New developments in molecular diagnostics of carcinomas of the salivary glands: “translocation carcinomas”

1. Mitelman F, Johansson B, Mertens F. The impact of translocations and gene fusions on cancer causation. Nat Rev Cancer 2007; 7(4): 233-245.

2. Stenman G. Fusion oncogenes and tumor type specificity – insight from salivary gland tumors. Semin Cancer Biol 2005; 15(3): 224-235.

3. Aman P. Fusion oncogenes in tumor development. Semin Cancer Biol 2005; 15(3): 236-243.

4. Mitelman F, Johansson B, Mertens F, eds. Mitelman database of chromosome aberrations and gene fusions in cancer: http://cgap.nci.nih.gov/Chromosomes/Mitelman, 2013.

5. Asp J, Persson F, Kost-Alimova M, Stenman G. CHCHD7-PLAG1 and TCEA1-PLAG1 gene fusions resulting from cryptic, intrachromosomal 8q rearrangements in pleomorphic salivary gland adenomas. Genes Chromosomes Cancer 2006; 45(9): 820-828.

6. Persson F, Winnes M, Andrén Y, et al. High-resolution array CGH analysis of salivary gland tumors reveals fusion and amplification of the FGFR1 and PLAG1 genes in ring chromosomes. Oncogene 2008; 27(21): 3072-3080.

7. Persson F, Andrén Y,Winnes M, et al. High-resolution genomic profiling of adenomas and carcinomas of the salivary glands reveals amplification, rearrangement, and fusion of HMGA2. Genes Chromosomes Cancer 2009; 48(1): 69-82.

8. Stenman G, Andersson MK, Andrén Y. New tricks from an old oncogene: gene fusions and copy number alterations of MYB in human cancer. Cell Cycle 2010; 9(15): 2986-2995.

9. Skalova A, Vaněček T, Šíma R, et al. Mammary analogue secretory carcinoma of salivary glands, containing the ETV6-NTRK3 fusion gene: a hitherto undescribed salivary gland tumor entity. Am J Surg Pathol 2010; 34(5): 599–608.

10. Knezevich SR, McFadden DE, Tao W, Lim JF, Sorensen PH. A novel ETV6-NTRK3 gene fusion in congenital fibrosarcoma. Nat Genet 1998; 18(2): 184–187.

11. Knezevich SR, Garnett MJ, Pysher TJ, Beckwith JB, Grundy PE, Sorensen PH. ETV6-NTRK3 gene fusions and trisomy 11 establish a histogenetic link between mesoblastic nephroma and congenital fibrosarcoma. Cancer Res 1998; 58(22): 5046–5048.

12. Bourgeois JM, Knezevich SR, Mathers JA, Sorensen PH. Molecular detection of the ETV6-NTRK3 gene fusion differentiates congenital fibrosarcoma from other childhood spindle cell tumors. Am J Surg Pathol 2000; 24(7): 937–946.

13. Rubin BP, Chen CJ, Morgan TW, et al. Congenital mesoblastic nephroma t(12;15) is associated with ETV6-NTRK3 gene fusion: cytogenetic and molecular relationship to congenital (infantile) fibrosarcoma. Am J Pathol 1998; 153(5): 1451–1458.

14. Alassiri A, Lum A, Goytain A, et al. ETV6-NTRK3 is expressed in a subset of ALK-negative inflammatory myofibroblastic tumors: case series of 20 patients. Mod Pathol 2015; 28(Supplement 2s): 13A.

15. Kralik JM, Kranewitter W, Boesmueller H, et al. Characterization of a newly identified ETV6 NTRK3 fusion transcript in acute myeloid leukemia. Diagn Pathol 2011; 6:19.

16. Tognon CE, Knezevich SR, Huntsman D, et al. Expression of the ETV6-NTRK3 gene fusion as a primary event in human secretory breast carcinoma. Cancer Cell 2002; 2(5): 367–376.

17. Leeman-Neill RJ, Kelly LM, Liu P, et al. ETV6-NTRK3 is a common chromosomal rearrangement in radiation-associated thyroid cancer. Cancer 2014; 120(6): 799–807.

18. Behboudi A, Enlund F, Winnes M, et al. Molecular classification of mucoepidermoid carcinoma – prognostic significance of the MECT1-MAML2 fusion oncogene. Genes Chromosomes Cancer 2006; 45(5): 470-481.

19. Goode RK, El-Naggar AK. Mucoepidermoid carcinoma. In: Barnes L, Eveson J, Reichart P, Sidransky D, eds. Pathology and genetics of head and neck tumours. World Health Organization classification of tumours. Lyon: IARC Press; 2005: 219-220.

20. Hellquist H, Skalova A. Histopathology of the salivary glands. Berlin, Heidelberg: Springer Verlag; 2014.

21. Tonon G, Modi S, Wu L, et al. t(11;19)(q21;p13) translocation in mucoepidermoid carcinoma creates a novel fusion product that disrupts a Notch signaling pathway. Nat Genet 2003; 33(2): 208-213.

22. Okabe M, Miyabe S, Nagatsuka H, et al. MECT1-MAML2 fusion transcript defines a favorable subset of mucoepidermoid carcinoma. Clin Cancer Res 2006; 12(13): 3902-3907.

23. Seethala RR, Dacic S, Cieply K, Kelly LM, Nikiforova MN. A reappraisal of the MECT1/MAML2 translocation in salivary mucoepidermoid carcinomas. Am J Surg Pathol 2010; 34(8): 1106-1121.

24. Okumura Y, Miyabe S, Nakayama T, Fujiyoshi Y, Hattori H, Shimozato K, Inagaki H. Impact of CRTC1 ⁄ 3–MAML2 fusions on histological classification and prognosis of mucoepidermoid carcinoma. Histopathology 2011; 59(1): 90–97.

25. Fehr A, Röser K, Heidorn K, Hallas C, Löning T, Bullerdiek J. A new type of MAML2 fusion in mucoepidermoid carcinoma. Genes Chromosomes Cancer 2008; 47(3): 203-206.

26. Nakayama T, Miyabe S, Okabe M, et al. Clinicopathological significance of the CRTC3-MAML2 fusion transcript in mucoepidermoid carcinoma. Mod Pathol 2009; 22(12): 1575-1581.

27. Bell D, Luna MA, Weber RS, Kaye FJ, El-Naggar AK. CRTC1/MAML2 fusion transcript in Warthin’s tumor and mucoepidermoid carcinoma: evidence for a common genetic association. Genes Chromosomes Cancer 2008; 47(4): 309–314.

28. Fehr A, Roser K, Belge G, Löning T, Bullerdiek J. A closer look at Warthin tumors and the t(11;19). Cancer Genet Cytogenet 2008; 180(2): 135–139.

29. Skálová A, Vaněček T, Hauer L, et al. CRTC1-MAML2 and CRTC3-MAML2 fusions were not detected in metaplastic Warthin´s tumor and metaplastic pleomorphic adenoma of salivary glands. Am J Surg Pathol 2013; 37(11): 1743-1750.

30. García JJ, Hunt JL, Weinreb I, et al. Fluorescence in situ hybridization for detection of MAML2 rearrangements in oncocytic mucoepidermoid carcinomas: utility as a diagnostic test. Hum Pathol 2011; 42(12): 2001–2009.

31. Bell D, Holsinger CF, El-Naggar AK. CRTC1/MAML2 fusion transcript in central mucoepidermoid carcinoma of mandible—diagnostic and histogenetic implications. Ann Diagn Pathol 2010; 14(6): 396–401.

32. Barnes L, Eveson JW, Reichart P, Sidransky D, eds. World Health Organization Classification of Tumours: Pathology and Genetics of Head and Neck Tumours. Lyon: IARC Press; 2005: 209–281.

33. Amit M, Binenbaum Y, Trejo-Leider L, et al. International collaborative validation of intraneural invasion as a prognostic marker in adenoid cystic carcinoma of the head and neck. Head Neck 2015; 37(7): 1038-1045.

34. Stenman G. Fusion oncogenes in salivary gland tumors: molecular and clinical consequences. Head Neck Pathol 2013; 7 Suppl 1: S12-S19.

35. Stenman G, Persson F, Andersson MK. Diagnostic and therapeutic implications of new molecular biomarkers in salivary gland cancers. Oral Oncol 2014; 50(8): 683-690.

36. Bell D, Hanna EY. Salivary gland cancers: biology and molecular targets for therapy. Curr Oncol Rep 2012; 14(2): 166-174.

37. Persson M, Andrén Y, Mark J, Horlings HM, Persson F, Stenman G. Recurrent fusion of MYB and NFIB transcription factor genes in carcinomas of the breast and head and neck. Proc Natl Acad Sci U S A 2009; 106(44): 18740-18744.

38. Simpson RH, Skálová A, Di Palma S, Leivo I. Recent advances in the diagnostic pathology of salivary carcinomas. Virchows Arch 2014; 465(4): 371-384.

39. Chenevert J, Duvvuri U, Chiosea S, et al. DOG1: a novel marker of salivary acinar and intercalated duct differentiation. Mod Pathol 2012; 25(7): 919–929.

40. Laco J, Svajdler M, Jr, Andrejs J, et al. Mammary analogue secretory carcinoma of salivary glands: a report of 2 cases with expression of basal/ myoepithelial markers (calponin, CD10 and p63 protein). Pathol Res Pract 2013; 209(3): 167-172.

41. Stevens TM, Kovalovsky AO, Velosa C, et al. Mammary analog secretory carcinoma,- low-grade salivary duct carcinoma, and mimickers: a comparative study. Mod Pathol 2015; 28(8): 1084-1100.

42. Reynolds S, Shaheen M, Olson G, Barry M, Wu J, Bocklage T. A case of primary mammary analog secretory carcinoma (MASC) of the thyroid masquerading as papillary thyroid carcinoma: potentially more than a one off. Head Neck Pathol. In press 2016.

43. Lannon CL, Martin MJ, Tognon CE, Jin W, Kim SJ, Sorensen PH. A highly conserved NTRK3 C-terminal sequence in the ETV6-NTRK3 oncoprotein binds the phosphotyrosine binding domain of insulin receptor substrate-1: an essential interaction for transformation. J Biol Chem 2004; 279(8): 6225-6234.

44. Chiosea SI, Griffith C, Assaad A, Seethala RR. Clinicopathological characterization of mammary analogue secretory carcinoma of salivary glands. Histopathology 2012; 61(3) :387–394.

45. Majewska H, Skalova A, Stodulski D, et al. Mammary analogue secretory carcinoma of salivary glands: a new entity associated with ETV6 gene rearrangement. Virchows Arch 2015; 466 (3): 245-254.

46. Skálová A, Vanecek T, Majewska H, et al. Mammary analogue secretory carcinoma of salivary glands with high-grade transformation: report of 3 cases with the ETV6-NTRK3 gene fusion and analysis of TP53, beta-catenin, EGFR, and CCND1 genes. Am J Surg Pathol 2014; 38(1): 23–33.

47. Skálová A, Vaněček T, Simpson RHW, et al. Mammary analogue secretory carcinoma of salivary glands: molecular analysis of 25 ETV6 gene rearranged tumors with lack of detection of classical ETV6-NTRK3 fusion transcript by standard RT-PCR: report of four cases harboring ETV6-X gene fusion. Am J Surg Pathol 2016; 40(1): 3-13.

48. Drilon A, Li G, Dogan S, et al. What hinds behind the MASC: Clinical response and acquired resistance to entrectinib after ETV6-NTRK3 identification in a mammary analogue secretory carcinoma (MASC). Annals Oncol Advance. In press 2016.

49. Milchgrub S, Gnepp DR, Vuitch F, Delgado R, Albores-Saavedra J. Hyalinizing clear cell carcinoma of salivary gland. Am J Surg Pathol 1994; 18(1): 74–82.

50. Michal M, Skálová A, Simpson RH, Rychterová V, Leivo I. Clear cell malignant myoepithelioma of the salivary glands. Histopathology 1996; 28(4): 309–315.

51. Skálová A, Weinreb I, Hyrcza M, et al. Clear cell myoepithelial carcinoma of salivary glands showing EWSR1 rearrangement. Molecular analysis of 94 salivary gland carcinomas with prominent clear cell component. Am J Surg Pathol 2015; 39(3): 338–348

52. Barnes L, Eveson JW, Reichart P, Sidransky D, eds. World Health Organization Classification of Tumours: Pathology and Genetics of Head and Neck Tumours. Lyon: IARC Press; 2005.

53. Antonescu CR, Katabi N, Zhang L, et al. EWSR1-ATF1 fusion is a novel and consistent finding in hyalinizing clear-cell carcinoma of salivary gland. Genes Chromosomes Cancer 2011; 50(7): 559–570.

54. Weinreb I. Translocation-associated salivary gland tumors: a review and update. Adv Anat Pathol 2013; 20(6): 367-377.

55. Bilodeau EA, Hoschar AP, Barnes EL, Hunt JL, Seethala RR. Clear cell carcinoma and clear cell odontogenic carcinoma: a comparative clinicopathologic and immunohistochemical study. Head Neck Pathol 2011; 5(2): 101-107.

56. Dardick I, Leong I. Clear cell carcinoma: review of its histomorphogenesis and classification as a squamous cell lesion. Oral Surg Oral Pathol Oral Radiol Endod 2009; 108(3): 399-405.

57. Shah AA, LeGallo RD, van Zante A, et al. EWSR1 genetic rearrangements in salivary gland tumors: a specific and very common feature of hyalinizing clear cell carcinoma. Am J Surg Pathol 2013; 37(4): 571–578.

58. Bilodeau EA, Weinreb I, Antonescu CR, et al. Clear cell odontogenic carcinomas show EWSR1 rearrangements: a novel finding & biologic link to salivary clear cell carcinomas. Mod Pathol 2012; 25 (Supplement 2s): 101:305A.

59. Bilodeau EA, Bilodeau EA, Weinreb I, et al. Clear cell odontogenic carcinomas show EWSR1 rearrangements: a novel finding and biological link to salivary clear cell carcinomas. Am J Surg Pathol 2013; 37(7): 1001-1005.

60. Stockman DL, Miettinen M, Suster S, et al. Malignant gastrointestinal neuroectodermal tumor: clinicopathologic, immunohistochemical, ultrastructural, and molecular analysis of 16 cases with a reappraisal of clear cell sarcoma-like tumors of the gastrointestinal tract. Am J Surg Pathol 2012; 36(6): 857–868.

61. Gru AA, Becker N, Pfeifer JD. Angiosarcoma of the parotid gland with a t(12;22) translocation creating a EWSR1-ATF1 fusion: a diagnostic dilemma. J Clin Pathol 2013; 66(5): 452–454.

62. Tanguay J, Weinreb I. What the EWSR1-ATF1 Fusion has taught us about hyalinizing clear cell carcinoma. Head and Neck Pathol 2013; 7(1): 28–34.

63. Simpson RWH, Skálová A, Di Palma S, Leivo I. Recent advances in the diagnostic pathology of salivary carcinomas. Virchows Arch 2014; 465(4): 371-384.