The native structure of annexin A2 peptides in hydrophilic environment determines their anti-angiogenic effects

Biochemical Pharmacology

Volumn 95, Issue 1, 2015, Pages 1-15

  Raddum, Aase M ^a   Hollås, Hanne ^a   Shumilin, Igor A ^b   Henklein, Petra ^c   Kretsinger, Robert ^b   Fossen, Torgils ^a   Vedeler, Anni ^a  

^a UNIVERSITY OF BERGEN   (Norway)

^b UNIVERSITY OF VIRGINIA   (United States)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

A2 Peptide; Annexin; Anti angiogenenic; Co culture; Folding

Indexed keywords

ANGIOGENESIS INHIBITOR; LIPOCORTIN 2; WATER;

AMINO ACID SEQUENCE; ANIMAL; BOVINE; CHEMICAL PHENOMENA; CHEMISTRY; COCULTURE; GENETICS; MOLECULAR GENETICS; PROTEIN SECONDARY STRUCTURE; X RAY DIFFRACTION;

AMINO ACID SEQUENCE; ANGIOGENESIS INHIBITORS; ANIMALS; ANNEXIN A2; CATTLE; COCULTURE TECHNIQUES; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, SECONDARY; WATER; X-RAY DIFFRACTION;

EID: 84930911897     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2015.02.013     Document Type: Article

References (59)

1. R.H. Adams, and K. Alitalo Molecular regulation of angiogenesis and lymphangiogenesis Nat. Rev. Mol. Cell Biol. 8 2007 464 478
2. P. Saharinen, L. Eklund, K. Pulkki, P. Bono, and K. Alitalo VEGF and angiopoietin signaling in tumor angiogenesis and metastasis Trends Mol. Med. 17 2011 347 362
3. P. Carmeliet Angiogenesis in life, disease and medicine Nature 438 2005 932 936
4. P. Carmeliet VEGF as a key mediator of angiogenesis in cancer Oncology 69 2005 4 10
5. P. Carmeliet Angiogenesis in health and disease Nat. Med. 9 2003 653 660
6. G. Bergers, and L.E. Benjamin Tumorigenesis and the angiogenic switch Nat. Rev. Cancer 3 2003 401 410
7. D. Hanahan, and R.A. Weinberg The hallmarks of cancer Cell 100 2000 57 70
8. D. Hanahan, and R.A. Weinberg Hallmarks of cancer: the next generation Cell 144 2011 646 674
9. M. Potente, H. Gerhardt, and P. Carmeliet Basic and therapeutic aspects of angiogenesis Cell 146 2011 873 887
10. V. Gerke, and S.E. Moss Annexins: from structure to function Physiol. Rev. 82 2002 331 371
11. U. Rescher, and V. Gerke Annexins-unique membrane binding proteins with diverse functions J. Cell Sci. 117 2004 2631 2639
12. 2+ signalling to membrane dynamics Nat. Rev. Mol. Cell Biol. 6 2005 449 461
13. P. Singh Role of Annexin-II in GI cancers: interaction with gastrins/progastrins Cancer Lett. 252 2007 19 35
14. N.R. Filipenko, and D.M. Waisman The C terminus of annexin II mediates binding to F-actin J. Biol. Chem. 276 2001 5310 5315
15. M.J. Hayes, D. Shao, M. Bailly, and S.E. Moss Regulation of actin dynamics by annexin 2 EMBO J. 25 2006 1816 1826
16. A.G. Grieve, S.E. Moss, and M.J. Hayes Annexin A2 at the interface of actin and membrane dynamics: a focus on its roles in endocytosis and cell polarization Int. J. Cell Biol. 2012 2012 852430
17. A. Vedeler, and H. Hollas Annexin II is associated with mRNAs which may constitute a distinct subpopulation Biochem. J. 348 2000 565 572
18. A. Vedeler, H. Hollås, A.K. Grindheim, and A.M. Raddum Multiple roles of annexin A2 in post-transcriptional regulation of gene expression Curr. Protein Pept. Sci. 13 2012 401 412
19. K.A. Hajjar, A.T. Jacovina, and J. Chacko An endothelial cell receptor for plasminogen/tissue plasminogen activator. I. Identity with annexin II J. Biol. Chem. 269 1994 21191 21197
20. S. Heyraud, M. Jaquinod, C. Durmort, E. Dambroise, E. Concord, J.P. Schaal, P. Huber, and D. Gulino-Debrac Contribution of annexin 2 to the architecture of mature endothelial adherens junctions Mol. Cell Biol. 28 2008 1657 1668
21. M.G. Lampugnani, M. Corada, P. Andriopoulou, S. Esser, W. Risau, and E. Dejana Cell confluence regulates tyrosine phosphorylation of adherens junction components in endothelial cells J. Cell Sci. 110 1997 2065 2077
22. S.C. Su, and S.A. Maxwell Bayless KJ. Annexin 2 regulates endothelial morphogenesis by controlling AKT activation and junctional integrity J. Biol. Chem. 285 2010 40624 40634
23. J. Kirshner, D. Schumann, and J.E.C.E.A.C.A.M1 Shively a cell-cell adhesion molecule, directly associates with annexin II in a three-dimensional model of mammary morphogenesis J. Biol. Chem. 278 2003 50338 50345
24. S. Ergün, N. Kilik, G. Ziegeler, A. Hansen, P. Nollau, J. Götze, J.H. Wurmbach, A. Horst, J. Weil, M. Fernando, and C. Wagener CEA-related cell adhesion molecule 1: a potent angiogenic factor and a major effector of vascular endothelial growth factor Mol. Cell 5 2000 311 320
25. B.R. Dempsey, A. Rezvanpour, T.W. Lee, K.R. Barber, M.S. Junop, and G.S. Shaw Structure of an asymmetric ternary protein complex provides insight for membrane interaction Structure 20 2012 1737 1745
26. G. Ozorowski, C.M. Ryan, J.P. Whitelegge, and H. Luecke Withaferin A binds covalently to the N-terminal domain of annexin A2 Biol. Chem. 393 2012 1151 1163
27. C. Benaud, B.J. Gentil, N. Assard, M. Court, J. Garin, C. Delphin, and J. Baudier AHNAK interaction with the annexin 2/S100A10 complex regulates cell membrane cytoarchitecture J. Cell Biol. 164 2004 133 144
28. B.J. Gentil, C. Benaud, C. Delphin, C. Remy, V. Berezowski, R. Cecchelli, O. Feraud, D. Vittet, J. Baudier, and A.H.N.A.K. Specific expression in brain endothelial cells with barrier properties J. Cell Physiol. 203 2005 362 371
29. A.M. Raddum, L. Evensen, H. Hollås, A.K. Grindheim, J.B. Lorens, and A. Vedeler Domains I and IV of Annexin A2 affect the formation and integrity of in vitro capillary-like networks PLoS One 8 2013 e60281
30. R. Huber, J. Römisch, and E.P. Paques The crystal and molecular structure of human annexin V, an anticoagulant protein that binds to calcium and membranes EMBO J. 9 1990 3867 3874
31. Y.H. Hong, H.S. Won, H.C. Ahn, and B.J. Lee Structural elucidation of the protein- and membrane-binding properties of the N-terminal tail domain of human annexin II J. Biochem. 134 2003 427 432
32. A. Rosengarth, H. Luecke, and A2. Annexin Does it induce membrane aggregation by a new multimeric state of the protein Annexins 1 2004 129 136
33. I. Aukrust, L. Evensen, H. Hollås, F. Berven, R.A. Atkinson, G. Travé, T. Flatmark, and A. Vedeler Engineering, biophysical characterisation and binding properties of a soluble mutant form of annexin A2 domain IV that adopts a partially folded conformation J. Mol. Biol. 363 2006 469 481
34. C.M. Edwards, M.A. Cohen, and S.R. Bloom Peptides as drugs QJM 92 1999 1 4
35. Y. Lu, J. Yang, and E. Sega Issues related to targeted delivery of proteins and peptides AAPS J. 8 2006 E466 E478
36. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
37. J. Leandro, N. Simonsen, J. Saraste, P. Leandro, and T. Flatmark Phenylketonuria as a protein misfolding disease: The mutation pG46S in phenylalanine hydroxylase promotes self-association and fibril formation Biochim. Biophys. Acta 1812 2011 106 120
38. W. Minor, M. Cymborowski, Z. Otwinowski, and M. Chruszcz HKL-3000: the integration of data reduction and structure solution - from diffraction images to an initial model in minutes Acta Crystallogr. D Biol. Crystallogr. 62 2006 859 866
39. Solbak SM∅, T.R. Reksten, F. Hahn, V. Wray, P. Henklein, P. Henklein, ∅. Halskau, U. Schubert, and T. Fossen HIV-1 p6 - a structured to flexible multifunctional membrane-interacting protein Biochim. Biophys. Acta 1828 2013 816 823
40. L. Evensen, D.R. Micklem, W. Link, and J.B. Lorens Mural cell associated VEGF is required for organotypic vessel formation PLoS One 4 2009 e5798
41. L. Evensen, D.R. Micklem, W. Link, and J.B. Lorens A novel imaging-based high-throughput screening approach to anti-angiogenic drug discovery Cytometry A 77 2010 41 51
42. L.K. Henchey, A.L. Jochim, and P.S. Arora Contemporary strategies for the stabilization of peptides in the alpha-helical conformation Curr. Opin. Chem. Biol. 12 2008 692 697
43. C. Shao, F. Zhang, M.M. Kemp, R.J. Linhardt, D.M. Waisman, J.F. Head, and B.A. Seaton Crystallographic analysis of calcium-dependent heparin binding to annexin A2 J. Biol. Chem. 281 2006 31689 31695
44. Y. Nominé, T. Ristriani, C. Laurent, J.F. Lefèvre, E. Weiss, and G. Travé Formation of soluble inclusion bodies by hpv e6 oncoprotein fused to maltose-binding protein Protein Expr. Purif. 23 2001 22 32
45. M.E. Cromwell, E. Hilario, and F. Jacobson Protein aggregation and bioprocessing AAPS J. 8 2006 E572 E579
46. D.S. Wishart, B.D. Sykes, and F.M. Richards The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy Biochemistry 31 1992 1647 1651
47. J. Drevs, R. Müller-Driver, C. Wittig, S. Fuxius, N. Esser, H. Hugenschmidt, M.A. Konerding, P.R. Allegrini, J. Wood, J. Hennig, and C. Unger Marmé D. PTK787/ZK 222584, a specific vascular endothelial growth factor-receptor tyrosine kinase inhibitor, affects the anatomy of the tumor vascular bed and the functional vascular properties as detected by dynamic enhanced magnetic resonance imaging Cancer Res. 62 2002 4015 4022
48. M.C. Sharma, and M. Sharma The role of annexin II in angiogenesis and tumor progression: a potential therapeutic target Curr. Pharm. 13 2007 3568 3575
49. H.J. Zhang, D.F. Yao, M. Yao, H. Huang, L. Wang, M.J. Yan, X.D. Yan, X. Gu, W. Wu, and S.L. Lu Annexin A2 silencing inhibits invasion, migration, and tumorigenic potential of hepatoma cells World J. Gastroenterol. 19 2013 3792 3801
50. P. Chames, M. Van Regenmortel, E. Weiss, and D. Baty Therapeutic antibodies: successes, limitations and hopes for the future Br. J. Pharmacol. 157 2009 220 233
51. K.C. Foy, M.J. Miller, and N. Moldovan Carson Iii WE, Kaumaya PT. Combined vaccination with HER-2 peptide followed by therapy with VEGF peptide mimics exerts effective anti-tumor and anti-angiogenic effects in vitro and in vivo OncoImmunology 1 2012 1 13
52. F. Cordier-Ochsenbein, R. Guerois, F. Baleux, T. Huynh-Dinh, A. Chaffotte, J.M. Neumann, and A. Sanson Folding properties of an annexin I domain: a 1H-15 N NMR and CD study Biochemistry 35 1996 10347 10357
53. P. Luo, and R.L. Baldwin Mechanism of helix induction by trifluoroethanol: a framework for extrapolating the helix-forming properties of peptides from trifluoroethanol/water mixtures back to water Biochemistry 36 1997 8413 8421
54. D. Roccatano, G. Colombo, M. Fioroni, and A.E. Mark Mechanism by which 2,2,2-trifluoroethanol/water mixtures stabilize secondary-structure formation in peptides: a molecular dynamics study Proc. Natl. Acad. Sci. USA 99 2002 12179 12184
55. E. Gasteiger, C. Hoogland, A. Gattiker, S. Duvaud, M.R. Wilkins, R.D. Appel, and A. Bairoch Protein identification and analysis tools on the ExPASy server J.M. Walker, The Proteomics Protocols Handbook 2005 Humana Press 571 607
56. S. Zhao, L. Huang, J. Wu, Y. Zhang, D. Pan, and X. Liu Vascular endothelial growth factor upregulates expression of annexin A2 in vitro and in a mouse model of ischemic retinopathy Mol. Vis. 15 2009 1231 1242
57. Q. Ling, A.T. Jacovina, A. Deora, M. Febbraio, R. Simantov, R.L. Silverstein, B. Hempstead, W.H. Mark, and K.A. Hajjar Annexin II regulates fibrin homeostasis and neoangiogenesis in vivo J. Clin. Invest. 113 2004 38 48
58. M. Valapala, S.I. Thamake, and J.K. Vishwanatha A competitive hexapeptide inhibitor of annexin A2 prevents hypoxia-induced angiogenic events J. Cell Sci. 124 2011 1453 1464
59. K. Kesavan, J. Ratliff, E.W. Johnson, W. Dahlberg, J.M. Asara, P. Misra, J.V. Frangioni, and D.B. Jacoby Annexin A2 is a molecular target for TM601, a peptide with tumor-targeting and anti-angiogenic effects J. Biol. Chem. 285 2010 4366 4374