Micronodular thymoma: An epithelial tumour with abnormal chemokine expression setting the stage for lymphoma development

Journal of Pathology

Volumn 207, Issue 1, 2005, Pages 72-82

  Ströbel, Philipp ^a   Marino, Mirella ^b   Feuchtenberger, Martin ^a   Rouzière, Anne Sophie ^a   Tony, Hans Peter ^a   Wulbrand, Ulrich ^c   Förster, Reinhold ^c   Zettl, Andreas ^a   Harris, Nancy Lee ^d   Kreipe, Hans ^c   Laeng, R Hubert ^e   Müller Hermelink, Hans Konrad ^a   Marx, Alexander ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^c LEIBNIZ UNIVERSITY HANNOVER   (Germany)

^d HARVARD MEDICAL SCHOOL   (United States)

^e CANTONAL HOSPITAL AARAU   (Switzerland)

Author keywords

B cell; Chemokine; Lymphoma; MALT; Mediastinal; Micronodular; Thymoma

Indexed keywords

CHEMOATTRACTANT; CHEMOKINE; CHEMOKINE RECEPTOR CCR6; IMMUNOGLOBULIN HEAVY CHAIN;

ADULT; AGED; ARTICLE; B LYMPHOCYTE; CARCINOGENESIS; CHRONIC INFLAMMATION; CLINICAL ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; EPITHELIUM TUMOR; FEMALE; GENE EXPRESSION; GENE SEQUENCE; HEREDITY; HUMAN; LYMPHOCYTE SUBPOPULATION; LYMPHOMA; MALE; MEDIASTINUM TUMOR; MUCOSA ASSOCIATED LYMPHOID TISSUE LYMPHOMA; PRIORITY JOURNAL; STATISTICAL ANALYSIS; STROMA; T LYMPHOCYTE; THYMOMA;

EID: 23944457621     PISSN: 00223417     EISSN: None     Source Type: Journal    
DOI: 10.1002/path.1808     Document Type: Article

References (52)

1. Harris NL. Mature B-cell neoplasms: Introduction. In World Health Organization of Tumours. Pathology and Genetics. Tumours of Haematopoietic and Lymphoid Tissues, Jaffe E, Harris NL, Stein H, Vardiman JW (eds). IARC Press: Lyon, 2001; 121-126.
2. Borisch B, Raphael M, Swerdlow SH, Jaffe ES, Lymphoproliferative diseases associated with primary immune disorders. In World Health Organization Classification of Tumours. Pathology and Genetics. Tumours of Haematopoietic and Lymphoid Tissues, Jaffe ES, Harris NL, Stein H, Vardiman JW (eds). IARC Press: Lyon, 2001; 257-259.
3. Rafael M, Borisch B, Jaffe ES. Lymphomas associated with infection by the human immunodeficiency virus (HIV). In World Health Organization of Tumours. Pathology and Genetics. Tumours of Haematopoietic and Lymphoid Tissues, Jaffe E, Harris NL, Stein H, Vardiman JW (eds). IARC Press: Lyon, 2001; 260-263.
4. Harris NL, Swerdlow SH, Frizzera G, Knowles DM. Posttransplant lymphoproliferative disorders. In World Health Organization of Tumours. Pathology and Genetics. Tumours of Haematopoietic and Lymphoid Tissues, Jaffe E, Harris NL, Stein H, Vardiman JW (eds). IARC Press: Lyon, 2001; 264-269.
5. Isaacson PG, Müller-Hermelink HK, Piris MA, Berger F, Nathwani BN, Swerdlow SH, et al. Extranodal marginal zone B-cell lymphoma of mucosa-associated lympoid tissue (MALT lymphoma). In World Health Organization Classification of Tumours. Pathology and Genetics. Tumours of Haematopoietic and Lymphoid Tissues, Jaffe ES, Harris NL, Stein H, Vardiman JW (eds). IARC Press: Lyon, 2001; 157-160.
6. Isaacson PG. Extranodal lymphomas: the MALT concept. Verh Dtsch Ges Pathol 1992;76:14-23.
7. Isaacson PG. Gastric MALT lymphoma: from concept to cure. Ann Oncol 1999;10:637-645.
8. Rodig SJ, Jones D, Shahsafaei A, Dorfman DM. CCR6 is a functional chemokine receptor that serves to identify select B-cell non-Hodgkin's lymphomas. Hum Pathol 2002;33:1227-1233.
9. Takagi N, Nakamura S, Yamamoto K, Kunishima K, Takagi I, Suyama M, et al. Malignant lymphoma of mucosa-associated lymphoid tissue arising in the thymus of a patient with Sjögren's syndrome. A morphologic, phenotypic, and genotypic study. Cancer 1992; 69:1347-1355.
10. Royer B, Cazals-Hatem D, Sibilia J, Agbalika F, Cayuela JM, Soussi T, et al. Lymphomas in patients with Sjögren's syndrome are marginal zone B-cell neoplasms, arise in diverse extranodal and nodal sites, and are not associated with viruses. Blood 1997; 90:766-775.
11. Yamasaki S, Matsushita H, Tanimura S, Nakatani T, Hara S, Endo Y, et al. B-cell lymphoma of mucosa-associated lymphoid tissue of the thymus: a report of two cases with a background of Sjögren's syndrome and monoclonal gammopathy. Hum Pathol 1998;29:1021-1024.
12. Nagasaka T, Lai R, Harada T, Chen YY, Chen WG, Arber DA, et al. Coexisting thymic and gastric lymphomas of mucosa-associated lymphoid tissues in a patient with Sjögren syndrome. Arch Pathol Lab Med 2000;124:770-773.
13. Yokose T, Kodama T, Matsuno Y, Shimosato Y, Nishimura M, Mukai K. Low-grade B cell lymphoma of mucosa-associated lymphoid tissue in the thymus of a patient with rheumatoid arthritis. Pathol Int 1998;48:74-81.
14. Lorsbach RB, Pinkus GS, Shahsafaei A, Dorfman DM. Primary marginal zone lymphoma of the thymus. Am J Clin Pathol 2000; 113:784-791.
15. McCluggage WG, McManus K, Qureshi R, McAleer S, Wotherspoon AC. Low-grade B-cell lymphoma of mucosa-associated lymphoid tissue (MALT) of thymus. Hum Pathol 2000;31:255-259.
16. Isaacson PG, Chan JK, Tang C, Addis BJ. Low-grade B-cell lymphoma of mucosa-associated lymphoid tissue arising in the thymus. A thymic lymphoma mimicking myoepithelial sialadenitis. Am J Surg Pathol 1990;14:342-351.
17. Levine GD, Rosai J. Thymic hyperplasia and neoplasia: a review of current concepts. Hum Pathol 1978;9:495-515.
18. Müller-Hermelink HK, Engel PJ, Harris NL, Menestrina F, Möller P, Kuo TT, et al. Tumours of the thymus. In Tumours of the Lung, Thymus, and Heart. Pathology and Genetics, Travis WD, Brambilla E, Müller-Hermelink HK, Harris CC, (eds). IARC Press: Lyon, 2004; 145-153.
19. Fend F, Kirchner T, Marx A, Muller-Hermelink HK. B-cells in thymic epithelial tumours. An immunohistochemcal analysis of intra- and extraepithelial B-cell compartments. Virchows Arch B Cell Pathol Incl Mol Pathol 1993;63:241-247.
20. Suster S, Moran CA. Micronodular thymoma with lymphoid B-cell hyperplasia: clinicopathologic and immunohistochemical study of eighteen cases of a distinctive morphologic variant of thymic epithelial neoplasm. Am J Sung Pathol 1999;23:955-962.
21. Tateyama H, Saito Y, Fujii Y, Okumura M, Nakamura K, Tada H, et al. The spectrum of micronodular thymic epithelial tumours with lymphoid B-cell hyperplasia. Histopathology 2001; 38:519-527.
22. Rudiger T, Ott G, Ott MM, Muller-Deubert SM, Muller-Hermelink HK. Differential diagnosis between classic Hodgkin's lymphoma, T-cell-rich B-cell lymphoma, and paragranuloma by paraffin immunohistochemistry. Am J Surg Pathol 1998;22:1184-1191.
23. Streubel B, Lamprecht A, Dierlamm J, Cerroni L, Stolte M, Ott G, et al. T(14;18)(q32;q21) involving IGH and MALT1 is a frequent chromosomal aberration in MALT lymphoma. Blood 2003; 101:2335-2339.
24. Inagaki H, Okabe M, Seto M, Nakamura S, Ueda R, Eimoto T. API2-MALT1 fusion transcripts involved in mucosa-associated lymphoid tissue lymphoma: multiplex RT-PCR detection using formalin-fixed paraffin-embedded specimens. Am J Pathol 2001;158:699-706.
25. Krober A, Seiler T, Benner A, Bullinger L, Bruckle E, Lichter P, et al. V(H) mutation status, CD38 expression level, genomic aberrations, and survival in chronic lymphocytic leukemia. Blood 2002;100:1410-1416.
26. Kuppers R, Zhao M, Rajewsky K, Hansmann ML. Detection of clonal B cell populations in paraffin-embedded tissues by polymerase chain reaction. Am J Pathol 1993;143:230-239.
27. Schutte ME, Ebeling SB, Akkermans KE, Gmelig-Meyling FH, Logtenberg T. Antibody specificity and immunoglobulin VH gene utilization of human monoclonal CD5+ B cell lines. Eur J Immunol 1991; 21:1115-1121.
28. Mau J. A statistical assessment of clinical equivalence. Stat Med 1988;7:1267-1277.
29. Tusher V, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 2001;98:5116-5121.
30. Strobel P, Preisshofen T, Helmreich M, Muller-Hermelink HK, Marx A. Pathomechanisms of paraneoplastic myasthenia gravis. Clin Dev Immunol 2003;10:7-12.
31. Dubois B, Massacrier C, Caux C. Selective attraction of naïve and memory B cells by dendritic cells. J Leukoc Biol 2001;70:633-641.
32. Knowles DM. Immunodeficiency-associated lymphoproliferative disorders. Mod Pathol 1999;12:200-217.
33. Chadburn A, Cesarman E, Liu YF, Addonizio L, Hsu D, Michler RE, et al. Molecular genetic analysis demonstrates that multiple posttransplantation lymphoproliferative disorders occurring in one anatomic site in a single patient represent distinct primary lymphoid neoplasms. Cancer 1995;75:2747-2756.
34. Kamel OW, van de Rijn M, LeBrun DP, Weiss LM, Warnke RA, Dorfman RF. Lymphoid neoplasms in patients with rheumatoid arthritis and dermatomyositis: frequency of Epstein-Barr virus and other features associated with immunosuppression. Hum Pathol 1994; 25:638-643.
35. Kojima M, Nakamura S, Futamura N, Kurabayashi Y, Ban S, Itoh H, et al. Malignant lymphoma in patients with rheumatic diseases other than Sjögren's syndrome: a clinicopathologic study of five cases and a review of the Japanese literature. Jpn J Clin Oncol 1997; 27:84-90.
36. Baecklund E, Ekbom A, Sparen P, Feltelius N, Klareskog L. Disease activity and risk of lymphoma in patients with rheumatoid arthritis: nested case-control study. Br Med J 1998; 317:180-181.
37. Aiello A, Du MQ, Diss TC, Peng HZ, Pezzella F, Papini D, et al. Simultaneous phenotypically distinct but clonally identical mucosa-associated lymphoid tissue and follicular lymphoma in a patient with Sjögren's syndrome. Blood 1999;94:2247-2251.
38. Kojima M, Nakamura S, Oyama T, Motoori T, Itoh H, Yoshida K, et al. Autoimmune disease-associated lymphadenopathy with histological appearance of T-zone dysplasia with hyperplastic follicles. A clinicopathological analysis of nine cases. Pathol Res Pract 2001;197:237-244.
39. Straus SE, Jaffe ES, Puck JM, Dale JK, Elkon KB, Rosen-Wolff A, et al. The development of lymphomas in families with autoimmune lymphoproliferative syndrome with germline Fas mutations and defective lymphocyte apoptosis. Blood 2001;98:194-200.
40. Auer IA, Gascoyne RD, Connors JM, Cotter FE, Greiner TC, Sanger WG, et al. t(11;18)(q21;q21) is the most common translocation in MALT lymphomas. Ann Oncol 1997;8:979-985.
41. Ott G, Katzenberger T, Greiner A, Kalla J, Rosenwald A, Heinrich U, et al. The t(11;18)(q21;q21) chromosome translocation is a frequent and specific aberration in low-grade but not high-grade malignant non-Hodgkin's lymphomas of the mucosa-associated lymphoid tissue (MALT-) type. Cancer Res 1997;57:3944-3948.
42. Starostik P, Patzner J, Greiner A, Schwarz S, Kalla J, Ott G, et al. Gastric marginal zone B-cell lymphomas of MALT type develop along 2 distinct pathogenetic pathways. Blood 2002;99:3-9.
43. Harris NL. Lymphoid proliferations of the salivary glands. Am J Clin Pathol 1999;111(Suppl 1):S94-S103.
44. Seeberger H, Starostik P, Schwarz S, Knorr C, Kalla J, Ott G, et al. Loss of Fas (CD95/APO-1) regulatory function is an important step in early MALT-type lymphoma development. Lab Invest 2001;81:977-986.
45. Wilson NS, El-Sukkari D, Belz GT, Smith CM, Steptoe RJ, Heath WR, et al. Most lymphoid organ dendritic cell types are phenotypically and functionally immature. Blood 2003; 102:2187-2194.
46. Greaves DR, Wang W, Dairaghi DJ, Dieu MC, Saint-Vis B, Franz-Bacon K, et al. CCR6, a CC chemokine receptor that interacts with macrophage inflammatory protein 3alpha and is highly expressed in human dendritic cells. J Exp Med 1997;186:837-844.
47. Krzysiek R, Lefevre EA, Bernard J, Foussat A, Galanaud P, Louache F, et al. Regulation of CCR6 chemokine receptor expression and responsiveness to macrophage inflammatory protein-3alpha/CCL20 in human B cells. Blood 2000;96:2338-2345.
48. Youn BS, Kim YJ, Mantel C, Yu KY, Broxmeyer HE. Blocking of c-FLIP(L)-independent cycloheximide-induced apoptosis or Fas-mediated apoptosis by the CC chemokine receptor 9/TECK interaction. Blood 2001;98:925-933.
49. Pinto LA, Williams MS, Dolan MJ, Henkart PA, Shearer GM. Beta-chemokines inhibit activation-induced death of lymphocytes from HIV-infected individuals. Eur J Immunol 2000;30:2048-2055.
50. Inagaki H, Chan JK, Ng JW, Okabe M, Yoshino T, Okamoto M, et al. Primary thymic extranodal marginal-zone B-cell lymphoma of mucosa-associated lymphoid tissue type exhibits distinctive clinicopathological and molecular features. Am J Pathol 2002; 160:1435-1443.
51. Di Loreto C, Mariuzzi L, De Grassi A, Beltrami CA. B cell lymphoma of the thymus and salivary gland. J Clin Pathol 1996; 49:595-597.
52. Schutyser E, Struyf S, Van Damme J. The CC chemokine CCL20 and its receptor CCR6. Cytokine Growth Factor Rev 2003; 14:409-426.