K5/K14-positive cells contribute to salivary gland-like breast tumors with myoepithelial differentiation

Modern Pathology

Volumn 26, Issue 8, 2013, Pages 1086-1100

  Boecker, Werner ^a,b   Stenman, Goeran ^c   Loening, Thomas ^d   Andersson, Mattias K ^c   Bankfalvi, Agnes ^e   Von Holstein, Sarah ^f,g   Heegaard, Steffen ^f,g   Lange, Alina ^a   Berg, Tobias ^a   Samoilova, Vera ^a   Tiemann, Katharina ^a   Buchwalow, Igor ^a  

^a Institute for Hematopathology Reference Centre for Gynaeco and Breast Pathology   (Germany)

^b UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

^d ALBERTINEN KRANKENHAUS   (Germany)

^e UNIVERSITY HOSPITAL ESSEN   (Germany)

^f UNIVERSITY OF COPENHAGEN   (Denmark)

^g GLOSTRUP UNIVERSITY HOSPITAL   (Denmark)

Author keywords

Keratin 14; Keratin 5; p63; Progenitor cells; Salivary gland like breast tumors; Triple immunofluorescence

Indexed keywords

COLLAGEN TYPE 4; CYTOKERATIN 10; CYTOKERATIN 14; CYTOKERATIN 5; LAMININ; PROTEIN P63; SMOOTH MUSCLE ACTIN;

ADENOID CYSTIC CARCINOMA; ADENOMYOEPITHELIOMA; ARTICLE; BREAST TUMOR; CELL DIFFERENTIATION; CELL LINEAGE; COMPARATIVE STUDY; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE; LACRIMAL GLAND TUMOR; MYOEPITHELIOMA; MYOEPITHELIUM CELL; PLEOMORPHIC ADENOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALIVARY GLAND TUMOR; SPINDLE CELL; SQUAMOUS CELL; SQUAMOUS CELL METAPLASIA; STEM CELL;

ADENOMA, PLEOMORPHIC; BREAST NEOPLASMS; CARCINOMA, ADENOID CYSTIC; CELL DIFFERENTIATION; CELL LINEAGE; DIAGNOSIS, DIFFERENTIAL; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MYOEPITHELIOMA; REAL-TIME POLYMERASE CHAIN REACTION; SALIVARY GLAND NEOPLASMS; STEM CELLS; TUMOR MARKERS, BIOLOGICAL;

EID: 84881311429     PISSN: 08933952     EISSN: 15300285     Source Type: Journal    
DOI: 10.1038/modpathol.2013.45     Document Type: Article

References (97)

1. Wick MR, Ockner DM, Mills SE, et al. Homologous carcinomas of the breasts, skin, and salivary glands. A histologic and immunohistochemical comparison of ductal mammary carcinoma, ductal sweat gland carcinoma, and salivary duct carcinoma. Am J Clin Pathol 1998;109:75-84.
2. Foschini MP, Pizzicannella G, Peterse JL, et al. Adenomyoepithelioma of the breast associated with lowgrade adenosquamous and sarcomatoid carcinomas. Virchows Arch 1995;427:243-250.
3. Pia-Foschini M, Reis-Filho JS, Eusebi V, et al. Salivary gland-like tumours of the breast: Surgical and molecular pathology. J Clin Pathol 2003;56:497-506.
4. Eveson JW, Auclair PL, Gnepp DR, et al. Tumours of the salivary glands: Introduction, In: Barnes L, Eveson JW, Reichert P, Sidransky D (eds) Pathology and Genetics of Head and Neck Tumours. IARC Press: Lyon; 2005, pp 212-215.
5. Sapino A, Sneige N, Euseby V. Adenoid cystic carcinoma, In: Lakhani SR, Ellis IO, Schnitt SJ, Tan PH, van de Vijver MJ (eds) WHO Classification of Tumors of the Breast. IARC: Lyon; 2012, pp 56-57.
6. Tavassoli FA, Eusebi V. Tumors of the Mammary Gland. American Registry of Pathology: Washington, DC, USA; 2009, pp 212-260.
7. Foschini MP, Simpson JF, O'Malley FO. Ductal adenoma, In: Lakhani SR, Ellis IO, Schnitt SJ, Tan PH, van de Vijver MJ (eds) WHO Classification of Tumors of the Breast. IARC: Lyon; 2012, pp 117-118.
8. Schmitt F, Tan PH, Dabbs S, et al. Myoepithelial and epithelial- myoepithelial lesions, In: Lakhani SR, Ellis IO, Schnitt SJ, Tan PH, van de Vijver MJ (eds) WHO Classification of tumors of the breast. IARC: Lyon; 2012, pp 119-123.
9. Diaz NM, McDivitt R, Wick MR. Pleomorphic adenoma of the breast: A clinicopathologic and immunohistochemical study of 10 cases. Hum Pathol 1991;22: 1206-1214.
10. Van Hoeven KH, Drudis T, Cranor ML, et al. Low-grade adenosquamous carcinoma of the breast. A clinocopathologic study of 32 cases with ultrastructural analysis. Am J Surg Pathol 1993;17:248-258.
11. Rosen PP. Rosen's Breast Pathology, 3rd edn. Wolters Kluwer, Lippincott Wiliams and Wilkins: Philadelphia, PA, USA; 2009, pp 56-57, 117-118, 119-123.
12. Moll R, Divo M, Langbein L. The human keratins: Biology and pathology. Histochem Cell Biol 2008;129:705-733.
13. Moll R, Krepler R, Franke WW. Complex cytokeratin polypeptide patterns observed in certain human carcinomas. Differentiation 1983;23:256-269.
14. Moll R. Cytokeratins as markers of differentiation in the diagnosis of epithelial tumors. Subcell Biochem 1998;31:205-262.
15. Reis-Filho JS, Schmitt FC. Taking advantage of basic research: P63 is a reliable myoepithelial and stem cell marker. Adv Anat Pathol 2002;9:280-289.
16. Reis-Filho JS, Simpson PT, Martins A, et al. Distribution of p63, cytokeratins 5/6 and cytokeratin 14 in 51 normal and 400 neoplastic human tissue samples using TARP-4 multi-tumor tissue microarray. Virchows Arch 2003;443:122-132.
17. Di Tommaso L, Pasquinelli G, Damiani S. Smooth muscle cell differentiation in mammary stromo-epithelial lesions with evidence of a dual origin: Stromal myofibroblasts and myoepithelial cells. Histopathology 2003;42:448-456.
18. Gusterson BA, Warburton MJ, Mitchell D, et al. Distribution of myoepithelial cells and basement membrane proteins in the normal breast and in benign and malignant breast diseases. Cancer Res 1982; 42:4763-4770.
19. Yeh IT, Mies C. Application of immunohistochemistry to breast lesions. Arch Pathol Lab Med 2008;132: 349-358.
20. Barnes L, Tse LLY, Hunt JL, et al. Tumours of the hypopharinx, larinx and trachea: Introduction. In: Barnes L, Eveson JW, Reichert P, Sidransky D (eds) Pathology and Genetics of Head and Neck Tumours. IARC Press: Lyon; 2005, pp 111-117.
21. El-Naggar A, Huvos AG. Adenoid cystic carcinoma, In: Barnes L, Eveson JW, Reichert P, Sidransky D (eds) Pathology and Genetics of Head and Neck Tumours. IARC Press: Lyon; 2005, pp 221-222.
22. Fonseca I, Soares J. Epithelial-myoepithelial carcinoma, In: Barnes L, Eveson JW, Reichert P, Sidransky D (eds) Pathology and Genetics of Head and Neck Tumours. IARC Press: Lyon; 2005, pp 225-226.
23. Skalova A, Jäkel KT. Myoepithelial carcinoma, In: Barnes L, Eveson JW, Reichert P, Sidransky D (eds) Tumours of the Hypopharinx, Larinx and Trachea: Introduction. IARC Press: Lyon; 2005, pp 240-241.
24. Gnepp DR. Metastasizing pleomorphic adenoma, In: Barnes L, Eveson JW, Reichert P, Sidransky D (eds) Pathology and Genetics of Head and Neck Tumours. IARC Press: Lyon; 2005, pp 245-246.
25. Eveson JW, Kusafuka K, Stenman G, et al. Pleomorphic adenoma, In: Barnes L, Eveson JW, Reichert P, Sidransky D (eds) Pathology and Genetics of Head and Neck Tumours. IARC Press: Lyon; 2005, pp 254-258.
26. Cardesa A, Alos L. Myoepithelioma, In: Barnes L, Eveson JW, Reichert P, Sidransky D (eds) Pathology and Genetics of Head and Neck Tumours. IARC Press: Lyon; 2005, pp 259-260.
27. Buchwalow IB, Boecker W. Immunohistochemistry: Basics and Methods. Springer: Heidelberg, Dordrecht, London, New York; 2010, pp 19-30, 69-76, 109-128.
28. Buchwalow IB, Minin EA, Boecker W. A multicolor fluorescence immunostaining technique for simultaneous antigen targeting. Acta Histochem 2005;107:143-148.
29. Brown JK, Pemberton AD, Wright SH, et al. Primary antibody-Fab fragment complexes: A flexible alternative to traditional direct and indirect immunolabeling techniques. J Histochem Cytochem 2004;52: 1219-1230.
30. Nordkvist A, Gustafsson H, Juberg-Ode M, et al. Recurrent rearrangements of 11q14-22 in mucoepidermoid carcinoma. Cancer Genet Cytogenet 1994;74: 77-83.
31. Persson H, Kvist A, Vallon-Christersson J, et al. The non-coding RNA of the multidrug resistance-linked vault particle encodes multiple regulatory small RNAs. Nat Cell Biol 2009;11:1268-1271.
32. Brill LB 2nd, Kanner WA, Fehr A, et al. Analysis of MYB expression and MYB-NFIB gene fusions in adenoid cystic carcinoma and other salivary neoplasms. Mod Pathol 2011;24:1169-1176.
33. Moran CA, Suster S, Carter D. Benign mixed tumors (pleomorphic adenomas) of the breast. Am J Surg Pathol 1990;14:913-921.
34. Williams RW, Leach WB. Mixed tumor of female breast of unusual duration and size. South Med J 1975;68: 97-100.
35. Soreide JA, Anda O, Eriksen L, et al. Pleomorphic adenoma of the human breast with local recurrence. Cancer 1988;61:997-1001.
36. Tavassoli FA, Devilee PWHO. Classification of Tumours, Tumours of the Breast and Female Genital Organs, In: Tavassoli FA, Devilee P (eds), IARC Press: Lyon, 2003.
37. Lakhani SR, Ellis IO, Schnitt SJ, et al. WHO Classification of Tumors of the Breast, 4th edn. IARC Press: Lyon, 2012.
38. Foschini MP, Krausz T. Salivary gland-type tumors of the breast: A spectrum of benign and malignant tumors including "triple negative carcinomas" of low malignant potential. Semin Diagn Pathol 2010;27:77-90.
39. Reis-Filho JS, Milanezi F, Silva P, et al. Maspin expression in myoepithelial tumors of the breast. Pathol Res Pract 2001;197:817-821.
40. Kasami M, Olson SJ, Simpson JF, et al. Maintenance of polarity and a dual cell population in adenoid cystic carcinoma of the breast: An immunohistochemical study. Histopathology 1998;32:232-238.
41. Lamovec J, Us-Krasovec M, Zidar A, et al. Adenoid cystic carcinoma of the breast: A histologic, cytologic, and immunohistochemical study. Semin Diagn Pathol 1989;6:153-164.
42. Marchio C, Weigelt B, Reis-Filho JS. Adenoid cystic carcinomas of the breast and salivary glands (or 'The strange case of Dr Jekyll and Mr Hyde' of exocrine gland carcinomas). J Clin Pathol 2010;63:220-228.
43. McLaren BK, Smith J, Schuyler PA, et al. Adenomyoepithelioma: Clinical, histologic, and immunohistologic evaluation of a series of related lesions. Am J Surg Pathol 2005;29:1294-1299.
44. Moritani S, Kushima R, Sugihara H, et al. Availability of CD10 immunohistochemistry as a marker of breast myoepithelial cells on paraffin sections. Mod Pathol 2002;15:397-405.
45. Hamperl H. The myothelia (myoepithelial cells). Normal state; regressive changes; hyperplasia; tumors. Curr Top Pathol 1970;53:161-220.
46. Loose JH, Patchefsky AS, Hollander IJ, et al. Adenomyoepithelioma of the breast. A spectrum of biologic behavior. Am J Surg Pathol 1992;16:868-876.
47. Tavassoli FA, Norris HJ. Mammary adenoid cystic carcinoma with sebaceous differentiation. A morphologic study of the cell types. Arch Pathol Lab Med 1986;110:1045-1053.
48. Hungermann D, Buerger H, Oehlschlegel C, et al. Adenomyoepithelial tumours and myoepithelial carcinomas of the breast-a spectrum of monophasic and biphasic tumours dominated by immature myoepithelial cells. BMC Cancer 2005;5:92.
49. Lim SK, Kovi J, Warner OG. Adenoid cystic carcinoma of breast with metastasis: A case report and review of the literature. J Natl Med Assoc 1979;71:329-330.
50. Qizilbash AH, Patterson MC, Oliveira KF. Adenoid cystic carcinoma of the breast. Light and electron microscopy and a brief review of the literature. Arch Pathol Lab Med 1977;101:302-306.
51. Rosen PP. Rosen's Breast Pathology, 3rd edn. Wolters Kluwer, Lippincott Wiliams and Wilkins: Philadelphia, PA, USA; 2009, pp 92.
52. Boecker W, Moll R, Poremba C, et al. Common adult stem cells in the human breast give rise to glandular and myoepithelial cell lineages: A new cell biological concept. Lab Invest 2002;82:737-746.
53. Dontu G, Al Hajj M, Abdallah WM, et al. Stem cells in normal breast development and breast cancer. Cell Prolif 2003;36(Suppl 1):59-72.
54. Prat A, Perou CM. Mammary development meets cancer genomics. Nat Med 2009;15:842-844.
55. Van Keymeulen A, Rocha AS, Ousset M, et al. Distinct stem cells contribute to mammary gland development and maintenance. Nature 2011;479:189-193.
56. Langbein L, Cribier B, Schirmacher P, et al. New concepts on the histogenesis of eccrine neoplasia from keratin expression in the normal eccrine gland, syringoma and poroma. Br J Dermatol 2008;159: 633-645.
57. Moll R, Franke WW, Schiller DL, et al. The catalog of human cytokeratins: Patterns of expression in normal epithelia, tumors and cultured cells. Cell 1982;31:11-24.
58. Hamperl H. The myothelia (myoepithelial cells). Normal state; regressive changes; hyperplasia; tumors. Curr Top Pathol 1970;53:161-120.
59. Rosen PP. Adenomyoepithelioma of the breast. Hum Pathol 1987;18:1232-1237.
60. Tavassoli FA. Myoepithelial lesions of the Breast. Myoepitheliosis, adenomyoepithelioma, and myoepithelial carcinoma. Am J Surg Pathol 1991;15:554-568.
61. Weidner N, Levine JD. Spindle-cell adenomyoepithelioma of the breast. A microscopic, ultrastructural, and immunocytochemical study. Cancer 1988;62: 1561-1567.
62. Loose JH, Patchefsky AS, Hollander IJ, et al. Adenomyoepithelioma of the breast. A spectrum of biologic behavior. Am J Surg Pathol 1992;16:868-876.
63. Cho KJ, el-Naggar AK, Ordonez NG, et al. Epithelial-myoepithelial carcinoma of salivary glands. A clinicopathologic, DNA flow cytometric, and immunohistochemical study of Ki-67 and HER-2/neu oncogene. Am J Clin Pathol 1995;103:432-437.
64. Corio RL, Sciubba JJ, Brannon RB, et al. Epithelialmyoepithelial carcinoma of intercalated duct origin. A clinicopathologic and ultrastructural assessment of sixteen cases. Oral Surg Oral Med Oral Pathol 1982;53:280-287.
65. Donath K, Seifert G, Schmitz R. Diagnosis and ultrastructure of the tubular carcinoma of salivary gland ducts. Epithelial-myoepithelial carcinoma of the intercalated ducts. Virchows Arch A Pathol Pathol Anat 1972;356:16-31.
66. Luna MA, Ordonez NG, Mackay B, et al. Salivary epithelial-myoepithelial carcinomas of intercalated ducts: A clinical, electron microscopic, and immunocytochemical study. Oral Surg Oral Med Oral Pathol 1985;59:482-490.
67. Lakhani SR, O'Hare MJ, Monaghan P, et al. Malignant myoepithelioma (myoepithelial carcinoma) of the breast: A detailed cytokeratin study. J Clin Pathol 1995;48:164-167.
68. Thorner PS, Kahn HJ, Baumal R, et al. Malignant myoepithelioma of the breast. An immunohistochemical study by light and electron microscopy. Cancer 1986;57:745-750.
69. Jennens RR, Rosenthal MA, Gonzales M. Metastatic myoepithelioma of the breast. ANZ J Surg 2004; 74:1135-1137.
70. Shiraishi T, Nakayama T, Fukutome K, et al. Malignant myoepithelioma of the breast metastasizing to the jaw. Virchows Arch 1999;435:520-523.
71. Chen PC, Chen CK, Nicastri AD, et al. Myoepithelial carcinoma of the breast with distant metastasis and accompanied by adenomyoepitheliomas. Histopathology 1994;24:543-548.
72. Lee AH, Rakha EA, Hodi Z, et al. Re-audit of revised method for assessing the mitotic component of histological grade in needle core biopsies of invasive carcinoma of the breast. Histopathology 2012;60: 1166-1167.
73. Ellis GL, Auclair PL. Tumours of the salivary glands, 3rd edn. Armed Forces Institute of Pathology: Washington DC, USA, 1996.
74. Cardesa A, Alos L. Myoepithelioma, In: Barnes L (ed) WHO: Head and Neck Tumours. IARS Press: Lyon; 2005, pp 259-260.
75. Seifert G, Sobin LH. Histological Typing of Salivary Gland Tumours, 2nd edn. Springer: Berlin, Germany, 1991.
76. Nagao T, Sugano I, Ishida Y, et al. Salivary gland malignant myoepithelioma: A clinicopathologic and immunohistochemical study of ten cases. Cancer 1998;83:1292-1299.
77. Rasbridge SA, Millis RR. Adenomyoepithelioma of the breast with malignant features. Virchows Arch 1998;432:123-130.
78. Ahmed AA, Heller DS. Malignant adenomyoepithelioma of the breast with malignant proliferation of epithelial and myoepithelial elements: A case report and review of the literature. Arch Pathol Lab Med 2000;124:632-636.
79. Sugano I, Nagao T, Tajima Y, et al. Malignant adenomyoepithelioma of the breast: A non-tubular and matrix-producing variant. Pathol Int 2001; 51:193-199.
80. Lakhani SR, O'Hare MJ. The mammary myoepithelial cell - Cinderella or ugly sister. Breast Cancer Res 2001;3:1-4.
81. Jones C, Foschini MP, Chaggar R, et al. Comparative genomic hybridization analysis of myoepithelial carcinoma of the breast. Lab Invest 2000;80:831-836.
82. Jones C, Nonni AV, Fulford L, et al. CGH analysis of ductal carcinoma of the breast with basaloid/myoepithelial cell differentiation. Br J Cancer 2001;85: 422-427.
83. Tsuda H, Takarabe T, Hasegawa T, et al. Myoepithelial differentiation in high-grade invasive ductal carcinomas with large central acellular zones. Hum Pathol 1999;30:1134-1139.
84. Damiani S, Riccioni L, Pasquinelli G, et al. Poorly differentiated myoepithelial cell rich carcinoma of the breast. Histopathology 1997;30:542-548.
85. Stenman G, Andersson MK, Andren Y. New tricks from an old oncogene: Gene fusion and copy number alterations of MYB in human cancer. Cell Cycle 2010;9:2986-2995.
86. Mitani Y, Li J, Rao PH, et al. Comprehensive analysis of the MYB-NFIB gene fusion in salivary adenoid cystic carcinoma: Incidence, variability, and clinicopathologic significance. Clin Cancer Res 2010;16:4722-4731.
87. Lakhani M, Saiful F, Bekheit S, et al. Use of intracardiac echocardiography for early detection of phrenic nerve injury during cryoballoon pulmonary vein isolation. J Cardiovasc Electrophysiol 2012; 23:874-876.
88. Billings KR, Fu YS, Calcaterra TC, et al. Hemangiopericytoma of the head and neck. Am J Otolaryngol 2000;21:238-243.
89. Wetterskog D, Lopez-Garcia MA, Lambros MB, et al. Adenoid cystic carcinomas constitute a genomically distinct subgroup of triple-negative and basal-like breast cancers. J Pathol 2012;226:84-96.
90. Rao PH, Roberts D, Zhao YJ, et al. Deletion of 1p32-p36 is the most frequent genetic change and poor prognostic marker in adenoid cystic carcinoma of the salivary glands. Clin Cancer Res 2008;14:5181-5187.
91. Persson M, Andren Y, Moskaluk CA, et al. Clinically significant copy number alterations and complex rearrangements of MYB and NFIB in head and neck adenoid cystic carcinoma. Genes Chromosomes Cancer 2012;51:805-817.
92. Altemani A, Martins MT, Freitas L, et al. Carcinoma ex pleomorphic adenoma (CXPA): Immunoprofile of the cells involved in carcinomatous progression. Histopathology 2005;46:635-641.
93. Hernmann ME, Bratthauer GL, Stamatakos MD, et al. Maligancies arising in adenomaoepithelioma (AME) of breast: Clinical outcome and immunohistochemical characterization [abstract]. Mod Pathol 2003;16:33a.
94. Michal M, Baumruk L, Burger J, et al. Adenomyoepithelioma of the breast with undifferentiated carcinoma component. Histopathology 1994;24: 274-276.
95. Saarto T, Blomqvist C, Risteli J, et al. Aminoterminal propeptide of type I procollagen (PINP) correlates to bone loss and predicts the efficacy of antiresorptive therapy in pre- and post-menopausal non-metastatic breast cancer patients. Br J Cancer 1998;78: 240-245.
96. Simpson RH, Cope N, Skalova A, et al. Malignant adenomyoepithelioma of the breast with mixed osteogenic, spindle cell, and carcinomatous differentiation. Am J Surg Pathol 1998;22:631-636.
97. Van Dorpe J, De Pauw A, Moerman P. Adenoid cystic carcinoma arising in an adenomyoepithelioma of the breast. Virchows Arch 1998;432:119-122.