Cxcl12 evolution - subfunctionalization of a ligand through altered interaction with the chemokine receptor

Development

Volumn 138, Issue 14, 2011, Pages 2909-2914

  Boldajipour, Bijan ^a,b,f   Doitsidou, Maria ^b,g   Tarbashevich, Katsiaryna ^a   Laguri, Cedric ^c   Yu, Shuizi Rachel ^d   Ries, Jonas ^d,h   Dumstrei, Karin ^b   Thelen, Sylvia ^e   Dörries, Julia ^b   Messerschmidt, Esther Maria ^a   Thelen, Marcus ^e   Schwille, Petra ^d   Brand, Michael ^d   Lortat Jacob, Hugues ^c   Raz, Erez ^a,b  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^c INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^d DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^e INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Switzerland)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g New York Presbyterian Morgan Stanley Children's Hospital   (United States)

^h ETH ZURICH   (Switzerland)

Author keywords

Cell migration; Chemokine; Cxcr4; Evolution; Germ cell; Zebrafish

Indexed keywords

AMINO ACID; CHEMOKINE RECEPTOR CXCR4; LIGAND;

ARTICLE; CELL MIGRATION; CONTROLLED STUDY; EMBRYO; EVOLUTION; GENE DUPLICATION; NONHUMAN; PARALOGY; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR AFFINITY; ZEBRA FISH;

AMINO ACID SUBSTITUTION; ANIMALS; CELL LINE; CELL MOVEMENT; CHEMOKINE CXCL12; EVOLUTION, MOLECULAR; GENE KNOCKDOWN TECHNIQUES; GERM CELLS; HUMANS; IN SITU HYBRIDIZATION; MICROSCOPY, CONFOCAL; RECEPTORS, CXCR4; SPECTROMETRY, FLUORESCENCE; ZEBRAFISH;

DANIO RERIO; VERTEBRATA;

EID: 79959475561     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.068379     Document Type: Article

References (37)

1. Aiuti, A., Webb, I., Bleul, C., Springer, T. and Gutierrez-Ramos, J. (1997). The chemokine SDF-1 is a chemoattractant for human CD34+ hematopoietic progenitor cells and provides a new mechanism to explain the mobilization of CD34+ progenitors to peripheral blood. J. Exp. Med. 185, 111-120.
2. Baysal, C. and Atilgan, A. R. (2001). Elucidating the structural mechanisms for biological activity of the chemokine family. Proteins 43, 150-160.
3. Blaser, H., Eisenbeiss, S., Neumann, M., Reichman-Fried, M., Thisse, B., Thisse, C. and Raz, E. (2005). Transition from non-motile behaviour to directed migration during early PGC development in zebrafish. J. Cell Sci. 118, 4027-4038.
4. Bleul, C. C., Farzan, M., Choe, H., Parolin, C., Clark-Lewis, I., Sodroski, J. and Springer, T. A. (1996). The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature 382, 829-833.
5. Boldajipour, B., Mahabaleshwar, H., Kardash, E., Reichman-Fried, M., Blaser, H., Minina, S., Wilson, D., Xu, Q. and Raz, E. (2008). Control of chemokineguided cell migration by ligand sequestration. Cell 132, 463-473.
6. Doitsidou, M., Reichman-Fried, M., Stebler, J., Koprunner, M., Dorries, J., Meyer, D., Esguerra, C. V., Leung, T. and Raz, E. (2002). Guidance of primordial germ cell migration by the chemokine SDF-1. Cell 111, 647-659.
7. 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.
8. He, X. and Zhang, J. (2005). Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 169, 1157-1164.
9. Kardash, E., Reichman-Fried, M., Maitre, J. L., Boldajipour, B., Papusheva, E., Messerschmidt, E. M., Heisenberg, C. P. and Raz, E. (2010). A role for Rho GTPases and cell-cell adhesion in single-cell motility in vivo. Nat. Cell Biol. 12, 47-53.
10. Knaut, H., Werz, C., Geisler, R. and Nusslein-Volhard, C. (2003). A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor. Nature 421, 279-282.
11. Knaut, H., Blader, P., Strahle, U. and Schier, A. F. (2005). Assembly of trigeminal sensory ganglia by chemokine signaling. Neuron 47, 653-666.
12. Kofuku, Y., Yoshiura, C., Ueda, T., Terasawa, H., Hirai, T., Tominaga, S., Hirose, M., Maeda, Y., Takahashi, H., Terashima, Y. et al. (2009). Structural basis of the interaction between chemokine stromal cell-derived factor-1/CXCL12 and its G-protein-coupled receptor CXCR4. J. Biol. Chem. 284, 35240-35250.
13. Köprunner, M., Thisse, C., Thisse, B. and Raz, E. (2001). A zebrafish nanosrelated gene is essential for the development of primordial germ cells. Genes Dev. 15, 2877-2885.
14. Lieberam, I., Agalliu, D., Nagasawa, T., Ericson, J. and Jessell, T. M. (2005). A Cxcl12-CXCR4 chemokine signaling pathway defines the initial trajectory of mammalian motor axons. Neuron 47, 667-679.
15. Minina, S., Reichman-Fried, M. and Raz, E. (2007). Control of receptor internalization, signaling level, and precise arrival at the target in guided cell migration. Curr. Biol. 17, 1164-1172.
16. Mizoguchi, T., Verkade, H., Heath, J. K., Kuroiwa, A. and Kikuchi, Y. (2008). Sdf1/Cxcr4 signaling controls the dorsal migration of endodermal cells during zebrafish gastrulation. Development 135, 2521-2529.
17. Molyneaux, K., Zinszner, H., Kunwar, P., Schaible, K., Stebler, J., Sunshine, M., O'Brien, W., Raz, E., Littman, D., Wylie, C. et al. (2003). The chemokine SDF1/CXCL12 and its receptor CXCR4 regulate mouse germ cell migration and survival. Development 130, 4279-4286.
18. Moreira, S., Stramer, B., Evans, I., Wood, W. and Martin, P. (2010). Prioritization of competing damage and developmental signals by migrating macrophages in the Drosophila embryo. Curr. Biol. 20, 464-470.
19. Muller, A., Homey, B., Soto, H., Ge, N., Catron, D., Buchanan, M. E., McClanahan, T., Murphy, E., Yuan, W., Wagner, S. N. et al. (2001). Involvement of chemokine receptors in breast cancer metastasis. Nature 410, 50-56.
20. Nair, S. and Schilling, T. F. (2008). Chemokine signaling controls endodermal migration during zebrafish gastrulation. Science 322, 89-92.
21. Oberlin, E., Amara, A., Bachelerie, F., Bessia, C., Virelizier, J. L., Arenzana-Seisdedos, F., Schwartz, O., Heard, J. M., Clark-Lewis, I., Legler, D. F. et al. (1996). The CXC chemokine SDF-1 is the ligand for LESTR/fusin and prevents infection by T-cell-line-adapted HIV-1. Nature 382, 833-835.
22. Orimo, A., Gupta, P. B., Sgroi, D. C., Arenzana-Seisdedos, F., Delaunay, T., Naeem, R., Carey, V. J., Richardson, A. L. and Weinberg, R. A. (2005). Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 121, 335-348.
23. Peled, A., Petit, I., Kollet, O., Magid, M., Ponomaryov, T., Byk, T., Nagler, A., Ben-Hur, H., Many, A., Shultz, L. et al. (1999). Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science 283, 845-848.
24. Proudfoot, A. E., Handel, T. M., Johnson, Z., Lau, E. K., LiWang, P., Clark-Lewis, I., Borlat, F., Wells, T. N. and Kosco-Vilbois, M. H. (2003). Glycosaminoglycan binding and oligomerization are essential for the in vivo activity of certain chemokines. Proc. Natl. Acad. Sci. USA 100, 1885-1890.
25. Richardson, B. E. and Lehmann, R. (2010). Mechanisms guiding primordial germ cell migration: strategies from different organisms. Nat. Rev. Mol. Cell Biol. 11, 37-49.
26. Ries, J., Yu, S. R., Burkhardt, M., Brand, M. and Schwille, P. (2009). Modular scanning FCS quantifies receptor-ligand interactions in living multicellular organisms. Nat. Methods 6, 643-645.
27. Rorth, P. (2011). Whence directionality: guidance mechanisms in solitary and collective cell migration. Dev. Cell 20, 9-18.
28. Siekmann, A. F., Standley, C., Fogarty, K. E., Wolfe, S. A. and Lawson, N. D. (2009). Chemokine signaling guides regional patterning of the first embryonic artery. Genes Dev. 23, 2272-2277.
29. Stebler, J., Spieler, D., Slanchev, K., Molyneaux, K. A., Richter, U., Cojocaru, V., Tarabykin, V., Wylie, C., Kessel, M. and Raz, E. (2004). Primordial germ cell migration in the chick and mouse embryo: the role of the chemokine SDF-1/CXCL12. Dev. Biol. 272, 351-361.
30. 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.
31. Thisse, C. and Thisse, B. (2008). High-resolution in situ hybridization to wholemount zebrafish embryos. Nat. Protoc. 3, 59-69.
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. Viola, A. and Luster, A. D. (2008). Chemokines and their receptors: drug targets in immunity and inflammation. Annu. Rev. Pharmacol. Toxicol. 48, 171-197.
34. Walters, K. B., Green, J. M., Surfus, J. C., Yoo, S. K. and Huttenlocher, A. (2010). Live imaging of neutrophil motility in a zebrafish model of WHIM syndrome. Blood 116, 2803-2811.
35. Wylie, C. (1999). Germ cells. Cell 96, 165-174.
36. Yu, S. R., Burkhardt, M., Nowak, M., Ries, J., Petrasek, Z., Scholpp, S., Schwille, P. and Brand, M. (2009). Fgf8 morphogen gradient forms by a source-sink mechanism with freely diffusing molecules. Nature 461, 533-536.
37. 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.