Involvement of the chemokine receptor CXCR4 and its ligand stromal cell-derived factor 1α in breast cancer cell migration through human brain microvascular endothelial cells

Molecular Cancer Research

Volumn 2, Issue 6, 2004, Pages 327-338

  Lee, Byeong Chel ^a   Lee, Tae Hee ^a   Avraham, Shalom ^a   Avraham, Hava Karsenty ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD INSTITUTES OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN KINASE B; STROMAL CELL DERIVED FACTOR 1ALPHA; WORTMANNIN;

ARTICLE; BLOOD VESSEL PERMEABILITY; BRAIN BLOOD VESSEL; BREAST CANCER; CANCER INVASION; CELL MIGRATION; ENDOTHELIUM CELL; ENZYME ACTIVATION; EPITHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MICROVASCULATURE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; BRAIN; BREAST NEOPLASMS; CALCIUM; CELL LINE, TUMOR; CELL MOVEMENT; CHEMOKINES, CXC; DNA-BINDING PROTEINS; ENDOTHELIAL CELLS; ENZYME ACTIVATION; FOCAL ADHESION KINASE 1; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; NEOPLASM INVASIVENESS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, CXCR4; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 3543065871     PISSN: 15417786     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (66)

1. Rollins BJ. Chemokines. Blood 1997;90:909-28.
2. Premack BA, Schall TJ. Chemokine receptors: gateways to inflammation and infection. Nat Med 1996;2:1174-8.
3. Bokoch GM. Chemoattractant signaling and leukocyte activation. Blood 1995;86:1649-60.
4. Gerard C, Gerard NP. The pro-inflammatory seven-transmembrane segment receptors of the leukocyte. Curr Opin Immunol 1994;6:140-5.
5. Taub DD, Oppenheim JJ. Chemokines, inflammation and the immune system. Ther Immunol 1994;1:229-46.
6. Luster AD. Chemokines-chemotactic cytokines that mediate inflammation. N Engl J Med 1998;338:436-45.
7. Hamada T, Tashiro K, Tada H, et al. Isolation and characterization of a novel secretory protein, stromal cell-derived factor-2 (SDF-2) using the signal sequence trap method. Gene 1996;176:211-4.
8. Bleul CC, Farzan M, Choe H, et al. The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature 1996;382:829-33.
9. Feng Y, Broder CC, Kennedy PE, Berger EA. HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 1996;272:872-7.
10. Shirozu M, Nakano T, Inazawa J, et al. Structure and chromosomal localization of the human stromal cell-derived factor 1 (SDF1) gene. Genomics 1995;28:495-500.
11. Baggiolini M. Chemokines and leukocyte traffic. Nature 1998;392:565-8.
12. Nagasawa T, Kikutani H, Kishimoto T. Molecular cloning and structure of a pre-B-cell growth-stimulating factor. Proc Natl Acad Sci USA 1994;91:2305-9.
13. Bleul CC, Fuhlbrigge RC, Casasnovas JM, Aiuti A, Springer TA. A highly efficacious lymphocyte chemoattractant, stromal cell-derived factor 1 (SDF-1). J7 Exp Med 1996;184:1101-9.
14. Ma Q, Jones D, Borghesani PR, et al. Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc Natl Acad Sci USA 1998;95:9448-53.
15. Federsppiel B, Melhado IG, Duncan AM, et al. Molecular cloning of the cDNA and chromosomal localization of the gene for a putative seven-transmembrane segment (7-TMS) receptor isolated from human spleen. Genomics 1993;16:707-12.
16. Nomura H, Nielsen BW, Matsushima K. Molecular cloning of cDNAs encoding a LD78 receptor and putative leukocyte chemotactic peptide receptors. Int Immunol 1993;5:1239-49.
17. Hesselgesser J, Halks-Miller M, DelVecchio V, et al. CD4-independent association between HIV-1 gp120 and CXCR4: functional chemokine receptors are expressed in human neurons. Curr Biol 1997;7:112-21.
18. Ohtani Y, Minami M, Kawaguchi N, et al. Expression of stromal cell-derived factor-1 and CXCR4 chemokine receptor mRNAs in cultured rat glial and neuronal cells. Neurosci Lett 1998;249:163-6.
19. Tanabe S, Heesen M, Yoshizawa I, et al. Functional expression of the CXC-chemokin receptor-4/fusin on mouse microglial cells and astrocytes. J Immunol 1997;159:905-11.
20. Volin MV, Joseph L, Shockley MS, Davies PF. Chemokine receptor CXCR4 expression in endothelium. Biochem Biophys Res Commun 1998;242:46-53.
21. Feil C, Augustin HG. Endothelial cells differentially express functional CXC-chemokine receptor-4 (CXCR-4/fusin) under the control of autocrine activity and exogenous cytokines. Biochem Biophys Res Commun 1998;247:3845.
22. Sehgal A, Keener C, Boynton AL, Warrick J, Murphy GP. CXCR4, a chemokine receptor, is overexpressed in and required for proliferation of glioblastoma tumor cells. J Surg Oncol 1998;69:99-104.
23. Sehgal A, Ricks S, Boynton AL, Warrick J, Murphy GP. Molecular characterization of CXCR-4: a potential brain tumor-associated gene. J Surg Oncol 1998;69:23948.
24. Berson JF, Long D, Doranz BJ, Rucker J, Jifik FR, Doms RW. A seven-transmembrane domain receptor involved in fusion and entry of T-cell-tropic human immunodeficiency virus type 1 strains. J Virol 1996;70:6288-95.
25. Oberlin E, Amara A, Bachelerie F, et al. The CXC chemokine SDF-1 is the ligand for LESTR/fusin and prevents infection by T-cell-line-adapted HIV-1. Nature 1996;382:833-5.
26. Herbein G, Mahlknecht U, Batliwalla F, et al. Apoptosis of CD8+ T cells is mediated by macrophages through interaction of HIV gp120 with chemokine receptor CXCR4. Nature 1998;395:189-94.
27. Ameisen JC. HIV. Setting death in motion. Nature 1998;395:117-9.
28. Zou YR, Kottmann AH, Kuroda M, Taniuchi I, Littman DR. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 1998;393:595-9.
29. Muller A, Homey B, Soto H, et al. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001;410:50-6.
30. Kato M, Kitayama J, Kazama S, Nagawa H. Expression pattern of CXC chemokine receptor-4 is correlated with lymph node metastasis in human invasive ductal carcinoma. Breast Cancer Res 2003;5:R144-50.
31. Helbig G, Christopherson KW 2nd, Bhat-Nakshatri P, et al. NF-κB promotes breast cancer cell migration and metastasis by inducing the expression of the chemokine receptor CXCR4. J Biol Chem 2003;278:21631-8.
32. Kang Y, Siegel PM, Shu W, et al. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 2003;3:537-49.
33. Chen Y, Stamatoyannopoulos G, Song CZ. Down-regulation of CXCR4 by inducible small interfering RNA inhibits breast cancer cell invasion in vitro. Cancer Res 2003;63:4801-4.
34. Kamath L, Meydani A, Foss F, Kuliopulos A. Signaling from protease-activated receptor-1 inhibits migration and invasion of breast cancer cells. Cancer Res 2001;61:5933-40.
35. Langlois AJ, Holder WD Jr, Iglehart JD, Nelson-Rees WA, Wells SA Jr, Bolognesi DP. Morphological and biochemical properties of a new human breast cancer cell line. Cancer Res 1979;39:2604-13.
36. Ganju RK, Brubaker SA, Meyer J, et al. The a-chemokine, stromal cell-derived factor-1α, binds to the transmembrane G-protein-coupled CXCR-4 receptor and activates multiple signal transduction pathways. J Biol Chem 1998;273:23169-75.
37. Park BK, Zeng X, Glazer RI. Akt1 induces extracellular matrix invasion and matrix metalloproteinase-2 activity in mouse mammary epithelial cells. Cancer Res 2001;61:7647-53.
38. Kim D, Kim S, Koh H, et al. Akt/PKB promotes cancer cell invasion via increased motility and metalloproteinase production. FASEB J 2001;15:1953-62.
39. Moorehead RA, Hojilla CV, De Belle I, et al. Insulin-like growth factor-II regulates PTEN expression in the mammary gland. J Biol Chem 2003;278:50422-7.
40. Brunet A, Bonni A, Zigmond MJ, et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 1999;96:857-68.
41. Heidkamp MC, Bayer AL, Kalina JA, Eble DM, Samarel AM. GFP-FRNK disrupts focal adhesions and induces anoikis in neonatal rat ventricular myocytes. Circ Res 2002;90:1282-9.
42. Geminder H, Sagi-Assif O, Goldberg L, et al. A possible role for CXCR4 and its ligand, the CXC chemokine stromal cell-derived factor-1, in the development of bone marrow metastases in neuroblastoma. J Immunol 2001;167:4747-57.
43. Rempel SA, Dudas S, Ge S, Gutierrez JA. Identification and localization of the cytokine SDF1 and its receptor, CXC chemokine receptor 4, to regions of necrosis and angiogenesis in human glioblastoma. Clin Cancer Res 2000;6:102-11.
44. Koshiba T, Hosotani R, Miyamoto Y, et al. Expression of stromal cell-derived factor 1 and CXCR4 ligand receptor system in pancreatic cancer: a possible role for tumor progression. Clin Cancer Res 2000;6:3530-5.
45. Han Y, He T, Huang DR, Pardo CA, Ransohoff RM. TNF-α mediates SDF-1α-induced NF-κB activation and cytotoxic effects in primary astrocytes. J Clin Invest 2001;108:425-35.
46. Cherla RP, Ganju RK. Stromal cell-derived factor 1α-induced chemotaxis in T cells is mediated by nitric oxide signaling pathways. J Immunol 2001;166:3067-4.
47. Nelson PJ, Krensky AM. Chemokines, chemokine receptors, and allograft rejection. Immunity 2001;14:377-86.
48. Lee TH, Avraham H, Lee SH, Avraham S. Vascular endothelial growth factor modulates neutrophil transendothelial migration via up-regulation of interleukin-8 in human brain microvascular endothelial cells. J Biol Chem 2002;277:10445-51.
49. Radisavljevic Z, Avraham H, Avraham S. Vascular endothelial growth factor up-regulates ICAM-1 expression via the phosphatidylinositol 3 OH-kinase/AKT/nitric oxide pathway and modulates migration of brain microvascular endothelial cells. J Biol Chem 2000;275:20770-4.
50. Vivanco I, Sawyers CL. The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat Rev Cancer 2002;2:489-501.
51. Sliva D, Rizzo MT, English D. Phosphatidylinositol 3-kinase and NF-κB regulate motility of invasive MDA-MB-231 human breast cancer cells by the secretion of urokinase-type plasminogen activator. J Biol Chem 2002;277:3150-7.
52. Ilic D, Furuta Y, Kanazawa S, et al. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 1995;377:539-44.
53. Hauck CR, Sieg DJ, Hsia DA, et al. Inhibition of focal adhesion kinase expression or activity disrupts epidermal growth factor-stimulated signaling promoting the migration of invasive human carcinoma cells. Cancer Res 2001;61:7079-90.
54. Fernandis AZ, Prasad A, Band H, Klosel R, Ganju RK. Regulation of CXCR4-mediated chemotaxis and chemoinvasion of breast cancer cells. Oncogene 2004;23:157-67.
55. Cumock AP, Sotsios Y, Wright KL, Ward SG. Optimal chemotactic responses of leukemic T cells to stromal cell-derived factor-1 requires the activation of both class IA and IB phosphoinositide 3-kinases. J Immunol 2003;170:4021-30.
56. Colamussi ML, Secchiero P, Gonelli A, Marchisio M, Zauli G, Capitani S. Stromal derived factor-1α (SDF-1α) induces CD4+ T cell apoptosis via the functional up-regulation of the Fas (CD95)/Fas ligand (CD95L) pathway. J Leukoc Biol 2001;69:263-70.
57. 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;99:1117-29.
58. Kijowski J, Baj-Krzyworzeka M, Majka M, et al. The SDF-1-CXCR4 axis stimulates VEGF secretion and activates integrins but does not affect proliferation and survival in lymphohematopoietic cells. Stem Cells 2001;19:453-66.
59. Tham TN, Lazarini F, Franceschini IA, Lachapelle F, Amara A, Dubois-Dalcq M. Developmental pattern of expression of the α chemokine stromal cell-derived factor 1 in the rat central nervous system. Eur J Neurosci 2001;13:845-56.
60. Bajetto A, Bonavia R, Barbero S, et al. Glial and neuronal cells express functional chemokine receptor CXCR4 and its natural ligand stromal cell-derived factor 1. J Neurochem 1999;73:2348-57.
61. Bajetto A, Barbero S, Bonavia R, et al. Stromal cell-derived factor-1α induces astrocyte proliferation through the activation of extracellular signal-regulated kinases 1/2 pathway. J Neurochem 2001;77:1226-36.
62. Bajetto A, Bonavia R, Barbero S, Florio T, Schettini G. Chemokines and their receptors in the central nervous system. Front Neuroendocrinol 2001;22:147-84.
63. Bachelder RE, Wendt MA, Mercurio AM. Vascular endothelial growth factor promotes breast carcinoma invasion in an autocrine manner by regulating the chemokine receptor CXCR4. Cancer Res 2002;62:7203-6.
64. Tamamura H, Hori A, Kanzaki N, et al. T140 analogs as CXCR4 antagonists identified as anti-metastatic agents in the treatment of breast cancer. FEBS Lett 2003;550:79-83.
65. Park SY, Avraham H, Avraham S. Characterization of the tyrosine kinases RAFTK/Pyk2 and FAK in nerve growth factor-induced neuronal differentiation. J Biol Chem 2000;275:19768-77.
66. Miralem T, Steinberg R, Price D, Avraham H. VEGF(165) requires extracellular matrix components to induce mitogenic effects and migratory response in breast cancer cells. Oncogene 2001;20:5511-24.