The peculiarities of the SDF-1/CXCL12 system: In some cells, CXCR4 and CXCR7 sing solos, in others, they sing duets

Cell and Tissue Research

Volumn 355, Issue 2, 2014, Pages 239-253

  Puchert, Malte ^a   Engele, Jürgen ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

Chemokines; CXCR7; CXCXL12; Organ development; Tissue repair; Tumors

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR7; STROMAL CELL DERIVED FACTOR 1;

BLADDER CANCER; BONE DEVELOPMENT; BRAIN DEVELOPMENT; BREAST TUMOR; CARDIOVASCULAR SYSTEM; CENTRAL NERVOUS SYSTEM; COLON TUMOR; GERM CELL TUMOR; GONAD DEVELOPMENT; HEART DEVELOPMENT; HEMATOPOIESIS; HEMATOPOIETIC SYSTEM; HUMAN; IMMUNE SYSTEM; KIDNEY DEVELOPMENT; LIVER CELL CARCINOMA; LUNG TUMOR; MUSCLE DEVELOPMENT; NONHUMAN; OVARY TUMOR; PANCREAS TUMOR; PRIORITY JOURNAL; PROSTATE TUMOR; REVIEW; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SKIN TUMOR;

ANIMALS; CHEMOKINE CXCL12; HUMANS; NEOPLASMS; ORGAN SPECIFICITY; RECEPTORS, CXCR; RECEPTORS, CXCR4; SIGNAL TRANSDUCTION;

EID: 84896713600     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-013-1747-y     Document Type: Review

References (166)

1. Agarwal U, Ghalayini W, Dong F, Weber K, Zou YR, Rabbany SY, Rafii S, Penn MS (2010) Role of cardiac myocyte CXCR4 expression in development and left ventricular remodeling after acute myocardial infarction. Circ Res 107:667-676
2. Ara T, Nakamura Y, Egawa T, Sugiyama T, Abe K, Kishimoto T, Matsui Y, Nagasawa T (2003) Impaired colonization of the gonads by primordial germ cells in mice lacking a chemokine, stromal cell-derived factor-1 (SDF-1). Proc Natl Acad Sci U S A 100:5319-5323
3. Ara T, Tokoyoda K, Okamoto R, Koni PA, Nagasawa T (2005) The role of CXCL12 in the organ-specific process of artery formation. Blood 105:3155-3161
4. Askari AT, Unzek S, Popovic ZB, Goldman CK, Forudi F, Kiedrowski M, Rovner A, Ellis SG, Thomas JD, DiCorleto PE, Topol EJ, Penn MS (2003) Effect of stromal-cell-derived factor 1 on stem-cell homing and tissue regeneration in ischaemic cardiomyopathy. Lancet 362:697-703
5. Bajetto A, Barbieri F, Dorcaratto A, Barbero S, Daga A, Porcile C, Ravetti JL, Zona G, Spaziante R, Corte G, Schettini G, Florio T (2006) Expression of CXC chemokine receptors 1-5 and their ligands in human glioma tissues: role of CXCR4 and SDF1 in glioma cell proliferation and migration. Neurochem Int 49:423-432
6. Bakondi B, Shimada IS, Peterson BM, Spees JL (2011) SDF-1α secreted by human CD133-derived multipotent stromal cells promotes neural progenitor cell survival through CXCR7. Stem Cells Dev 20:1021-1029
7. Balabanian K, Lagane B, Infantino S, Chow KY, Harriague J, Moepps B, Arenzana-Seisdedos F, Thelen M, 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
8. Banisadr G, Fontanges P, Haour F, Kitabgi P, Rostene W, 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. Beider K, Begin M, Abraham M, Wald H, Weiss ID, Wald O, Pikarsky E, Zeira E, Eizenberg O, Galun E, Hardan I, Engelhard D, Nagler A, Peled A (2011) CXCR4 antagonist 4F-benzoyl-TN14003 inhibits leukemia and multiple myeloma tumor growth. Exp Hematol 39:282-292
10. Belmadani A, Jung H, Ren D, Miller RJ (2009) The chemokine SDF-1/CXCL12 regulates the migration of melanocyte progenitors in mouse hair follicles. Differentiation 77:395-411
11. Berahovich RD, Penfold ME, Schall TJ (2010a) Nonspecific CXCR7 antibodies. Immunol Lett 133:112-114
12. Berahovich RD, Zabel BA, Penfold ME, Lewen S, Wang Y, Miao Z, Gan L, Pereda J, Dias J, Slukvin II, McGrath KE, Jaen JC, Schall TJ (2010b) CXCR7 protein is not expressed on human or mouse leukocytes. J Immunol 185:5130-5139
13. Bezzi P, Domercq M, Brambilla L, Galli R, Schols D, De Clercq E, Vescovi A, Bagetta G, Kollias G, Meldolesi J, Volterra A (2001) CXCR4-activated astrocyte glutamate release via TNFalpha: amplification by microglia triggers neurotoxicity. Nat Neurosci 4:702-710
14. Bian XW, Yang SX, Chen JH, Ping YF, Zhou XD, Wang QL, Jiang XF, Gong W, Xiao HL, Du LL, Chen ZQ, Zhao W, Shi JQ, Wang JM (2007) Preferential expression of chemokine receptor CXCR4 by highly malignant human gliomas and its association with poor patient survival. Neurosurgery 61:570-578
15. Bleul CC, Farzan M, Choe H, Parolin C, Clark-Lewis I, Sodroski J, Springer TA (1996) The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature 382:829-833
16. Boldajipour B, Mahabaleshwar H, Kardash E, Reichman-Fried M, Blaser H, Minina S, Wilson D, Xu Q, Raz E (2008) Control of chemokine-guided cell migration by ligand sequestration. Cell 132:463-473
17. Broxmeyer HE (2008) Chemokines in hematopoiesis. Curr Opin Hematol 15:49-58
18. Brzoska E, Kowalewska M, Markowska-Zagrajek A, Kowalski K, Archacka K, Zimowska M, Grabowska I, Czerwińska AM, Czarnecka-Góra M, Stremińska W, Jańczyk-Ilach K, Ciemerych MA (2012) Sdf-1 (CXCL12) improves skeletal muscle regeneration via the mobilisation of Cxcr4 and CD34 expressing cells. Biol Cell 104:722-737
19. Buckingham M, Bajard L, Chang T, Daubas P, Hadchouel J, Meilhac S, Montarras D, Rocancourt D, Relaix F (2003) The formation of skeletal muscle: from somite to limb. J Anat 202:59-68
20. Burger JA, Bürkle A (2007) The CXCR4 chemokine receptor in acute and chronic leukaemia: a marrow homing receptor and potential therapeutic target. Br J Haematol 137:288-296
21. Burger JA, Kipps TJ (2006) CXCR4: a key receptor in the crosstalk between tumor cells and their microenvironment. Blood 107:1761-1767
22. Burns JM, Summers BC, Wang Y, Melikian A, Berahovich R, Miao Z, Penfold ME, Sunshine MJ, Littman DR, Kuo CJ, Wei K, McMaster BE, Wright K, Howard MC, Schall TJ (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
23. Calatozzolo C, Canazza A, Pollo B, Pierro ED, Ciusani E, Maderna E, Salce E, Sponza V, Frigerio S, Meco FD (2011) Expression of the new CXCL12 receptor, CXCR7, in gliomas. Cancer Biol Ther 11:242-253
24. Carbajal KS, Schaumburg C, Strieter R, Kane J, Lane TE (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 U S A 107:11068-11073
25. Carbajal KS, Miranda JL, Tsukamoto MR, Lane TE (2011) CXCR4 signaling regulates remyelination by endogenous oligodendrocyte progenitor cells in a viral model of demyelination. Glia 59:1813-1821
26. Cole KE, Strick CA, Paradis TJ, Ogborne KT, Loetscher M, Gladue RP, Lin W, Boyd JG, Moser B, Wood DE, Sahagan BG, Neote K (2009) Interferon-inducible T cell alpha chemoattractant (I-TAC): a novel non-ELR CXC chemokine with potent activity on activated T cells through selective high affinity binding to CXCR3. J Exp Med 187:2009-2021
27. Conley-Lacomb MK, Saliganan A, Kandagatla P, Chen YQ, Cher ML, Chinni SR (2013) PTEN loss mediated Akt activation promotes prostate tumor growth and metastasis via CXCL12/CXCR4 signaling. Mol Cancer 12:85
28. Crameri RM, Langberg H, Magnusson P, Jensen CH, Schroder HD, Olesen JL, Suetta C, Teisner B, Kjaer M (2004) Changes in satellite cells in human skeletal muscle after a single bout of high intensity exercise. J Physiol (Lond) 558:333-340
29. Crump MP, Gong JH, Loetscher P, Rajarathnam K, Amara A, Arenzana-Seisdedos F, Virelizier JL, Baggiolini M, Sykes BD, Clark-Lewis I (1997) Solution structure and basis for functional activity of stromal cell-derived factor-1; dissociation of CXCR4 activation from binding and inhibition of HIV-1. EMBO J 16:6996-7007
30. Darash-Yahana M, Pikarsky E, Abramovitch R, Zeira E, Pal B, Karplus R, Beider K, Avniel S, Kasem S, Galun E, Peled A (2004) Role of high expression levels of CXCR4 in tumor growth, vascularization, and metastasis. FASEB J 18:1240-1242
31. de Nigris F, Schiano C, Infante T, Napoli C (2012) CXCR4 inhibitors: tumor vasculature and therapeutic challenges. Recent Patents Anticancer Drug Discov 7:251-264
32. Decaillot FM, Kazmi MA, Lin Y, Ray-Saha S, Sakmar TP, Sachdev P (2011) CXCR7/CXCR4 heterodimer constitutively recruits beta-arrestin to enhance cell migration. J Biol Chem 286:32188-32197
33. Ding L, Morrison SJ (2013) Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature 495:231-235
34. do Carmo A, Patricio I, Cruz MT, Carvalheiro H, Oliveira CR, Lopes MC (2010) CXCL12/CXCR4 promotes motility and proliferation of glioma cells. Cancer Biol Ther 9:56-65
35. Dong F, Harvey J, Finan A, Weber K, Agarwal U, Penn MS (2012) Myocardial CXCR4 expression is required for mesenchymal stem cell mediated repair following acute myocardial infarction. Circulation 126:314-324
36. Dziembowska M, Tham TN, Lau P, Vitry S, Lazarini F, Dubois-Dalcq M (2005) A role for CXCR4 signaling in survival and migration of neural and oligodendrocyte precursors. Glia 50:258-269
37. Ehtesham M, Mapara KY, Stevenson CB, Thompson RC (2009) CXCR4 mediates the proliferation of glioblastoma progenitor cells. Cancer Lett 274:305-312
38. Gerrits H, van Ingen Schenau DS, Bakker NE, van Disseldorp AJ, Strik A, Hermens LS, Koenen TB, Krajnc-Franken MA, Gossen JA (2008) Early postnatal lethality and cardiovascular defects in CXCR7-deficient mice. Genesis 46:235-245
39. Gilbert DC, Chandler I, McIntyre A, Goddard NC, Gabe R, Huddart RA, Shipley J (2009) Clinical and biological significance of CXCL12 and CXCR4 expression in adult testes and germ cell tumours of adults and adolescents. J Pathol 217:94-102
40. Göttle P, Kremer D, Jander S, Odemis V, Engele J, Hartung HP, Küry P (2010) Activation of CXCR7 receptor promotes oligodendroglial cell maturation. Ann Neurol 68:915-924
41. Griffin CA, Apponi LH, Long KK, Pavlath GK (2010) Chemokine expression and control of muscle cell migration during myogenesis. J Cell Sci 123:3052-3060
42. Grymula K, Tarnowski M, Wysoczynski M, Drukala J, Barr FG, Ratajczak J, Kucia M, Ratajczak MZ (2010) Overlapping and distinct role of CXCR7-SDF-1/ITAC and CXCR4-SDF-1 axes in regulating metastatic behavior of human rhabdomyosarcomas. Int J Cancer 127:2554-2568
43. Guleng B, Tateishi K, Ohta M, Kanai F, Jazag A, Ijichi H, Tanaka Y, Washida M, Morikane K, Fukushima Y, Yamori T, Tsuruo T, Kawabe T, Miyagishi M, Taira K, Sata M, Omata M (2005) Blockade of the stromal cell-derived factor-1/CXCR4 axis attenuates in vivo tumor growth by inhibiting angiogenesis in a vascular endothelial growth factor-independent manner. Cancer Res 65:5864-5871
44. Guyon A, Nahon JL (2007) Multiple actions of the chemokine stromal cell-derived factor-1alpha on neuronal activity. J Mol Endocrinol 38:365-376
45. Haege S, Einer C, Thiele S, Mueller W, Nietzsche S, Lupp A, Mackay F, Schulz S, Stumm R (2012) CXC chemokine receptor 7 (CXCR7) regulates CXCR4 protein expression and capillary tuft development in mouse kidney. PLoS One 7:e42814
46. Hao M, Zheng J, Hou K, Wang J, Chen X, Lu X, Bo J, Xu C, Shen K, Wang J (2012) Role of chemokine receptor CXCR7 in bladder cancer progression. Biochem Pharmacol 84:204-214
47. Haribabu B, Richardson RM, Fisher I, Sozzani S, Peiper SC, Horuk R, Ali H, Snyderman R (1997) Regulation of human chemokine receptors CXCR4. Role of phosphorylation in desensitization and internalization. J Biol Chem 272:28726-28731
48. Hartmann TN, Grabovsky V, Pasvolsky R, Shulman Z, Buss EC, Spiegel A, Nagler A, Lapidot T, Thelen M, Alon R (2008) A crosstalk between intracellular CXCR7 and CXCR4 involved in rapid CXCL12-triggered integrin activation but not in chemokine-triggered motility of human T lymphocytes and CD34+ cells. J Leukoc Biol 84:1130-1140
49. Hattermann K, Mentlein R (2013) An infernal trio: the chemokine CXCL12 and its receptors CXCR4 and CXCR7 in tumor biology. Ann Anat 195:103-110
50. Hattermann K, Held-Feindt J, Lucius R, Müerköster SS, Penfold ME, Schall TJ, Mentlein R (2010) The chemokine receptor CXCR7 is highly expressed in human glioma cells and mediates antiapoptotic effects. Cancer Res 70:3299-3308
51. Heinisch S, Kirby LG (2010) SDF-1alpha/CXCL12 enhances GABA and glutamate synaptic activity at serotonin neurons in the rat dorsal raphe nucleus. Neuropharmacology 58:501-514
52. Heinrich EL, Lee W, Lu J, Lowy AM, Kim J (2012) Chemokine CXCL12 activates dual CXCR4 and CXCR7-mediated signaling pathways in pancreatic cancer cells. J Transl Med 10:68
53. Hernandez L, Magalhaes MA, Coniglio SJ, Condeelis JS, Segall JE (2011) Opposing roles of CXCR4 and CXCR7 in breast cancer metastasis. Breast Cancer Res 13:R128
54. Horuk R (2001) Chemokine receptors. Cytokine Growth Factor Rev 12:313-335
55. Humpert ML, Tzouros M, Thelen S, Bignon A, Levoye A, Arenzana-Seisdedos F, Balabanian K, Bachelerie F, Langen H, Thelen M (2012) Complementary methods provide evidence for the expression of CXCR7 on human B cells. Proteomics 12:1938-1948
56. Hunger C, Ödemis V, Engele J (2012) Expression and function of the SDF-1 chemokine receptors CXCR4 and CXCR7 during mouse limb muscle development and regeneration. Exp Cell Res 318:2178-2190
57. Imitola J, Raddassi K, Park KI, Mueller FJ, Nieto M, Teng YD, Frenkel D, Li J, Sidman RL, Walsh CA, Snyder EY, Khoury SJ (2004) Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. Proc Natl Acad Sci U S A 101:18117-18122
58. Infantino S, Moepps B, Thelen M (2006) Expression and regulation of the orphan receptor RDC1 and its putative ligand in human dendritic and B cells. J Immunol 176:2197-2207
59. Itoh T, Satou T, Ishida H, Nishida S, Tsubaki M, Hashimoto S, Ito H (2009) The relationship between SDF-1alpha/CXCR4 and neural stem cells appearing in damaged area after traumatic brain injury in rats. Neurol Res 31:90-102
60. Juarez J, Bradstock KF, Gottlieb DJ, Bendall LJ (2003) Effects of inhibitors of the chemokine receptor CXCR4 on acute lymphoblastic leukemia cells in vitro. Leukemia 17:1294-1300
61. Kadi F, Eriksson A, Holmner S, Butler-Browne GS, Thornell LE (1999) Cellular adaptation of the trapezius muscle in strength-trained athletes. Histochem Cell Biol 111:189-195
62. Karin N (2010) The multiple faces of CXCL12 (SDF-1alpha) in the regulation of immunity during health and disease. J Leukoc Biol 88:463-473
63. Khan MZ, Brandimarti R, Shimizu S, Nicolai J, Crowe E, Meucci O (2008) The chemokine CXCL12 promotes survival of postmitotic neurons by regulating Rb protein. Cell Death Differ 15:1663-1672
64. Kim HY, Hwang JY, Oh YS, Kim SW, Lee HJ, Yun HJ, Kim S, Yang YJ, Jo DY (2001) Differential effects of CXCR4 antagonists on the survival and proliferation of myeloid leukemia cells in vitro. Korean J Hematol 46:244-252
65. Klein RS, Rubin JB, Gibson HD, DeHaan EN, Alvarez-Hernandez X, Segal RA, Luster AD (2001) SDF-1 alpha induces chemotaxis and enhances sonic hedgehog-induced proliferation of cerebellar granule cells. Development 128:1971-1981
66. Lagane B, Chow KY, Balabanian K, Levoye A, Harriague J, Planchenault T, Baleux F, Gunera-Saad N, Arenzana-Seisdedos F, Bachelerie F (2008) CXCR4 dimerization and beta-arrestin-mediated signaling account for the enhanced chemotaxis to CXCL12 in WHIM syndrome. Blood 112:34-44
67. Lee E, Han J, Kim K, Choi H, Cho EG, Lee TR (2013) CXCR7 mediates SDF1-induced melanocyte migration. Pigment Cell Melanoma Res 26:58-66
68. Levoye A, Balabanian K, Baleux F, Bachelerie F, Lagane B (2009) CXCR7 heterodimerizes with CXCR4 and regulates CXCL12-mediated G protein signaling. Blood 113:6085-6093
69. Li M, Ransohoff RM (2008) Multiple roles of chemokine CXCL12 in the central nervous system: a migration from immunology to neurobiology. Prog Neurobiol 84:116-131
70. Li M, Chang CJ, Lathia JD, Wang L, Pacenta HL, Cotleur A, Ransohoff RM (2011) Chemokine receptor CXCR4 signaling modulates the growth factor-induced cell cycle of self-renewing and multipotent neural progenitor cells. Glia 59:108-118
71. Li M, Hale JS, Rich JN, Ransohoff RM, Lathia JD (2012a) Chemokine CXCL12 in neurodegenerative diseases: an SOS signal for stem cell-based repair. Trends Neurosci 35:619-628
72. Li X, Ma Q, Xu Q, Liu H, Lei J, Duan W, Bhat K, Wang F, Wu E, Wang Z (2012b) SDF-1/CXCR4 signaling induces pancreatic cancer cell invasion and epithelial-mesenchymal transition in vitro through non-canonical activation of hedgehog pathway. Cancer Lett 322:169-176
73. Libura J, Drukala J, Majka M, Tomescu O, Navenot JM, Kucia M, Marquez L, Peiper SC, Barr FG, Janowska-Wieczorek A, Ratajczak MZ (2002) CXCR4-SDF-1 signaling is active in rhabdomyosarcoma cells and regulates locomotion, chemotaxis, and adhesion. Blood 100:2597-2606
74. Liehn EA, Tuchscheerer N, Kanzler I, Drechsler M, Fraemohs L, Schuh A, Koenen RR, Zander S, Soehnlein O, Hristov M, Grigorescu G, Urs AO, Leabu M, Bucur I, Merx MW, Zernecke A, Ehling J, Gremse F, Lammers T, Kiessling F, Bernhagen J, Schober A, Weber C (2011) Double-edged role of the CXCL12/CXCR4 axis in experimental myocardial infarction. J Am Coll Cardiol 58:2415-2423
75. Lipfert J, Ödemis V, Wagner DC, Boltze J, Engele J (2013) CXCR4 and CXCR7 form a functional receptor unit for SDF-1/CXCL12 in primary rodent microglia. Neuropathol Appl Neurobiol 39:667-680
76. Liu Y, Carson-Walter EB, Cooper A, Winans BN, Johnson MD, Walter KA (2010) Vascular gene expression patterns are conserved in primary and metastatic brain tumors. J Neurooncol 99:13-24
77. Liu C, Pham K, Luo D, Reynolds BA, Hothi P, Foltz G, Harrison JK (2013a) Expression and functional heterogeneity of chemokine receptors CXCR4 and CXCR7 in primary patient-derived glioblastoma cells. PLoS One 8:e59750
78. Liu S, Jia X, Li C, Han X, Yan W, Xing Y (2013b) CXCR7 silencing attenuates cell adaptive response to stromal cell derived factor 1α after hypoxia. PLoS One 8:e55290
79. Lu M, Grove EA, Miller RJ (2002) Abnormal development of the hippocampal dentate gyrus in mice lacking the CXCR4 chemokine receptor. Proc Natl Acad Sci U S A 99:7090-7095
80. Luker KE, Steele JM, Mihalko LA, Ray P, Luker GD (2010) Constitutive and chemokine-dependent internalization and recycling of CXCR7 in breast cancer cells to degrade chemokine ligands. Oncogene 29:4599-4610
81. Luker KE, Lewin SA, Mihalko LA, Schmidt BT, Winkler JS, Coggins NL, Thomas DG, Luker GD (2012) Scavenging of CXCL12 by CXCR7 promotes tumor growth and metastasis of CXCR4-positive breast cancer cells. Oncogene 31:4750-4758
82. Ma Q, Jones D, Borghesani PR, Segal RA, Nagasawa T, Kishimoto T, Bronson RT, Springer TA (1998) Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc Natl Acad Sci U S A 95:9448-9453
83. Ma W, Liu Y, Ellison N, Shen J (2013) Induction of C-X-C chemokine receptor type 7 (CXCR7) switches stromal cell-derived factor-1 (SDF-1) signaling and phagocytic activity in macrophages linked to atherosclerosis. J Biol Chem 288:15481-15494
84. Maishi N, Ohga N, Hida Y, Akiyama K, Kitayama K, Osawa T, Onodera Y, Shinohara N, Nonomura K, Shindoh M, Hida K (2012) CXCR7: a novel tumor endothelial marker in renal cell carcinoma. Pathol Int 62:309-317
85. Mavier P, Martin N, Couchie D, Preaux AM, Laperche Y, Zafrani ES (2004) Expression of stromal cell-derived factor-1 and of its receptor CXCR4 in liver regeneration from oval cells in rat. Am J Pathol 165:1969-1977
86. Mazzinghi B, Ronconi E, Lazzeri E, Sagrinati C, Ballerini L, Angelotti ML, Parente E, Mancina R, Netti GS, Becherucci F, Gacci M, Carini M, Gesualdo L, Rotondi M, Maggi E, Lasagni L, Serio M, Romagnani S, Romagnani P (2008) Essential but differential role for CXCR4 and CXCR7 in the therapeutic homing of human renal progenitor cells. J Exp Med 205:479-490
87. McCaig AM, Cosimo E, Leach MT, Michie AM (2012) Dasatinib inhibits CXCR4 signaling in chronic lymphocytic leukaemia cells and impairs migration towards CXCL12. PLoS One 7:e48929
88. McGinn OJ, Marinov G, Sawan S, Stern PL (2012) CXCL12 receptor preference, signal transduction, biological response and the expression of 5T4 oncofoetal glycoprotein. J Cell Sci 125:5467-5478
89. Melchionna R, Di Carlo A, De Mori R, Cappuzzello C, Barberi L, Musaro A, Cencioni C, Fujii N, Tamamura H, Crescenzi M, Capogrossi MC, Napolitano M, Germani A (2010) Induction of myogenic differentiation by SDF-1 via CXCR4 and CXCR7 receptors. Muscle Nerve 41:828-835
90. Miao Z, Luker KE, Summers BC, Berahovich R, Bhojani MS, Rehemtulla A, Kleer CG, Essner JJ, Nasevicius A, Luker GD, Howard MC, Schall TJ (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
91. Momcilovic M, Mostarica-Stojkovic M, Miljkovic D (2012) CXCL12 in control of neuroinflammation. Immunol Res 52:53-63
92. Nagasawa T, Kikutani H, Kishimoto T (1994) Molecular cloning and structure of a pre-B-cell growth-stimulating factor. Proc Natl Acad Sci U S A 91:2305-2309
93. Nagasawa T, Hirota S, Tachibana K, Takakura N, Nishikawa S, Kitamura Y, Yoshida N, Kikutani H, 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
94. Naumann U, Cameroni E, Pruenster M, Mahabaleshwar H, Raz E, Zerwes HG, Rot A, Thelen M (2010) CXCR7 functions as a scavenger for CXCL12 and CXCL11. PLoS One 5:e9175
95. Oberlin E, Amara A, Bachelerie F, Bessia C, Virelizier JL, Arenzana-Seisdedos F, Schwartz O, Heard JM, Clark-Lewis I, Legler DF, Loetscher M, Baggiolini M, Moser B (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
96. Ödemis V, Lamp E, Pezeshki G, Moepps B, Schilling K, Gierschik P, Littman DR, Engele J (2005) Mice deficient in the chemokine receptor CXCR4 exhibit impaired limb innervation and myogenesis. Mol Cell Neurosci 30:494-505
97. Ödemis V, Boosmann K, Dieterlen MT, Engele J (2007) The chemokine SDF1 controls multiple steps of myogenesis through atypical PKCzeta. J Cell Sci 120:4050-4059
98. Ödemis V, Boosmann K, Heinen A, Küry P, Engele J (2010) CXCR7 is an active component of SDF-1 signalling in astrocytes and Schwann cells. J Cell Sci 123:1081-1088
99. Ödemis V, Lipfert J, Kraft R, Hajek P, Abraham G, Hattermann K, Mentlein R, Engele J (2012) The presumed atypical chemokine receptor CXCR7 signals through G(i/o) proteins in primary rodent astrocytes and human glioma cells. Glia 60:372-381
100. Okamoto K, Tajima H, Nakanuma S, Sakai S, Makino I, Kinoshita J, Hayashi H, Nakamura K, Oyama K, Nakagawara H, Fujita H, Takamura H, Ninomiya I, Kitagawa H, Fushida S, Fujimura T, Harada S, Wakayama T, Iseki S, Ohta T (2012) Angiotensin II enhances epithelial-to-mesenchymal transition through the interaction between activated hepatic stellate cells and the stromal cell-derived factor-1/CXCR4 axis in intrahepatic cholangiocarcinoma. Int J Oncol 41:573-582
101. Onoue T, Uchida D, Begum NM, Tomizuka Y, Yoshida H, Sato M (2006) Epithelial-mesenchymal transition induced by the stromal cell-derived factor-1/CXCR4 system in oral squamous cell carcinoma cells. Int J Oncol 29:1133-1138
102. Patel JR, McCandless EE, Dorsey D, Klein RS (2010) CXCR4 promotes differentiation of oligodendrocyte progenitors and remyelination. Proc Natl Acad Sci U S A 107:11062-11067
103. Perez AL, Bachrach E, Illigens BM, Jun SJ, Bagden E, Steffen L, Flint A, McGowan FX, Del Nido P, Montecino-Rodriguez E, Tidball JG, Kunkel LM (2009) CXCR4 enhances engraftment of muscle progenitor cells. Muscle Nerve 40:562-572
104. Rajagopal S, Rajagopal K, Lefkowitz RJ (2010a) Teaching old receptors new tricks: biasing seven-transmembrane receptors. Nat Rev Drug Discov 9:373-386
105. Rajagopal S, Kim J, Ahn S, Craig S, Lam CM, Gerard NP, Gerard C, Lefkowitz R (2010b) Beta-arrestin- but not G protein-mediated signaling by the decoy receptor CXCR7. Proc Natl Acad Sci U S A 107:628-632
106. Robin AM, Zhang ZG, Wang L, Zhang RL, Katakowski M, Zhang L, Wang Y, Zhang C, Chopp M (2006) Stromal cell-derived factor 1alpha mediates neural progenitor cell motility after focal cerebral ischemia. J Cereb Blood Flow Metab 26:125-134
107. Rozengurt E (2007) Mitogenic signaling pathways induced by G protein-coupled receptors. J Cell Physiol 213:589-602
108. Salmaggi A, Maderna E, Calatozzolo C, Gaviani P, Canazza A, Milanesi I, Silvani A, DiMeco F, Carbone A, Pollo B (2009) CXCL12, CXCR4 and CXCR7 expression in brain metastases. Cancer Biol Ther 8:1608-1614
109. Sanchez-Alcaniz JA, Haege S, Mueller W, Pla R, Mackay F, Schulz S, Lopez-Bendito G, Stumm R, Marin O (2011) Cxcr7 controls neuronal migration by regulating chemokine responsiveness. Neuron 69:77-90
110. Sanematsu F, Hirashima M, Laurin M, Takii R, Nishikimi A, Kitajima K, Ding G, Noda M, Murata Y, Tanaka Y, Masuko S, Suda T, Meno C, Côté JF, Nagasawa T, Fukui Y (2010) DOCK180 is a Rac activator that regulates cardiovascular development by acting downstream of CXCR4. Circ Res 107:1102-1105
111. Sasaki T, Fukazawa R, Ogawa S, Kanno S, Nitta T, Ochi M, Shimizu K (2007) Stromal cell-derived factor-1alpha improves infarcted heart function through angiogenesis in mice. Pediatr Int 49:966-971
112. Saxena A, Fish JE, White MD, Yu S, Smyth JW, Shaw RM, DiMaio JM, Srivastava D (2008) Stromal cell-derived factor-1alpha is cardioprotective after myocardial infarction. Circulation 117:2224-2231
113. Schimanski CC, Bahre R, Gockel I, Müller A, Frerichs K, Hörner V, Teufel A, Simiantonaki N, Biesterfeld S, Wehler T, Schuler M, Achenbach T, Junginger T, Galle PR, Moehler M (2006) Dissemination of hepatocellular carcinoma is mediated via chemokine receptor CXCR4. Br J Cancer 95:210-217
114. Schönemeier B, Kolodziej A, Schulz S, Jacobs S, Hoellt V, Stumm R (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
115. Schönemeier B, Schulz S, Hoellt V, Stumm R (2008b) Enhanced expression of the CXCl12/SDF-1 chemokine receptor CXCR7 after cerebral ischemia in the rat brain. J Neuroimmunol 198:39-45
116. Shimizu S, Brown M, Sengupta R, Penfold ME, Meucci O (2011) CXCR7 protein expression in human adult brain and differentiated neurons. PLoS One 6:e20680
117. Shyu WC, Lin SZ, Yen PS, Su CY, Chen DC, Wang HJ, Li H (2008) Stromal cell-derived factor-1 alpha promotes neuroprotection, angiogenesis, and mobilization/homing of bone marrow-derived cells in stroke rats. J Pharmacol Exp Ther 324:834-849
118. Sierro F, Biben C, Martinez-Munoz L, Mellado M, Ransohoff RM, Li M, Woehl B, Leung H, Groom J, Batten M, Harvey RP, Martínez-A C, Mackay CR, Mackay F (2007) Disrupted cardiac development but normal hematopoiesis in mice deficient in the second CXCL12/SDF-1 receptor, CXCR7. Proc Natl Acad Sci U S A 104:14759-14764
119. Singh RK, Lokeshwar BL (2011) The IL-8-regulated chemokine receptor CXCR7 stimulates EGFR signaling to promote prostate cancer growth. Cancer Res 71:3268-3277
120. Singh AK, Arya RK, Trivedi AK, Sanyal S, Baral R, Dormond O, Briscoe DM, Datta D (2013) Chemokine receptor trio: CXCR3, CXCR4 and CXCR7 crosstalk via CXCL11 and CXCL12. Cytokine Growth Factor Rev 24:41-49
121. Sison EA, Brown P (2011) The bone marrow microenvironment and leukemia: biology and therapeutic targeting. Expert Rev Hematol 4:271-283
122. Skrzydelski D, Guyon A, Dauge V, Rovère C, Apartis E, Kitabgi P, Nahon JL, Rostène W, Parsadaniantz SM (2007) The chemokine stromal cell-derived factor-1/CXCL12 activates the nigrostriatal dopamine system. J Neurochem 102:1175-1183
123. Stumm RK, Rummel J, Junker V, Culmsee C, Pfeiffer M, Krieglstein J, Höllt V, 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
124. Sugiyama T, Kohara H, Noda M, Nagasawa T (2006) Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25:977-988
125. Sun X, Cheng G, Hao M, Zheng J, Zhou X, Zhang J, Taichman RS, Pienta KJ, Wang J (2010) CXCL12/CXCR4/CXCR7 chemokine axis and cancer progression.Cancer Metastasis Rev 29:709-722
126. Tachibana K, Hirota S, Iizasa H, Yoshida H, Kawabata K, Kataoka Y, Kitamura Y, Matsushima K, Yoshida N, Nishikawa S, Kishimoto T, Nagasawa T (1998) The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 393:591-594
127. Takeuchi H, Natsume A, Wakabayashi T, Aoshima C, Shimato S, Ito M, Ishii J, Maeda Y, Hara M, Kim SU, Yoshida J (2007) Intravenously transplanted human neural stem cells migrate to the injured spinal cord in adult mice in an SDF-1- and HGF-dependent manner. Neurosci Lett 426:69-74
128. Tang JM, Wang JN, Zhang L, Zheng F, Yang JY, Kong X, Guo LY, Chen L, Huang YZ, Wan Y, Chen SY (2011) VEGF/SDF-1 promotes cardiac stem cell mobilization and myocardial repair in the infarcted heart. Cardiovasc Res 91:402-411
129. Tarnowski M, Liu R, Wysoczynski M, Ratajczak J, Kucia M, Ratajczak MZ (2010) CXCR7: a new SDF-1-binding receptor in contrast to normal CD34(+) progenitors is functional and is expressed at higher level in human malignant hematopoietic cells. Eur J Haematol 85:472-483
130. Theiss HD, Vallaster M, Rischpler C, Krieg L, Zaruba MM, Brunner S, Vanchev Y, Fischer R, Gröbner M, Huber B, Wollenweber T, Assmann G, Mueller-Hoecker J, Hacker M, Franz WM (2011) Dual stem cell therapy after myocardial infarction acts specifically by enhanced homing via the SDF-1/CXCR4 axis. Stem Cell Res 7:244-255
131. Thelen M, Thelen S (2008) CXCR7, CXCR4 and CXCL12: an eccentric trio? J Neuroimmunol 198:9-13
132. Tissir F, Wang CE, Goffinet AM (2004) Expression of the chemokine receptor Cxcr4 mRNA during mouse brain development. Brain Res Dev Brain Res 149:63-71
133. Tiveron MC, Boutin C, Daou P, Moepps B, Cremer H (2010) Expression and function of CXCR7 in the mouse forebrain. J Neuroimmunol 224:72-79
134. Totonchy JE, Osborn JM, Botto S, Clepper L, Moses AV (2013) Aberrant proliferation in CXCR7+ endothelial cells via degradation of the retinoblastoma protein. PLoS One 8:e69828
135. Tran PB, Miller RJ (2003) Chemokine receptors: signposts to brain development and disease. Nat Rev Neurosci 4:444-455
136. Trecki J, Brailoiu GC, Unterwald EM (2010) Localization of CXCR4 in the forebrain of the adult rat. Brain Res 1315:53-62
137. Tsuchiya A, Imai M, Kamimura H, Takamura M, Yamagiwa S, Sugiyama T, Nomoto M, Heike T, Nagasawa T, Nakahata T, Aoyagi Y (2012) Increased susceptibility to severe chronic liver damage in CXCR4 conditional knock-out mice. Dig Dis Sci 57:2892-2900
138. Vasyutina E, Stebler J, Brand-Saberi B, Schulz S, Raz E, Birchmeier C (2005) CXCR4 and Gab1 cooperate to control the development of migrating muscle progenitor cells. Genes Dev 19:2187-2198
139. Venkatakrishnan AJ, Deupi X, Lebon G, Tate CG, Schertler GF, Babu MM (2013) Molecular signatures of G-protein-coupled receptors. Nature 494:185-194
140. Wang J, Wang J, Sun Y, Song W, Nor JE, Wang CY, Taichman RS (2005) Diverse signaling pathways through the SDF-1/CXCR4 chemokine axis in prostate cancer cell lines leads to altered patterns of cytokine secretion and angiogenesis. Cell Signal 17:1578-1592
141. Wang J, Shiozawa Y, Wang J, Wang Y, Jung Y, Pienta KJ, Mehra R, Loberg R, Taichman RS (2008) The role of CXCR7/RDC1 as a chemokine receptor for CXCL12/SDF-1 in prostate cancer. J Biol Chem 283:4283-4294
142. Wang Y, Li G, Stanco A, Long JE, Crawford D, Potter GB, Pleasure SJ, Behrens T, Rubenstein JL (2011) CXCR4 and CXCR7 have distinct functions in regulating interneuron migration. Neuron 69:61-76
143. Wang H, Beaty N, Chen S, Qi CF, Masiuk M, Shin DM, Morse HC 3rd (2012a) The CXCR7 chemokine receptor promotes B-cell retention in the splenic marginal zone and serves as a sink for CXCL12. Blood 119:465-468
144. Wang K, Zhao X, Kuang C, Qian D, Wang H, Jiang H, Deng M, Huang L (2012b) Overexpression of SDF-1α enhanced migration and engraftment of cardiac stem cells and reduced infarcted size via CXCR4/PI3K pathway. PLoS One 7:e43922
145. Wang Y, Huang J, Li Y, Yang GY (2012c) Roles of chemokine CXCL12 and its receptors in ischemic stroke. Curr Drug Targets 13:166-172
146. Weisberg E, Azab AK, Manley PW, Kung AL, Christie AL, Bronson R, Ghobrial IM, Griffin JD (2012) Inhibition of CXCR4 in CML cells disrupts their interaction with the bone marrow microenvironment and sensitizes them to nilotinib. Leukemia 26:985-990
147. Xiang ZL, Zeng ZC, Tang ZY, Fan J, Zhuang PY, Liang Y, Tan YS, He J (2009) Chemokine receptor CXCR4 expression in hepatocellular carcinoma patients increases the risk of bone metastases and poor survival. BMC Cancer 9:176
148. Xu H, Wu Q, Dang S, Jin M, Xu J, Cheng Y, Pan M, Wu Y, Zhang C, Zhang Y (2011) Alteration of CXCR7 expression mediated by TLR4 promotes tumor cell proliferation and migration in human colorectal carcinoma. PLoS One 6:e27399
149. Xue TC, Chen RX, Han D, Chen J, Xue Q, Gao DM, Sun RX, Tang ZY, Ye SL (2012) Down-regulation of CXCR7 inhibits the growth and lung metastasis of human hepatocellular carcinoma cells with highly metastatic potential. Exp Ther Med 3:117-123
150. Yan X, Cai S, Xiong X, Sun W, Dai X, Chen S, Ye Q, Song Z, Jiang Q, Xu Z (2012) Chemokine receptor CXCR7 mediates human endothelial progenitor cells survival, angiogenesis, but not proliferation. J Cell Biochem 113:1437-1446
151. Yates TJ, Knapp J, Gosalbez M, Lokeshwar SD, Gomez CS, Benitez A, Ekwenna OO, Young EE, Manoharan M, Lokeshwar VB (2013) C-X-C chemokine receptor 7: a functionally associated molecular marker for bladder cancer. Cancer 119:61-71
152. Yu S, Crawford D, Tsuchihashi T, Behrens TW, Srivastava D (2011) The chemokine receptor CXCR7 functions to regulate cardiac valve remodeling. Dev Dyn 240:384-393
153. Yusuf F, Rehimi R, Moroşan-Puopolo G, Dai F, Zhang X, Brand-Saberi B (2006) Inhibitors of CXCR4 affect the migration and fate of CXCR4+ progenitors in the developing limb of chick embryos. Dev Dyn 235:3007-3015
154. Zabel BA, Wang Y, Lewén S, Berahovich RD, Penfold ME, Zhang P, Powers J, Summers BC, Miao Z, Zhao B, Jalili A, Janowska-Wieczorek A, Jaen JC, Schall TJ (2009) Elucidation of CXCR7-mediated signaling events and inhibition of CXCR4-mediated tumor cell transendothelial migration by CXCR7 ligands. J Immunol 183:3204-3211
155. Zhang M, Mal N, Kiedrowski M, Chacko M, Askari AT, Popovic ZB, Koc ON, Penn MS (2007) SDF-1 expression by mesenchymal stem cells results in trophic support of cardiac myocytes after myocardial infarction. FASEB J 21:3197-3207
156. Zhang SS, Han ZP, Jing YY, Tao SF, Li TJ, Wang H, Wang Y, Li R, Yang Y, Zhao X, Xu XD, Yu ED, Rui YC, Liu HJ, Zhang L, Wei LX (2012a) CD133(+)CXCR4(+) colon cancer cells exhibit metastatic potential and predict poor prognosis of patients. BMC Med 10:85
157. Zhang Y, Patel S, Abdelouahab H, Wittner M, Willekens C, Shen S, Betems A, Joulin V, Opolon P, Bawa O, Pasquier F, Ito M, Fujii N, Gonin P, Solary E, Vainchenker W, Coppo P, De Botton S, Louache F (2012b) CXCR4 inhibitors selectively eliminate CXCR4-expressing human acute myeloid leukemia cells in NOG mouse model. Cell Death Dis 3:e396
158. Zhao Y, Tan Y, Xi S, Li Y, Li C, Cui J, Yan X, Li X, Wang G, Li W, Cai L (2013) A novel mechanism by which SDF-1β protects cardiac cells from palmitate-induced endoplasmic reticulum stress and apoptosis via CXCR7 and AMPK/p38 MAPK-mediated interleukin-6 generation. Diabetes 62:2545-2558
159. Zheng K, Li HY, Su XL, Wang XY, Tian T, Li F, Ren GS (2010) Chemokine receptor CXCR7 regulates the invasion, angiogenesis and tumor growth of human hepatocellular carcinoma cells. J Exp Clin Cancer Res 29:31
160. Zhou Y, Larsen PH, Hao C, Yong VW (2002) CXCR4 is a major chemokine receptor on glioma cells and mediates their survival. J Biol Chem 277:49481-49487
161. Zhu Y, Murakami F (2012) Chemokine CXCL12 and its receptors in the developing central nervous system: emerging themes and future perspectives. Dev Neurobiol 72:1349-1362
162. Zhu W, Liang G, Huang Z, Doty SB, Boskey AL (2011) Conditional inactivation of the CXCR4 receptor in osteoprecursors reduces postnatal bone formation due to impaired osteoblast development. J Biol Chem 286:26794-26805
163. Zhu B, Xu D, Deng X, Chen Q, Huang Y, Peng H, Li Y, Jia B, Thoreson WB, Ding W, Ding J, Zhao L, Wang Y, Wavrin KL, Duan S, Zheng J (2012) CXCL12 enhances human neural progenitor cell survival through a CXCR7- and CXCR4-mediated endocytotic signaling pathway. Stem Cells 30:2571-2583
164. Zimmerman NP, Vongsa RA, Faherty SL, Salzman NH, Dwinell MB (2011) Targeted intestinal epithelial deletion of the chemokine receptor CXCR4 reveals important roles for extracellular-regulated kinase-1/2 in restitution. Lab Invest 91:1040-1055
165. Zlotnik A, Burkhardt AM, Homey B (2011) Homeostatic chemokine receptors and organ-specific metastasis. Nat Rev Immunol 11:597-606
166. Zou YR, Kottmann AH, Kuroda M, Taniuchi I, Littman DR (1998) Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393:595-599