Increase of bone marrow-derived secretory lineage epithelial cells during regeneration in the human intestine

Tomoko Matsumoto, Ryuichi Okamoto, Tomoharu Yajima, Takehiko Mori, Shinichiro Okamoto, Yasuo Ikeda, Makio Mukai, Motomi Yamazaki, Shigeru Oshima, Kiichiro Tsuchiya, Tetsuya Nakamura, Takanori Kanai, Hideyuki Okano, Johji Inazawa, Toshifumi Hibi, Mamoru Watanabe

Research output: Contribution to journalArticle

72 Citations (Scopus)

Abstract

Background & Aims: We have previously reported that bone marrow (BM)-derived cells contribute to the regeneration of the human intestinal epithelium. To analyze further how these cells arise, proliferate, and differentiate as epithelial cells, histologic analysis was conducted using endoscopic specimens. Methods: Thirty biopsy specimens from 14 female, sex-mismatched BM-transplantation recipients were examined. BM-derived cells were identified by fluorescent in situ hybridization (FISH) for the Y chromosome and immunohistochemistry. Multicolor FISH was used to exclude cell fusion. These cells were further analyzed for various differentiation or proliferation markers. Results: No evidence of cell fusion was detected. BM-derived cells did not distribute within the crypt as stem cells and rarely expressed Musashi-1. However, BM-derived epithelial cells frequently expressed Ki-67, and some of these cells appeared as pairs of adjacent cells. These cells also expressed markers of all 4 lineages of terminally differentiated cells. During regeneration following graft-vs-host disease, the number of BM-derived cells was substantially increased within Ki-67-positive cells. Interestingly, the number of cells expressing markers for secretory lineage cells was significantly increased within BM-derived cells. This change was unique for BM-derived cells, resulting in a significantly increased proportion of BM-derived cells among secretory lineage cells. Conclusions: BM-derived epithelial cells arise via a mechanism other than cell fusion and rarely give rise to stem cells. However, a small proportion of these cells express proliferation markers, and a majority reside as terminally differentiated cells. During regeneration BM-derived cells increase as secretory lineage cells, thereby contributing to restore epithelial functions.

Original languageEnglish
Pages (from-to)1851-1867
Number of pages17
JournalGastroenterology
Volume128
Issue number7
DOIs
Publication statusPublished - 2005 Jun

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Intestines
Regeneration
Bone Marrow
Epithelial Cells
Bone Marrow Cells
Cell Fusion
Fluorescence In Situ Hybridization
Stem Cells
Y Chromosome
Graft vs Host Disease
Intestinal Mucosa
Bone Marrow Transplantation
Cell Count
Immunohistochemistry
Cell Proliferation
Biopsy

ASJC Scopus subject areas

  • Gastroenterology

Cite this

Increase of bone marrow-derived secretory lineage epithelial cells during regeneration in the human intestine. / Matsumoto, Tomoko; Okamoto, Ryuichi; Yajima, Tomoharu; Mori, Takehiko; Okamoto, Shinichiro; Ikeda, Yasuo; Mukai, Makio; Yamazaki, Motomi; Oshima, Shigeru; Tsuchiya, Kiichiro; Nakamura, Tetsuya; Kanai, Takanori; Okano, Hideyuki; Inazawa, Johji; Hibi, Toshifumi; Watanabe, Mamoru.

In: Gastroenterology, Vol. 128, No. 7, 06.2005, p. 1851-1867.

Research output: Contribution to journalArticle

Matsumoto, T, Okamoto, R, Yajima, T, Mori, T, Okamoto, S, Ikeda, Y, Mukai, M, Yamazaki, M, Oshima, S, Tsuchiya, K, Nakamura, T, Kanai, T, Okano, H, Inazawa, J, Hibi, T & Watanabe, M 2005, 'Increase of bone marrow-derived secretory lineage epithelial cells during regeneration in the human intestine', Gastroenterology, vol. 128, no. 7, pp. 1851-1867. https://doi.org/10.1053/j.gastro.2005.03.085
Matsumoto, Tomoko ; Okamoto, Ryuichi ; Yajima, Tomoharu ; Mori, Takehiko ; Okamoto, Shinichiro ; Ikeda, Yasuo ; Mukai, Makio ; Yamazaki, Motomi ; Oshima, Shigeru ; Tsuchiya, Kiichiro ; Nakamura, Tetsuya ; Kanai, Takanori ; Okano, Hideyuki ; Inazawa, Johji ; Hibi, Toshifumi ; Watanabe, Mamoru. / Increase of bone marrow-derived secretory lineage epithelial cells during regeneration in the human intestine. In: Gastroenterology. 2005 ; Vol. 128, No. 7. pp. 1851-1867.
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AU - Matsumoto, Tomoko

AU - Okamoto, Ryuichi

AU - Yajima, Tomoharu

AU - Mori, Takehiko

AU - Okamoto, Shinichiro

AU - Ikeda, Yasuo

AU - Mukai, Makio

AU - Yamazaki, Motomi

AU - Oshima, Shigeru

AU - Tsuchiya, Kiichiro

AU - Nakamura, Tetsuya

AU - Kanai, Takanori

AU - Okano, Hideyuki

AU - Inazawa, Johji

AU - Hibi, Toshifumi

AU - Watanabe, Mamoru

PY - 2005/6

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N2 - Background & Aims: We have previously reported that bone marrow (BM)-derived cells contribute to the regeneration of the human intestinal epithelium. To analyze further how these cells arise, proliferate, and differentiate as epithelial cells, histologic analysis was conducted using endoscopic specimens. Methods: Thirty biopsy specimens from 14 female, sex-mismatched BM-transplantation recipients were examined. BM-derived cells were identified by fluorescent in situ hybridization (FISH) for the Y chromosome and immunohistochemistry. Multicolor FISH was used to exclude cell fusion. These cells were further analyzed for various differentiation or proliferation markers. Results: No evidence of cell fusion was detected. BM-derived cells did not distribute within the crypt as stem cells and rarely expressed Musashi-1. However, BM-derived epithelial cells frequently expressed Ki-67, and some of these cells appeared as pairs of adjacent cells. These cells also expressed markers of all 4 lineages of terminally differentiated cells. During regeneration following graft-vs-host disease, the number of BM-derived cells was substantially increased within Ki-67-positive cells. Interestingly, the number of cells expressing markers for secretory lineage cells was significantly increased within BM-derived cells. This change was unique for BM-derived cells, resulting in a significantly increased proportion of BM-derived cells among secretory lineage cells. Conclusions: BM-derived epithelial cells arise via a mechanism other than cell fusion and rarely give rise to stem cells. However, a small proportion of these cells express proliferation markers, and a majority reside as terminally differentiated cells. During regeneration BM-derived cells increase as secretory lineage cells, thereby contributing to restore epithelial functions.

AB - Background & Aims: We have previously reported that bone marrow (BM)-derived cells contribute to the regeneration of the human intestinal epithelium. To analyze further how these cells arise, proliferate, and differentiate as epithelial cells, histologic analysis was conducted using endoscopic specimens. Methods: Thirty biopsy specimens from 14 female, sex-mismatched BM-transplantation recipients were examined. BM-derived cells were identified by fluorescent in situ hybridization (FISH) for the Y chromosome and immunohistochemistry. Multicolor FISH was used to exclude cell fusion. These cells were further analyzed for various differentiation or proliferation markers. Results: No evidence of cell fusion was detected. BM-derived cells did not distribute within the crypt as stem cells and rarely expressed Musashi-1. However, BM-derived epithelial cells frequently expressed Ki-67, and some of these cells appeared as pairs of adjacent cells. These cells also expressed markers of all 4 lineages of terminally differentiated cells. During regeneration following graft-vs-host disease, the number of BM-derived cells was substantially increased within Ki-67-positive cells. Interestingly, the number of cells expressing markers for secretory lineage cells was significantly increased within BM-derived cells. This change was unique for BM-derived cells, resulting in a significantly increased proportion of BM-derived cells among secretory lineage cells. Conclusions: BM-derived epithelial cells arise via a mechanism other than cell fusion and rarely give rise to stem cells. However, a small proportion of these cells express proliferation markers, and a majority reside as terminally differentiated cells. During regeneration BM-derived cells increase as secretory lineage cells, thereby contributing to restore epithelial functions.

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