Bone marrow macrophages support prostate cancer growth in bone

Oncotarget

Volumn 6, Issue 34, 2015, Pages 35782-35796

  Soki, Fabiana N ^a   Cho, Sun Wook ^b   Kim, Yeo Won ^a   Jones, Jacqueline D ^a   Park, Serk In ^c,d   Koh, Amy J ^a   Entezami, Payam ^a   Daignault Newton, Stephanie ^e   Pienta, Kenneth J ^f   Roca, Hernan ^a   McCauley, Laurie K ^a,g  

^a UNIVERSITY OF MICHIGAN SCHOOL OF DENTISTRY   (United States)

^b National Medical Center   (South Korea)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^d Korea University College of Medicine   (South Korea)

^e UNIVERSITY OF MICHIGAN   (United States)

^f JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Clodronate liposome; Efferocytosis; Macrophages; MAFIA mouse; Prostate cancer; Skeletal metastasis

Indexed keywords

CLODRONIC ACID; COLONY STIMULATING FACTOR 1; COLONY STIMULATING FACTOR RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE; BONE MARROW DERIVED MACROPHAGE; BONE METASTASIS; CONTROLLED STUDY; MALE; MICRO-COMPUTED TOMOGRAPHY; MORPHOMETRICS; MOUSE; MOUSE MODEL; NONHUMAN; PROSTATE CANCER; PROSTATE CANCER CELL LINE; TIBIA; TUMOR GROWTH; ANIMAL; BONE MARROW CELL; BONE REGENERATION; BONE TUMOR; C57BL MOUSE; CARCINOGENESIS; CELL GROWTH; HUMAN; IMMUNOLOGY; MACROPHAGE; METABOLISM; PATHOLOGY; PROSTATE TUMOR; SECONDARY; TRANSGENIC MOUSE; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALS; BONE MARROW CELLS; BONE NEOPLASMS; BONE REGENERATION; CARCINOGENESIS; CELL GROWTH PROCESSES; CELL LINE, TUMOR; CLODRONIC ACID; HUMANS; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PROSTATIC NEOPLASMS; RECEPTOR, MACROPHAGE COLONY-STIMULATING FACTOR; TUMOR BURDEN;

EID: 84946865859     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6042     Document Type: Article

References (39)

1. Weilbaecher, K. N., Guise, T. A., and McCauley, L. K. (2011) Cancer to bone: a fatal attraction. Nat. Rev. Cancer 11, 411-425
2. Loberg, R. D., Gayed, B. A., Olson, K. B., and Pienta, K. J. (2005) A paradigm for the treatment of prostate cancer bone metastases based on an understanding of tumor cellmicroenvironment interactions. J. Cell Biochem. 96, 439-446
3. Pettit, A. R., Chang, M. K., Hume, D. A., and Raggatt, L. J. (2008) Osteal macrophages: a new twist on coupling during bone dynamics. Bone 43, 976-982
4. Pollard, J. W. (2009) Trophic macrophages in development and disease. Nat. Rev. Immunol. 9, 259-270
5. Pollard, J. W. (2004) Tumour-educated macrophages promote tumour progression and metastasis. Nat. Rev. Cancer 4, 71-78
6. Lewis, C. E. and Pollard, J. W. (2006) Distinct role of macrophages in different tumor microenvironments. Cancer Res. 66, 605-612
7. Mantovani, A. and Sica, A. (2010) Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr. Opin. Immunol. 22, 231-237
8. Mantovani, A. (2010) La mala educacion of tumorassociated macrophages: Diverse pathways and new players. Cancer Cell 17, 111-112
9. Richardsen, E., Uglehus, R. D., Due, J., Busch, C., and Busund, L. T. (2008) The prognostic impact of M-CSF, CSF-1 receptor, CD68 and CD3 in prostatic carcinoma. Histopathology 53, 30-38
10. Park, S. I., Liao, J., Berry, J. E., Li, X., Koh, A. J., Michalski, M. E., Eber, M. R., Soki, F. N., Sadler, D., Sud, S., Tisdelle, S., Daignault, S. D., Nemeth, J. A., Snyder, L. A., Wronski, T. J., Pienta, K. J., and McCauley, L. K. (2012) Cyclophosphamide creates a receptive microenvironment for prostate cancer skeletal metastasis. Cancer Res. 72, 2522-2532
11. Mizutani, K., Sud, S., McGregor, N. A., Martinovski, G., Rice, B. T., Craig, M. J., Varsos, Z. S., Roca, H., and Pienta, K. J. (2009) The chemokine CCL2 increases prostate tumor growth and bone metastasis through macrophage and osteoclast recruitment. Neoplasia. 11, 1235-1242
12. Loberg, R. D., Ying, C., Craig, M., Yan, L., Snyder, L. A., and Pienta, K. J. (2007) CCL2 as an important mediator of prostate cancer growth in vivo through the regulation of macrophage infiltration. Neoplasia. 9, 556-562
13. Loberg, R. D., Ying, C., Craig, M., Day, L. L., Sargent, E., Neeley, C., Wojno, K., Snyder, L. A., Yan, L., and Pienta, K. J. (2007) Targeting CCL2 with systemic delivery of neutralizing antibodies induces prostate cancer tumor regression in vivo. Cancer Res. 67, 9417-9424
14. Roca, H., Varsos, Z. S., Sud, S., Craig, M. J., Ying, C., and Pienta, K. J. (2009) CCL2 and interleukin-6 promote survival of human CD11b+ peripheral blood mononuclear cells and induce M2-type macrophage polarization. J. Biol. Chem. 284, 34342-34354
15. Rozel, S., Galban, C. J., Nicolay, K., Lee, K. C., Sud, S., Neeley, C., Snyder, L. A., Chenevert, T. L., Rehemtulla, A., Ross, B. D., and Pienta, K. J. (2009) Synergy between anti-CCL2 and docetaxel as determined by DW-MRI in a metastatic bone cancer model. J. Cell Biochem. 107, 58-64
16. Austyn, J. M. and Gordon, S. (1981) F4/80, a monoclonal antibody directed specifically against the mouse macrophage. Eur. J. Immunol. 11, 805-815
17. Chang, M. K., Raggatt, L. J., Alexander, K. A., Kuliwaba, J. S., Fazzalari, N. L., Schroder, K., Maylin, E. R., Ripoll, V. M., Hume, D. A., and Pettit, A. R. (2008) Osteal tissue macrophages are intercalated throughout human and mouse bone lining tissues and regulate osteoblast function in vitro and in vivo. J. Immunol. 181, 1232-1244
18. Alexander, K. A., Chang, M. K., Maylin, E. R., Kohler, T., Muller, R., Wu, A. C., van, R. N., Sweet, M. J., Hume, D. A., Raggatt, L. J., and Pettit, A. R. (2011) Osteal macrophages promote in vivo intramembranous bone healing in a mouse tibial injury model. J. Bone Miner. Res. 26, 1517-1532
19. Winkler, I. G., Sims, N. A., Pettit, A. R., Barbier, V., Nowlan, B., Helwani, F., Poulton, I. J., van, R. N., Alexander, K. A., Raggatt, L. J., and Levesque, J. P. (2010) Bone marrow macrophages maintain hematopoietic stem cell (HSC) niches and their depletion mobilizes HSCs. Blood 116, 4815-4828
20. Cho, S. W., Soki, F. N., Koh, A. J., Eber, M. R., Entezami, P., Park, S. I., van, R. N., and McCauley, L. K. (2014) Osteal macrophages support physiologic skeletal remodeling and anabolic actions of parathyroid hormone in bone. Proc. Natl. Acad. Sci. U. S. A 111, 1545-1550
21. Burnett, S. H., Kershen, E. J., Zhang, J., Zeng, L., Straley, S. C., Kaplan, A. M., and Cohen, D. A. (2004) Conditional macrophage ablation in transgenic mice expressing a Fasbased suicide gene. J. Leukoc. Biol. 75, 612-623
22. Power, C. A., Pwint, H., Chan, J., Cho, J., Yu, Y., Walsh, W., and Russell, P. J. (2009) A novel model of bonemetastatic prostate cancer in immunocompetent mice. Prostate 69, 1613-1623
23. Koh, A. J., Demiralp, B., Neiva, K. G., Hooten, J., Nohutcu, R. M., Shim, H., Datta, N. S., Taichman, R. S., and McCauley, L. K. (2005) Cells of the osteoclast lineage as mediators of the anabolic actions of parathyroid hormone in bone. Endocrinology 146, 4584-4596
24. Mantovani, A., Sica, A., Sozzani, S., Allavena, P., Vecchi, A., and Locati, M. (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25, 677-686
25. Siveen, K. S. and Kuttan, G. (2009) Role of macrophages in tumour progression. Immunol. Lett. 123, 97-102
26. Murdoch, C., Muthana, M., Coffelt, S. B., and Lewis, C. E. (2008) The role of myeloid cells in the promotion of tumour angiogenesis. Nat. Rev. Cancer 8, 618-631
27. McCauley, L. K. and Martin, T. J. (2012) Twenty-five years of PTHrP progress: from cancer hormone to multifunctional cytokine. J. Bone Miner. Res. 27, 1231-1239
28. Li, X., Loberg, R., Liao, J., Ying, C., Snyder, L. A., Pienta, K. J., and McCauley, L. K. (2009) A destructive cascade mediated by CCL2 facilitates prostate cancer growth in bone. Cancer Res. 69, 1685-1692
29. Zhang, J., Patel, L., and Pienta, K. J. (2010) CC chemokine ligand 2 (CCL2) promotes prostate cancer tumorigenesis and metastasis. Cytokine Growth Factor Rev. 21, 41-48
30. Fridlender, Z. G., Kapoor, V., Buchlis, G., Cheng, G., Sun, J., Wang, L. C., Singhal, S., Snyder, L. A., and Albelda, S. M. (2010) CCL2 Blockade Inhibits Lung Cancer Tumor Growth by Altering Macrophage Phenotype and Activating CD8+ Cells. Am. J. Respir. Cell Mol. Biol.
31. Soki, F. N., Park, S. I., and McCauley, L. K. (2012) The multifaceted actions of PTHrP in skeletal metastasis. Future. Oncol. 8, 803-817
32. Park, S. I., Lee, C., Sadler, W. D., Koh, A. J., Jones, J., Seo, J. W., Soki, F. N., Cho, S. W., Daignault, S. D., and McCauley, L. K. (2013) Parathyroid hormone-related protein drives a CD11b+Gr1+ cell-mediated positive feedback loop to support prostate cancer growth. Cancer Res. 73, 6574-6583
33. Reiter, I., Krammer, B., and Schwamberger, G. (1999) Cutting edge: differential effect of apoptotic versus necrotic tumor cells on macrophage antitumor activities. J. Immunol. 163, 1730-1732
34. Michlewska, S., Dransfield, I., Megson, I. L., and Rossi, A. G. (2009) Macrophage phagocytosis of apoptotic neutrophils is critically regulated by the opposing actions of pro-inflammatory and anti-inflammatory agents: key role for TNF-alpha. FASEB J. 23, 844-854
35. Gregory, C. D. and Pound, J. D. (2011) Cell death in the neighbourhood: direct microenvironmental effects of apoptosis in normal and neoplastic tissues. J. Pathol. 223, 177-194
36. Soki, F. N., Koh, A. J., Jones, J. D., Kim, Y. W., Dai, J., Keller, E. T., Pienta, K. J., Atabai, K., Roca, H., and McCauley, L. K. (2014) Polarization of prostate cancerassociated macrophages is induced by milk fat globule-EGF factor 8 (MFG-E8)-mediated efferocytosis. J. Biol. Chem. 289, 24560-24572
37. Schneider, A., Kalikin, L. M., Mattos, A. C., Keller, E. T., Allen, M. J., Pienta, K. J., and McCauley, L. K. (2005) Bone turnover mediates preferential localization of prostate cancer in the skeleton. Endocrinology 146, 1727-1736
38. Park, S. I., Kim, S. J., McCauley, L. K., and Gallick, G. E. (2010) Pre-clinical mouse models of human prostate cancer and their utility in drug discovery. Curr. Protoc. Pharmacol. Chapter 14, Unit 14.15
39. Dempster, D. W., Compston, J. E., Drezner, M. K., Glorieux, F. H., Kanis, J. A., Malluche, H., Meunier, P. J., Ott, S. M., Recker, R. R., and Parfitt, A. M. (2013) Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee. J. Bone Miner. Res. 28, 2-17