Targeting ROR1 inhibits epithelial-mesenchymal transition and metastasis

Cancer Research

Volumn 73, Issue 12, 2013, Pages 3649-3660

  Cui, Bing ^a   Zhang, Suping ^a   Chen, Liguang ^a   Yu, Jianqiang ^a   Widhopf II, George F ^a   Fecteau, Jessie F ^a   Rassenti, Laura Z ^a   Kipps, Thomas J ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKERATIN 19; MEMBRANE RECEPTOR; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY D10; PROTEIN TYROSINE KINASE; PROTEIN ZO1; RECEPTOR TYROSINE KINASE LIKE ORPHAN RECEPTOR 1; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SNAIL1; TRANSCRIPTION FACTOR SNAIL2; TRANSCRIPTION FACTOR ZEB1; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE METASTASIS; BRAIN METASTASIS; BREAST ADENOCARCINOMA; BREAST CANCER; CANCER CELL CULTURE; CANCER INHIBITION; CANCER RECURRENCE; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; DRUG TARGETING; EPITHELIAL MESENCHYMAL TRANSITION; EX VIVO STUDY; FEMALE; GENE EXPRESSION; GENE SILENCING; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; MAJOR CLINICAL STUDY; METASTASIS INHIBITION; METASTASIS POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ANTIBODIES, MONOCLONAL; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOBLOTTING; KAPLAN-MEIER ESTIMATE; MAMMARY NEOPLASMS, EXPERIMENTAL; MCF-7 CELLS; MICE; MICE, KNOCKOUT; NEOPLASM METASTASIS; PROGNOSIS; RECEPTOR TYROSINE KINASE-LIKE ORPHAN RECEPTORS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TRANSPLANTATION, HETEROLOGOUS;

EID: 84879098667     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-3832     Document Type: Article

References (49)

1. Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science 2011;331:1559-64.
2. Valastyan S, Weinberg RA. Tumor metastasis: molecular insights and evolving paradigms. Cell 2011;147:275-92.
3. Nguyen DX, Bos PD, Massague J. Metastasis: from dissemination to organ-speci fic colonization. Nat Rev Cancer 2009;9:274-84.
4. Scheel C, Weinberg RA. Cancer stem cells and epithelial-mesenchymal transition: concepts and molecular links. Semin Cancer Biol 2012;22:396-403.
5. Chiang AC, Massague J. Molecular basis of metastasis. N Engl J Med 2008;359:2814-23.
6. Nguyen DX, Massague J. Genetic determinants of cancer metastasis. Nat Rev Genet 2007;8:341-52. (Pubitemid 46625811)
7. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009;139:871-90.
8. Reiman JM, Knutson KL, Radisky DC. Immune promotion of epithelial-mesenchymal transition and generation of breast cancer stem cells. Cancer Res 2010;70:3005-8.
9. Scheel C, Eaton EN, Li SH, Chaffer CL, Reinhardt F, Kah KJ, et al. Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast. Cell 2011;145:926-40.
10. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
11. Mani SA, Guo W, Liao M-J, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008;133:704-15. (Pubitemid 351636299)
12. Rhim AD, Mirek ET, Aiello NM, Maitra A, Bailey JM, McAllister F, et al. EMT and dissemination precede pancreatic tumor formation. Cell 2012;148:349-61.
13. Singh A, Settleman J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene 2010;29:4741-51.
14. Green JL, Kuntz SG, Sternberg PW. Ror receptor tyrosine kinases: orphans no more. Trends Cell Biol 2008;18:536-44.
15. Yamaguchi T, Yanagisawa K, Sugiyama R, Hosono Y, Shimada Y, Arima C, et al. NKX2-1/TITF1/TTF-1-induced ROR1 is required to sustain EGFR survival signaling in lung adenocarcinoma. Cancer Cell 2012;21:348-61.
16. Klemm F, Bleckmann A, Siam L, Chuang HN, Rietkotter E, Behme D, et al. Beta-catenin-independent WNT signaling in basal-like breast cancer and brain metastasis. Carcinogenesis 2011;32:434-42.
17. Minami Y, Oishi I, Endo M, Nishita M. Ror-family receptor tyrosine kinases in noncanonical Wnt signaling: their implications in developmental morphogenesis and human diseases. Dev Dyn 2010;239:1-15.
18. Forrester WC, Dell M, Perens E, Garriga G. A C. elegans Ror receptor tyrosine kinase regulates cell motility and asymmetric cell division. Nature 1999;400:881-5. (Pubitemid 29406725)
19. Yoda A, Oishi I, Minami Y. Expression and function of the Ror-family receptor tyrosine kinases during development: lessons from genetic analyses of nematodes, mice, and humans. J Recept Signal Transduct Res 2003;23:1-15. (Pubitemid 36368941)
20. Endo M, Doi R, Nishita M, Minami Y. Ror family receptor tyrosine kinases regulate the maintenance of neural progenitor cells in the developing neocortex. J Cell Sci 2012;125:2017-29.
21. Zhang S, Chen L, Wang-Rodriguez J, Zhang L, Cui B, Frankel W, et al. The onco-embryonic antigen ROR1 is expressed by a variety of human cancers. Am J Pathol 2012;181:1903-10.
22. Fukuda T, Chen L, Endo T, Tang L, Lu D, Castro JE, et al. Antisera induced by infusions of autologous Ad-CD154-leukemia B cells identify ROR1 as an oncofetal antigen and receptor for Wnt5a. Proc Natl Acad Sci U S A 2008;105:3047-52. (Pubitemid 351723665)
23. Gentile A, Lazzari L, Benvenuti S, Trusolino L, Comoglio PM. Ror1 is a pseudokinase that is crucial for Met-driven tumorigenesis. Cancer Res 2011;71:3132-41.
24. Baskar S, Kwong KY, Hofer T, Levy JM, Kennedy MG, Lee E, et al. Unique cell surface expression of receptor tyrosine kinase ROR1 in human B-cell chronic lymphocytic leukemia. Clin Cancer Res 2008;14:396-404. (Pubitemid 351226106)
25. Daneshmanesh AH, Mikaelsson E, Jeddi-Tehrani M, Bayat AA, Ghods R, Ostadkarampour M, et al. Ror1, a cell surface receptor tyrosine kinase is expressed in chronic lymphocytic leukemia and may serve as a putative target for therapy. Int J Cancer 2008;123:1190-5.
26. Masiakowski P, Carroll RD. A novel family of cell surface receptors with tyrosine kinase-like domain. J Biol Chem 1992;267:26181-90. (Pubitemid 23014033)
27. Zhang S, Chen L, Cui B, Chuang HY, Yu J, Wang-Rodriguez J, et al. ROR1 is expressed in human breast cancer and associated with enhanced tumor-cell growth. PLoS ONE 2012;7:e31127.
28. Neve RM, Chin K, Fridlyand J, Yeh J, Baehner FL, Fevr T, et al. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 2006;10:515-27. (Pubitemid 44854747)
29. Zhang XH, Wang Q, Gerald W, Hudis CA, Norton L, Smid M, et al. Latent bone metastasis in breast cancer tied to Src-dependent survival signals. Cancer Cell 2009;16:67-78.
30. Pishvaian MJ, Feltes CM, Thompson P, Bussemakers MJ, Schalken JA, Byers SW. Cadherin-11 is expressed in invasive breast cancer cell lines. Cancer Res 1999;59:947-52. (Pubitemid 29086753)
31. Thiery JP, Sleeman JP. Complex networks orchestrate epithelial- mesenchymal transitions. Nat Rev Mol Cell Biol 2006;7:131-42. (Pubitemid 43278296)
32. Fenouille N, Tichet M, Dufies M, Pottier A, Mogha A, Soo JK, et al. The epithelial-mesenchymal transition (EMT) regulatory factor SLUG (SNAI2) is a downstream target of SPARC and AKT in promoting melanoma cell invasion. PLoS ONE 2012;7:e40378.
33. Polytarchou C, Iliopoulos D, Hatziapostolou M, Kottakis F, Maroulakou I, Struhl K, et al. Akt2 regulates all Akt isoforms and promotes resistance to hypoxia through induction of miR-21 upon oxygen deprivation. Cancer Res 2011;71:4720-31.
34. Qiao M, Sheng S, Pardee AB. Metastasis and AKT activation. Cell Cycle 2008;7:2991-6.
35. Sheng S, Qiao M, Pardee AB. Metastasis and AKT activation. J Cell Physiol 2009;218:451-4.
36. Zlotnik A, Burkhardt AM, Homey B. Homeostatic chemokine receptors and organ-specific metastasis. Nat Rev Immunol 2011;11:597-606.
37. Burger JA, Kipps TJ. CXCR4: a key receptor in the crosstalk between tumor cells and their microenvironment. Blood 2006;107:1761-7. (Pubitemid 43289351)
38. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest 2009;119:1420-8.
39. Bitler BG, Nicodemus JP, Li H, Cai Q, Wu H, Hua X, et al. Wnt5a suppresses epithelial ovarian cancer by promoting cellular senescence. Cancer Res 2011;71:6184-94.
40. Leris AC, Roberts TR, Jiang WG, Newbold RF, Mokbel K. WNT5A expression in human breast cancer. Anticancer Res 2005;25:731-4. (Pubitemid 40546838)
41. Dejmek J, Leandersson K, Manjer J, Bjartell A, Emdin SO, Vogel WF, et al. Expression and signaling activity of Wnt-5a/discoidin domain receptor-1 and Syk plays distinct but decisive roles in breast cancer patient survival. Clin Cancer Res 2005;11:520-8. (Pubitemid 40116875)
42. Geng M, Cao YC, Chen YJ, Jiang H, Bi LQ, Liu XH. Loss of Wnt5a and Ror2 protein in hepatocellular carcinoma associated with poor prognosis. World J Gastroenterol 2012;18:1328-38.
43. Blanc E, Roux GL, Benard J, Raguenez G. Low expression of Wnt-5a gene is associated with high-risk neuroblastoma. Oncogene 2005;24:1277-83. (Pubitemid 40313929)
44. Hanaki H, Yamamoto H, Sakane H, Matsumoto S, Ohdan H, Sato A, et al. An anti-Wnt5a antibody suppresses metastasis of gastric cancer cells in vivo by inhibiting receptor-mediated endocytosis. Mol Cancer Ther 2012;11:298-307.
45. Badiglian Filho L, Oshima CT, De Oliveira Lima F, De Oliveira Costa H, De Sousa Damiao R, Gomes TS, et al. Canonical and noncanonical Wnt pathway: a comparison among normal ovary, benign ovarian tumor and ovarian cancer. Oncol Rep 2009;21:313-20.
46. Zhu Y, Tian Y, Du J, Hu Z, Yang L, Liu J, et al. Dvl2-dependent activation of Daam1 and RhoA regulates Wnt5a-induced breast cancer cell migration. PLoS ONE 2012;7:e37823.
47. Kikuchi A, Yamamoto H, Sato A, Matsumoto S. Wnt5a: its signalling, functions and implication in diseases. Acta Physiol 2012;204:17-33.
48. Nishita M, Enomoto M, Yamagata K, Minami Y. Cell/tissue-tropic functions of Wnt5a signaling in normal and cancer cells. Trends Cell Biol 2010;20:346-54.
49. McDonald SL, Silver A. The opposing roles of Wnt-5a in cancer. Br J Cancer 2009;101:209-14.