CXCR7 is induced by hypoxia and mediates glioma cell migration towards SDF-1α

BMC Cancer

Volumn 13, Issue , 2013, Pages

  Esencay, Mine ^a,b   Sarfraz, Yasmeen ^a,b   Zagzag, David ^a,b  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

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

Author keywords

CXCR4; CXCR7; Glioma; Hypoxia; Migration

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR7; LENTIVIRUS VECTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEIN KINASE B; SHORT HAIRPIN RNA; STROMAL CELL DERIVED FACTOR 1ALPHA; CHEMOKINE RECEPTOR CXCR; CXCL12 PROTEIN, HUMAN; CXCR4 PROTEIN, HUMAN; CXCR7 PROTEIN, HUMAN; STROMAL CELL DERIVED FACTOR 1;

ARTICLE; CANCER CELL CULTURE; CELL HYPOXIA; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; CULTURE TECHNIQUE; DRUG DEVELOPMENT; DRUG TARGETING; ENZYME PHOSPHORYLATION; GLIOMA CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; PROTEIN EXPRESSION; PROTEIN INDUCTION; STUDENT T TEST; UPREGULATION; WESTERN BLOTTING; CELL MOTION; GENE SILENCING; GLIOMA; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; TUMOR INVASION;

BLOTTING, WESTERN; CELL HYPOXIA; CELL LINE, TUMOR; CELL MOVEMENT; CHEMOKINE CXCL12; GENE KNOCKDOWN TECHNIQUES; GLIOMA; HUMANS; IMMUNOPRECIPITATION; NEOPLASM INVASIVENESS; RECEPTORS, CXCR; RECEPTORS, CXCR4;

EID: 84880182849     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-13-347     Document Type: Article

References (30)

1. Heesen M, Berman MA, Charest A, Housman D, Gerard C, Dorf ME. Cloning and chromosomal mapping of an orphan chemokine receptor: mouse RDC1. Immunogenetics 1998, 47:364-370. 10.1007/s002510050371, 9510554.
2. Balabanian K, Lagane B, Infantino S, Chow KY, Harriague J, Moepps B, Arenzana-Seisdedos F, Thelen M, Bachelerie F. The chemokine SDF-1/CXCL12 binds to and signals through the orphan receptor RDC1 in T lymphocytes. J Biol Chem 2005, 280:35760-35766. 10.1074/jbc.M508234200, 16107333.
3. Shimizu N, Soda Y, Kanbe K, Liu HY, Mukai R, Kitamura T, Hoshino H. A putative G protein-coupled receptor, RDC1, is a novel co-receptor for human and simian immunodeficiency viruses. J Virol 2000, 74:619-626. 10.1128/JVI.74.2.619-626.2000, 111581, 10623723.
4. Raman D, Baugher PJ, Thu YM, Richmond A. Role of chemokines in tumor growth. Cancer Lett 2007, 256:137-165. 10.1016/j.canlet.2007.05.013, 2065851, 17629396.
5. Schutyser E, Su Y, Yu Y, Gouwy M, Zaja-Milatovic S, Van Damme J, Richmond A. Hypoxia enhances CXCR4 expression in human microvascular endothelial cells and human melanoma cells. Eur Cytokine Netw 2007, 18:59-70. 2665278, 17594938.
6. Miao Z, Luker KE, Summers BC, Berahovich R, Bhojani MS, Rehemtulla A, Kleer CG, Essner JJ, Nasevicius A, Luker GD, Howard MC, Schall TJ. CXCR7 (RDC1) promotes breast and lung tumor growth in vivo and is expressed on tumor-associated vasculature. Proc Natl Acad Sci USA 2007, 104:15735-15740. 10.1073/pnas.0610444104, 1994579, 17898181.
7. Wang J, Shiozawa Y, Wang J, Wang Y, Jung Y, Pienta KJ, Mehra R, Loberg R, Taichman RS. The role of CXCR7/RDC1 as a chemokine receptor for CXCL12/SDF-1 in prostate cancer. J Biol Chem 2008, 283:4283-4294.
8. 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. A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development. J Exp Med 2006, 203:2201-2213. 10.1084/jem.20052144, 2118398, 16940167.
9. Zagzag D, Esencay M, Mendez O, Yee H, Smirnova I, Huang Y, Chiriboga L, Lukyanov E, Liu M, Newcomb EW. Hypoxia- and vascular endothelial growth factor-induced stromal cell-derived factor-1alpha/CXCR4 expression in glioblastomas: one plausible explanation of Scherer's structures. Am J Pathol 2008, 173:545-560. 10.2353/ajpath.2008.071197, 2475791, 18599607.
10. Zagzag D, Lukyanov Y, Lan L, Ali MA, Esencay M, Mendez O, Yee H, Voura EB, Newcomb EW. Hypoxia-inducible factor 1 and VEGF upregulate CXCR4 in glioblastoma: implications for angiogenesis and glioma cell invasion. Lab Invest 2006, 86:1221-1232. 10.1038/labinvest.3700482, 17075581.
11. Zhang J, Sarkar S, Yong VW. The chemokine stromal cell derived factor-1 (CXCL12) promotes glioma invasiveness through MT2-matrix metalloproteinase. Carcinogenesis 2005, 26:2069-2077. 10.1093/carcin/bgi183, 16033774.
12. Ehtesham M, Winston JA, Kabos P, Thompson RC. CXCR4 expression mediates glioma cell invasiveness. Oncogene 2006, 25:2801-2806. 10.1038/sj.onc.1209302, 16407848.
13. Sheng Z, Li L, Zhu LJ, Smith TW, Demers A, Ross AH, Moser RP, Green MR. A genome-wide RNA interference screen reveals an essential CREB3L2/ATF5/MCL1 survival pathway in malignant glioma with therapeutic implications. Nat Med 2010, 16:671-677. 10.1038/nm.2158, 2882506, 20495567.
14. Boldajipour B, Mahabaleshwar H, Kardash E, Reichman-Fried M, Blaser H, Minina S, Wilson D, Xu Q, Raz E. Control of chemokine-guided cell migration by ligand sequestration. Cell 2008, 132:463-473. 10.1016/j.cell.2007.12.034, 18267076.
15. Zheng K, Li HY, Su XL, Wang XY, Tian T, Li F, Ren GS. Chemokine receptor CXCR7 regulates the invasion, angiogenesis and tumor growth of human hepatocellular carcinoma cells. J Exp Clin Cancer Res 2010, 29:31. 10.1186/1756-9966-29-31, 2859378, 20380740.
16. Rajagopal S, Kim J, Ahn S, Craig S, Lam CM, Gerard NP, Gerard C, Lefkowitz RJ. Beta-arrestin- but not G protein-mediated signaling by the "decoy" receptor CXCR7. Proc Natl Acad Sci USA 2010, 107:628-632. 10.1073/pnas.0912852107, 2818968, 20018651.
17. Wang Y, Li G, Stanco A, Long JE, Crawford D, Potter GB, Pleasure SJ, Behrens T, Rubenstein JL. CXCR4 and CXCR7 have distinct functions in regulating interneuron migration. Neuron 2011, 69:61-76. 10.1016/j.neuron.2010.12.005, 3025760, 21220099.
18. 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. Essential but differential role for CXCR4 and CXCR7 in the therapeutic homing of human renal progenitor cells. J Exp Med 2008, 205:479-490. 10.1084/jem.20071903, 2271008, 18268039.
19. Sánchez-Alcañiz JA, Haege S, Mueller W, Pla R, Mackay F, Schulz S, López-Bendito G, Stumm R, Marín O. CXCR7 controls neuronal migration by regulating chemokine responsiveness. Neuron 2010, 69:77-90.
20. Odemis V, Lipfert J, Kraft R, Hajek P, Abraham G, Hattermann K, Mentlein R, Engele J. The presumed atypical chemokine receptor CXCR7 signals through G(i/o) proteins in primary rodent astrocytes and human glioma cells. Glia 2012, 60:372-381. 10.1002/glia.22271, 22083878.
21. Hattermann K, Held-Feindt J, Lucius R, Müerköster SS, Penfold ME, Schall TJ, Mentlein R. The chemokine receptor CXCR7 is highly expressed in human glioma cells and mediates antiapoptotic effects. Cancer Res 2010, 70:3299-3308. 10.1158/0008-5472.CAN-09-3642, 20388803.
22. Hattermann K, Mentlein R, Held-Feindt J. CXCL12 mediates apoptosis resistance in rat C6 glioma cells. Oncol Rep 2012, 27:1348-1352.
23. Calatozzolo C, Canazza A, Pollo B, Di Pierro E, Ciusani E, Maderna E, Salce E, Sponza V, Frigerio S, Di Meco F, Schinelli S, Salmaggi A. Expression of the new CXCL12 receptor, CXCR7, in gliomas. Cancer Biol Ther 2011, 11:242-253. 10.4161/cbt.11.2.13951, 21084856.
24. Schönemeier B, Kolodziej A, Schulz S, Jacobs S, Hoellt V, Stumm RJ. Regional and cellular localization of the CXCL12/SDF-1 chemokine receptor CXCR7 in the developing and adult rat brain. Comp Neurol 2008, 510:207-220.
25. Luker KE, Lewin SA, Mihalko LA, Schmidt BT, Winkler JS, Coggins NL, Thomas DG, Luker GD. Scavenging of CXCL12 by CXCR7 promotes tumor growth and metastasis of CXCR4-positive breast cancer cells. Oncogene 2012, 31:4750-4758. 10.1038/onc.2011.633, 3337948, 22266857.
26. 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. Elucidation of CXCR7-mediated signaling events and inhibition of CXCR4-mediated tumor cell transendothelial migration by CXCR7 ligands. J Immunol 2009, 183:3204-3211. 10.4049/jimmunol.0900269, 19641136.
27. 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. Disrupted cardiac development but normal hematopoiesis in mice deficient in the second CXCL12/SDF-1 receptor, CXCR7. Proc Natl Acad Sci USA 2007, 104:14759-14764. 10.1073/pnas.0702229104, 1976222, 17804806.
28. Levoye A, Balabanian K, Baleux F, Bachelerie F, Lagane B. CXCR7 heterodimerizes with CXCR4 and regulates CXCL12-mediated G protein signaling. Blood 2009, 113:6085-6093. 10.1182/blood-2008-12-196618, 19380869.
29. Odemis V, Boosmann K, Heinen A, Küry P, Engele J. CXCR7 is an active component of SDF-1 signalling in astrocytes and Schwann cells. J Cell Sci 2010, 123:1081-1088. 10.1242/jcs.062810, 20197403.
30. Mellado M, Rodríguez-Frade JM, Vila-Coro AJ, Fernández S, de MartínAna A, Jones DR, Torán JL, Martínez-A C. Chemokine receptor homo- or heterodimerization activates distinct signaling pathways. EMBO J 2001, 20:2497-2507. 10.1093/emboj/20.10.2497, 125458, 11350939.