The chemokine SDF-1 differentially regulates axonal elongation and branching in hippocampal neurons

Journal of Cell Science

Volumn 118, Issue 5, 2005, Pages 1071-1080

  Pujol, Fabien ^a   Kitabgi, Patrick ^a   Boudin, Hélène ^a,b  

^a HÔPITAL SAINT ANTOINE   (France)

^b INSERM   (France)

Author keywords

Axon; Cell culture; Chemokine; Development; Hippocampal neuron

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; STROMAL CELL DERIVED FACTOR 1;

ANIMAL CELL; ARTICLE; BRAIN DEVELOPMENT; BRAIN NERVE CELL; CELL MATURATION; CELL STRUCTURE; CELLULAR DISTRIBUTION; DENDRITE; EMBRYO PATTERN FORMATION; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; NERVE CELL DIFFERENTIATION; NERVE CELL STIMULATION; NERVE FIBER GROWTH; NERVE FIBER TRANSPORT; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT;

ANIMALS; AXONS; BLOTTING, WESTERN; CALCIUM; CELLS, CULTURED; CHEMOKINES, CXC; COS CELLS; DENDRITES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MICROSCOPY, PHASE-CONTRAST; NEURONS; RATS; RECEPTORS, CXCR4; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION;

ANIMALIA;

EID: 16844382247     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01694     Document Type: Article

References (51)

1. Albright, A. V., Shieh, J. T., Itoh, T., Lee, B., Pleasure, D., O'Connor, M. J., Doms, R. W. and Gonzalez-Scarano, F. (1999). Microglia express CCR5, CXCR4, and CCR3, but of these, CCR5 is the principal coreceptor for human immunodeficiency virus type 1 dementia isolates. J. Virol. 73, 205-213.
2. Amara, A., Gall, S. L., Schwartz, O., Salamero, J., Montes, M., Loetscher, P., Baggiolini, M., Virelizier, J. L. and Arenzana-Seisdedos, F. (1997). HIV coreceptor downregulation as antiviral principle: SDF-1alpha-dependent internalization of the chemokine receptor CXCR4 contributes to inhibition of HIV replication. J. Exp. Med. 186, 139-146.
3. Arakawa, Y., Bito, H., Furuyashiki, T., Tsuji, T., Takemoto-Kimura, S., Kimura, K., Nozaki, K., Hashimoto, N. and Narumiya, S. (2003). Control of axon elongation via an SDF-1alpha/Rho/mDia pathway in cultured cerebellar granule neurons. J. Cell Biol. 161, 381-391.
4. Bagnard, D., Lohrum, M., Uziel, D., Puschel, A. W. and Bolz, J. (1998). Semaphorins act as attractive and repulsive guidance signals during the development of cortical projections. Development 125, 5043-5053.
5. Bagri, A., Gurney, T., He, X., Zou, Y. R., Littman, D. R., Tessier-Lavigne, M. and Pleasure, S. J. (2002). The chemokine SDF1 regulates migration of dentate granule cells. Development 129 4249-4260.
6. Bagri, A., Cheng, H. J., Yaron, A., Pleasure, S. J. and Tessier-Lavigne, M. (2003). Stereotyped pruning of long hippocampal axon branches triggered by retraction inducers of the semaphorin family. Cell 113, 285-299.
7. Bajetto, A., Bonavia, R., Barbero, S., Piccioli, P., Costa, A., Florio, T. and Schettini, G. (1999). Glial and neuronal cells express functional chemokine receptor CXCR4 and its natural ligand stromal cell-derived factor 1. J. Neurochem. 73, 2348-2357.
8. Banisadr, G., Fontanges, P., Haour, F., Kitabgi, P., Rostene, W. and Melik Parsadaniantz, S. (2002). Neuroanatomical distribution of CXCR4 in adult rat brain and its localization in cholinergic and dopaminergic neurons. Eur. J. Neurosci. 16, 1661-1671.
9. Banisadr, G., Skrzydelski, D., Kitabgi, P., Rostene, W. and Parsadaniantz, S. M. (2003). Highly regionalized distribution of stromal cell-derived factor-1/CXCL12 in adult rat brain: constitutive expression in cholinergic, dopaminergic and vasopressinergic neurons. Eur. J. Neurosci. 18, 1593-1606.
10. Boudin, H., Sarret, P., Mazella, J., Schonbrunn, A. and Beaudet, A. (2000). Somatostatin-induced regulation of SST(2A) receptor expression and cellsurface availability in central neurons: role of receptor internalization. J. Neurosci. 20, 5932-5939.
11. Bredt, D. S. and Nicoll, R. A. (2003). AMPA receptor trafficking at excitatory synapses. Neuron 40, 361-379.
12. Chalasani, S. H., Sabelko, K. A., Sunshine, M. J., Littman, D. R. and Raper, J. A. (2003). A chemokine, SDF-1, reduces the effectiveness of multiple axonal repellents and is required for normal axon pathfinding. J. Neurosci. 23, 1360-1371.
13. Craig, A. M. (1998). Activity and synaptic receptor targeting: the long view. Neuron 21, 459-162.
14. Craig, A. M. and Banker, G. (1994). Neuronal polarity. Annu. Rev. Neurosci. 17, 267-310.
15. Csaba, Z., Bernard, V., Helboe, L., Bluet-Pajot, M. T., Bloch, B., Epelbaum, J. and Dournaud, P. (2001). In vivo internalization of the somatostatin sst2A receptor in rat brain: evidence for translocation of cell-surface receptors into the endosomal recycling pathway. Mol. Cell Neurosci. 17, 646-661.
16. Dent, E. W., Barnes, A. M., Tang, F. and Kalil, K. (2004). Netrin-1 and semaphorin 3A promote or inhibit cortical axon branching, respectively, by reorganization of the cytoskeleton. J. Neurosci. 24, 3002-3012.
17. Dorf, M. E., Berman, M. A., Tanabe, S., Heesen, M. and Luo, Y. (2000). Astrocytes express functional chemokine receptors. J. Neuroimmunol. 111, 109-121.
18. Dotti, C. G., Sullivan, C. A. and Banker, G. A. (1988). The establishment of polarity by hippocampal neurons in culture. J. Neurosci. 8, 1454-1468.
19. Dumartin, B., Jaber, M., Gonon, F., Caron, M. G., Giros, B. and Bloch, B. (2000). Dopamine tone regulates D1 receptor trafficking and delivery in striatal neurons in dopamine transporter-deficient mice. Proc. Natl. Acad. Sci. USA 97, 1879-1884.
20. Floridi, F., Trettel, F., di Bartolomeo, S., Ciotti, M. T. and Limatola, C. (2003). Signalling pathways involved in the chemotactic activity of CXCL12 in cultured rat cerebellar neurons and CHP100 neuroepithelioma cells. J. Neuroimmunol. 135, 38-46.
21. Goslin, K., Asmussen, H. and Banker, G. (1998). Rat hippocampal neurons in low density culture. In Culturing Nerve Cells (eds G. Banker and K. Goslin) pp. 339-370. Cambridge, MA, MIT Press.
22. Hasegawa, A., Yasukawa, M., Sakai, I. and Fujita, S. (2001). Transcriptional down-regulation of CXC chemokine receptor 4 induced by impaired association of transcription regulator YY1 with c-Myc in human herpesvirus 6-infected cells. J. Immunol. 166, 1125-1131.
23. Hatse, S., Princen, K., Bridger, G., de Clercq, E. and Schols, D. (2002). Chemokine receptor inhibition by AMD3100 is strictly confined to CXCR4. FEBS Lett. 527, 255-262.
24. Lavi, E., Strizki, J. M., Ulrich, A. M., Zhang, W., Fu, L., Wang, Q., O'Connor, M., Roxie, J. A. and Gonzalez-Scarano, F. (1997). CXCR-4 (Fusin), a co-receptor for the type 1 human immunodeficiency virus (HIV-1), is expressed in the human brain in a variety of cell types, including microglia and neurons. Am. J. Pathol. 151, 1035-1042.
25. Lu, Q., Sun, E. E., Klein, R. S. and Flanagan, J. G. (2001). Ephrin-B reverse signaling is mediated by a novel PDZ-RGS protein and selectively inhibits G protein-coupled chemoattraction. Cell 105, 69-79.
26. Lu, M., Grove, E.A. and Miller, R. J. (2002). Abnormal development of the hippocampal dertate gyrus in mice lacking the CXCR4 chemokine receptor. Proc. Natl. Acad. Sci. USA 99, 7090-7095.
27. 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. USA 95, 9448-9453.
28. Mandell, J. W. and Banker, G. A. (1995). The microtubule cytoskeleton and the development of neuronal polarity. Neurobiol. Aging 16, 229-238.
29. Markus, A., Zhong, J. and Snider, W. D. (2002). Raf and akt mediate distinct aspects of sensory axon growth. Neuron 35 65-76.
30. Martinez, M. C., Ochiishi, T., Majewski, M. and Kosik, K. S. (2003). Dual regulation of neuronal morphogenesis by a delta-catenin-cortactin complex and Rho. J. Cell Biol. 162, 99-111.
31. McGrath, K. E., Koniski, A. D., Maltby, K. M., McGann, J. K. and Palis, J. (1999). Embryonic expression and function of the chemokine SDF-1 and its receptor, CXCR4. Dev. Biol. 213, 442-456.
32. 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 tacking the CXC chemokine PBSF/SDF-1. Nature 382, 635-638.
33. Neumann, H., Schweigreiter, R., Yamashita, T., Rosenkranz, K., Wekerle, H. and Barde, Y. A. (2002). Tumor necrosis factor inhibits neurite outgrowth and branching of hippocampal neurons by a rho-dependent mechanism. J. Neurosci. 22, 854-862.
34. Nguyen Ba-Charvet, K. T., Brose, K., Marillat, V., Kidd, T., Goodman, C. S., Tessier-Lavigne, M., Sotelo, C. and Chedotal, A. (1999). Slit2-Mediated chemorepulsion and collapse of developing forebrain axons. Neuron 22, 463-473.
35. Orsini, M. J., Parent, J. L., Mundell, S. J., Benovic, J. L. and Marchese, A. (1999). Trafficking of the HIV coreceptor CXCR4. Role of arrestins and identification of residues in the c-terminal tail that mediate receptor internalization. J. Biol. Chem. 274, 31076-31086.
36. Peng, H., Huang, Y., Rose, J., Erichsen, D., Herek, S., Fujii, N., Tamamura, H. and Zheng, J. (2004). Stromal cell-derived factor 1-mediated CXCR4 signaling in rat and human cortical neural progenitor cells. J. Neurosci. Res. 76, 35-50.
37. Polleux, F., Giger, R. J., Ginty, D. D., Kolodkin, A. L. and Ghosh, A. (1998). Patterning of cortical efferent projections by semaphorin-neuropilin interactions. Science 282, 1904-1906.
38. Polleux, F., Morrow, T. and Ghosh, A. (2000). Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature 404, 567-573.
39. Signoret, N., Rosenkilde, M. M., Klasse, P. J., Schwartz, T. W., Malim, M. H., Hoxie, J. A. and Marsh, M. (1998). Differential regulation of CXCR4 and CCR5 endocytosis. J. Cell Sci. 111, 2819-2830.
40. Stumm, R. K., Rummel, J., Junker, V., Culmsee, C., Pfeiffer, M., Krieglstein, J., Hollt, V. and Schulz, S. (2002). A dual role for the SDF-1/CXCR4 chemokine receptor system in adult brain: isoform-selective regulation of SDF-1 expression modulates CXCR4-dependent neuronal plasticity and cerebral leukocyte recruitment after focal ischemia. J. Neurosci. 22, 5865-5878.
41. Stumm, R. K., Zhou, C., Ara, T., Lazarini, F., Dubois-Dalcq, M., Nagasawa, T., Hollt, V. and Schulz, S. (2003). CXCR4 regulates interneuron migration in the developing neocortex. J. Neurosci. 23, 5123-5130.
42. 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.
43. 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.
44. Tham, T. N., Lazarini, F., Franceschini, I. A., Lachapelle, F., Amara, A. and Dubois-Dalcq, M. (2001). Developmental pattern of expression of the alpha chemokine stromal cell-derived factor 1 in the rat central nervous system. Eur. J. Neurosci. 13, 845-856.
45. Tissir, F., Wang, C. E. and Goffinet, A. M. (2004). Expression of the chemokine receptor Cxcr4 mRNA during mouse brain development. Brain. Res. Dev. Brain Res. 149, 63-71.
46. Wang, K. H., Brose, K., Arnott, D., Kidd, T., Goodman, C. S., Henzel, W. and Tessier-Lavigne, M. (1999). Biochemical purification of a mammalian slit protein as a positive regulator of sensory axon elongation and branching. Cell 96, 771-784.
47. Westmoreland, S. V., Rottman, J. B., Williams, K. C., Lackner. A. A. and Sasseville, V. G. (1998). Chemokine receptor expression on resident and inflammatory cells in the brain of macaques with simian immunodeficiency virus encephalitis. Am. J. Pathol. 152, 659-665.
48. Whitford, K. L., Marillat, V., Stein, E., Goodman, C. S., Tessier-Lavigne, M., Chedotal, A. and Ghosh, A. (2002). Regulation of cortical dendrite development by Slit-Robo interactions. Neuron 33, 47-61.
49. Xiang, Y., Li, Y., Zhang, Z., Cui, K., Wang, S., Yuan, X. B., Wu, C. P., Poo, M. M. and Duan, S. (2002). Nerve growth cone guidance mediated by G protein-coupled receptors. Nat. Neurosci. 5, 843-848.
50. Zhu, Y., Yu, T., Zhang, X. C., Nagasawa, T., Wu, J. Y. and Rao, Y. (2002). Role of the chemokine SDF-1 as the meningeal attractant for embryonic cerebellar neurons. Nat. Neurosci. 5 719-720.
51. Zou, Y. R., Kottmann, A. H., Kuroda, M., Taniuchi, I. and Litfman, D. R. (1998). Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393, 595-599.