Analysis of ROR1 protein expression in human cancer and normal tissues

Clinical Cancer Research

Volumn 23, Issue 12, 2017, Pages 3061-3071

  Balakrishnan, Ashwini ^a   Goodpaster, Tracy ^a   Randolph Habecker, Julie ^a   Hoffstrom, Benjamin G ^a   Jalikis, Florencia G ^b   Koch, Lisa K ^b   Berger, Carolina ^a,c   Kosasih, Paula L ^a   Rajan, Anusha ^a   Sommermeyer, Daniel ^a   Porter, Peggy L ^a   Riddell, Stanley R ^a,c,d  

^a USA   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 6D4; PROTEIN TYROSINE KINASE; ROR1 PROTEIN; UNCLASSIFIED DRUG; LYMPHOCYTE ANTIGEN RECEPTOR; RECEPTOR TYROSINE KINASE LIKE ORPHAN RECEPTOR; ROR1 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL SURFACE; CONTROLLED STUDY; DUODENUM; ESOPHAGUS; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; HUMAN VERSUS ANIMAL COMPARISON; IMMUNOHISTOCHEMISTRY; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TARGETING; RHESUS MONKEY; SENSITIVITY AND SPECIFICITY; STOMACH; WESTERN BLOTTING; CARCINOMA; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; IMMUNOTHERAPY; ISOLATION AND PURIFICATION; MALE; MOLECULARLY TARGETED THERAPY; PATHOLOGY; TUMOR CELL LINE;

ANTIBODIES, MONOCLONAL; CARCINOMA; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOTHERAPY; MALE; MOLECULAR TARGETED THERAPY; RECEPTOR TYROSINE KINASE-LIKE ORPHAN RECEPTORS; RECEPTORS, ANTIGEN, T-CELL;

EID: 85020879926     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-16-2083     Document Type: Article

References (50)

1. Al-Shawi R, Ashton SV, Underwood C, Simons JP. Expression of the Ror1 and Ror2 receptor tyrosine kinase genes during mouse development. Dev Genes Evol 2001;211:161-71.
2. 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.
3. Chang H, Jung WY, Kang Y, Lee H, Kim A, Kim BH. Expression of ROR1, pAkt, and pCREB in gastric adenocarcinoma. Ann Diagn Pathol 2015;19:330-4.
4. Chien HP, Ueng SH, Chen SC, Chang YS, Lin YC, Lo YF, et al. Expression of ROR1 has prognostic significance in triple negative breast cancer. Virchows Arch 2016;468:589-95.
5. Hudecek M, Schmitt TM, Baskar S, Lupo-Stanghellini MT, Nishida T, Yamamoto TN, et al. The B-cell tumor-associated antigen ROR1 can be targeted with T cells modified to express a ROR1-specific chimeric antigen receptor. Blood 2010;116:4532-41.
6. Zhang H, Qiu J, Ye C, Yang D, Gao L, Su Y, et al. ROR1 expression correlated with poor clinical outcome in human ovarian cancer. Sci Rep 2014;4:5811.
7. 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.
8. 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.
9. Zhang S, Cui B, Lai H, Liu G, Ghia EM, Widhopf GF2nd, et al. Ovarian cancer stem cells express ROR1, which can be targeted for anti-cancer-stem-cell therapy. Proc Natl Acad Sci U S A 2014;111:17266-71.
10. 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.
11. Liu Y, Yang H, Chen T, Luo Y, Xu Z, Li Y, et al. Silencing of receptor tyrosine kinase ROR1 inhibits tumor-cell proliferation via PI3K/AKT/mTOR signaling pathway in lung adenocarcinoma. PLoS One 2015;10:e0127092.
12. Dave H, Anver MR, Butcher DO, Brown P, Khan J, Wayne AS, et al. Restricted cell surface expression of receptor tyrosine kinase ROR1 in pediatric B-lineage acute lymphoblastic leukemia suggests targetability with therapeutic monoclonal antibodies. PLoS One 2012;7:e52655.
13. Rebagay G, Yan S, Liu C, Cheung NK. ROR1 and ROR2 in human malignancies: potentials for targeted therapy. Front Oncol 2012;2:34.
14. Klein U, Tu Y, Stolovitzky GA, Mattioli M, Cattoretti G, Husson H, et al. Gene expression profiling of B cell chronic lymphocytic leukemia reveals a homogeneous phenotype related to memory B cells. J Exp Med 2001;194:1625-38.
15. Rosenwald A, Alizadeh AA, Widhopf G, Simon R, Davis RE, Yu X, et al. Relation of gene expression phenotype to immunoglobulin mutation genotype in B cell chronic lymphocytic leukemia. J Exp Med 2001;194:1639-47.
16. Hamilton G, Rath B, Klameth L, Hochmair M. Receptor tyrosine kinase expression of circulating tumor cells in small cell lung cancer. Oncoscience 2015;2:629-34.
17. Karachaliou N, Gimenez-Capitan A, Drozdowskyj A, Viteri S, Moran T, Carcereny E, et al. ROR1 as a novel therapeutic target for EGFR-mutant non-small-cell lung cancer patients with the EGFR T790M mutation. Transl Lung Cancer Res 2014;3:122-30.
18. 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.
19. Berger C, Sommermeyer D, Hudecek M, Berger M, Balakrishnan A, Paszkiewicz PJ, et al. Safety of targeting ROR1 in primates with chimeric antigen receptor-modified T cells. Cancer Immunol Res 2015;3:206-16.
20. 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.
21. Cui B, Zhang S, Chen L, Yu J, Widhopf GFII, Fecteau JF, et al. Targeting ROR1 inhibits epithelial-mesenchymal transition and metastasis. Cancer Res 2013;73:3649-60.
22. Daneshmanesh AH, Hojjat-Farsangi M, Moshfegh A, Khan AS, Mikaelsson E, Osterborg A, et al. The PI3K/AKT/mTOR pathway is involved in direct apoptosis of CLL cells induced by ROR1 monoclonal antibodies. Br J Haematol 2015;169:455-8.
23. Bicocca VT, Chang BH, Masouleh BK, Muschen M, Loriaux MM, Druker BJ, et al. Crosstalk between ROR1 and the Pre-B cell receptor promotes survival of t(1;19) acute lymphoblastic leukemia. Cancer Cell 2012;22:656-67.
24. Yamaguchi T, Lu C, Ida L, Yanagisawa K, Usukura J, Cheng J, et al. ROR1 sustains caveolae and survival signalling as a scaffold of cavin-1 and caveolin-1. Nat Commun 2016;7:10060.
25. Baskar S, Wiestner A, Wilson WH, Pastan I, Rader C. Targeting malignant B cells with an immunotoxin against ROR1. mAbs 2012;4:349-61.
26. Daneshmanesh AH, Hojjat-Farsangi M, Khan AS, Jeddi-Tehrani M, Akhondi MM, Bayat AA, et al. Monoclonal antibodies against ROR1 induce apoptosis of chronic lymphocytic leukemia (CLL) cells. Leukemia 2012;26:1348-55.
27. Hojjat-Farsangi M, Ghaemimanesh F, Daneshmanesh AH, Bayat AA, Mahmoudian J, Jeddi-Tehrani M, et al. Inhibition of the receptor tyrosine kinase ROR1 by anti-ROR1 monoclonal antibodies and siRNA induced apoptosis of melanoma cells. PLoS One 2013;8:e61167.
28. Choi MY, Widhopf GFII, Wu CC, Cui B, Lao F, Sadarangani A, et al. Preclinical specificity and safety of UC-961, a first-in-class monoclonal antibody targeting ROR1. Clin Lymphoma Myeloma Leuk 2015;15Suppl:S167-9.
29. Hudecek M, Lupo-Stanghellini MT, Kosasih PL, Sommermeyer D, Jensen MC, Rader C, et al. Receptor affinity and extracellular domain modifications affect tumor recognition by ROR1-specific chimeric antigen receptor T cells. Clin Cancer Res 2013;19:3153-64.
30. Kloss CC, Condomines M, Cartellieri M, Bachmann M, Sadelain M. Combinatorial antigen recognition with balanced signaling promotes selective tumor eradication by engineered T cells. Nat Biotechnol 2013;31:71-5.
31. Roybal KT, Rupp LJ, Morsut L, Walker WJ, McNally KA, Park JS, et al. Precision tumor recognition by T cells with combinatorial antigen-sensing circuits. Cell 2016;164:770-9.
32. Budde LE, Berger C, Lin Y, Wang J, Lin X, Frayo SE, et al. Combining a CD20 chimeric antigen receptor and an inducible caspase 9 suicide switch to improve the efficacy and safety of T cell adoptive immunotherapy for lymphoma. PLoS One 2013;8:e82742.
33. Morgan RA, Yang JC, Kitano M, Dudley ME, Laurencot CM, Rosenberg SA. Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing ERBB2. Mol Ther 2010;18:843-51.
34. Sotillo E, Barrett DM, Black KL, Bagashev A, Oldridge D, Wu G, et al. Convergence of acquired mutations and alternative splicing of CD19 enables resistance to CART-19 immunotherapy. Cancer Discov 2015;5:1282-95.
35. Leisegang M, Engels B, Meyerhuber P, Kieback E, Sommermeyer D, Xue SA, et al. Enhanced functionality of T cell receptor-redirected T cells is defined by the transgene cassette. J Mol Med 2008;86:573-83.
36. Zaritskaya L, Shurin MR, Sayers TJ, Malyguine AM. New flow cytometric assays for monitoring cell-mediated cytotoxicity. Expert Rev Vaccines 2010;9:601-16.
37. Lamers CH, Sleijfer S, van Steenbergen S, van Elzakker P, van Krimpen B, Groot C, et al. Treatment of metastatic renal cell carcinoma with CAIX CAR-engineered T cells: clinical evaluation and management of on-target toxicity. Mol Ther 2013;21:904-12.
38. Hassan R, Bullock S, Premkumar A, Kreitman RJ, Kindler H, Willingham MC, et al. Phase I study of SS1P, a recombinant anti-mesothelin immunotoxin given as a bolus I.V. infusion to patients with mesothelin-expressing mesothelioma, ovarian, and pancreatic cancers. Clin Cancer Res 2007;13:5144-9.
39. Kaucka M, Krejci P, Plevova K, Pavlova S, Prochazkova J, Janovska P, et al. Post-translational modifications regulate signalling by Ror1. Acta Physiol 2011;203:351-62.
40. Deniger DC, Yu J, Huls MH, Figliola MJ, Mi T, Maiti SN, et al. Sleeping beauty transposition of chimeric antigen receptors targeting receptor tyrosine kinase-like orphan receptor-1 (ROR1) into diverse memory T-cell populations. PLoS One 2015;10:e0128151.
41. Reddy UR, Phatak S, Pleasure D. Human neural tissues express a truncated Ror1 receptor tyrosine kinase, lacking both extracellular and transmembrane domains. Oncogene 1996;13:1555-9.
42. Hojjat-Farsangi M, Khan AS, Daneshmanesh AH, Moshfegh A, Sandin A, Mansouri L, et al. The tyrosine kinase receptor ROR1 is constitutively phosphorylated in chronic lymphocytic leukemia (CLL) cells. PLoS One 2013;8:e78339.
43. Denucci CC, Mitchell JS, Shimizu Y. Integrin function in T-cell homing to lymphoid and nonlymphoid sites: getting there and staying there. Crit Rev Immunol 2009;29:87-109.
44. Sigmundsdottir H, Butcher EC. Environmental cues, dendritic cells and the programming of tissue-selective lymphocyte trafficking. Nat Immunol 2008;9:981-7.
45. Iwata M, Hirakiyama A, Eshima Y, Kagechika H, Kato C, Song SY. Retinoic acid imprints gut-homing specificity on T cells. Immunity 2004;21:527-38.
46. Beatty GL, Haas AR, Maus MV, Torigian DA, Soulen MC, Plesa G, et al. Mesothelin-specific chimeric antigen receptor mRNA-engineered T cells induce anti-tumor activity in solid malignancies. Cancer Immunol Res 2014;2:112-20.
47. Kershaw MH, Wang G, Westwood JA, Pachynski RK, Tiffany HL, Marincola FM, et al. Redirecting migration of T cells to chemokine secreted from tumors by genetic modification with CXCR2. Hum Gene Ther 2002;13:1971-80.
48. Craddock JA, Lu A, Bear A, Pule M, Brenner MK, Rooney CM, et al. Enhanced tumor trafficking of GD2 chimeric antigen receptor T cells by expression of the chemokine receptor CCR2b. J Immunother 2010;33:780-8.
49. Brown CE, Badie B, Barish ME, Weng L, Ostberg JR, Chang WC, et al. Bioactivity and safety of IL13Ralpha2-redirected chimeric antigen receptor CD8+ T cells in patients with recurrent glioblastoma. Clin Cancer Res 2015;21:4062-72.
50. Wu CY, Roybal KT, Puchner EM, Onuffer J, Lim WA. Remote control of therapeutic T cells through a small molecule-gated chimeric receptor. Science 2015;350:aab4077.