A novel model of dormancy for bone metastatic breast cancer cells

Cancer Research

Volumn 73, Issue 23, 2013, Pages 6886-6899

  Marlow, Rebecca ^a,b   Honeth, Gabriella ^a   Lombardi, Sara ^a   Cariati, Massimiliano ^b   Hessey, Sonya ^a   Pipili, Aikaterini ^a   Mariotti, Veronica ^a   Buchupalli, Bharath ^a   Foster, Katie ^c   Bonnet, Dominique ^c   Grigoriadis, Agamemnon ^b   Rameshwar, Pranela ^d   Purushotham, Anand ^a,b   Tutt, Andrew ^a,b   Dontu, Gabriela ^a,b  

^a GUY S HOSPITAL   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^d RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW; BONE METASTASIS; BREAST CANCER; CANCER CELL; CELL PROLIFERATION; CELL TYPE; COCULTURE; CONTROLLED STUDY; DORMANCY; FEMALE; HUMAN; HUMAN CELL; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEM CELL NICHE; TUMOR MICROENVIRONMENT;

EID: 84890259230     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-0991     Document Type: Article

References (51)

1. Husemann Y, Geigl JB, Schubert F, Musiani P, Meyer M, Burghart E, et al. Systemic spread is an early step in breast cancer. Cancer Cell 2008;13:58-68.
2. Fehm T, Muller V, Alix-Panabieres C, Pantel K. Micrometastatic spread in breast cancer: detection, molecular characterization and clinical relevance. Breast Cancer Res 2008;10 Suppl 1:S1.
3. Aguirre-Ghiso JA. Models, mechanisms and clinical evidence for cancer dormancy. Nat Rev Cancer 2007;7:834-46.
4. Klein CA. Framework models of tumor dormancy from patient-derived observations. Curr Opin Genet Dev. 2011;21:42-9.
5. Patel LR, Camacho DF, Shiozawa Y, Pienta KJ, Taichman RS. Mechanisms of cancer cell metastasis to the bone: a multistep process. Future Oncol. 2011;7:1285-97.
6. Weilbaecher KN, Guise TA, McCauley LK. Cancer to bone: a fatal attraction. Nat Rev Cancer 2011;11:411-25.
7. Uhr JW, Pantel K. Controversies in clinical cancer dormancy. Proc Natl Acad Sci USA 2011;108:12396-400.
8. Patel SA, Dave MA, Murthy RG, Helmy KY, Rameshwar P. Metastatic breast cancer cells in the bone marrow microenvironment: novel insights into oncoprotection. Oncol Rev 2011;5:93-102.
9. Goss PE, Chambers AF. Does tumour dormancy offer a therapeutic target? Nat Rev Cancer 2010;10:871-7.
10. Ema H, Suda T. Two anatomically distinct niches regulate stem cell activity. Blood 2012;120:2174-81.
11. Rao G, Patel PS, Idler SP, Maloof P, Gascon P, Potian JA, et al. Facilitating role of preprotachykinin-I gene in the integration of breast cancer cells within the stromal compartment of the bone marrow: a model of early cancer progression. Cancer Res 2004;64:2874-81.
12. Shiozawa Y, Pedersen EA, Havens AM, Jung Y, Mishra A, Joseph J, et al. Human prostate cancer metastases target the hematopoietic stem cell niche to establish footholds in mouse bone marrow. J Clin Invest 2011;121:1298-312.
13. Bragado P, Sosa MS, Keely P, Condeelis J, Aguirre-Ghiso JA. Microenvironments dictating tumor cell dormancy. Recent Results Cancer Res 2012;195:25-39.
14. Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, Finetti P, et al. Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res 2009;69:1302-13.
15. Kang Y, Siegel PM, Shu W, Drobnjak M, Kakonen SM, Cordon-Cardo C, et al. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 2003;3:537-49.
16. Grigoriadis A, Mackay A, Noel E, Wu PJ, Natrajan R, Frankum J, et al. Molecular characterisation of cell line models for triple-negative breast cancers. BMC Genomics 2012;13:619.
17. Liu S, Ginestier C, Ou SJ, Clouthier SG, Patel SH, Monville F, et al. Breast cancer stem cells are regulated by mesenchymal stem cells through cytokine networks. Cancer Res 2011;71:614-24.
18. Rohanizadeh R, Swain MV, Mason RS. Gelatin sponges (Gelfoam) as a scaffold for osteoblasts. J Mater Sci Mater Med 2008;19:1173-82.
19. Schneider A, Taboas JM, McCauley LK, Krebsbach PH. Skeletal homeostasis in tissue-engineered bone. J Orthop Res 2003;21:859-64.
20. Song J, Kiel MJ, Wang Z, Wang J, Taichman RS, Morrison SJ, et al. An in vivo model to study and manipulate the hematopoietic stem cell niche. Blood 2010;115:2592-600.
21. Aguirre-Ghiso JA, Liu D, Mignatti A, Kovalski K, Ossowski L. Urokinase receptor and fibronectin regulate the ERK(MAPK) to p38(MAPK) activity ratios that determine carcinoma cell proliferation or dormancy in vivo. Mol Biol Cell 2001;12:863-79.
22. Giampieri S, Manning C, Hooper S, Jones L, Hill CS, Sahai E. Localized and reversible TGFbeta signalling switches breast cancer cells from cohesive to single cell motility. Nat Cell Biol 2009;11:1287-96.
23. Kodera Y, Katanasaka Y, Kitamura Y, Tsuda H, Nishio K, Tamura T, et al. Sunitinib inhibits lymphatic endothelial cell functions and lymph node metastasis in a breast cancer model through inhibition of vascular endothelial growth factor receptor 3. Breast Cancer Res 2011;13:R66.
24. Nyati S, Schinske K, Ray D, Nyati MK, Ross BD, Rehemtulla A. Molecular imaging of TGFbeta-induced Smad2/3 phosphorylation reveals a role for receptor tyrosine kinases in modulating TGFbeta signaling. Clin Cancer Res 2011;17:7424-39.
25. Conley SJ, Gheordunescu E, Kakarala P, Newman B, Korkaya H, Heath AN, et al. Antiangiogenic agents increase breast cancer stem cells via the generation of tumor hypoxia. Proc Natl Acad Sci U S A 2012;109:2784-9.
26. Sukhtankar D, Okun A, Chandramouli A, Nelson MA, Vanderah TW, Cress AE, et al. Inhibition of p38-MAPK signaling pathway attenuates breast cancer induced bone pain and disease progression in a murine model of cancer-induced bone pain. Mol Pain 2011;7:81.
27. Scholzen T, Gerdes J. The Ki-67 protein: from the known and the unknown. J Cell Physiol 2000;182:311-22.
28. Kobayashi A, Okuda H, Xing F, Pandey PR, Watabe M, Hirota S, et al. Bone morphogenetic protein 7 in dormancy and metastasis of prostate cancer stem-like cells in bone. J Exp Med 2011;208:2641-55.
29. Ranganathan AC, Adam AP, Aguirre-Ghiso JA. Opposing roles of mitogenic and stress signaling pathways in the induction of cancer dormancy. Cell Cycle 2006;5:1799-807.
30. Ranganathan AC, Adam AP, Zhang L, Aguirre-Ghiso JA. Tumor cell dormancy induced by p38SAPK and ER-stress signaling: an adaptive advantage for metastatic cells? Cancer Biol Ther 2006;5:729-35.
31. Sosa MS, Avivar-Valderas A, Bragado P, Wen HC, Aguirre-Ghiso JA. ERK1/2 and p38alpha/beta signaling in tumor cell quiescence: opportunities to control dormant residual disease. Clin Cancer Res 2011;17:5850-7.
32. Massague J. TGFbeta signalling in context. Nat Rev Mol Cell Biol 2012;13:616-30.
33. Psaila B, Lyden D. The metastatic niche: adapting the foreign soil. Nat Rev Cancer 2009;9:285-93.
34. Malanchi I, Santamaria-Martinez A, Susanto E, Peng H, Lehr HA, Delaloye JF, et al. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature 2012;481:85-9.
35. Oskarsson T, Acharyya S, Zhang XH, Vanharanta S, Tavazoie SF, Morris PG, et al. Breast cancer cells produce tenascinCas a metastatic niche component to colonize the lungs. Nat Med 2011;17:867-74.
36. Gao H, Chakraborty G, Lee-Lim AP, Mo Q, Decker M, Vonica A, et al. The BMP inhibitor Coco reactivates breast cancer cells at lung metastatic sites. Cell 2012;150:764-79.
37. Shiozawa Y, Pedersen EA, Patel LR, Ziegler AM, Havens AM, Jung Y, et al. GAS6/AXL axis regulates prostate cancer invasion, proliferation, and survival in the bone marrow niche. Neoplasia 2010;12:116-27.
38. Nash KT, Phadke PA, Navenot JM, Hurst DR, Accavitti-Loper MA, Sztul E, et al. Requirement of KISS1 secretion for multiple organ metastasis suppression and maintenance of tumor dormancy. J Natl Cancer Inst 2007;99:309-21.
39. de Barros AP, Takiya CM, Garzoni LR, Leal-Ferreira ML, Dutra HS, Chiarini LB, et al. Osteoblasts and bone marrow mesenchymal stromal cells control hematopoietic stem cell migration and proliferation in 3D in vitro model. PLoS ONE 2010;5:e9093.
40. Gurkan UA, Kishore V, Condon KW, Bellido TM, Akkus O. A scaffold-free multicellular three-dimensional in vitro model of osteogenesis. Calcif Tissue Int 2011;88:388-401.
41. Heinemann C, Heinemann S, Worch H, Hanke T. Development of an osteoblast/osteoclast co-culture derived by human bone marrow stromal cells and human monocytes for biomaterials testing. Eur Cell Mater 2011;21:80-93.
42. Pallotta I, Lovett M, Rice W, Kaplan DL, Balduini A. Bone marrow osteoblastic niche: a new model to study physiological regulation of megakaryopoiesis. PLoS ONE 2009;4:e8359.
43. Nichols JE, Cortiella J, Lee J, Niles JA, Cuddihy M, Wang S, et al. In vitro analog of human bone marrow from 3D scaffolds with biomimetic inverted colloidal crystal geometry. Biomaterials 2009;30:1071-9.
44. Goldstein RH, Reagan MR, Anderson K, Kaplan DL, Rosenblatt M. Human bone marrow-derived MSCs can home to orthotopic breast cancer tumors and promote bone metastasis. Cancer Res 2010;70:10044-50.
45. Moreau JE, Anderson K, Mauney JR, Nguyen T, Kaplan DL, Rosenblatt M. Tissue-engineered bone serves as a target for metastasis of human breast cancer in a mouse model. Cancer Res 2007;67:10304-8.
46. Lu X, Mu E, Wei Y, Riethdorf S, Yang Q, Yuan M, et al. VCAM-1 promotes osteolytic expansion of indolent bone micrometastasis of breast cancer by engaging alpha4beta1-positive osteoclast progenitors. Cancer Cell 2011;20:701-14.
47. Sethi N, Dai X, Winter CG, Kang Y. Tumor-derived JAGGED1 promotes osteolytic bone metastasis of breast cancer by engaging notch signaling in bone cells. Cancer Cell 2011;19:192-205.
48. Barkan D, El Touny LH, Michalowski AM, Smith JA, Chu I, Davis AS, et al. Metastatic growth from dormant cells induced by a col-I-enriched fibrotic environment. Cancer Res 2010;70:5706-16.
49. Barkan D, Kleinman H, Simmons JL, Asmussen H, Kamaraju AK, Hoenorhoff MJ, et al. Inhibition of metastatic outgrowth from single dormant tumor cells by targeting the cytoskeleton. Cancer Res 2008;68:6241-50.
50. Ghajar CM, Peinado H, Mori H, Matei IR, Evason KJ, Brazier H, et al. The perivascular niche regulates breast tumour dormancy. Nat Cell Biol 2013;15:807-17.
51. Charafe-Jauffret E, Ginestier C, Iovino F, Tarpin C, Diebel M, Esterni B, et al. Aldehyde dehydrogenase 1-positive cancer stem cells mediate metastasis and poor clinical outcome in inflammatory breast cancer. Clin Cancer Res 2010;16:45-55.