CXCR7 participates in CXCL12-induced CD34+ cell cycling through b-arrestin-dependent Akt activation

Blood

Volumn 123, Issue 2, 2014, Pages 191-202

  Torossian, Frédéric ^a,b   Anginot, Adrienne ^a,b   Chabanon, Aurélie ^a,b   Clay, Denis ^a,b   Guerton, Bernadette ^a,b   Desterke, Christophe ^a,b   Boutin, Laetitia ^c   Marullo, Stefano ^d   Scott, Mark G H ^d   Lataillade, Jean Jacques ^a,c   Le Bousse Kerdilès, Marie Caroline ^a,b,e  

^a INSERM   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c Centre de Transfusion Sanguine des Armees   (France)

^d INSTITUT COCHIN   (France)

^e HÔPITAL PAUL BROUSSE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ARRESTIN; CD34 ANTIGEN; CHEMOKINE RECEPTOR CXCR7; CYCLIN A; CYCLIN B1; CYCLIN D1; MESSENGER RNA; PROTEIN KINASE B; STROMAL CELL DERIVED FACTOR 1; CHEMOKINE RECEPTOR CXCR; CXCR7 PROTEIN, HUMAN; RETINA S ANTIGEN;

ARTICLE; CELL MEMBRANE; CELL SURVIVAL; COLONY FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; CELL CYCLE; CFU COUNTING; HEMATOPOIETIC STEM CELL; INTRACELLULAR SPACE; METABOLISM; PHOSPHORYLATION; PROTEIN TRANSPORT;

ANTIGENS, CD34; ARRESTINS; CELL CYCLE; CELL SURVIVAL; CHEMOKINE CXCL12; COLONY-FORMING UNITS ASSAY; ENZYME ACTIVATION; HEMATOPOIETIC STEM CELLS; HUMANS; INTRACELLULAR SPACE; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, CXCR;

EID: 84897019225     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-05-500496     Document Type: Article

References (43)

1. Lataillade JJ, Clay D, Bourin P., et al Stromal cell-derived factor 1 regulates primitive hematopoiesis by suppressing apoptosis and by promoting G(0)/G(1) transition in CD34(+) cells: evidence for an autocrine/paracrine mechanism. Blood. 2002; 99(4): 1117-1129. (Pubitemid 34547062)
2. Lataillade JJ, Clay D, Dupuy C., et al Chemokine SDF-1 enhances circulating CD34(+) cell proliferation in synergy with cytokines: possible role in progenitor survival. Blood. 2000; 95(3): 756-768. (Pubitemid 30062693)
3. Chabanon A, Desterke C, Rodenburger E., et al A cross-talk between stromal cell-derived factor-1 and transforming growth factor-beta controls the quiescence/cycling switch of CD34(+) progenitors through FoxO3 and mammalian target of rapamycin. Stem Cells. 2008; 26(12): 3150-3161.
4. Bleul CC, Fuhlbrigge RC, Casasnovas J.M., Aiuti A., Springer TA A highly efficacious lymphocyte chemoattractant, stromal cell-derived factor 1 (SDF-1). J Exp Med. 1996; 184(3): 1101-1109. (Pubitemid 26313567)
5. Balabanian K, Lagane B, Infantino S., et al The chemokine SDF-1/CXCL12 binds to and signals through the orphan receptor RDC1 in T lymphocytes. J Biol Chem. 2005; 280(42): 35760-35766. (Pubitemid 41532769)
6. Burns JM, Summers BC, Wang Y, et al A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development. J Exp Med. 2006; 203(9): 2201-2213. (Pubitemid 44352240)
7. Sierro F, Biben C, Martínez-Muñoz L, et al. Disrupted cardiac development but normal hematopoiesis in mice deficient in the second CXCL12/SDF-1 receptor, CXCR7. Proc Natl Acad Sci U S A. 2007; 104(37): 14759-14764. (Pubitemid 350003216)
8. Nagasawa T, Hirota S, Tachibana K., et al Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature. 1996; 382(6592): 635-638. (Pubitemid 26268957)
9. Tachibana K, Hirota S, Iizasa H., et al The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature. 1998; 393(6685): 591-594. (Pubitemid 28319250)
10. Zou YR, Kottmann AH, Kuroda M, Taniuchi I., Littman DR Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature. 1998; 393(6685): 595-599. (Pubitemid 28319251)
11. Mazzinghi B, Ronconi E, Lazzeri E., et al Essential but differential role for CXCR4 and CXCR7 in the therapeutic homing of human renal progenitor cells. J Exp Med. 2008; 205(2): 479-490. (Pubitemid 351281611)
12. Infantino S, Moepps B, Thelen M. Expression and regulation of the orphan receptor RDC1 and its putative ligand in human dendritic and B cells. J Immunol. 2006; 176(4): 2197-2207. (Pubitemid 43201667)
13. Sánchez-Martín L, Estecha A, Samaniego R, Sánchez-Ramón S, Vega Má, Sánchez-Mateos P. The chemokine CXCL12 regulates monocyte-macrophage differentiation and RUNX3 expression. Blood. 2011; 117(1): 88-97.
14. Berahovich RD, Zabel BA, Penfold M.E., et al CXCR7 protein is not expressed on human or mouse leukocytes. J Immunol. 2010; 185(9): 5130-5139.
15. Tarnowski M, Liu R, Wysoczynski M., Ratajczak J, Kucia M, Ratajczak MZ 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. 2010; 85(6): 472-483.
16. Hartmann TN, Grabovsky V, Pasvolsky R., et al 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. 2008; 84(4): 1130-1140.
17. Levoye A, Balabanian K, Baleux F., Bachelerie F, Lagane B. CXCR7 heterodimerizes with CXCR4 and regulates CXCL12-mediated G protein signaling. Blood. 2009; 113(24): 6085-6093.
18. Lefkowitz RJ, Shenoy SK Transduction of receptor signals by beta-arrestins. Science. 2005; 308(5721): 512-517.
19. Zabel BA, Wang Y, Lewén S, et al Elucidation of CXCR7-mediated signaling events and inhibition of CXCR4-mediated tumor cell transendothelial migration by CXCR7 ligands. J Immunol. 2009; 183(5): 3204-3211.
20. Gravel S, Malouf C, Boulais P.E., et al The peptidomimetic CXCR4 antagonist TC14012 recruits beta-arrestin to CXCR7: roles of receptor domains. J Biol Chem. 2010; 285(49): 37939-37943.
21. Luker KE, Steele JM, Mihalko L.A., Ray P., Luker GD Constitutive and chemokine-dependent internalization and recycling of CXCR7 in breast cancer cells to degrade chemokine ligands. Oncogene. 2010; 29(32): 4599-4610.
22. Rajagopal S, Kim J, Ahn S., et al Beta-arrestin-but not G protein-mediated signaling by the "decoy" receptor CXCR7. Proc Natl Acad Sci U S A. 2010; 107(2): 628-632.
23. Proust R, Bertoglio J, Gesbert F. The adaptor protein SAP directly associates with CD3ζ chain and regulates T cell receptor signaling. PLoS ONE. 2012; 7(8):e43200.
24. Hatse S, Princen K, Liekens S., Vermeire K, de Clercq E, Schols D. Fluorescent CXCL12AF647 as a novel probe for nonradioactive CXCL12/CXCR4 cellular interaction studies. Cytometry A. 2004; 61(2): 178-188. (Pubitemid 39362292)
25. Ford LB, Hansell CA, Nibbs RJ Using fluorescent chemokine uptake to detect chemokine receptors by fluorescent activated cell sorting. Methods Mol Biol. 2013; 1013: 203-214.
26. Broxmeyer HE, Mejia JA, Hangoc G, Barese C., Dinauer M, Cooper S. SDF-1/CXCL12 enhances in vitro replating capacity of murine and human multipotential and macrophage progenitor cells. Stem Cells Dev. 2007; 16(4): 589-596. (Pubitemid 47378731)
27. Cashman J, Clark-Lewis I, Eaves A., Eaves C. Stromal-derived factor 1 inhibits the cycling of very primitive human hematopoietic cells in vitro and in NOD/SCID mice. Blood. 2002; 99(3): 792-799. (Pubitemid 34525537)
28. Shimizu S, Brown M, Sengupta R., Penfold ME, Meucci O. CXCR7 protein expression in human adult brain and differentiated neurons. PLoS ONE. 2011; 6(5):e20680.
29. Achour L, Labbé-Jullié C, Scott MG, Marullo S. An escort for GPCRs: implications for regulation of receptor density at the cell surface. Trends Pharmacol Sci. 2008; 29(10): 528-535.
30. Dai X, Tan Y, Cai S., et al The role of CXCR7 on the adhesion, proliferation and angiogenesis of endothelial progenitor cells. J Cell Mol Med. 2011; 15(6): 1299-1309.
31. Yoshida D, Nomura R, Teramoto A. Signalling pathway mediated by CXCR7, an alternative chemokine receptor for stromal-cell derived factor-1α, in AtT20 mouse adrenocorticotrophic hormone-secreting pituitary adenoma cells. J Neuroendocrinol. 2009; 21(5): 481-488.
32. Décaillot F.M., Kazmi MA, Lin Y, Ray-Saha S, Sakmar T.P., Sachdev P. CXCR7/CXCR4 heterodimer constitutively recruits beta-arrestin to enhance cell migration. J Biol Chem. 2011; 286(37): 32188-32197.
33. Wang J, Shiozawa Y, Wang J., et al The role of CXCR7/RDC1 as a chemokine receptor for CXCL12/SDF-1 in prostate cancer. J Biol Chem. 2008; 283(7): 4283-4294.
34. Odemis V, Lipfert J, Kraft R., et al The presumed atypical chemokine receptor CXCR7 signals through G(i/o) proteins in primary rodent astrocytes and human glioma cells. Glia. 2012; 60(3): 372-381.
35. Kang J, Shi Y, Xiang B., et al A nuclear function of beta-arrestin1 in GPCR signaling: regulation of histone acetylation and gene transcription. Cell. 2005; 123(5): 833-847. (Pubitemid 41721030)
36. Scott MG, Le Rouzic E, Périanin A, et al. Differential nucleocytoplasmic shuttling of beta-arrestins. Characterization of a leucine-rich nuclear export signal in beta-arrestin2. J Biol Chem. 2002; 277(40): 37693-37701.
37. Neuhaus EM, Mashukova A, Barbour J., Wolters D, Hatt H. Novel function of beta-arrestin2 in the nucleus of mature spermatozoa. J Cell Sci. 2006; 119(Pt 15): 3047-3056. (Pubitemid 44322119)
38. Lodeiro M, Theodoropoulou M, Pardo M., Casanueva FF, Camiña JP. c-Src regulates Akt signaling in response to ghrelin via beta-arrestin signaling-independent and -dependent mechanisms. PLoS ONE. 2009; 4(3):e4686.
39. Goel R, Phillips-Mason PJ, Raben D.M., Baldassare JJ alpha-Thrombin induces rapid and sustained Akt phosphorylation by beta-arrestin1-dependent and -independent mechanisms, and only the sustained Akt phosphorylation is essential for G1 phase progression. J Biol Chem. 2002; 277(21): 18640-18648. (Pubitemid 34952419)
40. Wang P, Kumar P, Wang C., Defea KA Differential regulation of class IA phosphoinositide 3-kinase catalytic subunits p110 alpha and beta by protease-activated receptor 2 and beta-arrestins. Biochem J. 2007; 408(2): 221-230. (Pubitemid 350206345)
41. Beaulieu JM, Sotnikova TD, Marion S, Lefkowitz R.J., Gainetdinov RR, Caron MG An Akt/beta-arrestin 2/PP2A signaling complex mediates dopaminergic neurotransmission and behavior. Cell. 2005; 122(2): 261-273. (Pubitemid 41032989)
42. Lima-Fernandes E., Enslen H, Camand E., et al Distinct functional outputs of PTEN signalling are controlled by dynamic association with β-arrestins. EMBO J. 2011; 30(13): 2557-2568.
43. Lataillade JJ, Domenech J, Le Bousse-Kerdilès MC. Stromal cell-derived factor-1 (SDF-1)couple plays multiple roles on haematopoietic progenitors at the border between the old cytokine and new chemokine worlds: survival, cell cycling and trafficking. Eur Cytokine Netw. 2004; 15(3): 177-188. (Pubitemid 39389913)