Immunohistochemistry of soft tissue tumours - review with emphasis on 10 markers

Histopathology

Volumn 64, Issue 1, 2014, Pages 101-118

  Miettinen, Markku ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

CD31; CD34; Desmin; DOG1; EMA; ERG; Immunohistochemistry; IT; Keratins; S100 protein; Sarcoma; SMA

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; BIOLOGICAL MARKER; CALDESMON; CD31 ANTIGEN; CD34 ANTIGEN; CLAUDIN 1; CYTOKERATIN 18; CYTOKERATIN 19; CYTOKERATIN 20; CYTOKERATIN 7; CYTOKERATIN AE1; CYTOKERATIN AE3; DESMIN; EPITHELIAL MEMBRANE ANTIGEN; MUCIN 1; MUCIN 4; MYOD1 PROTEIN; MYOGENIN; PROTEIN; PROTEIN DOG 1; PROTEIN S 100; TRANSCRIPTION FACTOR ERG; UNCLASSIFIED DRUG;

ANGIOSARCOMA; ANTIGEN PRESENTING CELL; CONNECTIVE TISSUE TUMOR; COST; DERMATOFIBROSARCOMA PROTUBERANS; DESMOPLASTIC SMALL ROUND CELL TUMOR; DIFFERENTIAL DIAGNOSIS; EPITHELIOID SARCOMA; EWING SARCOMA; FIBROSARCOMA; GASTROINTESTINAL STROMAL TUMOR; HEMANGIOMA; HUMAN; IMMUNOHISTOCHEMISTRY; KAPOSI SARCOMA; LANGERHANS CELL HISTIOCYTOSIS; LEIOMYOSARCOMA; MERKEL CELL TUMOR; MESOTHELIOMA; NERVE SHEATH TUMOR; NEURILEMOMA; NEUROFIBROMA; PARAGANGLIOMA; PRIORITY JOURNAL; REVIEW; RHABDOMYOSARCOMA; SOFT TISSUE TUMOR; SOLITARY FIBROUS TUMOR; SYNOVIAL SARCOMA; TRANSITIONAL CELL CARCINOMA;

MYOIDA;

CD31; CD34; DESMIN; DOG1; EMA; ERG; IMMUNOHISTOCHEMISTRY; IT; KERATINS; S100 PROTEIN; SARCOMA; SMA;

HUMANS; IMMUNOHISTOCHEMISTRY; SOFT TISSUE NEOPLASMS; TUMOR MARKERS, BIOLOGICAL;

EID: 84889675653     PISSN: 03090167     EISSN: 13652559     Source Type: Journal    
DOI: 10.1111/his.12298     Document Type: Review

References (86)

1. Van de Rijn M, Rouse RV. CD34 - a review. Appl. Immunohistochem. 1994; 2; 71-80.
2. Nickoloff BJ. The human progenitor cell antigen (CD34) is localized on endothelial cells, dermal dendritic cells, and perifollicular cells in formalin-fixed normal skin, and on proliferating endothelial cells and stromal spindle-shaped cells in Kaposi's sarcoma. Arch. Dermatol. 1991; 127; 523-529.
3. Poblet E, Jimenez-Acosta F, Rocamora A. QBEND/10 (anti-CD34 antibody) in external root sheath cells and follicular tumors. J. Cutan. Pathol. 1994; 21; 224-228.
4. Aiba S, Tabata N, Ishii H, Ootani H, Tagami H. Dermatofibrosarcoma protuberans is a unique fibrohistiocytic tumour expressing CD34. Br. J. Dermatol. 1992; 127; 79-84.
5. van de Rijn M, Lombard CM, Rouse RV. Expression of CD34 by solitary fibrous tumors of the pleura, mediastinum, and lung. Am. J. Surg. Pathol. 1994; 18; 814-820.
6. Kutzner H. Expression of the human progenitor cell antigen CD34 (HPCA-1) distinguishes dermatofibrosarcoma protuberans from fibrous histiocytoma in formalin-fixed, paraffin-embedded tissue. J. Am. Acad. Dermatol. 1993; 28; 613-617.
7. Fetsch JF, Laskin WB, Miettinen M. Superficial acral acral fibromyxoma. A clinicopathologic study of 30 cases. Hum. Pathol. 2001; 32; 704-714.
8. Suster S, Fisher C. Immunoreactivity for the human hematopoietic progenitor cell antigen (CD34) in lipomatous tumors. Am. J. Surg. Pathol. 1997; 21; 195-200.
9. Traweek ST, Kandalaft PL, Mehta P, Battifora H. The human hematopoietic progenitor cell antigen (CD34) in vascular neoplasia. Am. J. Clin. Pathol. 1991; 96; 25-31.
10. Miettinen M, Fanburg-Smith JC, Virolainen M, Shmookler BM, Fetsch JF. Epithelioid sarcoma: an immunohistochemical analysis of 112 classical and variant cases and a discussion of the differential diagnosis. Hum. Pathol. 1999; 30; 934-942.
11. Truong LD, Rangdaeng S, Cagle P, Ro JY, Hawkins H, Font RL. The diagnostic utility of desmin. A study of 584 cases and review of the literature. Am. J. Clin. Pathol. 1990; 93; 305-314.
12. Gerald WL, Miller HK, Battifora H, Miettinen M, Silva EG, Rosai J. Intra-abdominal desmoplastic small round-cell tumor. Report of 19 cases of a distinctive type of high-grade polyphenotypic malignancy affecting young individuals. Am. J. Surg. Pathol. 1991; 15; 499-513.
13. Ordóñez NG. Desmoplastic small round cell tumor: II: an ultrastructural and immunohistochemical study with emphasis on new immunohistochemical markers. Am. J. Surg. Pathol. 1998; 22; 1314-1327.
14. Fletcher CD. Angiomatoid 'malignant fibrous histiocytoma': an immunohistochemical study indicative of myoid differentiation. Hum. Pathol. 1991; 22; 563-568.
15. Fanburg-Smith JC, Miettinen M. Angiomatoid 'malignant' fibrous histiocytoma: a clinicopathologic study of 158 cases and further exploration of the myoid phenotype. Hum. Pathol. 1999; 30; 1336-1343.
16. Fetsch JF, Laskin WB, Lefkowitz M, Kindblom LG, Meis-Kindblom JM. Aggressive angiomyxoma: a clinicopathologic study of 29 female patients. Cancer 1996; 78; 79-90.
17. Folpe AL, Weiss SW, Fletcher CD, Gown AM. Tenosynovial giant cell tumors: evidence for a desmin-positive dendritic cell subpopulation. Mod. Pathol. 1998; 11; 939-944.
18. Ordóñez NG. Broad-spectrum immunohistochemical epithelial markers: a review. Hum. Pathol. 2013; 44; 1195-1215.
19. Theaker JM, Gatter KC, Esiri MM, Fleming KA. Epithelial membrane antigen and cytokeratin expression by meningiomas: an immunohistological study. J. Clin. Pathol. 1986; 39; 435-439.
20. Perentes E, Nakagawa Y, Ross GW, Stanton C, Rubinstein LJ. Expression of epithelial membrane antigen in perineurial cells and their derivatives. An immunohistochemical study with multiple markers. Acta Neuropathol. 1987; 75; 160-165.
21. Fetsch JF, Miettinen M. Sclerosing perineurioma: a clinicopathologic study of 19 cases of a distinctive soft tissue lesion with a predilection for the fingers and palms of young adults. Am. J. Surg. Pathol. 1997; 21; 1433-1442.
22. Hornick JL, Fletcher CD. Soft tissue perineurioma: clinicopathologic analysis of 81 cases including those with atypical histologic features [Review]. Am. J. Surg. Pathol. 2005; 29; 845-858.
23. Folpe AL, Billings SD, McKenney JK, Walsh SV, Nusrat A, Weiss SW. Expression of claudin-1, a recently described tight junction-associated protein, distinguishes soft tissue perineurioma from potential mimics. Am. J. Surg. Pathol. 2002; 26; 1620-1626.
24. Hornick JL, Bundock EA, Fletcher CD. Hybrid schwannoma/perineurioma: clinicopathologic analysis of 42 distinctive benign nerve sheath tumors. Am. J. Surg. Pathol. 2009; 33; 1554-1561.
25. Billings SD, Giblen G, Fanburg-Smith JC. Superficial low-grade fibromyxoid sarcoma (Evans tumor): a clinicopathologic analysis of 19 cases with a unique observation in the pediatric population. Am. J. Surg. Pathol. 2005; 29; 204-210.
26. Doyle LA, Möller E, Dal Cin P, Fletcher CD, Mertens F, Hornick JL. MUC4 is a highly sensitive and specific marker for low-grade fibromyxoid sarcoma. Am. J. Surg. Pathol. 2011; 35; 733-741.
27. Moll R, Franke WW, Schiller DL, Geiger B, Krepler R. The catalog of human cytokeratins: patterns of expression in normal epithelia, tumors and cultured cells. Cell 1982; 31; 11-24.
28. Cooper D, Schermer A, Sun TT. Classification of human epithelia and their neoplasms using monoclonal antibodies to keratins: strategies, applications, and limitations. Lab. Invest. 1985; 52; 243-256.
29. Miettinen M. Keratin immunohistochemistry: update of applications and pitfalls. Pathol. Annu. 1993; 28; 113-143.
30. Moll R, Löwe A, Laufer J, Franke WW. Cytokeratin 20 in human carcinomas. A new histodiagnostic marker detected by monoclonal antibodies. Am. J. Pathol. 1992; 140; 427-447.
31. Miettinen M. Keratin 20: immunohistochemical marker for gastrointestinal, urothelial, and Merkel cell carcinomas. Mod. Pathol. 1995; 8; 384-388.
32. Miettinen M, Limon J, Niezabitowski A, Lasota J. Patterns of keratin polypeptides in 110 biphasic, monophasic, and poorly differentiated synovial sarcomas. Virchows Arch. 2000; 437; 275-283.
33. Hornick JL, Fletcher CD. Myoepithelial tumors of soft tissue: a clinicopathologic and immunohistochemical study of 101 cases with evaluation of prognostic parameters. Am. J. Surg. Pathol. 2003; 27; 1183-1196.
34. Eusebi V, Carcangiu ML, Dina R, Rosai J. Keratin-positive epithelioid angio-sarcoma of thyroid. A report of four cases. Am. J. Surg. Pathol. 1990; 14; 737-747.
35. Miettinen M, Fetsch JF. Distribution of keratins in normal endothelial cells and a spectrum of vascular tumors: implications in tumor diagnosis. Hum. Pathol. 2000; 31; 1062-1067.
36. von Koskull H, Virtanen I. Induction of cytokeratin expression in human mesenchymal cells. J. Cell. Physiol. 1987; 133; 321-329.
37. Knapp AC, Franke WW. Spontaneous losses of control of cytokeratin gene expression in transformed, non-epithelial human cells occurring at different levels of regulation. Cell 1989; 59; 67-79.
38. Kriho VK, Yang HY, Moskal JR, Skalli O. Keratin expression in astrocytomas: an immunofluorescent and biochemical reassessment. Virchows Arch. 1997; 431; 39-47.
39. Fanburg-Smith JC, Majidi M, Miettinen M. Keratin expression in schwannoma; a study of 115 retroperitoneal and 22 peripheral schwannomas. Mod. Pathol. 2006; 19; 115-121.
40. Miettinen M. Immunohistochemistry of soft tissue tumors. In Miettinen M ed. Modern soft tissue pathology. Cambridge/New York: Cambridge University Press, 2010; 52-53.
41. Nakajima T, Watanabe S, Sato Y, Kameya T, Hirota T, Shimosato Y. An immunoperoxidase study of S-100 protein distribution in normal and neoplastic tissues. Am. J. Surg. Pathol. 1982; 6; 715-727.
42. Karamchandani JR, Nielsen TO, van de Rijn M, West RB. Sox10 and S100 in the diagnosis of soft-tissue neoplasms. Appl. Immunohistochem. Mol. Morphol. 2012; 20; 445-450.
43. Newman PJ, Berndt MC, Gorski J et al. PECAM-1 (CD31) cloning and relation to adhesion molecules of the immunoglobulin gene superfamily. Science 1990; 47; 1219-1222.
44. Kuzu I, Bicknell R, Harris AL, Jones M, Gatter KC, Mason DY. Heterogeneity of vascular endothelial cells with relevance to diagnosis of vascular tumours. J. Clin. Pathol. 1992; 45; 143-148.
45. de Young BR, Wick MR, Fitzgibbon JF, Sirgi KE, Swanson PE. CD31: an immunospecific marker for endothelial differentiation in human neoplasms. Appl. Immunohistochem. 1993; 1; 97-100.
46. Miettinen M, Lindenmayer AE, Chaubal A. Endothelial cell markers CD31, CD34, and BNH9 antibody to H- and Y-antigens - evaluation of their specificity and sensitivity in the diagnosis of vascular tumors and comparison with von Willebrand's factor. Mod. Pathol. 1994; 7; 82-90.
47. McKenney JK, Weiss SW, Folpe AL. CD31 expression in intratumoral macrophages: a potential diagnostic pitfall. Am. J. Surg. Pathol. 2001; 25; 1167-1173.
48. Miettinen M, Wang ZF, Paetau A et al. ERG transcription factor as an immunohistochemical marker for vascular endothelial tumors and prostatic carcinoma. Am. J. Surg. Pathol. 2011; 35; 432-441.
49. McKay KM, Doyle LA, Lazar AJ, Hornick JL. Expression of ERG, an ETS family transcription factor, distinguishes cutaneous angiosarcoma from histological mimics. Histopathology 2012; 61; 989-991.
50. Agaimy A, Kirsche H, Semrau S, Iro H, Hartmann A. Cytokeratin-positive epithelioid angiosarcoma presenting in the tonsil: a diagnostic challenge. Hum. Pathol. 2012; 43; 1142-1147.
51. Furusato B, Gao CL, Ravindranath L et al. Mapping of TMPRSS2-ERG fusions in the context of multi-focal prostate cancer. Mod. Pathol. 2008; 21; 67-75.
52. Yaskiv O, Rubin BP, He H, Falzarano S, Magi-Galluzzi C, Zhou M. ERG protein expression in human tumors detected with a rabbit monoclonal antibody. Am. J. Clin. Pathol. 2012; 138; 803-810.
53. Miettinen M, Wang Z, Sarlomo-Rikala M, Abdullaev Z, Pack SD, Fetsch JF. ERG expression in epithelioid sarcoma: a diagnostic pitfall. Am. J. Surg. Pathol. 2013; 37; 1580-1585.
54. Wang WL, Patel NR, Caragea M et al. Expression of ERG, an ETS family transcription factor, identifies ERG-rearranged Ewing sarcoma. Mod. Pathol. 2012; 25; 1378-1383.
55. Verdu M, Trias I, Roman R et al. ERG expression and prostatic adenocarcinoma. Virchows Arch. 2013; 462; 639-644.
56. Besmer P, Murphy JE, George PC et al. A new acute transforming feline retrovirus and relationship of its oncogene v-kit with the protein kinase gene family. Nature 1986; 320; 415-421.
57. Hirota S, Isozaki K, Moriyama Y et al. Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science 1998; 279; 577-580.
58. Kindblom LG, Remotti HE, Aldenborg F, Meis-Kindblom JM. Gastrointestinal pacemaker cell tumor (GIPACT): gastrointestinal stromal tumors show phenotypic characteristics of the interstitial cells of Cajal. Am. J. Pathol. 1998; 152; 1259-1269.
59. Sarlomo-Rikala M, Kovatich AJ, Barusevicius A, Miettinen M. CD117: a sensitive marker for gastrointestinal stromal tumors that is more specific than CD34. Mod. Pathol. 1998; 11; 728-734.
60. Miettinen M, Lasota J. KIT (CD117): a review on expression in normal and neoplastic tissues, and mutations and their clinicopathologic correlation. Appl. Immunohistochem. Mol. Morphol. 2005; 13; 205-220.
61. Tsuura Y, Hiraki H, Watanabe K et al. Preferential localization of c-kit product in tissue mast cells, basal cells of skin, epithelial cells of breast, small cell lung carcinoma and seminoma/dysgerminoma in human: immunohistochemical study on formalin-fixed, paraffin-embedded tissues. Virchows Arch. 1994; 424; 135-141.
62. Lammie A, Drobnjak M, Gerald W, Saad A, Cote R, Cordon-Cardo C. Expression of c-kit and kit ligand proteins in normal human tissues. J. Histochem. Cytochem. 1994; 42; 1417-1425.
63. Hornick JL, Fletcher CD. Immunohistochemical staining for KIT (CD117) in soft tissue sarcomas is very limited in distribution. Am. J. Clin. Pathol. 2002; 117; 188-193.
64. Miettinen M, Sobin LH, Sarlomo-Rikala M. Immunohistochemical spectrum of GISTs at different sites and their differential diagnosis with a reference to CD117 (KIT). Mod. Pathol. 2000; 13; 1134-1142.
65. West RB, Corless CL, Chen X et al. The novel marker, DOG1, is expressed ubiquitously in gastrointestinal stromal tumors irrespective of KIT or PDGFRA mutation status. Am. J. Pathol. 2004; 165; 107-113.
66. Espinosa I, Lee CH, Kim MK et al. A novel monoclonal antibody against DOG1 is a sensitive and specific marker for gastrointestinal stromal tumors. Am. J. Surg. Pathol. 2008; 32; 210-218.
67. Yang YD, Cho H, Koo JY et al. TMEM16A confers receptor-activated calcium-dependent chloride conductance. Nature 2008; 455; 1210-1215.
68. Miettinen M, Wang ZF, Lasota J. DOG1 antibody in the differential diagnosis of gastrointestinal stromal tumors: a study of 1840 cases. Am. J. Surg. Pathol. 2009; 33; 1401-1408.
69. Novelli M, Rossi S, Rodriguez-Justo M et al. DOG1 and CD117 are the antibodies of choice in the diagnosis of gastrointestinal stromal tumours. Histopathology 2010; 57; 259-270.
70. Sah SP, McCluggage WG. DOG1 immunoreactivity in uterine leiomyosarcomas. J. Clin. Pathol. 2013; 66; 40-43.
71. Hemminger J, Iwenofu OH. Discovered on gastrointestinal stromal tumours 1 (DOG1) expression in non-gastrointestinal stromal tumour (GIST) neoplasms. Histopathology 2012; 61; 170-177.
72. Akpalo H, Lange C, Zustin J. Discovered on gastrointestinal stromal tumour 1 (DOG1): a useful immunohistochemical marker for diagnosing chondroblastoma. Histopathology 2012; 60; 1099-1106.
73. Perez-Montiel MD, Plaza JA, Dominguez-Malagon H, Suster S. Differential expression of smooth muscle myosin, SMA, h-caldesmon, and calponin in the diagnosis of myofibroblastic and smooth muscle lesions of skin and soft tissue. Am. J. Dermatopathol. 2006; 28; 105-111.
74. Watanabe K, Kusakabe T, Hoshi N, Saito A, Suzuki T. h-Caldesmon in leiomyosarcoma and tumors with smooth muscle cell-like differentiation: its specific expression in the smooth muscle cell tumor. Hum. Pathol. 1999; 30; 392-396.
75. Miettinen M, Sarlomo-Rikala M, Kovatich AJ, Lasota J. Calponin and h-caldesmon in soft tissue tumors: consistent h-caldesmon immunoreactivity in gastrointestinal stromal tumors indicates traits of smooth muscle differentiation. Mod. Pathol. 1999; 12; 756-762.
76. Folpe AL, Kwiatkowski DJ. Perivascular epithelioid cell neoplasms: pathology and pathogenesis. Hum. Pathol. 2010; 41; 1-15.
77. Eusebi V, Damiani S, Pasquinelli G, Lorenzini P, Reuter VE, Rosai J. Small cell neuroendocrine carcinoma with skeletal muscle differentiation: report of three cases. Am. J. Surg. Pathol. 2000; 24; 223-230.
78. Cessna MH, Zhou H, Perkins SL et al. Are myogenin and myoD1 expression specific for rhabdomyosarcoma? A study of 150 cases, with emphasis on spindle cell mimics. Am. J. Surg. Pathol. 2001; 25; 1150-1157.
79. Weiss SW, Nickoloff BJ. CD-34 is expressed by a distinctive cell population in peripheral nerve, nerve sheath tumors, and related lesions. Am. J. Surg. Pathol. 1993; 17; 1039-1045.
80. Chaubal A, Paetau A, Zoltick P, Miettinen M. CD34 immunoreactivity in nervous system tumors. Acta Neuropathol. 1994; 88; 454-458.
81. Harder A, Wesemann M, Hagel C et al. Hybrid neurofibroma/schwannoma is overrepresented among schwannomatosis and neurofibromatosis patients. Am. J. Surg. Pathol. 2012; 36; 702-709.
82. Zhou H, Coffin CM, Perkins SL, Tripp SR, Liew M, Viskochil DH. Malignant peripheral nerve sheath tumor: a comparison of grade, immunophenotype, and cell cycle/growth activation marker expression in sporadic and neurofibromatosis 1-related lesions. Am. J. Surg. Pathol. 2003; 27; 1337-1345.
83. Pelmus M, Guillou L, Hostein I, Sierankowski G, Lussan C, Coindre JM. Monophasic fibrous and poorly differentiated synovial sarcoma: immunohistochemical reassessment of 60 t(X;18)(SYT-SSX)-positive cases. Am. J. Surg. Pathol. 2002; 26; 1434-1440.
84. Terry J, Saito T, Subramanian S et al. TLE1 as a diagnostic immunohisto-chemical marker for synovial sarcoma emerging from gene expression profiling studies. Am. J. Surg. Pathol. 2007; 31; 240-246.
85. Knösel T, Heretsch S, Altendorf-Hofmann A et al. TLE1 is a robust diagnostic biomarker for synovial sarcomas and correlates with t(X;18): analysis of 319 cases. Eur. J. Cancer 2010; 46; 1170-1176.
86. Matsuyama A, Hisaoka M, Iwasaki M, Iwashita M, Hisanaga S, Hashimoto H. TLE1 expression in malignant mesothelioma. Virchows Arch. 2010; 457; 577-583.