Withaferin A binds covalently to the N-terminal domain of annexin A2

Biological Chemistry

Volumn 393, Issue 10, 2012, Pages 1151-1163

  Ozorowski, Gabriel ^a   Ryan, Christopher M ^b   Whitelegge, Julian P ^b   Luecke, Hartmut ^a,c,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Irvine   (United States)

Author keywords

Actin polymerization; Annexin A2; Covalent modification; Mass spectrometry; Robert Huber; With aferin A

Indexed keywords

F ACTIN; LIPOCORTIN 2; WITHAFERIN A;

ACTIN POLYMERIZATION; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CELL INVASION; CHEMICAL MODIFICATION; DRUG PROTEIN BINDING; MASS SPECTROMETRY; PRIORITY JOURNAL;

ACTINS; ANIMALS; ANNEXIN A2; BINDING SITES; CATTLE; CYSTEINE; HUMANS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; SOLVENTS; WITHANOLIDES;

EID: 84869479021     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2012-0184     Document Type: Article

References (59)

1. Alhindawi, M., Alkhafaji, S., and Abdulnabi, M. (1992). Antigranuloma activity of Iraqi Withania somnifera . J. Ethno pharmacol. 37, 113-116.
2. Ayala-Sanmartin, J., Henry, J.-P., and Pradel, L.-A. (2001). Cholesterol regulates membrane binding and aggregation by annexin 2 at submicromolar Ca2+ concentration. Biochim. Biophys. Acta 1510, 18-28.
3. Becker, T., Weber, K., and Johnsson, N. (1990). Protein-protein recognition via short amphiphilic helices; a mutational analysis of the binding site of annexin II for p11. EMBO J. 9, 4207-4213.
4. Bhattacharya, A., Ghosal, S., and Bhattacharya, S.K. (2001). Anti-oxidant effect of Withania somnifera glycowithanolides in chronic footshock stress-induced perturbations of oxidative free radical scavenging enzymes and lipid peroxidation in rat frontal cortex and striatum. J. Ethnopharmacol. 74, 1-6.
5. Blackwood, R.A. and Ernst, J.D. (1990). Characterization of Ca2+ - dependent phospholipid binding, vesicle aggregation and membrane fusion by annexins. Biochem. J. 266, 195-200.
6. Burger, A., Berendes, R., Liemann, S., Benz, J., Hofmann, A., Gottig, P., Huber, R., Gerke, V., Thiel, C., Romisch, J., et al. (1996). The crystal structure and ion channel activity of human annexin II, a peripheral membrane protein. J. Mol. Biol. 257, 839-847.
7. Caplan, J.F., Filipenko, N.R., Fitzpatrick, S.L., and Waisman, D.M. (2004). Regulation of annexin A2 by reversible glutathionylation. J. Biol. Chem. 279, 7740-7750.
8. Collaborative Computational Project, Number 4 (1994). The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50, 760-763.
9. Darden, T., York, D., and Pedersen, L. (1993). Particle mesh Ewald: an N · log (N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089-10092.
10. DeLano, W. (2002). The PyMOL Molecular Graphics System 2002 (San Carlos CA: DeLano Scientific).
11. Emsley, P., Lohkamp, B., Scott, W.G., and Cowtan, K. (2010). Features and development of Coot. Acta Crystallographica Section D 66, 486-501.
12. Essmann, U., Perera, L., Berkowitz, M.L., Darden, T., Lee, H., and Pedersen, L.G. (1995). A smooth particle mesh Ewald method. J. Chem. Phys. 103, 8577-8593.
13. Falsey, R.R., Marron, M.T., Gunaherath, G.M.K.B., Shirahatti, N., Mahadevan, D., Gunatilaka, A.A.L., and Whitesell, L. (2005). Actin microfilament aggregation induced by withaferin A is mediated by annexin II. Nat. Chem. Biol. 2, 33-38.
14. Feller, S.E., Zhang, Y., Pastor, R.W., and Brooks, B.R. (1995). Constant pressure molecular dynamics simulation: the Langevin piston method. J. Chem. Phys. 103, 4613-4621.
15. Filipenko, N.R. and Waisman, D.M. (2001). The C terminus of annexin II mediates binding to F-actin. J. Biol. Chem. 276, 5310- 5315.
16. Furmanowa, M., Gajdzis-Kuls, D., Ruszkowska, J., Czarnocki, Z., Obidoska, G., Sadowska, A., Rani, R., and Upadhyay, S. (2001). In vitro propagation of Withania somnifera and isolation of withanolides with immunosuppressive activity. Planta Med. 67, 146-149.
17. Gerke, V. and Moss, S.E. (1997). Annexins and membrane dynamics. Biochim. Biophys. Acta 1357, 129-154.
18. Gerke, V. and Moss, S.E. (2002). Annexins: from structure to function. Physiol. Rev. 82, 331-371.
19. Glenney, J.R. and Tack, B.F. (1985). Amino-terminal sequence of p36 and associated p10: identification of the site of tyrosine phosphorylation and homology with S-100. Proc. Natl. Acad. Sci. USA 82, 7884-7888.
20. Glenney, J.R., Boudreau, M., Galyean, R., Hunter, T., and Tack, B. (1986). Association of the S-100-related calpactin I light chain with the NH 2 -terminal tail of the 36-kDa heavy chain. J. Biol. Chem. 261, 10485-10488.
21. Gould, K.L., Woodgett, J.R., Isacke, C.M., and Hunter, T. (1986). The protein-tyrosine kinase substrate p36 is also a substrate for protein kinase C in vitro and in vivo . Mol. Cell. Biol. 6, 2738-2744.
22. Grover, A., Shandilya, A., Bisaria, V., and Sundar, D. (2010a). Probing the anticancer mechanism of prospective herbal drug withaferin A on mammals: a case study on human and bovine proteasomes. BMC Genomics 11, S15.
23. Grover, A., Shandilya, A., Punetha, A., Bisaria, V., and Sundar, D. (2010b). Inhibition of the NEMO/IKKβ association complex formation, a novel mechanism associated with the NF-κB activation suppression by Withania somnifera' s key metabolite withaferin A. BMC Genomics 11, S25.
24. Grubmuller, H., Heller, H., Windemuth, A., and Schulten, K. (1991). Generalized Verlet algorithm for efficient molecular dynamics simulations with long-range interactions. Mol. Simul. 6, 121- 142.
25. Hajjar, K.A., Mauri, L., Jacovina, A.T., Zhong, F., Mirza, U.A., Padovan, J.C., and Chait, B.T. (1998). Tissue plasminogen activator binding to the annexin II tail domain. J. Biol. Chem. 273, 9987-9993.
26. Hayes, M.J., Shao, D., Bailly, M., and Moss, S.E. (2006). Regulation of actin dynamics by annexin 2. EMBO J. 25, 1816-1826.
27. Hayes, M.J., Shao, D.-M., Grieve, A., Levine, T., Bailly, M., and Moss, S.E. (2009). Annexin A2 at the interface between F-actin and membranes enriched in phosphatidylinositol 4,5,-bisphosphate. Biochim. Biophys. Acta 1793, 1086-1095.
28. Huber, R., Berendes, R., Burger, A., Luecke, H., and Karshikov, A. (1992). Annexin V - crystal structure and its implications on function. Behring Inst. Mitteilungen 91, 107-125.
29. Humphrey, W., Dalke, W., and Schulten, K. (1996). VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38.
30. Johnsson, N., Vandekerckhove, J., Van Damme, J., and Weber, K. (1986). Binding sites for calcium, lipid and p11 on p36, the substrate of retroviral tyrosine-specific protein kinases. FEBS Lett. 198, 361-364.
31. Jorgensen, W.L., Chandrasekhar, J., Madura, J.D., Impey, R.W., and Klein, M.L. (1983). Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926-935.
32. Kesavan, K., Ratliff, J., Johnson, E.W., Dahlberg, W., Asara, J.M., Misra, P., Frangioni, J.V., and Jacoby, D.B. (2010). Annexin A2 is a molecular target for TM601, a Peptide with tumor-targeting and anti-angiogenic effects. J. Biol. Chem. 285, 4366-4374.
33. Khanna, N.C., Helwig, E.D., Ikebuchi, N.W., Fitzpatrick, S., Bajwa, R., and Waisman, D.M. (1990). Purification and characterization of annexin proteins from bovine lung. Biochemistry 29, 4852- 4862.
34. Kube, E., Becker, T., Weber, K., and Gerke, V. (1992). Proteinprotein interaction studied by site-directed mutagenesis. Chara cterization of the annexin II-binding site on p11, a member of the S100 protein family. J. Biol. Chem. 267, 14175-14182.
35. Lambert, O., Gerke, V., Bader, M.-F., Porte, F., and Brisson, A. (1997). Structural analysis of junctions formed between lipid membranes and several annexins by cryo-electron microscopy. J. Mol. Biol. 272, 42-55.
36. Luecke, H., Chang, B.T., Mailliard, W.S., Schlaepfer, D.D., and Haigler, H.T. (1995). Crystal structure of the annexin XII hexamer and implications for bilayer insertion. Nature 378, 512-515.
37. MacKerell, A.D., Jr., Bashford, D., Bellott, M., Dunbrack, R.L., Jr., Evanseck, J.D., Field, M.J., Fischer, S., Gao, J., Guo, H., Ha, S., et al. (1998). All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102, 3586-3616.
38. Martin-Belmonte, F., Gassama, A., Datta, A., Yu, W., Rescher, U., Gerke, V., and Mostov, K. (2007). PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 128, 383-397.
39. Martyna, G.J., Tobias, D.J., and Klein, M.L. (1994). Constantpressure molecular-dynamics algorithms. J. Chem. Phys. 101, 4177-4189.
40. Mishra, L., Singh, B., and Dagenias, S. (2000). Scientific basis for the therapeutic use of Withania somnifera (ashwa-gandha): a review. Altern. Med. Rev. 5, 334-336.
41. Miyamoto, S. and Kollman, P. (1992). An analytical version of the SHAKE and RATTLE algorithm for rigid water models. J. Comput. Chem. 13, 952-962.
42. Morel, E., Parton, R.G., and Gruenberg, J. (2009). Annexin A2-dependent polymerization of actin mediates endosome biogenesis. Dev. Cell 16, 445-457.
43. Olson, M. and Sahai, E. (2009). The actin cytoskeleton in cancer cell motility. Clin. Exp. Metastasis 26, 273-287.
44. Owais, M., Sharad, K., Shehbaz, A., and Saleemuddin, M. (2005). Antibacterial efficacy of Withania somnifera (ashwagandha) an indigenous medicinal plant against experimental murine salmonellosis. Phytomedicine 12, 229-235.
45. Phillips, J.C., Braun, B., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R.D., Kalé, L., and Schulten, K. (2005). Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781-1802.
46. Rety, S., Sopkova, J., Renouard, M., Osterloh, D., Gerke, V., Tabaries, S., Russo-Marie, F., and Lewit-Bentley, A. (1999). The crystal structure of a complex of p11 with the annexin II N-terminal peptide. Nat. Struct. Mol. Biol. 6, 89-95.
47. Rosengarth, A. and Luecke, H. (2003). A calcium-driven conformational switch of the N-terminal and core domains of annexin A1. J. Mol. Biol. 326, 1317-1325.
48. Rosengarth, A. and Luecke, H. (2004). Annexin A2: does It induce membrane aggregation by a new multimeric state of the protein? Annexins 1, e35 - e41.
49. Rosengarth, A., Gerke, V., and Luecke, H. (2001). X-ray structure of full-length annexin 1 and implications for membrane aggregation. J. Mol. Biol. 306, 489-498.
50. Ryckaert, J.-P., Ciccotti, G., and Berendsen, H.J.C. (1977). Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n -alkanes. J. Comput. Phys. 23, 327-341.
51. Semov, A., Moreno, M.J., Onichtchenko, A., Abulrob, A., Ball, M., Ekiel, I., Pietrzynski, G., Stanimirovic, D., and Alakhov, V. (2005). Metastasis-associated protein S100A4 induces angiogenesis through interaction with annexin II and accelerated plasmin formation. J. Biol. Chem. 280, 20833- 20841.
52. Sharma, M., Koltowski, L., Ownbey, R., and Tuszynski, G. (2006). Angiogenesis-associated protein annexin II in breast cancer: selective expression in invasive breast cancer and contribution to tumor invasion and progression. Exp. Mol. Pathol. 81, 146-156.
53. Singh, P., Wu, H., Clark, C., and Owlia, A. (2006). Annexin II binds progastrin and gastrin-like peptides, and mediates growth factor effects of autocrine and exogenous gastrins on colon cancer and intestinal epithelial cells. Oncogene 26, 425-440.
54. Thiel, C., Weber, K., and Gerke, V. (1991). Characterization of a Ca2+ - binding site in human annexin II by site-directed mutagenesis. J. Biol. Chem. 266, 14732-14739.
55. Tran, J.T., Rosengarth, A., and Luecke, H. (2002). Cloning, purification and crystallization of full-length human annexin 2. Acta Crystallogr. D 58, 1854-1857.
56. Waisman, D.M. (1995). Annexin II tetramer: structure and function. Mol. Cell. Biochem. 149-150, 301-322.
57. Weng, X., Luecke, H., Song, I.S., Kang, D.S., Kim, S.-H., and Huber, R. (1993). Crystal structure of human annexin I at 2.5 Å resolution. Protein Sci. 2, 448-458.
58. Whitelegge, J.P., Gundersen, C.B., and Faull, K.F. (1998). Electrospray-ionization mass spectrometry of intact intrinsic membrane proteins. Protein Sci. 7, 1423-1430.
59. Whitelegge, J.P., le Coutre, J., Lee, J.C., Engel, C.K., Privé, G.G., Faull, K.F., and Kaback, H.R. (1999). Toward the bilayer proteome, electrospray ionization-mass spectrometry of large, intact transmembrane proteins. Proc. Natl. Acad. Sci. USA 96, 10695-10698.