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Review

Receptor tyrosine kinase-like orphan receptor 1: a novel target for cancer immunotherapy

, PhD, , MD & , PhD

Bibliography

  • Ko EC, Wang X, Ferrone S. Immunotherapy of malignant diseases. Challenges and strategies. Int Arch Allergy Immunol 2003;132(4):294-309
  • Vonderheide RH. Telomerase as a universal tumor-associated antigen for cancer immunotherapy. Oncogene 2002;21(4):674-9
  • Ambrosini G, Adida C, Altieri DC. A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat Med 1997;3(8):917-21
  • Novellino L, Castelli C, Parmiani G. A listing of human tumor antigens recognized by T cells: march 2004 update. Cancer Immunol Immunother 2005;54(3):187-207
  • Krause DS, Van Etten RA. Tyrosine kinases as targets for cancer therapy. N Engl J Med 2005;353(2):172-87
  • Hubbard SR, Till JH. Protein tyrosine kinase structure and function. Annu Rev Biochem 2000;69:373-98
  • Forrester WC. The Ror receptor tyrosine kinase family. Cell Mol Life Sci 2002;59(1):83-96
  • Hubbard SR, Mohammadi M, Schlessinger J. Autoregulatory mechanisms in protein-tyrosine kinases. J Biol Chem 1998;273(20):11987-90
  • Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2000;103(2):211-25
  • Nishikawa R, Ji XD, Harmon RC, et al. A mutant epidermal growth factor receptor common in human glioma confers enhanced tumorigenicity. Proc Natl Acad Sci USA 1994;91(16):7727-31
  • Bertram JS. The molecular biology of cancer. Mol Aspects Med 2000;21(6):167-223
  • Paul MK, Mukhopadhyay AK. Tyrosine kinase — Role and significance in Cancer. Int J Med Sci 2004;1(2):101-15
  • Druker BJ. STI571 (Gleevec) as a paradigm for cancer therapy. Trends Mol Med 2002;8(4 Suppl):S14-18
  • Davies SP, Reddy H, Caivano M, et al. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 2000;351(Pt 1):95-105
  • Slamon DJ, Leyland-Jones B, Shak S, et al. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N Engl J Med 2001;344(11):783-92
  • Fulda S, Debatin KM. Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene 2006;25(34):4798-811
  • Shabani M, Asgarian-Omran H, Vossough P, et al. Expression profile of orphan receptor tyrosine kinase (ROR1) and Wilms’ tumor gene 1 (WT1) in different subsets of B-cell acute lymphoblastic leukemia. Leuk Lymphoma 2008;49(7):1360-7
  • Daneshmanesh AH, Hojjat-Farsangi M, Khan AS, et al. Monoclonal antibodies against ROR1 induce apoptosis of chronic lymphocytic leukemia (CLL) cells. Leukemia 2012;26(6):1348-55
  • Masiakowski P, Carroll RD. A novel family of cell surface receptors with tyrosine kinase-like domain. J Biol Chem 1992;267(36):26181-90
  • Reddy UR, Phatak S, Allen C, et al. Localization of the human Ror1 gene (NTRKR1) to chromosome 1p31-p32 by fluorescence in situ hybridization and somatic cell hybrid analysis. Genomics 1997;41(2):283-5
  • Gong Y, Chitayat D, Kerr B, et al. Brachydactyly type B: clinical description, genetic mapping to chromosome 9q, and evidence for a shared ancestral mutation. Am J Hum Genet 1999;64(2):570-7
  • Oldridge M, Temple IK, Santos HG, et al. Brachydactyly type B: linkage to chromosome 9q22 and evidence for genetic heterogeneity. Am J Hum Genet 1999;64(2):578-85
  • Yang J, Baskar S, Kwong KY, et al. Therapeutic potential and challenges of targeting receptor tyrosine kinase ROR1 with monoclonal antibodies in B-cell malignancies. PLoS One 2011;6(6):e21018
  • 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):1-15
  • Wilson C, Goberdhan DC, Steller H. Dror, a potential neurotrophic receptor gene, encodes a Drosophila homolog of the vertebrate Ror family of Trk-related receptor tyrosine kinases. Proc Natl Acad Sci USA 1993;90(15):7109-13
  • Green JL, Kuntz SG, Sternberg PW. Ror receptor tyrosine kinases: orphans no more. Trends Cell Biol 2008;18(11):536-44
  • Gentile A, Lazzari L, Benvenuti S, et al. Ror1 is a pseudokinase that is crucial for Met-driven tumorigenesis. Cancer Res 2011;71(8):3132-41
  • Borcherding N, Kusner D, Liu GH, et al. ROR1, an embryonic protein with an emerging role in cancer biology. Protein Cell 2014;5(7):496-502
  • Oishi I, Takeuchi S, Hashimoto R, et al. Spatio-temporally regulated expression of receptor tyrosine kinases, mRor1, mRor2, during mouse development: implications in development and function of the nervous system. Genes Cells 1999;4(1):41-56
  • Yamaguchi T, Yanagisawa K, Sugiyama R, et al. NKX2-1/TITF1/TTF-1-Induced ROR1 is required to sustain EGFR survival signaling in lung adenocarcinoma. Cancer Cell 2012;21(3):348-61
  • Bicocca VT, Chang BH, Masouleh BK, et al. Crosstalk between ROR1 and the Pre-B cell receptor promotes survival of t(1;19) acute lymphoblastic leukemia. Cancer Cell 2012;22(5):656-67
  • Bainbridge TW, DeAlmeida VI, Izrael-Tomasevic A, et al. Evolutionary divergence in the catalytic activity of the CAM-1, ROR1 and ROR2 kinase domains. PLoS One 2014;9(7):e102695
  • Murphy JM, Zhang Q, Young SN, et al. A robust methodology to subclassify pseudokinases based on their nucleotide-binding properties. Biochem J 2014;457(2):323-34
  • Matsuda T, Nomi M, Ikeya M, et al. Expression of the receptor tyrosine kinase genes, Ror1 and Ror2, during mouse development. Mech Dev 2001;105(1-2):153-6
  • Forrester WC, Dell M, Perens E, et al. A C. elegans Ror receptor tyrosine kinase regulates cell motility and asymmetric cell division. Nature 1999;400(6747):881-5
  • Kim C, Forrester WC. Functional analysis of the domains of the C elegans Ror receptor tyrosine kinase CAM-1. Dev Biol 2003;264(2):376-90
  • Roszmusz E, Patthy A, Trexler M, et al. Localization of disulfide bonds in the frizzled module of Ror1 receptor tyrosine kinase. J Biol Chem 2001;276(21):18485-90
  • Paganoni S, Ferreira A. Neurite extension in central neurons: a novel role for the receptor tyrosine kinases Ror1 and Ror2. J Cell Sci 2005;118(Pt 2):433-46
  • Paganoni S, Ferreira A. Expression and subcellular localization of Ror tyrosine kinase receptors are developmentally regulated in cultured hippocampal neurons. J Neurosci Res 2003;73(4):429-40
  • Nomi M, Oishi I, Kani S, et al. Loss of mRor1 enhances the heart and skeletal abnormalities in mRor2-deficient mice: redundant and pleiotropic functions of mRor1 and mRor2 receptor tyrosine kinases. Mol Cell Biol 2001;21(24):8329-35
  • Al-Shawi R, Ashton SV, Underwood C, et al. Expression of the Ror1 and Ror2 receptor tyrosine kinase genes during mouse development. Dev Genes Evol 2001;211(4):161-71
  • Afzal AR, Rajab A, Fenske CD, et al. Recessive Robinow syndrome, allelic to dominant brachydactyly type B, is caused by mutation of ROR2. Nat Genet 2000;25(4):419-22
  • Oishi I, Sugiyama S, Liu ZJ, et al. A novel Drosophila receptor tyrosine kinase expressed specifically in the nervous system. Unique structural features and implication in developmental signaling. J Biol Chem 1997;272(18):11916-23
  • Burden SJ. The formation of neuromuscular synapses. Genes Dev 1998;12(2):133-48
  • Liu Y, Ross JF, Bodine PV, et al. Homodimerization of Ror2 tyrosine kinase receptor induces 14-3-3(beta) phosphorylation and promotes osteoblast differentiation and bone formation. Mol Endocrinol 2007;21(12):3050-61
  • Liu Y, Rubin B, Bodine PV, et al. Wnt5a induces homodimerization and activation of Ror2 receptor tyrosine kinase. J Cell Biochem 2008;105(2):497-502
  • Liu Y, Bhat RA, Seestaller-Wehr LM, et al. The orphan receptor tyrosine kinase Ror2 promotes osteoblast differentiation and enhances ex vivo bone formation. Mol Endocrinol 2007;21(2):376-87
  • DeChiara TM, Bowen DC, Valenzuela DM, et al. The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell 1996;85(4):501-12
  • Minami Y, Oishi I, Endo M, et al. Ror-family receptor tyrosine kinases in noncanonical Wnt signaling: their implications in developmental morphogenesis and human diseases. Dev Dyn 2010;239(1):1-15
  • Pukrop T, Binder C. The complex pathways of Wnt 5a in cancer progression. J Mol Med (Berl) 2008;86(3):259-66
  • Fukuda T, Chen L, Endo T, 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 USA 2008;105(8):3047-52
  • Cha J, Bartos A, Park C, et al. Appropriate crypt formation in the uterus for embryo homing and implantation requires Wnt5a-ROR signaling. Cell Rep 2014;8(2):382-92
  • Ma Y, Zhang P, Wang F, et al. The relationship between early embryo development and tumourigenesis. J Cell Mol Med 2010;14(12):2697-701
  • Murray MJ, Lessey BA. Embryo implantation and tumor metastasis: common pathways of invasion and angiogenesis. Semin Reprod Endocrinol 1999;17(3):275-90
  • Kani S, Oishi I, Yamamoto H, et al. The receptor tyrosine kinase Ror2 associates with and is activated by casein kinase Iepsilon. J Biol Chem 2004;279(48):50102-9
  • Afzal AR, Jeffery S. One gene, two phenotypes: ROR2 mutations in autosomal recessive Robinow syndrome and autosomal dominant brachydactyly type B. Hum Mutat 2003;22(1):1-11
  • Baskar S, Kwong KY, Hofer T, et al. Unique cell surface expression of receptor tyrosine kinase ROR1 in human B-cell chronic lymphocytic leukemia. Clin Cancer Res 2008;14(2):396-404
  • Daneshmanesh AH, Mikaelsson E, Jeddi-Tehrani 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(5):1190-5
  • Shabani M, Asgarian-Omran H, Jeddi-Tehrani M, et al. Overexpression of orphan receptor tyrosine kinase Ror1 as a putative tumor-associated antigen in Iranian patients with acute lymphoblastic leukemia. Tumour Biol 2007;28(6):318-26
  • Caligaris-Cappio F, Gobbi M, Bofill M, et al. Infrequent normal B lymphocytes express features of B-chronic lymphocytic leukemia. J Exp Med 1982;155(2):623-8
  • Broome HE, Rassenti LZ, Wang HY, et al. ROR1 is expressed on hematogones (non-neoplastic human B-lymphocyte precursors) and a minority of precursor-B acute lymphoblastic leukemia. Leuk Res 2011;35(10):1390-4
  • Uhrmacher S, Schmidt C, Erdfelder F, et al. Use of the receptor tyrosine kinase-like orphan receptor 1 (ROR1) as a diagnostic tool in chronic lymphocytic leukemia (CLL). Leuk Res 2011;35(10):1360-6
  • Caldwell CW, Poje E, Helikson MA. B-cell precursors in normal pediatric bone marrow. Am J Clin Pathol 1991;95(6):816-23
  • Malhotra S, Baba Y, Garrett KP, et al. Contrasting responses of lymphoid progenitors to canonical and noncanonical Wnt signals. J Immunol 2008;181(6):3955-64
  • Rosenwald A, Alizadeh AA, Widhopf G, et al. Relation of gene expression phenotype to immunoglobulin mutation genotype in B cell chronic lymphocytic leukemia. J Exp Med 2001;194(11):1639-47
  • Shabani M, Asgarian Omran H, Farsangi MH, et al. Comparative expression profile of orphan receptor tyrosine kinase ROR1 in Iranian patients with lymphoid and myeloid leukemias. Avicenna J Med Biotechnol 2011;3(3):119-25
  • Hamblin TJ, Davis Z, Gardiner A, et al. Unmutated Ig V(H) genes are associated with a more aggressive form of chronic lymphocytic leukemia. Blood 1999;94(6):1848-54
  • Kaucka M, Krejci P, Plevova K, et al. Post-translational modifications regulate signalling by Ror1. Acta Physiol (Oxf) 2011;203(3):351-62
  • Valenzuela DM, Stitt TN, DiStefano PS, et al. Receptor tyrosine kinase specific for the skeletal muscle lineage: expression in embryonic muscle, at the neuromuscular junction, and after injury. Neuron 1995;15(3):573-84
  • Hojjat-Farsangi M, Khan AS, Daneshmanesh AH, et al. The tyrosine kinase receptor ROR1 is constitutively phosphorylated in chronic lymphocytic leukemia (CLL) cells. PLoS One 2013;8(10):e78339
  • Daneshmanesh AH, Porwit A, Hojjat-Farsangi M, et al. Orphan receptors tyrosine kinase ROR1 and ROR2 in hematological malignancies. Leuk Lymphoma 2012;54(4):843-50
  • Barna G, Mihalik R, Timar B, et al. ROR1 expression is not a unique marker of CLL. Hematol Oncol 2011;29(1):17-21
  • Muller-Tidow C, Schwable J, Steffen B, et al. High-throughput analysis of genome-wide receptor tyrosine kinase expression in human cancers identifies potential novel drug targets. Clin Cancer Res 2004;10(4):1241-9
  • Rabbani H, Ostadkarampour M, Danesh Manesh AH, et al. Expression of ROR1 in patients with renal cancer—a potential diagnostic marker. Iran Biomed J 2010;14(3):77-82
  • Zhang S, Chen L, Wang-Rodriguez J, et al. The onco-embryonic antigen ROR1 is expressed by a variety of human cancers. Am J Pathol 2012;181(6):1903-10
  • Zhang S, Chen L, Cui B, et al. ROR1 is expressed in human breast cancer and associated with enhanced tumor-cell growth. PLoS One 2012;7(3):e31127
  • Cui B, Zhang S, Chen L, et al. Targeting ROR1 inhibits epithelial-mesenchymal transition and metastasis. Cancer Res 2013;73(12):3649-60
  • Zhang H, Qiu J, Ye C, et al. ROR1 expression correlated with poor clinical outcome in human ovarian cancer. Sci Rep 2014;4:5811
  • Zhang S, Cui B, Lai H, et al. Ovarian cancer stem cells express ROR1, which can be targeted for anti-cancer-stem-cell therapy. Proc Natl Acad Sci USA 2014;111(48):17266-71
  • Hojjat-Farsangi M, Ghaemimanesh F, Daneshmanesh AH, 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(4):e61167
  • Gentile A, Lazzari L, Benvenuti S, et al. The ROR1 pseudokinase diversifies signaling outputs in MET-addicted cancer cells. Int J Cancer 2014;135(10):2305-16
  • MacKeigan JP, Murphy LO, Blenis J. Sensitized RNAi screen of human kinases and phosphatases identifies new regulators of apoptosis and chemoresistance. Nat Cell Biol 2005;7(6):591-600
  • Choudhury A, Derkow K, Daneshmanesh AH, et al. Silencing of ROR1 and FMOD with siRNA results in apoptosis of CLL cells. Br J Haematol 2010;151(4):327-35
  • Mikaelsson E, Danesh-Manesh AH, Luppert A, et al. Fibromodulin, an extracellular matrix protein: characterization of its unique gene and protein expression in B-cell chronic lymphocytic leukemia and mantle cell lymphoma. Blood 2005;105(12):4828-35
  • Widhopf GF2nd, Cui B, Ghia EM, et al. ROR1 can interact with TCL1 and enhance leukemogenesis in Emu-TCL1 transgenic mice. Proc Natl Acad Sci USA 2014;111(2):793-8
  • Lagneaux L, Delforge A, Bron D, et al. Chronic lymphocytic leukemic B cells but not normal B cells are rescued from apoptosis by contact with normal bone marrow stromal cells. Blood 1998;91(7):2387-96
  • Lu D, Zhao Y, Tawatao R, et al. Activation of the Wnt signaling pathway in chronic lymphocytic leukemia. Proc Natl Acad Sci USA 2004;101(9):3118-23
  • Memarian A, Hojjat-Farsangi M, Asgarian-Omran H, et al. Variation in WNT genes expression in different subtypes of chronic lymphocytic leukemia. Leuk Lymphoma 2009;50(12):2061-70
  • Hudecek M, Schmitt TM, Baskar S, 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(22):4532-41
  • Li P, Harris D, Liu Z, et al. Stat3 activates the receptor tyrosine kinase like orphan receptor-1 gene in chronic lymphocytic leukemia cells. PLoS One 2010;5(7):e11859
  • Katoh M. STAT3-induced WNT5A signaling loop in embryonic stem cells, adult normal tissues, chronic persistent inflammation, rheumatoid arthritis and cancer (Review). Int J Mol Med 2007;19(2):273-8
  • Hao J, Li TG, Qi X, et al. WNT/beta-catenin pathway up-regulates Stat3 and converges on LIF to prevent differentiation of mouse embryonic stem cells. Dev Biol 2006;290(1):81-91
  • Kim WB, Lewis CJ, McCall KD, et al. Overexpression of Wnt-1 in thyrocytes enhances cellular growth but suppresses transcription of the thyroperoxidase gene via different signaling mechanisms. J Endocrinol 2007;193(1):93-106
  • Vervoordeldonk SF, Merle PA, van Leeuwen EF, et al. Preclinical studies with radiolabeled monoclonal antibodies for treatment of patients with B-cell malignancies. Cancer 1994;73(3 Suppl):1006-11
  • Boyd K, Dearden CE. Alemtuzumab in the treatment of chronic lymphocytic lymphoma. Expert Rev Anticancer Ther 2008;8(4):525-33
  • Cui B, Widhopf GFII, Yu J, et al. Targeting of Chronic Lymphocytic Leukemia B Cells with a Novel Monoclonal Antibody to ROR1 53rd ASH Annual Meeting and Exposition. American Society of Hematology; Washington, DC, USA: 2011
  • Baskar S, Wiestner A, Wilson WH, et al. Targeting malignant B cells with an immunotoxin against ROR1. Mabs 2012;4(3):349-61
  • O’Connell MP, Marchbank K, Webster MR, et al. Hypoxia induces phenotypic plasticity and therapy resistance in melanoma via the tyrosine kinase receptors ROR1 and ROR2. Cancer Discov 2013;3(12):1378-93
  • Narayanan R, Yepuru M, Coss CC, et al. Discovery and preclinical characterization of novel small molecule TRK and ROS1 tyrosine kinase inhibitors for the treatment of cancer and inflammation. PLoS ONE 2013;8(12):e83380
  • Akinleye A, Chen Y, Mukhi N, et al. Ibrutinib and novel BTK inhibitors in clinical development. J Hematol Oncol 2013;6:59
  • Ponader S, Chen SS, Buggy JJ, et al. The Bruton tyrosine kinase inhibitor PCI-32765 thwarts chronic lymphocytic leukemia cell survival and tissue homing in vitro and in vivo. Blood 2012;119(5):1182-9
  • Mellstedt H, Khan AS, Vagberg J, et al. Effect of ROR1-targeting small molecules on chronic lymphocytic leukemia (CLL) cells. ASCO Annual Meeting. Chicago, IL, USA. J Clin Oncol 2012;30(Suppl):Abstract 6557
  • Hojjat-Farsangi M. Small-molecule inhibitors of the receptor tyrosine kinases: promising tools for targeted cancer therapies. Int J Mol Sci 2014;15(8):13768-801
  • Garuti L, Roberti M, Bottegoni G. Non-ATP competitive protein kinase inhibitors. Curr Med Chem 2010;17(25):2804-21
  • Pillay V, Allaf L, Wilding AL, et al. The plasticity of oncogene addiction: implications for targeted therapies directed to receptor tyrosine kinases. Neoplasia 2009;11(5):448-58. 2 p following 58
  • Stommel JM, Kimmelman AC, Ying H, et al. Coactivation of receptor tyrosine kinases affects the response of tumor cells to targeted therapies. Science 2007;318(5848):287-90
  • Gordus A, Krall JA, Beyer EM, et al. Linear combinations of docking affinities explain quantitative differences in RTK signaling. Mol Syst Biol 2009;5:235
  • Xu AM, Huang PH. Receptor tyrosine kinase coactivation networks in cancer. Cancer Res 2010;70(10):3857-60
  • Asgarian Omran H, Shabani M, Shahrestani T, et al. Immunophenotypic subtyping of leukemic cells from Iranian patients with acute lymphoblastic leukaemia: association to disease outcome. Iran J Immunol 2007;4(1):15-25
  • Tseng HC, Lyu PC, Lin WC. Nuclear localization of orphan receptor protein kinase (Ror1) is mediated through the juxtamembrane domain. BMC Cell Biol 2010;11:48

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