Heparin oligosaccharides inhibit chemokine (CXC motif) ligand 12 (CXCL12) cardioprotection by binding orthogonal to the dimerization interface, promoting oligomerization, and competing with the chemokine (CXC motif) receptor 4 (CXCR4) N terminus

Journal of Biological Chemistry

Volumn 288, Issue 1, 2013, Pages 737-746

  Ziarek, Joshua J ^a   Veldkamp, Christopher T ^b   Zhang, Fuming ^a   Murray, Nathan J ^c   Kartz, Gabriella A ^a   Liang, Xinle ^c   Su, Jidong ^a   Baker, John E ^a   Linhardt, Robert J ^c   Volkman, Brian F ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b UNIVERSITY OF WISCONSIN WHITEWATER   (United States)

^c RENSSELAER POLYTECHNIC INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIAC ISCHEMIA; CARDIOPROTECTION; CELL MIGRATION; CELL SURFACES; CHEMOKINES; DIMER INTERFACE; EX-VIVO; EXPERIMENTAL MODELS; GLYCOSAMINOGLYCANS; HEPARIN BINDING; IN-VITRO; MYOCARDIAL INFARCTION; N-TERMINALS; NMR ANALYSIS; PROTECTIVE EFFECTS; RAT HEART; STRUCTURAL BASIS;

CELL MEMBRANES; DIMERIZATION; DIMERS; OLIGOMERIZATION; OLIGOSACCHARIDES; PEPTIDES;

POLYSACCHARIDES;

CHEMOKINE RECEPTOR CXCR4; GLYCOSAMINOGLYCAN; HEPARIN; STROMAL CELL DERIVED FACTOR 1;

AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; BINDING ASSAY; BINDING COMPETITION; BINDING SITE; BIOPHYSICS; CONTROLLED STUDY; DIMERIZATION; DISEASE MODEL; EX VIVO STUDY; HEART INFARCTION; HEART PROTECTION; IN VITRO STUDY; INHIBITION KINETICS; MOLECULAR MODEL; MOLECULAR RECOGNITION; MUTAGENESIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN MOTIF; RAT;

ANIMALS; BINDING SITES; BIOPHYSICS; CARDIOTONIC AGENTS; CHEMOKINE CXCL12; CHEMOKINES; DIMERIZATION; GLYCOSAMINOGLYCANS; HEPARIN; HUMANS; INHIBITORY CONCENTRATION 50; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MYOCARDIAL INFARCTION; OLIGOSACCHARIDES; PERFUSION; PROTEIN STRUCTURE, TERTIARY; RATS; RECEPTORS, CXCR4;

RATTUS;

EID: 84872066189     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.394064     Document Type: Article

References (46)

1. Fuster, V., and Hurst, J. W. (2004) Hurst's the Heart, 11th Ed., McGraw-Hill, Medical Publishing Division, New York
2. Antman, E. M., Anbe, D. T., Armstrong, P. W., Bates, E. R., Green, L. A., Hand, M., Hochman, J. S., Krumholz, H. M., Kushner, F. G., Lamas, G. A., Mullany, C. J., Ornato, J. P., Pearle, D. L., Sloan, M. A., Smith, S. C., Jr., Alpert, J. S., Anderson, J. L., Faxon, D. P., Fuster, V., Gibbons, R. J., Gregoratos, G., Halperin, J. L., Hiratzka, L. F., Hunt, S. A., and Jacobs, A. K. (2004) ACC/AHA guidelines for the management of patients with STelevation myocardial infarction-Executive summary. A report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Writing Committee to Revise the 1999 Guidelines for the Management of Patients With Acute Myocardial Infarction). Circulation 110, 588-636 (Pubitemid 39036178)
3. Rosenberg, R. D., and Damus, P. S. (1973) The purification and mechanism of action of human antithrombin-heparin cofactor. J. Biol. Chem. 248, 6490-6505
4. Handel, T. M., Johnson, Z., Crown, S. E., Lau, E. K., and Proudfoot, A. E. (2005) Regulation of protein function by glycosaminoglycans - as exemplified by chemokines. Annu. Rev. Biochem. 74, 385-410 (Pubitemid 40995512)
5. Johnson, Z., Proudfoot, A. E., and Handel, T. M. (2005) Interaction of chemokines and glycosaminoglycans. A new twist in the regulation of chemokine function with opportunities for therapeutic intervention. Cytokine Growth Factor Rev. 16, 625-636 (Pubitemid 41509199)
6. Proudfoot, A. E. (2006) The biological relevance of chemokine- proteoglycan interactions. Biochem. Soc. Trans. 34, 422-426
7. Nagasawa, T., Hirota, S., Tachibana, K., Takakura, N., Nishikawa, S., Kitamura, Y., Yoshida, N., Kikutani, H., and Kishimoto, T. (1996) Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 382, 635-638 (Pubitemid 26268957)
8. Burns, J. M., Summers, B. C., Wang, Y., Melikian, A., Berahovich, R., Miao, Z., Penfold, M. E., Sunshine, M. J., Littman, D. R., Kuo, C. J., Wei, K., McMaster, B. E., Wright, K., Howard, M. C., and Schall, T. J. (2006) A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development. J. Exp. Med. 203, 2201-2213 (Pubitemid 44352240)
9. Sierro, F., Biben, C., Martínez-Muñoz, L., Mellado, M., Ransohoff, R. M., Li, M., Woehl, B., Leung, H., Groom, J., Batten, M., Harvey, R. P., Martínez, A. C., Mackay, C. R., and Mackay, F. (2007) Disrupted cardiac development but normal hematopoiesis in mice deficient in the second CXCL12/SDF-1 receptor, CXCR7. Proc. Natl. Acad. Sci. U.S.A. 104, 14759-14764 (Pubitemid 350003216)
10. Zou, Y. R., Kottmann, A. H., Kuroda, M., Taniuchi, I., and Littman, D. R. (1998) Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393, 595-599 (Pubitemid 28319251)
11. Ma, Q., Jones, D., Borghesani, P. R., Segal, R. A., Nagasawa, T., Kishimoto, T., Bronson, R. T., and Springer, T. A. (1998) Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 95, 9448-9453 (Pubitemid 28506251)
12. Hu, X., Dai, S., Wu, W. J., Tan, W., Zhu, X., Mu, J., Guo, Y., Bolli, R., and Rokosh, G. (2007) Stromal cell derived factor-1α confers protection against myocardial ischemia/reperfusion injury. Role of the cardiac stromal cell derived factor-1α CXCR4 axis. Circulation 116, 654-663 (Pubitemid 47356350)
13. Saxena, A., Fish, J. E., White, M. D., Yu, S., Smyth, J. W., Shaw, R. M., DiMaio, J. M., and Srivastava, D. (2008) Stromal cell-derived factor-1α is cardioprotective after myocardial infarction. Circulation 117, 2224-2231
14. Proulx, C., El-Helou, V., Gosselin, H., Clement, R., Gillis, M. A., Villeneuve, L., and Calderone, A. (2007) Antagonism of stromal cell-derived factor-1α reduces infarct size and improves ventricular function after myocardial infarction. Pflugers Arch. 455, 241-250 (Pubitemid 47546792)
15. Segers, V. F., Tokunou, T., Higgins, L. J., MacGillivray, C., Gannon, J., and Lee, R. T. (2007) Local delivery of protease-resistant stromal cell derived factor-1 for stem cell recruitment after myocardial infarction. Circulation 116, 1683-1692 (Pubitemid 47537842)
16. Sasaki, T., Fukazawa, R., Ogawa, S., Kanno, S., Nitta, T., Ochi, M., and Shimizu, K. (2007) Stromal cell-derived factor-1α improves infarcted heart function through angiogenesis in mice. Pediatr. Int. 49, 966-971 (Pubitemid 350197152)
17. Koch, K. C., Schaefer, W. M., Liehn, E. A., Rammos, C., Mueller, D., Schroeder, J., Dimassi, T., Stopinski, T., and Weber, C. (2006) Effect of catheter-based transendocardial delivery of stromal cell-derived factor 1α on left ventricular function and perfusion in a porcine model of myocardial infarction. Basic Res. Cardiol. 101, 69-77 (Pubitemid 43323434)
18. Zhang, G., Nakamura, Y., Wang, X., Hu, Q., Suggs, L. J., and Zhang, J. (2007) Controlled release of stromal cell-derived factor-1α in situ increases c-kit+ cell homing to the infarcted heart. Tissue Eng. 13, 2063-2071 (Pubitemid 47294002)
19. Veldkamp, C. T., Ziarek, J. J., Su, J., Basnet, H., Lennertz, R., Weiner, J. J., Peterson, F. C., Baker, J. E., and Volkman, B. F. (2009) Monomeric structure of the cardioprotective chemokine SDF-1/CXCL12. Protein Sci. 18, 1359-1369
20. Penn, M. S., Zhang, M., Deglurkar, I., and Topol, E. J. (2004) Role of stem cell homing in myocardial regeneration. Int. J. Cardiol. 95, S23-S25 (Pubitemid 39178504)
21. Abbott, J. D., Huang, Y., Liu, D., Hickey, R., Krause, D. S., and Giordano, F. J. (2004) Stromal cell-derived factor-1α plays a critical role in stem cell recruitment to the heart after myocardial infarction but is not sufficient to induce homing in the absence of injury. Circulation 110, 3300-3305 (Pubitemid 39557491)
22. Yamaguchi, J., Kusano, K. F., Masuo, O., Kawamoto, A., Silver, M., Murasawa, S., Bosch-Marce, M., Masuda, H., Losordo, D. W., Isner, J. M., and Asahara, T. (2003) Stromal cell-derived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization. Circulation 107, 1322-1328 (Pubitemid 36314418)
23. Hattori, K., Heissig, B., Tashiro, K., Honjo, T., Tateno, M., Shieh, J. H., Hackett, N. R., Quitoriano, M. S., Crystal, R. G., Rafii, S., and Moore, M. A. (2001) Plasma elevation of stromal cell-derived factor-1 induces mobilization of mature and immature hematopoietic progenitor and stem cells. Blood 97, 3354-3360
24. Heissig, B., Hattori, K., Dias, S., Friedrich, M., Ferris, B., Hackett, N. R., Crystal, R. G., Besmer, P., Lyden, D., Moore, M. A., Werb, Z., and Rafii, S. (2002) Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 109, 625-637 (Pubitemid 34628725)
25. Fermas, S., Gonnet, F., Sutton, A., Charnaux, N., Mulloy, B., Du, Y., Baleux, F., and Daniel, R. (2008) Sulfated oligosaccharides (heparin and fucoidan) binding and dimerization of stromal cell-derived factor-1 (SDF-1/CXCL 12) are coupled as evidenced by affinity CE-MS analysis. Glycobiology 18, 1054-1064 (Pubitemid 352762840)
26. Veldkamp, C. T., Peterson, F. C., Pelzek, A. J., and Volkman, B. F. (2005) The monomer-dimer equilibrium of stromal cell-derived factor-1 (CXCL 12) is altered by pH, phosphate, sulfate, and heparin. Protein Sci. 14, 1071-1081 (Pubitemid 40389378)
27. Sadir, R., Baleux, F., Grosdidier, A., Imberty, A., and Lortat-Jacob, H. (2001) Characterization of the stromal cell-derived factor-1α-heparin complex. J. Biol. Chem. 276, 8288-8296
28. Amara, A., Lorthioir, O., Valenzuela, A., Magerus, A., Thelen, M., Montes, M., Virelizier, J. L., Delepierre, M., Baleux, F., Lortat-Jacob, H., and Arenzana-Seisdedos, F. (1999) Stromal cell-derived factor-1α associates with heparan sulfates through the first β-strand of the chemokine. J. Biol. Chem. 274, 23916-23925
29. Sadir, R., Imberty, A., Baleux, F., and Lortat-Jacob, H. (2004) Heparan sulfate/heparin oligosaccharides protect stromal cell-derived factor-1 (SDF-1)/CXCL12 against proteolysis induced by CD26/dipeptidyl peptidase IV. J. Biol. Chem. 279, 43854-43860 (Pubitemid 39390692)
30. Murphy, J. W., Cho, Y., Sachpatzidis, A., Fan, C., Hodsdon, M. E., and Lolis, E. (2007) Structural and functional basis of CXCL12 (stromal cell-derived factor-1α) binding to heparin. J. Biol. Chem. 282, 10018-10027 (Pubitemid 47104591)
31. 13C-Labeled heparan sulfate analogue as a tool to study protein/heparan sulfate interactions by NMR spectroscopy. Application to the CXCL12α chemokine. J. Am. Chem. Soc. 133, 9642-9645
32. Veldkamp, C. T., Seibert, C., Peterson, F. C., De la Cruz, N. B., Haugner, J. C., 3rd, Basnet, H., Sakmar, T. P., and Volkman, B. F. (2008) Structural basis of CXCR4 sulfotyrosine recognition by the chemokine SDF-1/CXCL12. Sci. Signal. 1, ra4
33. Baker, J. E., Curry, B. D., Olinger, G. N., and Gross, G. J. (1997) Increased tolerance of the chronically hypoxic immature heart to ischemia. Contribution of the KATP channel. Circulation 95, 1278-1285 (Pubitemid 27097841)
34. Baker, J. E., Konorev, E. A., Gross, G. J., Chilian, W. M., and Jacob, H. J. (2000) Resistance to myocardial ischemia in five rat strains. Is there a genetic component of cardioprotection? Am. J. Physiol. Heart Circ. Physiol. 278, H1395-H1400 (Pubitemid 30235519)
35. Keller, R. (2004) The Computer Aided Resonance Assignment/Tutorial, Cantina, Zurich, Switzerland
36. Zhang, F., Yang, B., Ly, M., Solakyildirim, K., Xiao, Z., Wang, Z., Beaudet, J. M., Torelli, A. Y., Dordick, J. S., and Linhardt, R. J. (2011) Structural characterization of heparins from different commercial sources. Anal. Bioanal. Chem. 401, 2793-2803
37. Veldkamp, C. T., Seibert, C., Peterson, F. C., Sakmar, T. P., and Volkman, B. F. (2006) Recognition of a CXCR4 sulfotyrosine by the chemokine stromal cell-derived factor-1α (SDF-1α/CXCL12). J. Mol. Biol. 359, 1400-1409 (Pubitemid 43903502)
38. Crump, M. P., Gong, J. H., Loetscher, P., Rajarathnam, K., Amara, A., Arenzana-Seisdedos, F., Virelizier, J. L., Baggiolini, M., Sykes, B. D., and Clark-Lewis, I. (1997) Solution structure and basis for functional activity of stromal cell-derived factor-1. Dissociation of CXCR4 activation from binding and inhibition of HIV-1. EMBO J. 16, 6996-7007 (Pubitemid 27520800)
39. Takekoshi, T., Ziarek, J. J., Volkman, B. F., and Hwang, S. T. (2012) A locked, dimeric CXCL12 variant effectively inhibits pulmonary metastasis of CXCR4-expressing melanoma cells due to enhanced serum stability. Mol. Cancer Ther. 11, 2516-2525
40. Seibert, C., Veldkamp, C. T., Peterson, F. C., Chait, B. T., Volkman, B. F., and Sakmar, T. P. (2008) Sequential tyrosine sulfation of CXCR4 by tyrosylprotein sulfotransferases. Biochemistry 47, 11251-11262
41. Thoma, R., Löffler, B., Stihle, M., Huber, W., Ruf, A., and Hennig, M. (2003) Structural basis of proline-specific exopeptidase activity as observed in human dipeptidyl peptidase-IV. Structure 11, 947-959 (Pubitemid 36966784)
42. Boonacker, E., and Van Noorden, C. J. (2003) The multifunctional or moonlighting protein CD26/DPPIV. Eur. J. Cell Biol. 82, 53-73 (Pubitemid 36285042)
43. Chien, C. H., Huang, L. H., Chou, C. Y., Chen, Y. S., Han, Y. S., Chang, G. G., Liang, P. H., and Chen, X. (2004) One site mutation disrupts dimer formation in human DPP-IV proteins. J. Biol. Chem. 279, 52338-52345
44. McQuibban, G. A., Butler, G. S., Gong, J. H., Bendall, L., Power, C., Clark-Lewis, I., and Overall, C. M. (2001) Matrix metalloproteinase activity inactivates the CXC chemokine stromal cell-derived factor-1. J. Biol. Chem. 276, 43503-43508
45. Delgado, M. B., Clark-Lewis, I., Loetscher, P., Langen, H., Thelen, M., Baggiolini, M., and Wolf, M. (2001) Rapid inactivation of stromal cellderived factor-1 by cathepsin G associated with lymphocytes. Eur. J. Immunol. 31, 699-707 (Pubitemid 32237105)
46. Valenzuela-Fernández, A., Planchenault, T., Baleux, F., Staropoli, I., Le-Barillec, K., Leduc, D., Delaunay, T., Lazarini, F., Virelizier, J. L., Chignard, M., Pidard, D., and Arenzana-Seisdedos, F. (2002) Leukocyte elastase negatively regulates Stromal cell-derived factor-1 (SDF-1)/CXCR4 binding and functions by N-terminal processing of SDF-1 and CXCR4. J. Biol. Chem. 277, 15677-15689 (Pubitemid 34967841)