. Biol. Chem. 273 , 17297 (1998).
7. Ohyama , K. , Yamano , Y. , Chaki , S. , Kondo , T. & Inagami , T. Domains for g-protein coupling in angiotensin II receptor type i: Studies by site-directed mutagenesis. Biochem. Biophys. Res. Commun. 189 , 677-683 (1992).
8. Thomas , W. , Pipolo , L. & Qian , H. Identification of a ca2 binding domain within the carboxyl-terminus of the angiotensin II (at1a) receptor. FEBS Lett. 455 , 367-371 (1999).
9. Mozsolits , H. , Unabia , S. , Ahmad , A. , Morton , C. , Thomas , W. & Aguilar , M. Electrostatic and hydrophobic forces tether the proximal region of the angiotensin II receptor (at1a) carboxyl terminus to anionic lipids. Biochemistry 41 , 7830-7840 (2002).
10. Huynh , J. , Thomas , W. G. , Aguilar , M.-I. & Pattenden , L. K. Role of helix 8 in g protein-coupled receptors based on structure- function studies on the type 1 angiotensin receptor. Mol. Cell. Endocrinol. 302 , 118-127 (2009).
11. Kamimori , H. , Unabia , S. , Thomas , W. & Aguilar , M. Evaluation of the membrane-binding properties of the proximal region of the angiotensin II receptor (at1a) carboxyl terminus by surface plasmon resonance. Anal. Sci. 21 , 171-174 (2005).
12. Rasmussen , S. , Choi , H.-J. , Rosenbaum , D. , Kobilka , T. , Thian , F. , Edwards , P. , Burghammer , M. , Ratnala , V. , Sanishvili , R. , Fischetti , R. , Schertler , G. , Weis , W. & Kobilka , B. Crystal structure of the human b2 adrenergic g-protein-coupled receptor. Nature 450 , 383-387 (2007).
13. Jaakola , V. , Griffith , M. , Hanson , M. , Cherezov , V. , Chien , E. , Lane , J. , Ijzerman , A. & Stevens , R. The 2.6 angstrom crystal structure of a hunan a2a adenosine receptor bound to an antagonist. Science 322 , 1211-1217 (2008).
14. Xu , F. , Wu , H. , Katritch , V. , Han , G. , Jacobson , K. , Gao , Z. -G. , Cherezov , V. & Stevens , R. Structure of an agonist-bound human a2a adenosine receptor. Science 332 , 322-327 (2011).
15. Lemmon , M. Membrane recognition by phospholipid-binding domains. Nat. Rev. Mol. Cell. Bio. 9 , 99-111 (2008).
16. Oates , J. & Watts , A. Uncovering the intimate relationship between lipids , cholesterol and gpcr activation. Curr. Opin. Struct. Biol. 21 , 1-6 (2011).
17. Phillips , R. , Ursell , T. , Wiggins , P. & Sens , P. Emerging roles for lipids in shaping membrane-protein function. Nature 459 , 379-385 (2009).
18. Heo , W. , Inoue , T. , Park , W. , Kim , M. , Park , B. , Wandless , T. & Meyer , T. Pi(3,4,5)p3 and pi(4,5)p2 lipids target proteins with polybasic clusters to the plasma membrane. Science 314 , 1458-1461 (2006).
19. Hruby , V. , Alves , I. , Cowell , S. , Salamon , Z. & Tollin , G. Use of plasmon waveguide resonance (pwr) spectroscopy for examining binding , signaling and lipid domain partitioning of membrane proteins. Life Sci. 86 , 569-574 (2010).
20. Li , L. , Shi , X. , Guo , X. , Li , H. & Xu , C. Ionic protein-lipid interaction at the plasma membrane: What can the charge do? Trends Biochem. Sci. 39 , 130-140 (2014).
21. Soubias , O. , Niu , S. , Mitchell , D. & Gawrisch , K. Lipid-rhodopsin hydrophobic mismatch alters rhodopsin helical content. J. Am. Chem. Soc. 130 , 12465-12471 (2008).
22. Anraku , K. , Fukuda , R. , Takamune , N. , Misumi , S. , Okamoto , Y. , Otsuka , M. & Fujita , M. Highly sensitive analysis of the interaction between HIV-1 gag and phosphoinositide derivatives based on surface plasmon resonance. Biochemistry 49 , 5109- 5116 (2010).
23. Paolo , G. D. & Camilli , P. D. Phosphoinositides in cell regulation and membrane dynamics. Nature 443 , 651-657 (2006).
24. Golebiewska , U. , Gambhir , A. , Hangyas-Mihalyne , G. , Zaitseva , I. , Radler , J. & Mclaughlin , S. Membrane-bound basic peptides sequester multivalent (pip2) , but not monovalent (ps) , acidic lipids. Biophys. J. 91 , 588-599 (2006).
25. Hirst , D. , Lee , T.-H. , Swann , M. & Aguilar , M. Combined mass and structural kinetic analysis of multistate antimicrobial peptidemembrane interactions. Anal. Chem. 85 , 9296-9304 (2013).
26. Hirst , D. , Lee , T.-H. , Swann , M. , Unabia , S. , Park , Y. , Hahm , K.-S. & Aguilar , M. Effect of acyl chain structure and bilayer phase state of binding and penetration of a supported lipid bilayer by hpa3. Eur. Biophys. J. 40 , 503-514 (2011).
27. Hall , K. , Lee , T.-H. , Mechler , A. , Swann , M. & Aguilar , M. Real-time measurement of membrane conformational states induced by antimicrobial peptides: Balance between recovery and lysis. Sci. Rep. 4 , 5479 DOI:10.1038/srep05479 (2014).
28. Lee , T. , Hall , K. , Swann , M. , Popplewell , J. , Unabia , S. , Park , Y. , Hahm , K. & Aguilar , M. The membrane insertion of helical antimicrobial peptides from the n-terminus of helicobacter pylori risbosomal protein l1. Biochim. Biophys. Acta , Biomembr. 1798 , 544-557 (2010).
29. Lee , T. , Heng , C. , Separovic , F. & Aguilar , M. Comparison of reversible membrane destabilisation induced by antimicrobial peptides derived from australian frogs. Biochim. Biophys. Acta 1838 , 2205-2215 (2014).
30. Andreu-Fernádez , V. , Genoves , A. , Lee , T. , Stellato , M. , Lucantoni , F. , Orzáez , M. , Mingarro , I. , Aguilar , M. & Pérez-Payá E. Peptides derived from the transmembrane domain of bcl-2 proteins as potential mitochondrial priming tools. ACS Chem. Biol. 9 , 1799-1811 (2014).
31. Rosenhouse-Dantsker , A. , Sui , J. , Zhao , Q. , Rusinova , R. , Rodríguez-Menchaca , A. , Zhang , Z. & Logothetis , D. A sodiummediated structural switch that controls the sensitivity of kir channels to ptdins(4,5)p2. Nat. Chem. Biol. 4 , 624-631 (2008).
32. Escorihuela , J. , González-Martinez , M. , Lóez-Paz , J. , Puchades , R. , Maquieira , A. & Gimenez-Romero , D. Dual-polarization interferometry: A novel technique to light up the nanomolecular world. Chem. Rev. 115 , 265-294 (2015).
33. Fernandez , D. , Sani , T. L. M. , Aguilar , M. & Separovic , F. Proline facilitates membrane insertion of the antimicrobial peptide maculatin 1.1 via surface indentation and subsequent lipid disordering. Biophys. J. 104 , 1495-1507 (2013).
34. Fernandez , D. , Brun , A. L. , Whitwell , T. , Sani , M. , James , M. & Separovic , F. The antimicrobial peptide aurein 1.2 disrupts model membranes via the carpet mechanism. Phys. Chem. Chem. Phys. 14 , 15739-15751 (2012).
35. Baumann , M. K. , Swann , M. J. , Textor , M. & Reimhult , E. Pleckstrin homology-phospholipase c-delta(1) interaction with phosphatidylinositol 4,5-bisphosphate containing supported lipid bilayers monitored in situ with dual polarization interferometry. Anal. Chem. 83 , 6267-6274 (2011).
36. Lee , T.-H. , Heng , C. , Swann , M. , Gehman , J. , Separovic , F. & Aguilar , M. Real-time quantitative analysis of lipid disordering by aurein 1.2 during membrane adsorption , destabilisation and lysis. Biochim. Biophys. Acta , Biomembr. 1798 , 1977-1986 (2010).
37. Tan , O. & Cross , G. Surface anchoring structure of a liquid crystal monolayer studied via dual polarization interferometry. Phys. Rev. E 79 , 021703 (2009).
38. Bruno , S. , Adsorption of molecular layers on hydrophilic sioxny probed by dpi technique , Masters Thesis , Durham University (2010).
39. Mashaghi , A. , Swann , M. , Textor , J. P. M. & Reimhult , E. Optical anisotropy of supported lipid structures probed by waveguide spectroscopy and its application to study of supported lipid bilayer formation kinetics. Anal. Chem. 80 , 3666-3676 (2008).
40. Singh , S. , Kasetty , G. , Schmidtchen , A. & Malmsten , M. Membrane and lipopolysaccharide interactions of c-terminal peptides from s1 peptidases. Biochim. Biophys. Acta 1818 , 2244-2251 (2012).
41. Ouberai , M. , Wang , J. , Swann , M. , Galvagnion , C. , Guilliams , T. , Dobson , C. & Welland , M. A-synuclein senses lipid packing defects and induces lateral expansion of lipids leading to membrane reordering. J. Biol. Chem. 288 , 20883-20895 (2013).
42. Horvath , R. , Kobzi , B. , Keul , H. , Moeller , M. & Kiss , E. Molecular interaction of a new antibacterial polymer with a supported lipid bilayer measured by an in situ label-free optical technique. Int. J. Mol. Sci. 14 , 1482-1492 (2013).
43. Singh , S. , Papareddy , P. , Kalle , M. , Schmidtchen , A. & Malmsten , M. Importance of lipopolysaccaride aggregate disruption for the anti-endotoxic effects of heparin cofactor II peptides. Biochim. Biophys. Acta 1828 , 2709-2719 (2013).
44. Singh , S. , Kalle , M. , Papareddy , P. , Schmidtchen , A. & Malmsten , M. Lipopolysaccharide interactions of c-terminal peptides from human thrombin. Biomacromolecules 14 , 1482-1492 (2013).
45. Yu , L. , Guo , L. , Ding , J. , Ho , B. , Feng , S. , Popplewell , J. , Swann , M. & Wohland , T. Interaction of an artificial antimicrobial peptide with lipid membranes. Biochim. Biophys. Acta 1788 , 333-344 (2009).
46. Horvath , R. & Ramsden , J. Quasi-isotropic analysis of anisotropic thin films on optical waveguides. Langmuir 23 , 9330-9334 (2007).
47. Schaaf , P. & Talbot , M. Surface exclusion effects in adsorption processes. J. Chem. Phys. 91 , 4401 (1989).
48. Rabe , M. , Verdes , D. & Seeger , S. Understanding protein adsorption phenomena at solid surfaces. Adv. Colloid Interfac. 162 , 87-106 (2011).