Duodenal follicular lymphoma lacks AID but expresses BACH2 and has memory B-cell characteristics

Katsuyoshi Takata, Yasuharu Sato, Naoya Nakamura, Mami Tokunaka, Yukari Miki, Yara Yukie Kikuti, Kazuhiko Igarashi, Etsuro Ito, Hideo Harigae, Seiichi Kato, Eiko Hayashi, Takashi Oka, Yoshinobu Hoshii, Akira Tari, Hiroyuki Okada, Abd Alkader Lamia Mohamad, Yoshinobu Maeda, Mitsune Tanimoto, Tomohiro Kinoshita, Tadashi Yoshino

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Abstract

We have reported previously that duodenal follicular lymphoma (FL) is distinct from nodal FL and showed more resemblance to mucosa-associated lymphoid tissue lymphoma, and that FL frequently involved the duodenal second portion. In the present study, we examined duodenal FLs and gastric/colonic FLs to clarify the clinicopathological and immunological differences between the tumor types. We analyzed 8 samples of gastric FL, 17 of duodenal ones, and 5 of colonic/rectal ones, and characterized them by immunohistochemistry, immunogenotyping, and histology. Gastric and colonic FLs presented in submucosal to subserosal areas, whereas duodenal ones presented in the mucosal to submucosal layers. Immunohistochemical analysis revealed that duodenal FLs exhibited the following phenotypes: CD10 (+), B-cell lymphoma 2 (BCL-2) (+), BCL-6 (+), activation-induced cytidine deaminase (AID) (-), BACH2 (+), CD27 (+), MUM-1 (-), Blimp-1 (-), and loose CD21 network (duodenal pattern). Gastric/colonic FLs exhibited the following phenotypes: CD10 (+), BCL-2 (+), BCL-6 (+), AID (+), BACH2 (+), CD27 (-), MUM-1 (-), Blimp-1 (-), and a dense CD21 network (nodal pattern). Expression of AID and CD27 in lymphoma cells and the CD21 network pattern were considerably different between duodenal FLs and gastric/colonic ones. Moreover, in situ hybridization revealed that, in the duodenal FLs, BACH2 was expressed at the periphery of the tumor follicle and tumor villi. The number of immunoglobulin heavy-chain variable domains VH4 and VH5 were higher in duodenal follicular lymphomoas than in gastric FLs. The lymphoma cells of duodenal FLs are different from those of gastric/colonic FLs, and duodenal FL is distinct even within the gastrointestinal tract. Somatic hypermutation in immunoglobulin genes and CD27 expression are hallmarks of memory B cells. We suggest that duodenal FL cells are in the memory B-cell stage, and require BACH2 instead of AID for ongoing mutation.

Original languageEnglish
Pages (from-to)22-31
Number of pages10
JournalModern Pathology
Volume26
Issue number1
DOIs
Publication statusPublished - Jan 2013

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Follicular Lymphoma
Stomach
B-Lymphocytes
B-Cell Lymphoma
Lymphoma
Phenotype
Marginal Zone B-Cell Lymphoma
Neoplasms
Immunoglobulin Heavy Chains
Immunoglobulin Genes
In Situ Hybridization
Gastrointestinal Tract
AICDA (activation-induced cytidine deaminase)
Histology
Immunohistochemistry
Gene Expression
Mutation

Keywords

  • BACH2
  • gastrointestinal follicular lymphoma
  • memory B cell

ASJC Scopus subject areas

  • Pathology and Forensic Medicine

Cite this

Duodenal follicular lymphoma lacks AID but expresses BACH2 and has memory B-cell characteristics. / Takata, Katsuyoshi; Sato, Yasuharu; Nakamura, Naoya; Tokunaka, Mami; Miki, Yukari; Yukie Kikuti, Yara; Igarashi, Kazuhiko; Ito, Etsuro; Harigae, Hideo; Kato, Seiichi; Hayashi, Eiko; Oka, Takashi; Hoshii, Yoshinobu; Tari, Akira; Okada, Hiroyuki; Mohamad, Abd Alkader Lamia; Maeda, Yoshinobu; Tanimoto, Mitsune; Kinoshita, Tomohiro; Yoshino, Tadashi.

In: Modern Pathology, Vol. 26, No. 1, 01.2013, p. 22-31.

Research output: Contribution to journalArticle

Takata, K, Sato, Y, Nakamura, N, Tokunaka, M, Miki, Y, Yukie Kikuti, Y, Igarashi, K, Ito, E, Harigae, H, Kato, S, Hayashi, E, Oka, T, Hoshii, Y, Tari, A, Okada, H, Mohamad, AAL, Maeda, Y, Tanimoto, M, Kinoshita, T & Yoshino, T 2013, 'Duodenal follicular lymphoma lacks AID but expresses BACH2 and has memory B-cell characteristics', Modern Pathology, vol. 26, no. 1, pp. 22-31. https://doi.org/10.1038/modpathol.2012.127
Takata, Katsuyoshi ; Sato, Yasuharu ; Nakamura, Naoya ; Tokunaka, Mami ; Miki, Yukari ; Yukie Kikuti, Yara ; Igarashi, Kazuhiko ; Ito, Etsuro ; Harigae, Hideo ; Kato, Seiichi ; Hayashi, Eiko ; Oka, Takashi ; Hoshii, Yoshinobu ; Tari, Akira ; Okada, Hiroyuki ; Mohamad, Abd Alkader Lamia ; Maeda, Yoshinobu ; Tanimoto, Mitsune ; Kinoshita, Tomohiro ; Yoshino, Tadashi. / Duodenal follicular lymphoma lacks AID but expresses BACH2 and has memory B-cell characteristics. In: Modern Pathology. 2013 ; Vol. 26, No. 1. pp. 22-31.
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T1 - Duodenal follicular lymphoma lacks AID but expresses BACH2 and has memory B-cell characteristics

AU - Takata, Katsuyoshi

AU - Sato, Yasuharu

AU - Nakamura, Naoya

AU - Tokunaka, Mami

AU - Miki, Yukari

AU - Yukie Kikuti, Yara

AU - Igarashi, Kazuhiko

AU - Ito, Etsuro

AU - Harigae, Hideo

AU - Kato, Seiichi

AU - Hayashi, Eiko

AU - Oka, Takashi

AU - Hoshii, Yoshinobu

AU - Tari, Akira

AU - Okada, Hiroyuki

AU - Mohamad, Abd Alkader Lamia

AU - Maeda, Yoshinobu

AU - Tanimoto, Mitsune

AU - Kinoshita, Tomohiro

AU - Yoshino, Tadashi

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N2 - We have reported previously that duodenal follicular lymphoma (FL) is distinct from nodal FL and showed more resemblance to mucosa-associated lymphoid tissue lymphoma, and that FL frequently involved the duodenal second portion. In the present study, we examined duodenal FLs and gastric/colonic FLs to clarify the clinicopathological and immunological differences between the tumor types. We analyzed 8 samples of gastric FL, 17 of duodenal ones, and 5 of colonic/rectal ones, and characterized them by immunohistochemistry, immunogenotyping, and histology. Gastric and colonic FLs presented in submucosal to subserosal areas, whereas duodenal ones presented in the mucosal to submucosal layers. Immunohistochemical analysis revealed that duodenal FLs exhibited the following phenotypes: CD10 (+), B-cell lymphoma 2 (BCL-2) (+), BCL-6 (+), activation-induced cytidine deaminase (AID) (-), BACH2 (+), CD27 (+), MUM-1 (-), Blimp-1 (-), and loose CD21 network (duodenal pattern). Gastric/colonic FLs exhibited the following phenotypes: CD10 (+), BCL-2 (+), BCL-6 (+), AID (+), BACH2 (+), CD27 (-), MUM-1 (-), Blimp-1 (-), and a dense CD21 network (nodal pattern). Expression of AID and CD27 in lymphoma cells and the CD21 network pattern were considerably different between duodenal FLs and gastric/colonic ones. Moreover, in situ hybridization revealed that, in the duodenal FLs, BACH2 was expressed at the periphery of the tumor follicle and tumor villi. The number of immunoglobulin heavy-chain variable domains VH4 and VH5 were higher in duodenal follicular lymphomoas than in gastric FLs. The lymphoma cells of duodenal FLs are different from those of gastric/colonic FLs, and duodenal FL is distinct even within the gastrointestinal tract. Somatic hypermutation in immunoglobulin genes and CD27 expression are hallmarks of memory B cells. We suggest that duodenal FL cells are in the memory B-cell stage, and require BACH2 instead of AID for ongoing mutation.

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