Myeloid progenitor cells in the premetastatic lung promote metastases by inducing mesenchymal to epithelial transition

Cancer Research

Volumn 72, Issue 6, 2012, Pages 1384-1394

  Gao, Dingcheng ^a   Joshi, Natasha ^a   Choi, Hyejin ^a   Ryu, Seongho ^a   Hahn, Mary ^a   Catena, Raul ^a   Sadik, Helen ^b   Argani, Pedram ^b   Wagner, Patrick ^a   Vahdat, Linda T ^a   Port, Jeffrey L ^a   Stiles, Brendon ^a   Sukumar, Saraswati ^b   Altorki, Nasser K ^a   Rafii, Shahin ^a   Mittal, Vivek ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEOGLYCAN; SMAD2 PROTEIN; VERSICAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER CELL; CANCER IMMUNOLOGY; CANCER PATIENT; CD11B+ GR+ MYELOID PROGENITOR CELL; CD11B+ LY6C+ MONOCYTE; CELL FRACTIONATION; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; GENE EXPRESSION PROFILING; HEMATOPOIETIC STEM CELL; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; LUNG METASTASIS; MALE; METASTASIS; MONOCYTE; MOUSE; MYELOID PROGENITOR CELL; NONHUMAN; PREMETASTASIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; STROMA CELL;

ANIMALS; ANTIGENS, CD11B; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HUMANS; LUNG NEOPLASMS; MALE; MAMMARY NEOPLASMS, ANIMAL; MICE; MICE, TRANSGENIC; MYELOID PROGENITOR CELLS; SMAD2 PROTEIN; VERSICANS;

EID: 84858199187     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-2905     Document Type: Article

References (41)

1. Townson JL, Chambers AF. Dormancy of solitary metastatic cells. Cell Cycle 2006;5:1744-50. (Pubitemid 44435316)
2. Naumov GN, Bender E, Zurakowski D, Kang SY, Sampson D, Flynn E, et al. A model of human tumor dormancy: an angiogenic switch from the nonangiogenic phenotype. J Natl Cancer Inst 2006;98:316-25. (Pubitemid 43338211)
3. Gupta GP, Massague J. Cancer metastasis: building a framework. Cell 2006;127:679-95. (Pubitemid 44781029)
4. Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat Rev Cancer 2009;9:239-52.
5. Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 2009;9:265-73.
6. Fidler IJ. The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat Rev Cancer 2003;3:453-8. (Pubitemid 37328849)
7. Kaplan RN, Psaila B, Lyden D. Bone marrow cells in the 'pre-metastatic niche': within bone and beyond. Cancer Metastasis Rev 2006;25:521-9. (Pubitemid 46071861)
8. Gao D, Nolan DJ, Mellick AS, Bambino K, McDonnell K, Mittal V. Endothelial progenitor cells control the angiogenic switch in mouse lung metastasis. Science 2008;319:195-8.
9. Chaffer CL, Thompson EW, Williams ED. Mesenchymal to epithelial transition in development and disease. Cells Tissues Organs 2007;185:7-19. (Pubitemid 46956838)
10. Dutt S, Cassoly E, Dours-Zimmermann MT, Matasci M, Stoeckli ET, Zimmermann DR. Versican V0 and V1 direct the growth of peripheral axons in the developing chick hindlimb. J Neurosci 2011;31:5262-70.
11. Guy CT, Cardiff RD, Muller WJ. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol Cell Biol 1992;12:954-61.
12. Nolan DJ, Ciarrocchi A, Mellick AS, Jaggi JS, Bambino K, Gupta S, et al. Bone marrow-derived endothelial progenitor cells are a major determinant of nascent tumor neovascularization. Genes Dev 2007;21:1546-58. (Pubitemid 46955726)
13. Wight TN. Versican: a versatile extracellular matrix proteoglycan in cell biology. Curr Opin Cell Biol 2002;14:617-23. (Pubitemid 35247746)
14. Ricciardelli C, Brooks JH, Suwiwat S, Sakko AJ, Mayne K, Raymond WA, et al. Regulation of stromal versican expression by breast cancer cells and importance to relapse-free survival in patients with nodenegative primary breast cancer. Clin Cancer Res 2002;8:1054-60. (Pubitemid 35177355)
15. Suwiwat S, Ricciardelli C, Tammi R, Tammi M, Auvinen P, Kosma VM, et al. Expression of extracellular matrix components versican, chondroitin sulfate, tenascin, and hyaluronan, and their association with disease outcome in node-negative breast cancer. Clin Cancer Res 2004;10:2491-8. (Pubitemid 38445711)
16. Pukkila M, Kosunen A, Ropponen K, Virtaniemi J, Kellokoski J, Kumpulainen E, et al. High stromal versican expression predicts unfavourable outcome in oral squamous cell carcinoma. J Clin Pathol 2007;60:267-72. (Pubitemid 46447741)
17. Kodama J, Hasengaowa, Kusumoto T, Seki N, Matsuo T, Ojima Y, et al. Prognostic significance of stromal versican expression in human endometrial cancer. Ann Oncol 2007;18:269-74.
18. Pirinen R, Leinonen T, Bohm J, Johansson R, Ropponen K, Kumpulainen E, et al. Versican in nonsmall cell lung cancer: relation to hyaluronan, clinicopathologic factors, and prognosis. Hum Pathol 2005;36:44-50. (Pubitemid 40220332)
19. Pukkila MJ, Kosunen AS, Virtaniemi JA, Kumpulainen EJ, Johansson RT, Kellokoski JK, et al. Versican expression in pharyngeal squamous cell carcinoma: an immunohistochemical study. J Clin Pathol 2004;57:735-9. (Pubitemid 38901489)
20. Krystal G, Sly L, Antignano F, Ho V, Ruschmann J, Hamilton M. Re: The terminology issue for myeloid-derived suppressor cells. Cancer Res 2007;67:3986. (Pubitemid 46762189)
21. Gabrilovich DI, Bronte V, Chen SH, Colombo MP, Ochoa A, Ostrand-Rosenberg S, et al. The terminology issue for myeloid-derived suppressor cells. Cancer Res 2007;67:425; author reply 426.
22. Coffelt SB, Lewis CE, Naldini L, Brown JM, Ferrara N, De Palma M. Elusive identities and overlapping phenotypes of proangiogenic myeloid cells in tumors. Am J Pathol 2010;176:1564-76.
23. Ricciardelli C, Sakko AJ, Ween MP, Russell DL, Horsfall DJ. The biological role and regulation of versican levels in cancer. Cancer Metastasis Rev 2009;28:233-45.
24. Zimmermann DR, Ruoslahti E. Multiple domains of the large fibroblast proteoglycan, versican. EMBO J 1989;8:2975-81. (Pubitemid 19274999)
25. Sheng W, Wang G, Wang Y, Liang J, Wen J, Zheng PS, et al. The roles of versican V1 and V2 isoforms in cell proliferation and apoptosis. Mol Biol Cell 2005;16:1330-40. (Pubitemid 40349568)
26. Padua D, Massague J. Roles of TGFbeta in metastasis. Cell Res 2009;19:89-102.
27. Shi Y, Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 2003;113:685-700. (Pubitemid 36724933)
28. Song J. EMT or apoptosis: a decision for TGF-beta. Cell Res 2007;17:289-90.
29. Hata A, Shi Y, Massague J. TGF-beta signaling and cancer: structural and functional consequences of mutations in Smads. Mol Med Today 1998;4:257-62.
30. Hugo H, Ackland ML, Blick T, Lawrence MG, Clements JA, Williams ED, et al. Epithelial-mesenchymal and mesenchymal-epithelial transitions in carcinoma progression. J Cell Physiol 2007;213:374-83. (Pubitemid 47509716)
31. Chaffer CL, Brennan JP, Slavin JL, Blick T, Thompson EW, Williams ED. Mesenchymal-to-epithelial transition facilitates bladder cancer metastasis: role of fibroblast growth factor receptor-2. Cancer Res 2006;66:11271-8. (Pubitemid 46009956)
32. Kowanetz M, Wu X, Lee J, Tan M, Hagenbeek T, Qu X, et al. Granulocyte- colony stimulating factor promotes lung metastasis through mobilization of Ly6G+Ly6C +granulocytes. Proc Natl Acad Sci U S A 2010;107:21248-55.
33. Erler JT, Bennewith KL, Cox TR, Lang G, Bird D, Koong A, et al. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 2009;15:35-44.
34. Yang L, Huang J, Ren X, Gorska AE, Chytil A, Aakre M, et al. Abrogation of TGF beta signaling in mammary carcinomas recruits Gr-1+CD11b +myeloid cells that promote metastasis. Cancer Cell 2008;13:23-35. (Pubitemid 350309741)
35. Ostrand-Rosenberg S, Sinha P. Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol 2009;182:4499-506.
36. Youn JI, Nagaraj S, Collazo M, Gabrilovich DI. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol 2008;181:5791-802.
37. Kim S, Takahashi H, Lin WW, Descargues P, Grivennikov S, Kim Y, et al. Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature 2009;457:102-6.
38. Vainio S, Lin Y. Coordinating early kidney development: lessons from gene targeting. Nat Rev Genet 2002;3:533-43. (Pubitemid 34746878)
39. Prudkin L, Liu DD, Ozburn NC, Sun M, Behrens C, Tang X, et al. Epithelial-to-mesenchymal transition in the development and progression of adenocarcinoma and squamous cell carcinoma of the lung. Mod Pathol 2009;22:668-78.
40. Mur C, Martínez-Carpio PA, Fernández-Montolí ME, Ramon JM, Rosel P, Navarro MA. Growth of MDA-MB-231 cell line: different effects of TGF-beta(1), EGF and estradiol depending on the length of exposure. Cell Biol Int 1998;22:679-84. (Pubitemid 29370942)
41. Zugmaier G, Ennis BW, Deschauer B, Katz D, Knabbe C, Wilding G, et al. Transforming growth factors type beta 1 and beta 2 are equipotent growth inhibitors of human breast cancer cell lines. J Cell Physiol 1989;141:353-61. (Pubitemid 19272278)