Secreted CXCL12 (SDF-1) forms dimers under physiological conditions

Biochemical Journal

Volumn 442, Issue 2, 2012, Pages 433-442

  Ray, Paramita ^a   Lewin, Sarah A ^a   Mihalko, Laura Anne ^a   Lesher Perez, Sasha Cai ^a   Takayama, Shuichi ^a   Luker, Kathryn E ^a   Luker, Gary D ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Bioluminescence; Breast cancer; Chemokine; Chemokine receptor; Luciferase; Protein fragment complementation

Indexed keywords

BETA ARRESTIN 2; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR7; DIMER; HOMODIMER; MONOMER; STROMAL CELL DERIVED FACTOR 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOLUMINESCENCE; BREAST CANCER; CANCER CELL; CELL ASSAY; CELL FUNCTION; CHEMOTAXIS; EXTRACELLULAR SPACE; FEMALE; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MAMMAL CELL; MOUSE; NONHUMAN; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CHEMOKINE CXCL12; DIMERIZATION; EXTRACELLULAR SPACE; FEMALE; HEK293 CELLS; HUMANS; LUCIFERASES, FIREFLY; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASM TRANSPLANTATION; PROTEIN STRUCTURE, QUATERNARY; RECEPTORS, CXCR; RECEPTORS, CXCR4; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; TRANSPLANTATION, HETEROLOGOUS;

MAMMALIA;

EID: 84856859387     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20111341     Document Type: Article

References (52)

1. Tashiro, K., Tada, H., Heilker, R., Shirozu, M., Nakano, T. and Honjo, T. (1993) Signal sequence trap: a cloning strategy for secreted proteins and type I membrane proteins. Science 261, 600-603 (Pubitemid 23278369)
2. 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)
3. Tachibana, K., Hirota, S., Iizasa, H., Yoshida, H., Kawabata, K., Kataoka, Y., Kitamura, Y., Matsushima, K., Yoshida, N., Nishikawa, S. et al. (1998) The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 393, 591-594 (Pubitemid 28319250)
4. Chen, W., Tzeng, Y., Li, H., Tien, W. and Tsai, Y. (2010) Lung defects in neonatal and adult stromal-derived factor-1 conditional knockout mice. Cell Tissue Res. 342, 75-85
5. Pusic, I. and DiPersio, J. (2010) Update on clinical experience with AMD3100, an SDF-1/CXCL12-CXCR4 inhibitor, in mobilization of hematopoietic stem and progenitor cells. Curr. Opin. Hematol. 17, 319-326
6. Duda, D., Kozin, S., Kirkpatrick, N., Xu, L., Fukumura, D. and Jain, R. (2011) CXCL12 (SDF1α)-CXCR4/CXCR7 pathway inhibition: an emerging sensitizer for anticancer therapies? Clin. Cancer Res. 17, 2074-2080
7. Jiang, Y., Wu, X., Shi, B., Wu, W. and Yin, G. (2006) Expression of chemokine CXCL12 and its receptor CXCR4 in human epithelial ovarian cancer: an independent prognostic factor for tumor progression. Gynecol. Oncol. 103, 226-233 (Pubitemid 44374693)
8. Li, Y., Pan, Y., Wei, Y., Cheng, X., Zhou, B., Tan, M., Zhou, X., Xia, W., Hortobagyi, G., Yu, D. et al. (2004) Upregulation of CXCR4 is essential for HER2-mediated tumor metastasis. Cancer Cell 6, 459-469 (Pubitemid 39469982)
9. Zernecke, A., Bidhzhkov, K., Noels, H., Shaqdarsuren, E., Gan, L., Denecke, B., Hristov, M., Koppel, T., Jahantigh, M., Lutgens, E. et al. (2009) Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci. Signaling 2, ra81
10. Bogoslovsky, T., Spatz, M., Chaudhry, A., Maric, D., Luby, M., Frank, J. and Warach, S. (2011) Stromal-derived factor-1α correlates with circulating endothelial progenitor cells and with acute lesion volume in stroke patients. Stroke 42, 618-625
11. Santiago, B., Baleux, F., Palao, G., Gutierrez-Canas, I., Ramirez, J., Arenzana-Seisdedos, F. and Pablos, J. (2006) CXCL12 is displayed by rheumatoid endothelial cells through its basic amino-terminal motif on heparan sulfate proteoglycans. Arthritis Res. Ther. 8, R43
12. Cruz-Orengo, L., Holman, D., Dorsey, D., Zhou, L., Zhang, P., Wright, M., McCandless, E., Patel, J., Luker, G., Littman, D. et al. (2011) CXCR7 influences leukocyte entry into the CNS parenchyma by controlling abluminal CXCL12 abundance during autoimmunity. J. Exp. Med. 208, 327-329
13. Nesmelova, I., Sham, Y., Gao, J. and Mayo, K. (2008) CXC and CC chemokines form mixed heterodimers: association free energies from molecular dynamics simulations and experimental correlations. J. Biol. Chem. 283, 24155-24166
14. Nesmelova, I., Sham, Y., Dudek, A., van Eijk, L., Wu, G., Slungaard, A., Mortari, F., Griffioen, A. and Mayo, K. (2005) Platelet factor 4 and interleukin-8 CXC chemokine heterodimer formation modulates function at the quaternary structural level. J. Biol. Chem. 280, 4948-4958 (Pubitemid 40288670)
15. Dealwis, C., Fernandez, E., Thompson, D., Simon, R., Siani, M. and Lolis, E. (1998) Crystal structure of chemically synthesized [N33A] stromal cell-derived factor 1α, a potent ligand for the HIV-1 'fusin' coreceptor. Proc. Natl. Acad. Sci. U.S.A. 95, 6941-6946
16. Ohnishi, Y., Senda, T., Nandhagopal, N., Sugimoto, K., Shioda, T., Nagal, Y. and Mitsui, Y. (2000) Crystal structure of recombinant native SDF-1α with additional mutagenesis studies: an attempt at a more comprehensive interpretation of accumulated structure - activity relationship data. J. Interferon Cytokine Res. 20, 691-700 (Pubitemid 30636953)
17. Baryshnikova, O. and Sykes, B. (2006) Backbone dynamics of SDF-1α determined by NMR: interpretation in the presence of monomer-dimer equilibrium. Protein Sci. 15, 2568-2578 (Pubitemid 44771694)
18. Kjellen, L., Pettersson, I. and Hook, M. (1981) Cell-surface heparan sulfate: an intercalated membrane proteoglycan. Proc. Natl. Acad. Sci. U.S.A. 78, 5371-5375 (Pubitemid 12248588)
19. Veldkamp, C., Peterson, F., Pelzek, A. and Volkman, B. (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)
20. Murphy, J., Cho, Y., Sachpatzidis, A., Fan, C., Hodsdon, M. 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)
21. 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)
22. Veldkamp, C., Seibert, C., Peterson, F., De la Cruz, N., Haugner, 3rd, J. R., Basnet, H., Sakmar, T. and Volkman, B. (2008) Structural basis of CXCR4 sulfotyrosine recognition by the chemokine SDF-1/CXCL12. Sci. Signaling 16, ra4
23. Veldkamp, C., Ziarek, J., Su, J., Basnet, H., Lennertz, R., Weiner, J., Peterson, F., Baker, J. and Volkman, B. (2009) Monomeric structure of the cardioprotective chemokine SDF-1/CXCL12. Protein Sci. 18, 1359-1369
24. Luker, K., Gupta, M. and Luker, G. (2009) Bioluminescent CXCL12 fusion protein for cellular studies of CXCR4 and CXCR7. Biotechniques 47, 625-632
25. Luker, K., Mihalko, L., Schmidt, B., Lewin, S., Ray, P., Shcherbo, D., Chudakov, D. and Luker, G. (2011) In vivo imaging of ligand receptor binding with Gaussia luciferase complementation. Nat. Med., doi:10.1038/nm.2590
26. Shcherbo, D., Shemiakina, I., Ryabova, A., Luker, K., Schmidt, B., Souslova, E., Gorodnicheva, T., Strukova, L., Shidlovskiy, K., Britanova, O. et al. (2010) Near infrared fluorescent proteins. Nat. Methods 7, 827-829
27. Tung, Y., Hsiao, A., Allen, S., Torisawa, Y., Ho, M. and Takayama, S. (2011) High-throughput 3D spheroid culture and drug testing using a 384 hanging drop array. Analyst 136, 473-478
28. Luker, K., Gupta, M. and Luker, G. (2008) Imaging CXCR4 signaling with firefly luciferase complementation. Anal. Chem. 80, 5565-5573
29. Luker, K., Gupta, M., Steele, J., Foerster, B. and Luker, G. (2009) Imaging ligand-dependent activation of CXCR7. Neoplasia 11, 1022-1035
30. Tannous, B., Kim, D., Fernandez, J., Weissleder, R. and Breakefield, X. (2005) Codon-optimized Gaussia luciferase cDNA for mammalian gene expression in culture and in vivo. Mol. Ther. 11, 435-443 (Pubitemid 40277320)
31. Wurdinger, T., Badr, C., Pike, L., de Kleine, R., Weissleder, R., Breakefield, X. and Tannous, B. (2008) A secreted luciferase for ex-vivo monitoring of in vivo processes. Nat. Methods 5, 171-173 (Pubitemid 351181745)
32. Wang, A., Miralem, T. and Templeton, D. (1999) Heparan sulfate chains with antimitogenic properties arise from mesangial cell-surface proteoglycans. Metabolism 48, 1220-1229 (Pubitemid 29496067)
33. Suzuki, T., Kondo, C., Kanamori, T. and Inouye, S. (2011) Video-rate bioluminescence imaging of matrix metalloproteinase-2 secreted from a migrating cell. PLoS ONE 6, e25243
34. Remy, I. and Michnick, S. (2006) A highly sensitive protein-protein interaction assay based on Gaussia luciferase. Nat. Methods 3, 977-979 (Pubitemid 44782695)
35. Balabanian, K., Lagane, B., Infantino, S., Chow, K., Harriague, J., Moepps, B., Arenzana-Seisdedos, F., Thelen, M. and Bachelerie, F. (2005) The chemokine SDF-1/CXCL12 binds to and signals through the orphan receptor RDC1 in T lymphocytes. J. Biol. Chem. 280, 35760-35766 (Pubitemid 41532769)
36. Burns, J., Summers, B., Wang, Y., Melikian, A., Berahovich, R., Miao, Z., Penfold, M., Sunshine, M., Littman, D., Kuo, C. et al. (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)
37. Boldajipour, B., Mahabaleshwar, S., Kardash, E., Reichman-Fried, M., Blaser, H., Minina, S., Wilson, D., Xu, Q. and Raz, E. (2008) Control of chemokine-guided cell migration by ligand sequestration. Cell 132, 463-473 (Pubitemid 351191997)
38. Luker, K., Steele, J., Mihalko, L. and Luker, G. (2010) Constitutive and chemokine-dependent internalization and recycling of CXCR7 in breast cancer cells to degrade chemokine ligands. Oncogene 29, 4599-4610
39. Hall, J. and Korach, K. (2003) Stromal cell-derived factor 1, a novel target of estrogen receptor action, mediates the mitogenic effects of estradiol in ovarian and breast cancer cells. Mol. Endocrinol. 17, 792-803 (Pubitemid 36539573)
40. Miao, Z., Luker, K., Summers, B., Berahovich, R., Bhojani, M., Rehemtulla, A., Kleer, C., Essner, J., Nasevicius, A., Luker, G. et al. (2007) CXCR7 (RDC1) promotes breast and lung tumor growth in vivo and is expressed on tumor-associated vasculature. Proc. Natl. Acad. Sci. U.S.A. 104, 15735-15740 (Pubitemid 350035369)
41. Zabel, B., Wang, Y., Lewen, S., Berahovich, R., Penfold, M., Zhang, P., Powers, J., Summers, B., Miao, Z., Zhao, N. et al. (2009) Elucidation of CXCR7-mediated signaling events and inhibition of CXCR4-mediated tumor cell transendothelial migration by CXCR7 ligands. J. Immunol. 183, 3204-3211
42. Luker, K. E., Lewin, S. A., Mihalko, L. A., Schmidt, B. T., Winkler, J. S., Coggins, N. L., Thomas, D. G. and Luker, G. D. (2012) Scavenging of CXCL12 by CXCR7 promotes tumor growth and metastasis of CXCR4-positive breast cancer cells. Oncogene, in the press
43. Parameswaran, R., Yu, M., Lim, M., Groffen, J. and Heisterkamp, N. (2011) Combination of drug therapy in acute lymphoblastic leukemia with a CXCR4 antagonist. Leukemia 25, 1314-1323
44. Tamamura, H., Hori, A., Kanzaki, N., Hiramatsu, K., Mizumoto, M., Nakashima, H., Yamamoto, N., Otaka, A. and Fujii, N. (2003) T140 analogs as CXCR4 antagonists identified as anti-metastatic agents in the treatment of breast cancer. FEBS Lett. 550, 79-83 (Pubitemid 37281361)
45. Atluri, P. and Woo, Y. (2008) Pro-angiogenic cytokines as cardiovascular therapeutics: assessing the potential. BioDrugs 22, 209-222 (Pubitemid 351969829)
46. Ghadge, S., Muhlstedt, S., Ozcelik, C. and Bader, M. (2011) SDF-1α as a therapeutic stem cell homing factor in myocardial infarction. Pharmacol. Ther. 129, 97-108
47. Mbemba, E., Gluckman, J. and Gettegno, L. (2000) Glycan and glycosaminoglycan binding properties of stromal cell-derived factor (SDF)-1α. Glycobiology 10, 21-29 (Pubitemid 30122196)
48. Hamon, M., Mbemba, E., Charnaux, N., Slimani, H., Brule, S., Saffar, L., Vassy, R., Prost, C., Lievre, N., Starzec, N. et al. (2004) A syndecan-4/CXCR4 complex expressed on human primary lymphocytes and macrophages and HeLa cell line binds the CXC chemokine stromal cell-derived factor-1 (SDF-1). Glycobiology 14, 311-323 (Pubitemid 38655906)
49. Drury, L., Ziarek, J., Gravel, S., Veldkamp, C., Takekoshi, T., Hwang, S., Heveker, N., Volkman, B. and Dwinell, M. (2011) Monomeric and dimeric CXCL12 inhibit metastasis through distinct CXCR4 interactions and signaling pathways. Proc. Natl. Acad. Sci. U.S.A. 108, 17655-17660
50. Fong, A., Premont, R., Richarson, R., Yu, Y., Lefkowitz, R. and Patel, D. (2002) Defective lymphocyte chemotaxis in β-arrestin2- and GRK6-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 99, 7478-7483 (Pubitemid 34568716)
51. Sanchez-Alcaniz, J., Haege, S., Mueller, W., Pla, R., Mackay, F., Schulz, S., Lopez-Bendito, G., Stumm, R. and Marin, O. (2011) Cxcr7 controls neuronal migration by regulating chemokine responsiveness. Neuron 69, 77-90
52. Wang, Y., Li, G., Stanco, A., Long, J., Crawford, D., Potter, G., Pleasure, S., Behrens, T. and Rubenstein, J. (2011) CXCR4 and CXCR7 have distinct functions in regulating interneuron migration. Neuron 69, 61-76