CXCR7 influences leukocyte entry into the CNS parenchyma by controlling abluminal CXCL12 abundance during autoimmunity

Journal of Experimental Medicine

Volumn 208, Issue 2, 2011, Pages 327-339

  Cruz Orengo, Lillian ^a   Holman, David W ^a   Dorsey, Denise ^a   Zhou, Liang ^b   Zhang, Penglie ^c   Wright, Melissa ^a   McCandless, Erin E ^a   Patel, Jigisha R ^a   Luker, Gary D ^d   Littman, Dan R ^e   Russell, John H ^a   Klein, Robyn S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c ChemoCentryx Inc   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CCX 771; CHEMOKINE RECEPTOR ANTAGONIST; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR7; GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 1BETA; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; BRAIN CELL; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DRUG DOSE INCREASE; DRUG DOSE REDUCTION; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATORY INFILTRATE; INTERNALIZATION; LEUKOCYTE; MALE; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PARENCHYMA; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANALYSIS OF VARIANCE; ANIMALS; AUTOIMMUNITY; BLOOD-BRAIN BARRIER; CELL MOVEMENT; CELL PROLIFERATION; CHEMOKINE CXCL12; CHEMOTAXIS, LEUKOCYTE; FLOW CYTOMETRY; GENE KNOCK-IN TECHNIQUES; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; POLYMERASE CHAIN REACTION; RECEPTORS, CXCR; SPINAL CORD; T-LYMPHOCYTES;

EID: 79951694551     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20102010     Document Type: Article

References (50)

1. Abbott, N.J., L. Rönnbäck, and E. Hansson. 2006. Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 7:41-53. doi:10.1038/nrn1824 (Pubitemid 41828930)
2. Afonso, P.V., S. Ozden, M.C. Prevost, C. Schmitt, D. Seilhean, B. Weksler, P.O. Couraud, A. Gessain, I.A. Romero, and P.E. Ceccaldi. 2007. Human blood-brain barrier disruption by retroviral-infected lymphocytes: role of myosin light chain kinase in endothelial tight-junction disorganization. J. Immunol. 179:2576-2583.
3. Argaw, A.T.,Y. Zhang, B.J. Snyder, M.L. Zhao, N. Kopp, S.C. Lee, C.S. Raine, C.F. Brosnan, and G.R. John. 2006. IL-1beta regulates blood-brain barrier permeability via reactivation of the hypoxia-angiogenesis program. J. Immunol. 177:5574-5584. (Pubitemid 44527632)
4. Axtell, R.C., B.A. de Jong, K. Boniface, L.F. van der Voort, R. Bhat, P. De Sarno, R. Naves, M. Han, F. Zhong, J.G. Castellanos, et al. 2010. T helper type 1 and 17 cells determine efficacy of interferon-beta in multiple sclerosis and experimental encephalomyelitis. Nat. Med. 16:406-412. doi:10.1038/nm.2110
5. Baron, J.L., J.A. Madri, N.H. Ruddle, G. Hashim, and C.A. Janeway Jr. 1993. Surface expression of alpha 4 integrin by CD4 T cells is required for their entry into brain parenchyma. J. Exp. Med. 177:57-68. doi:10.1084/jem.177. 1.57 (Pubitemid 23008085)
6. Bartholomäus, I., N. Kawakami, F. Odoardi, C. Schläger, D. Miljkovic, J.W. Ellwart, W.E. Klinkert, C. Flügel-Koch, T.B. Issekutz, H. Wekerle, and A. Flügel. 2009. Effector T cell interactions with meningeal vascular structures in nascent autoimmune CNS lesions. Nature. 462:94-98. doi:10.1038/nature08478
7. Belachew, S., R. Phan-Ba, E. Bartholomé, V. Delvaux, I. Hansen, P. Calay, K.E. Hafsi, G. Moonen, L. Tshibanda, and M. Vokaer. 2011. Natalizumab induces a rapid improvement of disability status and ambulation after failure of previous therapy in relapsing-remitting multiple sclerosis. Eur. J. Neurol. 18:240-245. doi:10.1111/j.1468-1331.2010.03112.x
8. Boldajipour, B., H. Mahabaleshwar, E. Kardash, M. Reichman-Fried, H. Blaser, S. Minina, D. Wilson, Q. Xu, and E. Raz. 2008. Control of chemokine-guided cell migration by ligand sequestration. Cell. 132:463-473. doi:10.1016/j.cell.2007.12.034 (Pubitemid 351191997)
9. Burns, J.M., B.C. Summers, Y. Wang, A. Melikian, R. Berahovich, Z. Miao, M.E. Penfold, M.J. Sunshine, D.R. Littman, C.J. Kuo, 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. doi:10.1084/jem.20052144 (Pubitemid 44352240)
10. Carbajal, K.S., C. Schaumburg, R. Strieter, J. Kane, and T.E. Lane. 2010. Migration of engrafted neural stem cells is mediated by CXCL12 signaling through CXCR4 in a viral model of multiple sclerosis. Proc. Natl. Acad. Sci. USA. 107:11068-11073. doi:10.1073/pnas.1006375107
11. Clifford, D.B. 2008. Natalizumab and PML: a risky business? Gut. 57:1347-1349. doi:10.1136/gut.2008.155770
12. Craigie, E.H. 1920. On the relative vasculatiry of various parts of the central nervous sytsem of the albino rat. J. Comp. Neurol. 31:429-464. doi:10.1002/cne.900310504
13. Fabis, M.J., T.W. Phares, R.B. Kean, H. Koprowski, and D.C. Hooper. 2008. Blood-brain barrier changes and cell invasion differ between therapeutic immune clearance of neurotrophic virus and CNS autoimmunity. Proc. Natl. Acad. Sci. USA. 105:15511-15516. doi:10.1073/pnas.0807656105
14. Frohman, E.M., M.K. Racke, and C.S. Raine. 2006. Multiple sclerosis - the plaque and its pathogenesis. N. Engl. J. Med. 354:942-955. doi:10.1056/ NEJMra052130
15. Gimenez, M.A., J.E. Sim, and J.H. Russell. 2004. TNFR1-dependent VCAM-1 expression by astrocytes exposes the CNS to destructive inflammation. J. Neuroimmunol. 151:116-125. doi:10.1016/j.jneuroim.2004.02.012 (Pubitemid 38624406)
16. Gimenez, M.A., J. Sim, A.S. Archambault, R.S. Klein, and J.H. Russell. 2006. A tumor necrosis factor receptor 1-dependent conversation between central nervous system-specific T cells and the central nervous system is required for inflammatory infiltration of the spinal cord. Am. J. Pathol. 168:1200-1209. doi:10.2353/ajpath.2006.050332
17. Huppert, J., D. Closhen, A. Croxford, R. White, P. Kulig, E. Pietrowski, I. Bechmann, B. Becher, H.J. Luhmann, A. Waisman, and C.R. Kuhlmann. 2010. Cellular mechanisms of IL-17-induced blood-brain barrier disruption. FASEB J. 24:1023-1034. doi:10.1096/fj.09-141978
18. Infantino, S., B. Moepps, and M. Thelen. 2006. Expression and regulation of the orphan receptor RDC1 and its putative ligand in human dendritic and B cells. J. Immunol. 176:2197-2207. (Pubitemid 43201667)
19. Kebir, H., K. Kreymborg, I. Ifergan, A. Dodelet-Devillers, R. Cayrol, M. Bernard, F. Giuliani, N. Arbour, B. Becher, and A. Prat. 2007. Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat. Med. 13:1173-1175. doi:10.1038/nm1651 (Pubitemid 47530640)
20. Klein, R.S., L. Izikson, T. Means, H.D. Gibson, E. Lin, R.A. Sobel, H.L. Weiner, and A.D. Luster. 2004. IFN-inducible protein 10/CXC chemokine ligand 10-independent induction of experimental autoimmune encephalomyelitis. J. Immunol. 172:550-559. (Pubitemid 38020512)
21. Klein, R.S., E. Lin, B. Zhang, A.D. Luster, J. Tollett, M.A. Samuel, M. Engle, and M.S. Diamond. 2005. Neuronal CXCL10 directs CD8+ T-cell recruitment and control of West Nile virus encephalitis. J. Virol. 79:11457-11466. doi:10.1128/JVI.79.17.11457-11466.2005 (Pubitemid 41170686)
22. Körner, H., D.S. Riminton, D.H. Strickland, F.A. Lemckert, J.D. Pollard, and J.D. Sedgwick. 1997. Critical points of tumor necrosis factor action in central nervous system autoimmune inflammation defined by gene targeting. J. Exp. Med. 186:1585-1590. doi:10.1084/jem.186.9.1585 (Pubitemid 27479818)
23. Kroenke, M.A., S.W. Chensue, and B.M. Segal. 2010. EAE mediated by a non-IFN-γ/non-IL-17 pathway. Eur. J. Immunol. 40:2340-2348. doi:10.1002/eji.201040489
24. Lees, J.R., P.T. Golumbek, J. Sim, D. Dorsey, and J.H. Russell. 2008. Regional CNS responses to IFN-γ determine lesion localization patterns during EAE pathogenesis. J. Exp. Med. 205:2633-2642. doi:10.1084/jem.20080155
25. Libert, F., M. Parmentier, A. Lefort, J.E. Dumont, and G. Vassart. 1990. Complete nucleotide sequence of a putative G protein coupled receptor: RDC1. Nucleic Acids Res. 18:1917. doi:10.1093/nar/18.7.1917 (Pubitemid 20139025)
26. Luker, K., M. Gupta, and G. Luker. 2009. Bioluminescent CXCL12 fusion protein for cellular studies of CXCR4 and CXCR7. Biotechniques. 47:625-632. doi:10.2144/000113126
27. Luker, K.E., J.M. Steele, L.A. Mihalko, P. Ray, and G.D. Luker. 2010. Constitutive and chemokine-dependent internalization and recycling of CXCR7 in breast cancer cells to degrade chemokine ligands. Oncogene. 29:4599-4610. doi:10.1038/onc.2010.212
28. Mahabaleshwar, H., B. Boldajipour, and E. Raz. 2008. Killing the messenger: The role of CXCR7 in regulating primordial germ cell migration. Cell Adh. Migr. 2:69-70. doi:10.4161/cam.2.2.6027
29. Man, S., E.E. Ubogu, and R.M. Ransohoff. 2007. Inflammatory cell migration into the central nervous system: a few new twists on an old tale. Brain Pathol. 17:243-250. doi:10.1111/j.1750-3639.2007.00067.x (Pubitemid 46466143)
30. McCandless, E.E., Q. Wang, B.M. Woerner, J.M. Harper, and R.S. Klein. 2006. CXCL12 limits inflammation by localizing mononuclear infiltrates to the perivascular space during experimental autoimmune encephalomyelitis. J. Immunol. 177:8053-8064. (Pubitemid 44846323)
31. McCandless, E.E., L. Piccio, B.M. Woerner, R.E. Schmidt, J.B. Rubin, A.H. Cross, and R.S. Klein. 2008a. Pathological expression of CXCL12 at the blood-brain barrier correlates with severity of multiple sclerosis. Am. J. Pathol. 172:799-808. doi:10.2353/ajpath.2008.070918 (Pubitemid 351354551)
32. McCandless, E.E., B. Zhang, M.S. Diamond, and R.S. Klein. 2008b. CXCR4 antagonism increases T cell trafficking in the central nervous system and improves survival from West Nile virus encephalitis. Proc. Natl. Acad. Sci. USA. 105:11270-11275. doi:10.1073/pnas.0800898105
33. McCandless, E.E., M. Budde, J.R. Lees, D. Dorsey, E. Lyng, and R.S. Klein. 2009. IL-1R signaling within the central nervous system regulates CXCL12 expression at the blood-brain barrier and disease severity during experimental autoimmune encephalomyelitis. J. Immunol. 183:613-620. doi:10.4049/jimmunol. 0802258
34. McFarland, H.F., and R. Martin. 2007. Multiple sclerosis: a complicated picture of autoimmunity. Nat. Immunol. 8:913-919. doi:10.1038/ni1507
35. Mueller, S.N., K.A. Hosiawa-Meagher, B.T. Konieczny, B.M. Sullivan, M.F. Bachmann, R.M. Locksley, R. Ahmed, and M. Matloubian. 2007. Regulation of homeostatic chemokine expression and cell trafficking during immune responses. Science. 317:670-674. doi:10.1126/science.1144830 (Pubitemid 47229967)
36. Nagase, H., M. Miyamasu, M. Yamaguchi, M. Imanishi, N.H. Tsuno, K. Matsushima, K. Yamamoto, Y. Morita, and K. Hirai. 2002. Cytokine-mediated regulation of CXCR4 expression in human neutrophils. J. Leukoc. Biol. 71:711-717.
37. Naumann, U., E. Cameroni, M. Pruenster, H. Mahabaleshwar, E. Raz, H.G. Zerwes, A. Rot, and M. Thelen. 2010. CXCR7 functions as a scavenger for CXCL12 and CXCL11. PLoS One. 5:e9175. doi:10.1371/journal.pone.0009175
38. Perrière, N., P. Demeuse, E. Garcia, A. Regina, M. Debray, J.P. Andreux, P. Couvreur, J.M. Scherrmann, J. Temsamani, P.O. Couraud, et al. 2005. Puromycin-based purification of rat brain capillary endothelial cell cultures. Effect on the expression of blood-brain barrier-specific properties. J. Neurochem. 93:279-289. doi:10.1111/j.1471-4159.2004.03020.x (Pubitemid 40547485)
39. Rajagopal, S., J. Kim, S. Ahn, S. Craig, C.M. Lam, N.P. Gerard, C. Gerard, and R.J. Lefkowitz. 2010. Beta-arrestin- but not G protein-mediated signaling by the "decoy" receptor CXCR7. Proc. Natl. Acad. Sci. USA. 107:628-632. doi:10.1073/pnas.0912852107
40. Schönemeier, B., A. Kolodziej, S. Schulz, S. Jacobs, V. Hoellt, and R. Stumm. 2008a. Regional and cellular localization of the CXCl12/SDF-1 chemokine receptor CXCR7 in the developing and adult rat brain. J. Comp. Neurol. 510:207-220. doi:10.1002/cne.21780
41. Schönemeier, B., S. Schulz, V. Hoellt, and R. Stumm. 2008b. Enhanced expression of the CXCl12/SDF-1 chemokine receptor CXCR7 after cerebral ischemia in the rat brain. J. Neuroimmunol. 198:39-45. doi:10.1016/j.jneuroim.2008.04. 010
42. Sierro, F., C. Biben, L. Martínez-Muñoz, M. Mellado, R.M. Ransohoff, M. Li, B. Woehl, H. Leung, J. Groom, M. Batten, et al. 2007. Disrupted cardiac development but normal hematopoiesis in mice deficient in the second CXCL12/SDF-1 receptor, CXCR7. Proc. Natl. Acad. Sci. USA. 104:14759-14764. doi:10.1073/pnas.0702229104 (Pubitemid 350003216)
43. Stromnes, I.M., L.M. Cerretti, D. Liggitt, R.A. Harris, and J.M. Goverman. 2008. Differential regulation of central nervous system autoimmunity by T(H)1 and T(H)17 cells. Nat. Med. 14:337-342. doi:10.1038/nm1715 (Pubitemid 351347910)
44. Stumm, R.K., J. Rummel, V. Junker, C. Culmsee, M. Pfeiffer, J. Krieglstein, V. Höllt, and S. Schulz. 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. (Pubitemid 35387631)
45. Sutton, C., C. Brereton, B. Keogh, K.H. Mills, and E.C. Lavelle. 2006. A crucial role for interleukin (IL)-1 in the induction of IL-17-producing T cells that mediate autoimmune encephalomyelitis. J. Exp. Med. 203: 1685-1691. doi:10.1084/jem.20060285 (Pubitemid 44036274)
46. Vajkoczy, P., M. Laschinger, and B. Engelhardt. 2001. Alpha4-integrin-VCAM-1 binding mediates G protein-independent capture of encephalitogenic T cell blasts to CNS white matter microvessels. J. Clin. Invest. 108:557-565. (Pubitemid 32777735)
47. Valentin, G., P. Haas, and D. Gilmour. 2007. The chemokine SDF1a coordinates tissue migration through the spatially restricted activation of Cxcr7 and Cxcr4b. Curr. Biol. 17:1026-1031. doi:10.1016/j.cub.2007.05.020 (Pubitemid 46899533)
48. Walters, M.J., Y. Wang, N. Lai, T. Baumgart, B.N. Zhao, D.J. Dairaghi, P. Bekker, L.S. Ertl, M.E. Penfold, J.C. Jaen, et al. 2010. Characterization of CCX282-B, an orally bioavailable antagonist of the CCR9 chemokine receptor, for treatment of inflammatory bowel disease. J. Pharmacol. Exp. Ther. 335:61-69. doi:10.1124/jpet.110.169714
49. Yednock, T.A., C. Cannon, L.C. Fritz, F. Sanchez-Madrid, L. Steinman, and N. Karin. 1992. Prevention of experimental autoimmune encephalomyelitis by antibodies against alpha 4 beta 1 integrin. Nature. 356:63-66. doi:10.1038/356063a0
50. Zabel, B.A., Y. Wang, S. Lewén, R.D. Berahovich, M.E. Penfold, P. Zhang, J. Powers, B.C. Summers, Z. Miao, B. Zhao, 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. doi:10.4049/jimmunol.0900269