Characterization of a reduced form of plasma plasminogen as the precursor for angiostatin formation

Journal of Biological Chemistry

Volumn 289, Issue 5, 2014, Pages 2992-3000

  Butera, Diego ^a   Wind, Troels ^a   Lay, Angelina J ^a   Beck, Julia ^b   Castellino, Francis J ^b   Hogg, Philip J ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; COVALENT BONDS; CRYSTAL ATOMIC STRUCTURE; MASS SPECTROMETRY; PEPTIDES; SULFUR COMPOUNDS;

ALKYLATING AGENTS; CONFORMATIONAL CHANGE; DISULFIDE BONDS; FUNCTIONAL SIMILARITY; PEPTIDE BACKBONES; PHOSPHOGLYCERATE KINASE; SERINE PROTEASE; TUMOR ANGIOGENESIS;

REDUCTION;

ALKYLATING AGENT; ANGIOSTATIN; ANION; CYSTEINE; DISULFIDE; PHOSPHOGLYCERATE KINASE; PLASMIN; PLASMINOGEN; PROTEIN PRECURSOR; SULFUR; THIOL;

ALLOSTERISM; ARTICLE; CONFORMATIONAL TRANSITION; DISULFIDE BOND; GEOMETRY; HUMAN; MASS SPECTROMETRY; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN STRUCTURE;

ALLOSTERIC REGULATION; ANGIOGENESIS; DISULFIDE; PLASMIN; PLASMINOGEN;

ALLOSTERIC REGULATION; ANGIOSTATINS; CYSTEINE; DISULFIDES; FIBRINOLYSIN; HUMANS; OXIDATION-REDUCTION; PLASMINOGEN; PROTEIN PRECURSORS; PROTEIN STRUCTURE, TERTIARY; SULFHYDRYL COMPOUNDS;

EID: 84893501102     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.539924     Document Type: Article

References (57)

1. Lijnen, H. R. (2001) Elements of the fibrinolytic system. Ann. N. Y. Acad. Sci. 936, 226-236
2. O'Reilly, M. S., Holmgren, L., Shing, Y., Chen, C., Rosenthal, R. A., Moses, M., Lane, W. S., Cao, Y., Sage, E. H., and Folkman, J. (1994) Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell 79, 315-328
3. Stathakis, P., Fitzgerald, M., Matthias, L. J., Chesterman, C. N., and Hogg, P. J. (1997) Generation of angiostatin by reduction and proteolysis of plasmin: catalysis by a plasmin reductase secreted by cultured cells. J. Biol. Chem. 272, 20641-20645
4. Stathakis, P., Lay, A. J., Fitzgerald, M., Schlieker, C., Matthias, L. J., and Hogg, P. J. (1999) Angiostatin formation involves disulfide bond reduction and proteolysis in kringle 5 of plasmin. J. Biol. Chem. 274, 8910-8916
5. Hogg, P. J. (2003) Disulfide bonds as switches for protein function. Trends Biochem. Sci. 28, 210-214
6. Schmidt, B., Ho, L., and Hogg, P. J. (2006) Allosteric disulfide bonds. Biochemistry 45, 7429-7433
7. Schmidt, B., and Hogg, P. J. (2007) Search for allosteric disulfide bonds in NMR structures. BMC Struct. Biol. 7, 49
8. Cook, K. M., and Hogg, P. J. (2013) Post-translational control of protein function by disulfide bond cleavage. Antioxid. Redox Signal. 18, 1987-2015
9. Hogg, P. J. (2013) Targeting allosteric disulphide bonds in cancer. Nat. Rev. Cancer 13, 425-431
10. Lay, A. J., Jiang, X. M., Daly, E., Sun, L., and Hogg, P. J. (2002) Plasmin reduction by phosphoglycerate kinase is a thiol-independent process. J. Biol. Chem. 277, 9062-9068
11. Lay, A. J., Jiang, X. M., Kisker, O., Flynn, E., Underwood, A., Condron, R., and Hogg, P. J. (2000) Phosphoglycerate kinase acts in tumour angiogenesis as a disulphide reductase. Nature 408, 869-873
12. Daly, E. B., Wind, T., Jiang, X. M., Sun, L., and Hogg, P. J. (2004) Secretion of phosphoglycerate kinase from tumour cells is controlled by oxygensensing hydroxylases. Biochim. Biophys. Acta 1691, 17-22
13. Wang, J., Wang, J., Dai, J., Jung, Y., Wei, C. L., Wang, Y., Havens, A. M., Hogg, P. J., Keller, E. T., Pienta, K. J., Nor, J. E., Wang, C. Y., and Taichman, R. S. (2007) A glycolytic mechanism regulating an angiogenic switch in prostate cancer. Cancer Res. 67, 149-159
14. Wang, J., Ying, G., Jung, Y., Lu, J., Zhu, J., Pienta, K. J., and Taichman, R. S. (2010) Characterization of phosphoglycerate kinase-1 expression of stromal cells derived from tumor microenvironment in prostate cancer progression. Cancer Res. 70, 471-480
15. Zieker, D., Königsrainer, I., Tritschler, I., Löffler, M., Beckert, S., Traub, F., Nieselt, K., Bühler, S., Weller, M., Gaedcke, J., Taichman, R. S., Northoff, H., Brücher, B. L., and Königsrainer, A. (2010) Phosphoglycerate kinase 1 a promoting enzyme for peritoneal dissemination in gastric cancer. Int. J. Cancer 126, 1513-1520
16. Castellino, F. J., and Powell, J. R. (1981) Human plasminogen. Methods Enzymol. 80, 365-378
17. Lay, A. J., and Hogg, P. J. (2002) Measurement of reduction of disulfide bonds in plasmin by phosphoglycerate kinase. Methods Enzymol. 348, 87-92
18. Riddles, P. W., Blakeley, R. L., and Zerner, B. (1983) Reassessment of Ellman's reagent. Methods Enzymol. 91, 49-60
19. Sottrup-Jensen, L., Claeys, H., Zajdel, M., Petersen, T. E., and Magnusson, S. (1978) in Progress in Chemical Fibrinolysis and Thrombolysis (Davidson, J. F., Rowan, R. M., Samama, M. M., and Desnoyers, P. C., eds) Vol. 3, pp. 191-209, Raven Press, New York
20. Jacobson, G. R., Schaffer, M. H., Stark, G. R., and Vanaman, T. C. (1973) Specific chemical cleavage in high yield at the amino peptide bonds of cysteine and cystine residues. J. Biol. Chem. 248, 6583-6591
21. Wu, J., Gage, D. A., and Watson, J. T. (1996) A strategy to locate cysteine residues in proteins by specific chemical cleavage followed by matrixassisted laser desorption/ionization time-of-flight mass spectrometry. Anal. Biochem. 235, 161-174
22. Ganderton, T., Wong, J. W., Schroeder, C., and Hogg, P. J. (2011) Lateral self-association of VWF involves the Cys2431-Cys2453 disulfide/dithiol in the C2 domain. Blood 118, 5312-5318
23. Wong, J. W., and Hogg, P. J. (2010) Analysis of disulfide bonds in protein structures. J. Thromb. Haemost. 8, 2345
24. Kwon, M., Caplan, J. F., Filipenko, N. R., Choi, K. S., Fitzpatrick, S. L., Zhang, L., and Waisman, D. M. (2002) Identification of annexin II heterotetramer as a plasmin reductase. J. Biol. Chem. 277, 10903-10911
25. Wang, H., Schultz, R., Hong, J., Cundiff, D. L., Jiang, K., and Soff, G. A. (2004) Cell surface-dependent generation of angiostatin4. 5. Cancer Res. 64, 162-168
26. Mulligan-Kehoe, M. J., Wagner, R., Wieland, C., and Powell, R. (2001) A truncated plasminogen activator inhibitor-1 protein induces and inhibits angiostatin (kringles 1-3), a plasminogen cleavage product. J. Biol. Chem. 276, 8588-8596
27. Torchinski, Y. M. (1974) in Thiol and Disulfide Groups of Proteins (Dixon, H. B., ed.), p. 24, Consultants Bureau, New York
28. Law, R. H., Caradoc-Davies, T., Cowieson, N., Horvath, A. J., Quek, A. J., Encarnacao, J. A., Steer, D., Cowan, A., Zhang, Q., Lu, B. G., Pike, R. N., Smith, A. I., Coughlin, P. B., and Whisstock, J. C. (2012) The X-ray crystal structure of full-length human plasminogen. Cell Rep. 1, 185-190
29. Schwertassek, U., Balmer, Y., Gutscher, M., Weingarten, L., Preuss, M., Engelhard, J., Winkler, M., and Dick, T. P. (2007) Selective redox regulation of cytokine receptor signaling by extracellular thioredoxin-1. EMBO J. 26, 3086-3097
30. Nakamura, H. (2005) Thioredoxin and its related molecules: update 2005. Antioxid. Redox Signal. 7, 823-828
31. Yamada, Y., Nakamura, H., Adachi, T., Sannohe, S., Oyamada, H., Kayaba, H., Yodoi, J., and Chihara, J. (2003) Elevated serum levels of thioredoxin in patients with acute exacerbation of asthma. Immunol. Lett. 86, 199-205
32. Lillig, C. H., and Holmgren, A. (2007) Thioredoxin and related molecules: from biology to health and disease. Antioxid. Redox Signal. 9, 25-47
33. Kassam, G., Kwon, M., Yoon, C. S., Graham, K. S., Young, M. K., Gluck, S., and Waisman, D. M. (2001) Purification and characterization of A61: an angiostatin-like plasminogen fragment produced by plasmin autodigestion in the absence of sulfhydryl donors. J. Biol. Chem. 276, 8924-8933
34. Wu, H. L., Shi, G. Y., and Bender, M. L. (1987) Preparation and purification of microplasmin. Proc. Natl. Acad. Sci. U. S. A. 84, 8292-8295
35. Wu, H. L., Shi, G. Y., Wohl, R. C., and Bender, M. L. (1987) Structure and formation of microplasmin. Proc. Natl. Acad. Sci. U. S. A. 84, 8793-8795
36. Chivers, P. T., and Raines, R. T. (1997) General acid/base catalysis in the active site of Escherichia coli thioredoxin. Biochemistry 36, 15810-15816
37. Hansen, R. E., Østergaard, H., and Winther, J. R. (2005) Increasing the reactivity of an artificial dithiol-disulfide pair through modification of the electrostatic milieu. Biochemistry 44, 5899-5906
38. Giannakopoulos, B., and Krilis, S. A. (2013) The pathogenesis of the antiphospholipid syndrome. N Engl. J. Med. 368, 1033-1044
39. Ioannou, Y., Zhang, J. Y., Passam, F. H., Rahgozar, S., Qi, J. C., Giannakopoulos, B., Qi, M., Yu, P., Yu, D. M., Hogg, P. J., and Krilis, S. A. (2010) Naturally occurring free thiols within β2-glycoprotein I in vivo: nitrosylation, redox modification by endothelial cells, and regulation of oxidative stress-induced cell injury. Blood 116, 1961-1970
40. Passam, F. H, Rahgozar, S., Qi, M., Raftery, M. J., Wong, J. W., Tanaka, K., Ioannou, Y., Zhang, J. Y., Gemmell, R., Qi, J. C., Giannakopoulos, B., Hughes, W. E., Hogg, P. J., and Krilis, S. A. (2010) β2-Glycoprotein I is a substrate of thiol oxidoreductases. Blood 116, 1995-1997
41. Ioannou, Y., Zhang, J. Y., Qi, M., Gao, L., Qi, J. C., Yu, D. M., Lau, H, Sturgess, A. D., Vlachoyiannopoulos, P. G., Moutsopoulos, H. M., Rahman, A., Pericleous, C., Atsumi, T., Koike, T., Heritier, S., Giannakopoulos, B., and Krilis, S. A. (2011) Novel assays of thrombogenic pathogenicity in the antiphospholipid syndrome based on the detection of molecular oxidative modification of the major autoantigen β2-glycoprotein I. Arthritis Rheum. 63, 2774-2782
42. Crowley, S. D., and Coffman, T. M. (2012) Recent advances involving the renin-angiotensin system. Exp. Cell Res. 318, 1049-1056
43. Zhou, A., Carrell, R. W., Murphy, M. P., Wei, Z., Yan, Y., Stanley, P. L., Stein, P. E., Broughton Pipkin, F., and Read, R. J. (2010) A redox switch in angiotensinogen modulates angiotensin release. Nature 468, 108-111
44. Giannakopoulos, B., Gao, L., Qi, M., Wong, J. W., Yu, D. M., Vlachoyiannopoulos, P. G., Moutsopoulos, H. M., Atsumi, T., Koike, T., Hogg, P., Qi, J. C., and Krilis, S. A. (2012) Factor XI is a substrate for oxidoreductases: enhanced activation of reduced FXI and its role in antiphospholipid syndrome thrombosis. J. Autoimmun. 39, 121-129
45. Waldmann, T. A. (2006) The biology of interleukin-2 and interleukin-15: implications for cancer therapy and vaccine design. Nat. Rev. Immunol. 6, 595-601
46. Metcalfe, C., Cresswell, P., and Barclay, A. N. (2012) Interleukin-2 signalling is modulated by a labile disulfide bond in the CD132 chain of its receptor. Open Biol. 2, 110036
47. Cuneo, M. J., and London, R. E. (2010) Oxidation state of the XRCC1 N-terminal domain regulates DNA polymerase β binding affinity. Proc. Natl. Acad. Sci. U. S. A. 107, 6805-6810
48. Lohela, M., Bry, M., Tammela, T., and Alitalo, K. (2009) VEGFs and receptors involved in angiogenesis versus lymphangiogenesis. Curr. Opin. Cell Biol. 21, 154-165
49. Toivanen, P. I., Nieminen, T., Viitanen, L., Alitalo, A., Roschier, M., Jauhiainen, S., Markkanen, J. E., Laitinen, O. H., Airenne, T. T., Salminen, T. A., Johnson, M. S., Airenne, K. J., and Ylä-Herttuala, S. (2009) Novel vascular endothelial growth factor D variants with increased biological activity. J. Biol. Chem. 284, 16037-16048
50. Leppänen, V. M., Prota, A. E., Jeltsch, M., Anisimov, A., Kalkkinen, N, Strandin, T., Lankinen, H., Goldman, A., Ballmer-Hofer, K., and Alitalo, K. (2010) Structural determinants of growth factor binding and specificity by VEGF receptor 2. Proc. Natl. Acad. Sci. U. S. A. 107, 2425-2430
51. Davydova, N, Streltsov, V. A., Roufail, S., Lovrecz, G. O., Stacker, S. A., Adams, T. E., and Achen, M. G. (2012) Preparation of human vascular endothelial growth factor-D for structural and preclinical therapeutic studies. Protein Expr. Purif. 82, 232-239
52. Passam, F. H., Rahgozar, S., Qi, M., Raftery, M. J., Wong, J. W., Tanaka, K., Ioannou, Y., Zhang, J. Y., Gemmell, R., Qi, J. C, Giannakopoulos, B., Hughes, W. E., Hogg, P. J., and Krilis, S. A. (2010) Redox control of β2-glycoprotein I-von Willebrand factor interaction by thioredoxin-1. J. Thromb. Haemost. 8, 1754-1762
53. Leppänen, V. M., Jeltsch, M., Anisimov, A., Tvorogov, D., Aho, K., Kalkkinen, N., Toivanen, P., Ylä-Herttuala, S., Ballmer-Hofer, K., and Alitalo, K. (2011) Structural determinants of vascular endothelial growth factor-D receptor binding and specificity. Blood 117, 1507-1515
54. La Porte, S. L., Juo, Z. S., Vaclavikova, J., Colf, L. A., Qi, X., Heller, N. M., Keegan, A. D., and Garcia, K. C. (2008) Molecular and structural basis of cytokine receptor pleiotropy in the interleukin-4/13 system. Cell 132, 259-272
55. Stauber, D. J, Debler, E. W, Horton, P. A, Smith, K. A, and Wilson, I. A. (2006) Crystal structure of the IL-2 signaling complex: paradigm for aheterotrimeric cytokine receptor. Proc. Natl. Acad. Sci. U. S. A. 103, 2788-2793
56. Wang, X., Rickert, M., and Garcia, K. C. (2005) Structure of the quaternary complex of interleukin-2 with its a, β, and 7c receptors. Science 310, 1159-1163
57. Chiu, J., Wong, J. W., Gerometta, M., and Hogg, P. J. (2013) Mechanism of dimerisation of a recombinant mature vascular endothelial growth factor C. Biochemistry. 10.1021/bi401518b