Screening for ROS1 gene rearrangements in non-small-cell lung cancers using immunohistochemistry with FISH confirmation is an effective method to identify this rare target

Histopathology

Volumn 70, Issue 3, 2017, Pages 402-411

  Selinger, Christina I ^a   Li, Bob T ^b,c,d   Pavlakis, Nick ^b,d   Links, Matthew ^e   Gill, Anthony J ^b,d   Lee, Adrian ^b   Clarke, Stephen ^b,d   Tran, Thang N ^a   Lum, Trina ^a   Yip, Po Y ^f,g,h,i   Horvath, Lisa ^a,d,f   Yu, Bing ^a,d   Kohonen Corish, Maija R J ^f,g,j   O'Toole, Sandra A ^a,d,f   Cooper, Wendy A ^a,d,g  

^a ROYAL PRINCE ALFRED HOSPITAL   (Australia)

^b ROYAL NORTH SHORE HOSPITAL   (Australia)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d UNIVERSITY OF SYDNEY   (Australia)

^e ST GEORGE HOSPITAL   (Australia)

^f GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^g UNIVERSITY OF WESTERN SYDNEY   (Australia)

^h Chris O Brien Lifehouse   (Australia)

ⁱ CAMPBELLTOWN HOSPITAL   (Australia)

^j UNIVERSITY OF NEW SOUTH WALES   (Australia)

more..

Author keywords

c ros oncogene 1 (ROS1); fluorescence in situ hybridization (FISH); immunohistochemistry (IHC); non small cell lung cancer (NSCLC)

Indexed keywords

ANAPLASTIC LYMPHOMA KINASE; EPIDERMAL GROWTH FACTOR RECEPTOR; PROTEIN; PROTEIN ROS1; UNCLASSIFIED DRUG; ONCOPROTEIN; PROTEIN TYROSINE KINASE; ROS1 PROTEIN, HUMAN; TUMOR MARKER;

ADULT; AGED; ARTICLE; CONTROLLED STUDY; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; GENE MUTATION; GENE REARRANGEMENT; HUMAN; IMMUNOHISTOCHEMISTRY; LUNG ADENOCARCINOMA; MAJOR CLINICAL STUDY; MALE; NON SMALL CELL LUNG CANCER; PREDICTIVE VALUE; PRIORITY JOURNAL; RETROSPECTIVE STUDY; SENSITIVITY AND SPECIFICITY; VERY ELDERLY; GENETICS; LUNG TUMOR; MIDDLE AGED;

ADULT; AGED; AGED, 80 AND OVER; BIOMARKERS, TUMOR; CARCINOMA, NON-SMALL-CELL LUNG; FEMALE; GENE REARRANGEMENT; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION, FLUORESCENCE; LUNG NEOPLASMS; MALE; MIDDLE AGED; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS;

EID: 85003475292     PISSN: 03090167     EISSN: 13652559     Source Type: Journal    
DOI: 10.1111/his.13076     Document Type: Article

References (48)

1. Ou S-HI, Tan J, Yen Y, Soo RA. ROS1 as a ‘druggable’ receptor tyrosine kinase: lessons learned from inhibiting the ALK pathway. Expert Rev. Anticancer Ther. 2012; 12; 447–456.
2. Shibuya M, Hanafusa H, Balduzzi PC. Cellular sequences related to three new onc genes of avian sarcoma virus (fps, yes, and ros) and their expression in normal and transformed cells. J. Virol. 1982; 42; 143–152.
3. Wang LH, Hanafusa H, Notter MF, Balduzzi PC. Genetic structure and transforming sequence of avian sarcoma virus UR2. J. Virol. 1982; 41; 833–841.
4. Balduzzi PC, Notter MF, Morgan HR, Shibuya M. Some biological properties of two new avian sarcoma viruses. J. Virol. 1981; 40; 268–275.
5. Uttamsingh S, Zong CS, Wang L-H. Matrix-independent activation of phosphatidylinositol 3-kinase, Stat3, and cyclin A-associated Cdk2 Is essential for anchorage-independent growth of v-Ros-transformed chicken embryo fibroblasts. J. Biol. Chem. 2003; 278; 18798–18810.
6. Charest A, Wilker EW, McLaughlin ME et al. ROS fusion tyrosine kinase activates a SH2 domain-containing phosphatase-2/phosphatidylinositol 3-kinase/mammalian target of rapamycin signaling axis to form glioblastoma in mice. Cancer Res. 2006; 66; 7473–7481.
7. Nguyen KT, Zong CS, Uttamsingh S et al. The role of phosphatidylinositol 3-kinase, rho family GTPases, and STAT3 in Ros-induced cell transformation. J. Biol. Chem. 2002; 277; 11107–11115.
8. Takeuchi K, Soda M, Togashi Y et al. RET, ROS1 and ALK fusions in lung cancer. Nat. Med. 2012; 18; 378–381.
9. Birchmeier C, Sharma S, Wigler M. Expression and rearrangement of the ROS1 gene in human glioblastoma cells. Proc. Natl Acad. Sci. USA 1987; 84; 9270–9274.
10. Liu P, Wu Y, Sun L, Zuo Q, Shi M. ROS kinase fusions are not common in Chinese patients with cholangiocarcinoma. Nan Fang Yi Ke Da Xue Xue Bao 2013; 33; 474–478.
11. Gu T-L, Deng X, Huang F et al. Survey of tyrosine kinase signaling reveals ROS kinase fusions in human cholangiocarcinoma. PLoS One 2011; 6; e15640.
12. Peraldo Neia C, Cavalloni G, Balsamo A et al. Screening for the FIG-ROS1 fusion in biliary tract carcinomas by nested PCR. Genes Chromosom. Cancer 2014; 53; 1033–1040.
13. Birch AH, Arcand SL, Oros KK et al. Chromosome 3 anomalies investigated by genome wide SNP analysis of benign, low malignant potential and low grade ovarian serous tumours. PLoS One 2011; 6; e28250.
14. Lee J, Lee SE, Kang SY et al. Identification of ROS1 rearrangement in gastric adenocarcinoma. Cancer 2013; 119; 1627–1635.
15. Aisner DL, Nguyen TT, Paskulin DD et al. ROS1 and ALK fusions in colorectal cancer, with evidence of intratumoral heterogeneity for molecular drivers. Mol. Cancer Res. 2014; 12; 111–118.
16. Davies KD, Le AT, Theodoro MF et al. Identifying and targeting ROS1 gene fusions in non-small cell lung cancer. Clin. Cancer Res. 2012; 18; 4570–4579.
17. Bergethon K, Shaw AT, Ou S-HI et al. ROS1 rearrangements define a unique molecular class of lung cancers. J. Clin. Oncol. 2012; 30; 863–870.
18. Tanizaki J, Okamoto I, Okamoto K et al. MET tyrosine kinase inhibitor crizotinib (PF-02341066) shows differential antitumor effects in non-small cell lung cancer according to MET alterations. J. Thorac. Oncol. 2011; 6; 1624–1631.
19. Shaw AT, Ou S-HI, Bang Y-J et al. Crizotinib in ROS1-rearranged non-small-cell lung cancer. N. Engl. J. Med. 2014; 371; 1963–1971.
20. Suehara Y, Arcila M, Wang L et al. Identification of KIF5B–RET and GOPC–ROS1 fusions in lung adenocarcinomas through a comprehensive mRNA-based screen for tyrosine kinase fusions. Clin. Cancer Res. 2012; 18; 6599–6608.
21. Rimkunas VM, Crosby KE, Li D et al. Analysis of receptor tyrosine kinase ROS1-positive tumors in non-small cell lung cancer: identification of a FIG-ROS1 fusion. Clin. Cancer Res. 2012; 18; 4449–4457.
22. Rikova K, Guo A, Zeng Q et al. Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 2007; 131; 1190–1203.
23. Warth A, Muley T, Dienemann H et al. ROS1 expression and translocations in non-small-cell lung cancer: clinicopathological analysis of 1478 cases. Histopathology 2014; 65; 187–194.
24. Yoshida A, Tsuta K, Wakai S et al. Immunohistochemical detection of ROS1 is useful for identifying ROS1 rearrangements in lung cancers. Mod. Pathol. 2014; 27; 711–720.
25. Sholl LM, Sun H, Butaney M et al. ROS1 immunohistochemistry for detection of ROS1-rearranged lung adenocarcinomas. Am. J. Surg. Pathol. 2013; 37; 1441–1449.
26. Shan L, Lian F, Guo L et al. Detection of ROS1 gene rearrangement in lung adenocarcinoma: comparison of IHC, FISH and real-time RT–PCR. PLoS One 2015; 10; e0120422.
27. Mescam-Mancini L, Lantuéjoul S, Moro-Sibilot D et al. On the relevance of a testing algorithm for the detection of ROS1-rearranged lung adenocarcinomas. Lung Cancer 2014; 83; 168–173.
28. Cha YJ, Lee JS, Kim HR et al. Screening of ROS1 rearrangements in lung adenocarcinoma by immunohistochemistry and comparison with ALK rearrangements. PLoS One 2014; 9; e103333.
29. Cao B, Wei P, Liu Z et al. Detection of lung adenocarcinoma with ROS1 rearrangement by IHC, FISH, and RT–PCR and analysis of its clinicopathologic features. OncoTargets Ther. 2016; 9; 131–138.
30. Boyle TA, Masago K, Ellison KE, Yatabe Y, Hirsch FR. ROS1 Immunohistochemistry among major genotypes of non-small-cell lung cancer. Clin. Lung Cancer 2015; 16; 106–111.
31. Lee SE, Lee B, Hong M et al. Comprehensive analysis of RET and ROS1 rearrangement in lung adenocarcinoma. Mod. Pathol. 2015; 28; 468–479.
32. Selinger CI, Rogers T-M, Russell PA et al. Testing for ALK rearrangement in lung adenocarcinoma: a multicenter comparison of immunohistochemistry and fluorescent in situ hybridization. Mod. Pathol. 2013; 26; 1545–1553.
33. Boland JM, Erdogan S, Vasmatzis G et al. Anaplastic lymphoma kinase immunoreactivity correlates with ALK gene rearrangement and transcriptional up-regulation in non-small cell lung carcinomas. Hum. Pathol. 2009; 40; 1152–1158.
34. Camidge DR, Hirsch FR, Varella-Garcia M, Franklin WA. Finding ALK-positive lung cancer: what are we really looking for? J. Thorac. Oncol. 2011; 6; 411–413.
35. Houang M, Toon CW, Clarkson A et al. Reflex ALK immunohistochemistry is feasible and highly specific for ALK gene rearrangements in lung cancer. Pathology 2014; 46; 383–388.
36. Mino-Kenudson M, Chirieac LR, Law K et al. A novel, highly sensitive antibody allows for the routine detection of ALK-rearranged lung adenocarcinomas by standard immunohistochemistry. Clin. Cancer Res. 2010; 16; 1561–1571.
37. Takeuchi K, Choi YL, Togashi Y et al. KIF5B-ALK, a novel fusion oncokinase identified by an immunohistochemistry-based diagnostic system for ALK-positive lung cancer. Clin. Cancer Res. 2009; 15; 3143–3149.
38. Yip PY, Yu B, Cooper WA et al. Patterns of DNA mutations and ALK rearrangement in resected node negative lung adenocarcinoma. J. Thorac. Oncol. 2013; 8; 408–414.
39. Selinger CI, Cooper WA, Al-Sohaily S et al. Loss of special AT-rich binding protein 1 expression is a marker of poor survival in lung cancer. J. Thorac. Oncol. 2011; 6; 1179–1189.
40. Cooper WA, Kohonen-Corish MRJ, Chan C et al. Prognostic significance of DNA repair proteins MLH1, MSH2 and MGMT expression in non-small-cell lung cancer and precursor lesions. Histopathology 2008; 52; 613–622.
41. Tran TN, Selinger CI, Yu B et al. Alterations of insulin-like growth factor-1 receptor gene copy number and protein expression are common in non-small cell lung cancer. J. Clin. Pathol. 2014; 67; 985–991.
42. Tran TN, Selinger CI, Kohonen-Corish MRJ et al. Alterations of MET gene copy number and protein expression in primary non-small-cell lung cancer and corresponding nodal metastases. Clin. Lung Cancer 2016; 17; 30–38.
43. Lira ME, Choi Y-L, Lim SM et al. A single-tube multiplexed assay for detecting ALK, ROS1, and RET fusions in lung cancer. J. Mol. Diagn. 2014; 16; 229–243.
44. Scheffler M, Schultheis A, Teixido C et al. ROS1 rearrangements in lung adenocarcinoma: prognostic impact, therapeutic options and genetic variability. Oncotarget 2015; 6; 10577–10585.
45. Mazières J, Zalcman G, Crinò L et al. Crizotinib therapy for advanced lung adenocarcinoma and a ROS1 rearrangement: results from the EUROS1 cohort. J. Clin. Oncol. 2015; 33; 992–999.
46. Rosell R, Karachaliou N, Wolf J, Ou S-HI. ALK and ROS1 non-small-cell lung cancer: two molecular subgroups sensitive to targeted therapy. Lancet Respir. Med. 2014; 2; 966–968.
47. Gainor JF, Shaw AT. Novel targets in non-small cell lung cancer: ROS1 and RET fusions. Oncologist 2013; 18; 865–875.
48. Wiesner T, Lee W, Obenauf AC et al. Alternative transcription initiation leads to expression of a novel ALK isoform in cancer. Nature 2015; 526; 453–457.