Stress-induced CXCR4 promotes migration and invasion of Ewing sarcoma

Molecular Cancer Research

Volumn 12, Issue 6, 2014, Pages 953-964

  Krook, Melanie A ^a   Nicholls, Lauren A ^a   Scannell, Christopher A ^a   Chugh, Rashmi ^a   Thomas, Dafydd G ^b   Lawlor, Elizabeth R ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; GROWTH FACTOR; PLERIXAFOR; PROTEIN CDC42; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; CXCL12 PROTEIN, HUMAN; RAC1 PROTEIN, HUMAN; STROMAL CELL DERIVED FACTOR 1;

ARTICLE; CELL LINE; CELL STRESS; CONTROLLED STUDY; EWING SARCOMA; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HYPOXIA; IMMUNOHISTOCHEMISTRY; METASTASIS; PHENOTYPE; PRIMARY TUMOR; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SARCOMA CELL; STAINING; TUMOR INVASION; UPREGULATION; BIOSYNTHESIS; BONE TUMOR; CELL GROWTH; CELL HYPOXIA; CELL MOTION; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; TUMOR CELL LINE;

BONE NEOPLASMS; CDC42 GTP-BINDING PROTEIN; CELL GROWTH PROCESSES; CELL HYPOXIA; CELL LINE, TUMOR; CELL MOVEMENT; CHEMOKINE CXCL12; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HUMANS; NEOPLASM INVASIVENESS; RAC1 GTP-BINDING PROTEIN; RECEPTORS, CXCR4; SARCOMA, EWING; STRESS, PHYSIOLOGICAL;

EID: 84902654940     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-13-0668     Document Type: Article

References (39)

1. Balamuth NJ, Womer RB. Ewing's sarcoma. Lancet Oncol 2010. 11:184-92.
2. Gorlick R, Janeway K, Lessnick S, Randall RL, Marina N. COG Bone Tumor Committee. Children's Oncology Group's 2013 blueprint for research: bone tumors. Pediatr Blood Cancer 2013;60: 1009 -15.
3. Domanska UM, Kruizinga RC, Nagengast WB, Timmer-Bosscha H, Huls G, de Vries EG, et al. A review on CXCR4/CXCL12 axis in oncology: no place to hide. Eur J Cancer 2013;49:219-30.
4. Bennani-Baiti IM, Cooper A, Lawlor ER, Kauer M, Ban J, Aryee DN, et al. Intercohort gene expression co-analysis reveals chemokine receptors as prognostic indicators in Ewing's sarcoma. Clin Cancer Res 2010;16:3769-78.
5. Cojoc M, Peitzsch C, Trautmann F, Polishchuk L, Telegeev GD, Dubrovska A. Emerging targets in cancer management: role of the CXCL12/CXCR4 axis. Onco Targets Ther 2013;6:1347-61.
6. Muller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, et al. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001;410:50-6. (Pubitemid 32225831)
7. Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, et al. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 2007;1:313-23. (Pubitemid 47355323)
8. Mohle R, Failenschmid C, Bautz F, Kanz L. Overexpression of the chemokine receptor CXCR4 in B cell chronic lymphocytic leukemia is associated with increased functional response to stromal cell-derived factor-1 (SDF-1). Leukemia 1999;13:1954 -9.
9. Libura J, Drukala J, Majka M, Tomescu O, Navenot JM, Kucia M, et al. CXCR4-SDF-1 signaling is active in rhabdomyosarcoma cells and regulates locomotion, chemotaxis, and adhesion. Blood 2002;100: 2597-606.
10. Strahm B, Durbin AD, Sexsmith E, Malkin D. The CXCR4-SDF1alpha axis is a critical mediator of rhabdomyosarcoma metastatic signaling induced by bone marrow stroma. Clin Exp Metastasis 2008; 5:1-10. (Pubitemid 351191222)
11. Tarnowski M, Grymula K, Reca R, Jankowski K, Maksym R, Tarnowska J, et al. Regulation of expression of stromal-derived factor-1 receptors: CXCR4 and CXCR7 in human rhabdomyosarcomas. Mol Cancer Res 2010;8:1- 14.
12. Laverdiere C, Hoang BH, Yang R, Sowers R, Qin J, Meyers PA, et al. Messenger RNA expression levels of CXCR4 correlate with metastatic behavior and outcome in patients with osteosarcoma. Clin Cancer Res 2005;11:2561-7. (Pubitemid 40569454)
13. Lin F, Zheng SE, Shen Z, Tang LN, Chen P, Sun YJ, et al. Relationships between levels of CXCR4 and VEGF and blood-borne metastasis and survival in patients with osteosarcoma. Med Oncol 2011;28:649 - 53.
14. Namlos HM, Kresse SH, Müller CR, Henriksen J, Holdhus R, Sæter G, et al. Global gene expression profiling of human osteosarcomas reveals metastasis-associated chemokine pattern. Sarcoma 2012;2012:639038.
15. Lawlor ER, Scheel C, Irving J, Sorensen PH. Anchorage-independent multi-cellular spheroids as an in vitro model of growth signaling in Ewing tumors. Oncogene 2002;21:307-18. (Pubitemid 34102139)
16. Berghuis D, Schilham MW, Santos SJ, Savola S, Knowles HJ, Dirksen U, et al. The CXCR4-CXCL12 axis in Ewing sarcoma: promotion of tumor growth rather than metastatic disease. Clin Sarcoma Res 2012; 2:24.
17. Harvey JM, Clark GM, Osborne CK, Allred DC. Estrogen receptor status by immunohistochemistry is superior to the ligand-binding assay for predicting response to adjuvant endocrine therapy in breast cancer. J Clin Oncol 1999;7:1474-81. (Pubitemid 29220854)
18. Don-Salu-Hewage AS, Chan SY, McAndrews KM, Chetram MA, Dawson MR, Bethea DA, et al. Cysteine (C)-X-C receptor 4 undergoes transportin 1-dependent nuclear localization and remains functional at the nucleus of metastatic prostate cancer cells. PLoS ONE 2013;8: e57194.
19. Xu TP, Shen H, Liu LX, Shu YQ. The impact of chemokine receptor CXCR4 on breast cancer prognosis: a meta-analysis. Cancer Epidemiol 2013;37:725-31.
20. Orimo A, Gupta PB, Sgroi DC, Arenzana-Seisdedos F, Delaunay T, Naeem R, et al. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 2005;121:335-48. (Pubitemid 40692295)
21. Liu H, Xue W, Ge G, Luo X, Li Y, Xiang H, et al. Hypoxic preconditioning advances CXCR4 and CXCR7 expression by activating HIF-1a in MSCs. Biochem Biophys Res Commun 2010:401:509 -15.
22. Oh YS, Kim HY, Song IC, Yun HJ, Jo DY, Kim S, et al. Hypoxia induces CXCR4 expression and biological activity in gastric cancer cells through activation of hypoxia-inducible factor-1alpha. Oncol Rep 2012;28:2239-46.
23. Valastyan S, Weinberg RA. Tumor metastasis: molecular insights and evolving paradigms. Cell 2011;147:275-92.
24. Benton G, Kleinman HK, George J, Arnaoutova I. Multiple uses of basement membrane-like matrix (BME/Matrigel) in vitro and in vivo with cancer cells. Int J Cancer 2011:128:1751-7.
25. Gassmann P, Haier J, Schlüter K, Domikowsky B, Wendel C, Wiesner U, et al. CXCR4 regulates the early extravasation of metastatic tumor cells in vivo. Neoplasia 2009;11:651-61.
26. Yagi H, Tan W, Dillenburg-Pilla P, Armando S, Amornphimoltham P, Simaan M, et al. A synthetic biology approach reveals a CXCR4-G13-Rho signaling axis driving transendothelial migration of metastatic breast cancer cells. Sci Signal 2011;4:ra60.
27. Mendoza-Naranjo A, El-Naggar A, Wai DH, Mistry P, Lazic N, Ayala FR, et al. ERBB4 confers metastatic capacity in Ewing sarcoma. EMBO Mol Med 2013;5:1019-34.
28. Chansky HA, Barahmand-Pour F, Mei Q, Kahn-Farooqi W, Zielinska- Kwiatkowska A, Blackburn M, et al. Targeting of EWS/FLI-1 by RNA interference attenuates the tumor phenotype of Ewing's sarcoma cells in vitro. J Orthop Res 2004;22:910-7. (Pubitemid 38756277)
29. Jin Z, Zhao C, Han X, Han Y. Wnt5a promotes Ewing sarcoma cell migration through upregulating CXCR4 expression. BMC Cancer 2012;12:480.
30. Shukla N, Schiffman J, Reed D, Davis IJ, Womer RB, Lessnick SL, et al. Biomarkers in Ewing sarcoma: the promise and challenge of personalized medicine. a report from the Children's Oncology Group. Front Oncol 2013;3:141.
31. Saunders NA, Simpson F, Thompson EW, Hill MM, Endo-Munoz L, Leggatt G, et al. Role of intratumoural heterogeneity in cancer drug resistance: molecular and clinical perspectives. EMBO Mol Med 2012;4:675-84.
32. De Craene B, Berx G. Regulatory networks defining EMT during cancer initiation and progression. Nat Rev Cancer 2013;13:97-110.
33. Carlisle AJ, Lyttle CA, Carlisle RY, Maris JM. CXCR4 expression heterogeneity in neuroblastoma cells due to ligand-independent regulation. Mol Cancer 2009;8:126.
34. Zhang L, Yeger H, Das B, Irwin MS, Baruchel S. Tissue microenvironment modulates CXCR4 expression and tumor metastasis in neuroblastoma. Neoplasia 2007;9:36-46. (Pubitemid 46203933)
35. Duda DG, Kozin SV, Kirkpatrick ND, Xu L, Fukumura D, Jain RK. CXCL12 (SDF1alpha)-CXCR4/CXCR7 pathway inhibition: an emerging sensitizer for anticancer therapies? Clin Cancer Res 2011;17:2074-80.
36. Ikegaki N, Shimada H, Fox AM, Regan PL, Jacobs JR, Hicks SL, et al. Transient treatment with epigenetic modifiers yields stable neuroblastoma stem cells resembling aggressive large-cell neuroblastomas. Proc Natl Acad Sci U S A 2013;110:6097-102.
37. Gupta PB, Fillmore CM, Jiang G, Shapira SD, Tao K, Kuperwasser C, et al. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 2011;146:633-44.
38. Steeg PS. Perspective: the right trials. Nature 2012;485:S58-9.
39. Ma M, Ye JY, Deng R, Dee CM, Chan GC. Mesenchymal stromal cells may enhance metastasis of neuroblastoma via SDF-1/CXCR4 and SDF-1/CXCR7 signaling. Cancer Lett 2011;312:1-10.