Alternative C-terminal helix orientation alters chemokine function: Structure of the anti-angiogenic chemokine, CXCL4L1

Journal of Biological Chemistry

Volumn 288, Issue 19, 2013, Pages 13522-13533

  Kuo, Je Hung ^a   Chen, Ya Ping ^a   Liu, Jai Shin ^a   Dubrac, Alexandre ^c,d   Quemener, Cathy ^c   Prats, Hervé ^e   Bikfalvi, Andreas ^c,d   Wu, Wen Guey ^a,b   Sue, Shih Che ^a,b  

^a Institute of Bioinformatics and Structural Biology   (Taiwan)

^b NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^c UNIVERSITÉ DE BORDEAUX   (France)

^d INSERM U1029 ^*  (France)

^e CANCER RESEARCH CENTER OF TOULOUSE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-ANGIOGENIC ACTIVITY; ANTI-TUMORS; BINDING ABILITIES; GLYCOSAMINOGLYCANS; HELIX CONFORMATION; HELIX ORIENTATION; STRUCTURAL INFORMATION; X-RAY STRUCTURE;

BIOCHEMISTRY;

BIOLOGY;

ANGIOGENESIS INHIBITOR; CHEMOKINE; CXCL4L1 CHEMOKINE; GLYCOSAMINOGLYCAN; UNCLASSIFIED DRUG;

ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; HUMAN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN STRUCTURE; REGULATORY MECHANISM; STRUCTURE ANALYSIS; SURFACE PROPERTY;

ANGIOGENESIS; CHEMOKINES; CXCL4L1; HEPARIN; PLATELET FACTOR 4; PLATELETS; X-RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANGIOGENIC PROTEINS; CRYSTALLOGRAPHY, X-RAY; CYSTINE; DITHIOTHREITOL; HEPARIN; HUMANS; HYDROGEN BONDING; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; OXIDATION-REDUCTION; PLATELET FACTOR 4; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STABILITY; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; REDUCING AGENTS;

EID: 84877697801     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.455329     Document Type: Article

References (55)

1. Raman, D., Sobolik-Delmaire, T., and Richmond, A. (2011) Chemokines in health and disease. Exp. Cell Res. 317, 575-589
2. Keeley, E. C., Mehrad, B., and Strieter, R. M. (2011) Chemokines as mediators of tumor angiogenesis and neovascularization. Exp. Cell Res. 317, 685-690
3. Mukaida, N., and Baba, T. (2012) Chemokines in tumor development and progression. Exp. Cell Res. 318, 95-102
4. Bikfalvi, A. (2012) Angiogenesis and invasion in cancer. Handb. Clin. Neurol. 104, 35-43
5. Balkwill, F. R. (2012) The chemokine system and cancer. J. Pathol. 226, 148-157
6. Kiefer, F., and Siekmann, A. F. (2011) The role of chemokines and their receptors in angiogenesis. Cell. Mol. Life Sci. 68, 2811-2830
7. Bikfalvi, A., Moenner, M., Javerzat, S., North, S., and Hagedorn, M. (2011) Inhibition of angiogenesis and the angiogenesis/invasion shift. Biochem. Soc. Trans. 39, 1560-1564
8. Bikfalvi, A. (2009) Tumoral angiogenesis. Models, targets, and inhibition. J. Soc. Biol. 203, 167-170
9. Scholten, D. J., Canals, M., Maussang, D., Roumen, L., Smit, M. J., Wijtmans, M., de Graaf, C., Vischer, H. F., and Leurs, R. (2012) Pharmacological modulation of chemokine receptor function. Br. J. Pharmacol. 165, 1617-1643
10. Koelink, P. J., Overbeek, S. A., Braber, S., de Kruijf, P., Folkerts, G., Smit, M. J., and Kraneveld, A. D. (2012) Targeting chemokine receptors in chronic inflammatory diseases. An extensive review. Pharmacol. Ther. 133, 1-18
11. Van Sweringen, H. L., Sakai, N., Tevar, A. D., Burns, J. M., Edwards, M. J., and Lentsch, A. B. (2011)CXCchemokine signaling in the liver. Impact on repair and regeneration. Hepatology 54, 1445-1453
12. Flad, H. D., and Brandt, E. (2010) Platelet-derived chemokines. Pathophysiology and therapeutic aspects. Cell. Mol. Life Sci. 67, 2363-2386
13. Gleissner, C. A., von Hundelshausen, P., and Ley, K. (2008) Platelet chemokines in vascular disease. Arterioscler. Thromb. Vasc. Biol. 28, 1920-1927
14. Salanga, C. L., and Handel, T. M. (2011) Chemokine oligomerization and interactions with receptors and glycosaminoglycans. The role of structural dynamics in function. Exp. Cell Res. 317, 590-601
15. Zlotnik, A., and Yoshie, O. (2012) The chemokine superfamily revisited. Immunity 36, 705-716
16. Nomiyama, H., Osada, N., and Yoshie, O. (2010) The evolution of mammalian chemokine genes. Cytokine Growth Factor Rev. 21, 253-262
17. Balestrieri, M. L., Balestrieri, A., Mancini, F. P., and Napoli, C. (2008) Understanding the immunoangiostatic CXC chemokine network. Cardiovasc. Res. 78, 250-256
18. Allen, S. J., Crown, S. E., and Handel, T. M. (2007) Chemokine. Receptor structure, interactions, and antagonism. Annu. Rev. Immunol. 25, 787-820
19. Kowalska, M. A., Rauova, L., and Poncz, M. (2010) Role of the platelet chemokine platelet factor 4 (PF4) in hemostasis and thrombosis. Thromb. Res. 125, 292-296
20. Gleissner, C. A. (2012) Platelet-derived chemokines in atherogenesis. What's new? Curr. Vasc. Pharmacol. 10, 563-569
21. Koenen, R. R., and Weber, C. (2011) Chemokines. established and novel targets in atherosclerosis. EMBO Mol. Med. 3, 713-725
22. Aidoudi, S., and Bikfalvi, A. (2010) Interaction of PF4 (CXCL4) with the vasculature. A role in atherosclerosis and angiogenesis. Thromb. Haemost 104, 941-948
23. Vandercappellen, J., Van Damme, J., and Struyf, S. (2011) The role of the CXC chemokines platelet factor-4 (CXCL4/PF-4) and its variant (CXCL4L1/PF-4var) in inflammation, angiogenesis, and cancer. Cytokine Growth Factor Rev. 22, 1-18
24. Dubrac, A., Quemener, C., Lacazette, E., Lopez, F., Zanibellato, C., Wu, W. G., Bikfalvi, A., and Prats, H. (2010) Functional divergence between 2 chemokines is conferred by single amino acid change. Blood 116, 4703-4711
25. Aidoudi, S., Bujakowska, K., Kieffer, N., and Bikfalvi, A. (2008) The CXCchemokine CXCL4 interacts with integrins implicated in angiogenesis. PLoS One 3, e2657
26. Reilly, M. P., Taylor, S. M., Hartman, N. K., Arepally, G. M., Sachais, B. S., Cines, D. B., Poncz, M., and McKenzie, S. E. (2001) Heparin-induced thrombocytopenia/thrombosis in a transgenic mouse model requires human platelet factor 4 and platelet activation through FcγRIIA. Blood 98, 2442-2447
27. Pouplard, C., May, M. A., Iochmann, S., Amiral, J., Vissac, A. M., Marchand, M., and Gruel, Y. (1999) Antibodies to platelet factor 4-heparin after cardiopulmonary bypass in patients anticoagulated with unfractionated heparin or a low-molecular-weight heparin. clinical implications for heparin-induced thrombocytopenia. Circulation 99, 2530-2536
28. Yeaman, M. R., Yount, N. Y., Waring, A. J., Gank, K. D., Kupferwasser, D., Wiese, R., Bayer, A. S., and Welch, W. H. (2007) Modular determinants of antimicrobial activity in platelet factor-4 family kinocidins. Biochim. Biophys. Acta 1768, 609-619
29. Cole, A. M., Ganz, T., Liese, A. M., Burdick, M. D., Liu, L., and Strieter, R. M. (2001) Cutting edge. IFN-inducible ELR-CXC chemokines display defensin-like antimicrobial activity. J. Immunol. 167, 623-627
30. Auerbach, D. J., Lin, Y., Miao, H., Cimbro, R., Difiore, M. J., Gianolini, M. E., Furci, L., Biswas, P., Fauci, A. S., and Lusso, P. (2012) Identification of the platelet-derived chemokine CXCL4/PF-4 as a broad-spectrum HIV-1 inhibitor. Proc. Natl. Acad. Sci. U.S.A. 109, 9569-9574
31. Schwartzkopff, F., Grimm, T. A., Lankford, C. S., Fields, K., Wang, J., Brandt, E., and Clouse, K. A. (2009) Platelet factor 4 (CXCL4) facilitates human macrophage infection with HIV-1 and potentiates virus replication. Innate Immun. 15, 368-379
32. Struyf, S., Salogni, L., Burdick, M. D., Vandercappellen, J., Gouwy, M., Noppen, S., Proost, P., Opdenakker, G., Parmentier, M., Gerard, C., Sozzani, S., Strieter, R. M., and Van Damme, J. (2011) Angiostatic and chemotactic activities of the CXC chemokine CXCL4L1 (platelet factor-4 variant) are mediated by CXCR3. Blood 117, 480-488
33. de Jong, E. K., de Haas, A. H., Brouwer, N., van Weering, H. R., Hensens, M., Bechmann, I., Pratley, P., Wesseling, E., Boddeke, H. W., and Biber, K. (2008) Expression of CXCL4 in microglia in vitro and in vivo and its possible signaling through CXCR3. J. Neurochem. 105, 1726-1736
34. Fiore, M. M., and Mackie, I. J. (2009) Dual effect of platelet factor 4 on the activities of factor Xa. Biochem. Biophys. Res. Commun. 379, 1072-1075
35. Sarabi, A., Kramp, B. K., Drechsler, M., Hackeng, T. M., Soehnlein, O., Weber, C., Koenen, R. R., and Von Hundelshausen, P. (2011) CXCL4L1 inhibits angiogenesis and induces undirected endothelial cell migration without affecting endothelial cell proliferation and monocyte recruitment. J. Thromb. Haemost. 9, 209-219.
36. Struyf, S., Burdick, M. D., Peeters, E., Van den Broeck, K., Dillen, C., Proost, P., Van Damme, J., and Strieter, R. M. (2007) Platelet factor-4 variant chemokine CXCL4L1 inhibits melanoma and lung carcinoma growth and metastasis by preventing angiogenesis. Cancer Res. 67, 5940-5948
37. Struyf, S., Burdick, M. D., Proost, P., Van Damme, J., and Strieter, R. M. (2004) Platelets release CXCL4L1, a nonallelic variant of the chemokine platelet factor-4/CXCL4 and potent inhibitor of angiogenesis. Circ. Res. 95, 855-857
38. Vandercappellen, J., Liekens, S., Bronckaers, A., Noppen, S., Ronsse, I., Dillen, C., Belleri, M., Mitola, S., Proost, P., Presta, M., Struyf, S., and Van Damme, J. (2010) The COOH-terminal peptide of platelet factor-4 variant (CXCL4L1/PF-4var47-70) strongly inhibits angiogenesis and suppresses B16 melanoma growth in vivo. Mol. Cancer Res. 8, 322-334
39. Mayo, K. H., Roongta, V., Ilyina, E., Milius, R., Barker, S., Quinlan, C., La Rosa, G., and Daly, T. J. (1995) NMR solution structure of the 32-kDa platelet factor 4 ELR-motif N-terminal chimera. A symmetric tetramer. Biochemistry 34, 11399-11409
40. Zhang, X., Chen, L., Bancroft, D. P., Lai, C. K., and Maione, T. E. (1994) Crystal structure of recombinant human platelet factor 4. Biochemistry 33, 8361-8366
41. Bezzine, S., Koduri, R. S., Valentin, E., Murakami, M., Kudo, I., Ghomashchi, F., Sadilek, M., Lambeau, G., and Gelb, M. H. (2000) Exogenously added human group X secreted phospholipase A2 but not the group IB, IIA, and V enzymes efficiently release arachidonic acid from adherent mammalian cells. J. Biol. Chem. 275, 3179-3191
42. 2+-and heparan sulfate-dependent transcriptional regulation of endothelial cell adhesion molecules. J. Biol. Chem. 285, 37872-37883
43. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMR Pipe. A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
44. Goddard, T. D., and Kneller, D. G. SPARKY 3. University of California, San Francisco
45. Collaborative Computational Project, Number 4 (1994) The CCP4 suite. programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763
46. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography and NMR system. A new software suite for macromolecular structure determination. Acta Crystallogr. D. Biol. Crystallogr. 54, 905-921
47. Emsley, P., and Cowtan, K. (2004) Coot. Model-building tools for molecular graphics. Acta Crystallogr. D. Biol. Crystallogr. 60, 2126-2132
48. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX. A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D. Biol. Crystallogr. 66, 213-221
49. Laskowski, R. A. (2001) PDBsum. Summaries and analyses of PDB structures. Nucleic Acids Res. 29, 221-222
50. Lortat-Jacob, H., Grosdidier, A., and Imberty, A. (2002) Structural diversity of heparan sulfate binding domains in chemokines. Proc. Natl. Acad. Sci. U.S.A. 99, 1229-1234
51. Lasagni, L., Grepin, R., Mazzinghi, B., Lazzeri, E., Meini, C., Sagrinati, C., Liotta, F., Frosali, F., Ronconi, E., Alain-Courtois, N., Ballerini, L., Netti, G. S., Maggi, E., Annunziato, F., Serio, M., Romagnani, S., Bikfalvi, A., and Romagnani, P. (2007) PF-4/CXCL4 and CXCL4L1 exhibit distinct subcellular localization and a differentially regulated mechanism of secretion. Blood 109, 4127-4134
52. Nesmelova, I. V., Sham, Y., Gao, J., and Mayo, K. H. (2008) CXC and CC chemokines form mixed heterodimers. Association free energies from molecular dynamics simulations and experimental correlations. J. Biol. Chem. 283, 24155-24166
53. Koenen, R. R., von Hundelshausen, P., Nesmelova, I. V., Zernecke, A., Liehn, E. A., Sarabi, A., Kramp, B. K., Piccinini, A. M., Paludan, S. R., Kowalska, M. A., Kungl, A. J., Hackeng, T. M., Mayo, K. H., and Weber, C. (2009) Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice. Nat. Med. 15, 97-103
54. Gouwy, M., Struyf, S., Noppen, S., Schutyser, E., Springael, J. Y., Parmentier, M., Proost, P., and Van Damme, J. (2008) Synergy between coproduced CC and CXC chemokines in monocyte chemotaxis through receptor-mediated events. Mol. Pharmacol. 74, 485-495
55. Nesmelova, I. V., Sham, Y., Dudek, A. Z., van Eijk, L. I., Wu, G., Slungaard, A., Mortari, F., Griffioen, A. W., and Mayo, K. H. (2005) Platelet factor 4 and interleukin-8 CXC chemokine heterodimer formation modulates function at the quaternary structural level. J. Biol. Chem. 280, 4948-4958