Tracking of intertissue migration reveals the origins of tumor-infiltrating monocytes

Myeloid cells such as monocytes and monocyte-derived macrophages promote tumor progression. Recent reports suggest that extramedullary hematopoiesis sustains a sizable reservoir of tumor-infiltrating monocytes in the spleen. However, the influence of the spleen on tumor development and the extent to...

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Published in:	Proceedings of the National Academy of Sciences - PNAS Vol. 111; no. 21; p. 7771
Main Authors:	Shand, Francis H W, Ueha, Satoshi, Otsuji, Mikiya, Koid, Suang Suang, Shichino, Shigeyuki, Tsukui, Tatsuya, Kosugi-Kanaya, Mizuha, Abe, Jun, Tomura, Michio, Ziogas, James, Matsushima, Kouji
Format:	Journal Article
Language:	English
Published:	United States 27.05.2014
Subjects:	Analysis of Variance Animals Bone Marrow Cells - immunology Carcinogenesis - immunology Cell Movement - immunology Fluorescence Hematopoiesis - physiology Male Mice Mice, Inbred C57BL Monocytes - immunology Spleen - cytology Spleen - immunology tumor-associated macrophage KikGR Fucci cancer immunity monocytopoiesis
ISSN:	1091-6490, 1091-6490
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Abstract	Myeloid cells such as monocytes and monocyte-derived macrophages promote tumor progression. Recent reports suggest that extramedullary hematopoiesis sustains a sizable reservoir of tumor-infiltrating monocytes in the spleen. However, the influence of the spleen on tumor development and the extent to which spleen monocytes populate the tumor relative to bone marrow (BM) monocytes remain controversial. Here, we used mice expressing the photoconvertible protein Kikume Green-Red to track the redistribution of monocytes from the BM and spleen, and mice expressing fluorescent ubiquitination-based cell-cycle indicator proteins to monitor active hematopoiesis in these tissues. In mice bearing late-stage tumors, the BM, besides being the major site of monocyte production, supplied the expansion of the spleen reservoir, replacing 9% of spleen monocytes every hour. Deployment of monocytes was equally rapid from the BM and the spleen. However, BM monocytes were younger than those in the spleen and were 2.7 times more likely to migrate into the tumor from the circulation. Partly as a result of this intrinsic difference in migration potential, spleen monocytes made only a minor contribution to the tumor-infiltrating monocyte population. At least 27% of tumor monocytes had traveled from the BM in the last 24 h, compared with only 2% from the spleen. These observations highlight the importance of the BM as the primary hematopoietic tissue and monocyte reservoir in tumor-bearing mice, despite the changes that occur in the spleen monocyte reservoir during tumor development.
AbstractList	Myeloid cells such as monocytes and monocyte-derived macrophages promote tumor progression. Recent reports suggest that extramedullary hematopoiesis sustains a sizable reservoir of tumor-infiltrating monocytes in the spleen. However, the influence of the spleen on tumor development and the extent to which spleen monocytes populate the tumor relative to bone marrow (BM) monocytes remain controversial. Here, we used mice expressing the photoconvertible protein Kikume Green-Red to track the redistribution of monocytes from the BM and spleen, and mice expressing fluorescent ubiquitination-based cell-cycle indicator proteins to monitor active hematopoiesis in these tissues. In mice bearing late-stage tumors, the BM, besides being the major site of monocyte production, supplied the expansion of the spleen reservoir, replacing 9% of spleen monocytes every hour. Deployment of monocytes was equally rapid from the BM and the spleen. However, BM monocytes were younger than those in the spleen and were 2.7 times more likely to migrate into the tumor from the circulation. Partly as a result of this intrinsic difference in migration potential, spleen monocytes made only a minor contribution to the tumor-infiltrating monocyte population. At least 27% of tumor monocytes had traveled from the BM in the last 24 h, compared with only 2% from the spleen. These observations highlight the importance of the BM as the primary hematopoietic tissue and monocyte reservoir in tumor-bearing mice, despite the changes that occur in the spleen monocyte reservoir during tumor development. Myeloid cells such as monocytes and monocyte-derived macrophages promote tumor progression. Recent reports suggest that extramedullary hematopoiesis sustains a sizable reservoir of tumor-infiltrating monocytes in the spleen. However, the influence of the spleen on tumor development and the extent to which spleen monocytes populate the tumor relative to bone marrow (BM) monocytes remain controversial. Here, we used mice expressing the photoconvertible protein Kikume Green-Red to track the redistribution of monocytes from the BM and spleen, and mice expressing fluorescent ubiquitination-based cell-cycle indicator proteins to monitor active hematopoiesis in these tissues. In mice bearing late-stage tumors, the BM, besides being the major site of monocyte production, supplied the expansion of the spleen reservoir, replacing 9% of spleen monocytes every hour. Deployment of monocytes was equally rapid from the BM and the spleen. However, BM monocytes were younger than those in the spleen and were 2.7 times more likely to migrate into the tumor from the circulation. Partly as a result of this intrinsic difference in migration potential, spleen monocytes made only a minor contribution to the tumor-infiltrating monocyte population. At least 27% of tumor monocytes had traveled from the BM in the last 24 h, compared with only 2% from the spleen. These observations highlight the importance of the BM as the primary hematopoietic tissue and monocyte reservoir in tumor-bearing mice, despite the changes that occur in the spleen monocyte reservoir during tumor development.Myeloid cells such as monocytes and monocyte-derived macrophages promote tumor progression. Recent reports suggest that extramedullary hematopoiesis sustains a sizable reservoir of tumor-infiltrating monocytes in the spleen. However, the influence of the spleen on tumor development and the extent to which spleen monocytes populate the tumor relative to bone marrow (BM) monocytes remain controversial. Here, we used mice expressing the photoconvertible protein Kikume Green-Red to track the redistribution of monocytes from the BM and spleen, and mice expressing fluorescent ubiquitination-based cell-cycle indicator proteins to monitor active hematopoiesis in these tissues. In mice bearing late-stage tumors, the BM, besides being the major site of monocyte production, supplied the expansion of the spleen reservoir, replacing 9% of spleen monocytes every hour. Deployment of monocytes was equally rapid from the BM and the spleen. However, BM monocytes were younger than those in the spleen and were 2.7 times more likely to migrate into the tumor from the circulation. Partly as a result of this intrinsic difference in migration potential, spleen monocytes made only a minor contribution to the tumor-infiltrating monocyte population. At least 27% of tumor monocytes had traveled from the BM in the last 24 h, compared with only 2% from the spleen. These observations highlight the importance of the BM as the primary hematopoietic tissue and monocyte reservoir in tumor-bearing mice, despite the changes that occur in the spleen monocyte reservoir during tumor development.
Author	Ueha, Satoshi Ziogas, James Shichino, Shigeyuki Shand, Francis H W Koid, Suang Suang Tomura, Michio Kosugi-Kanaya, Mizuha Otsuji, Mikiya Tsukui, Tatsuya Abe, Jun Matsushima, Kouji
Author_xml	– sequence: 1 givenname: Francis H W orcidid: 0000-0002-4222-6564 surname: Shand fullname: Shand, Francis H W organization: Department of Molecular Preventive Medicine, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan;Department of Pharmacology and Therapeutics, The University of Melbourne, Parkville, Victoria 3010, Australia – sequence: 2 givenname: Satoshi surname: Ueha fullname: Ueha, Satoshi organization: Department of Molecular Preventive Medicine, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan – sequence: 3 givenname: Mikiya surname: Otsuji fullname: Otsuji, Mikiya organization: Department of Molecular Preventive Medicine, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan – sequence: 4 givenname: Suang Suang surname: Koid fullname: Koid, Suang Suang organization: Department of Pharmacology and Therapeutics, The University of Melbourne, Parkville, Victoria 3010, Australia;St. Vincent's Institute of Medical Research, Fitzroy, Victoria 3065, Australia – sequence: 5 givenname: Shigeyuki surname: Shichino fullname: Shichino, Shigeyuki organization: Department of Molecular Preventive Medicine, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan – sequence: 6 givenname: Tatsuya surname: Tsukui fullname: Tsukui, Tatsuya organization: Department of Molecular Preventive Medicine, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan – sequence: 7 givenname: Mizuha surname: Kosugi-Kanaya fullname: Kosugi-Kanaya, Mizuha organization: Department of Molecular Preventive Medicine, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan;Department of Hematology, Hokkaido University Graduate School of Medicine, Kita-15 Nishi-7, Kita-ku, Sapporo, Hokkaido 060-8638, Japan; and – sequence: 8 givenname: Jun surname: Abe fullname: Abe, Jun organization: Department of Molecular Preventive Medicine, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan – sequence: 9 givenname: Michio surname: Tomura fullname: Tomura, Michio organization: Center for Innovation in Immunoregulative Technology and Therapeutics, Graduate School of Medicine, Kyoto University, Yoshidakonoe-cho, Sakyo-ku, Kyoto 606-8501, Japan – sequence: 10 givenname: James surname: Ziogas fullname: Ziogas, James organization: Department of Pharmacology and Therapeutics, The University of Melbourne, Parkville, Victoria 3010, Australia – sequence: 11 givenname: Kouji surname: Matsushima fullname: Matsushima, Kouji email: koujim@m.u-tokyo.ac.jp organization: Department of Molecular Preventive Medicine, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan; koujim@m.u-tokyo.ac.jp
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Snippet	Myeloid cells such as monocytes and monocyte-derived macrophages promote tumor progression. Recent reports suggest that extramedullary hematopoiesis sustains a...
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SubjectTerms	Analysis of Variance Animals Bone Marrow Cells - immunology Carcinogenesis - immunology Cell Movement - immunology Fluorescence Hematopoiesis - physiology Male Mice Mice, Inbred C57BL Monocytes - immunology Spleen - cytology Spleen - immunology
Title	Tracking of intertissue migration reveals the origins of tumor-infiltrating monocytes
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