Loss of the Timp gene family is sufficient for the acquisition of the CAF-like cell state

Nature Cell Biology

Volumn 16, Issue 9, 2014, Pages 889-901

  Shimoda, Masayuki ^a   Principe, Simona ^a   Jackson, Hartland W ^a   Luga, Valbona ^b   Fang, Hui ^a   Molyneux, Sam D ^a   Shao, Yang W ^a   Aiken, Alison ^a   Waterhouse, Paul D ^a   Karamboulas, Christina ^a   Hess, Franz M ^c   Ohtsuka, Takashi ^d   Okada, Yasunori ^d   Ailles, Laurie ^a   Ludwig, Andreas ^c   Wrana, Jeffrey L ^b   Kislinger, Thomas ^a   Khokha, Rama ^a  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b MOUNT SINAI HOSPITAL   (Canada)

^c RWTH AACHEN UNIVERSITY   (Germany)

^d KEIO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADAM PROTEINS; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; EXOSOMES; FEMALE; FIBROBLASTS; HUMANS; LUNG NEOPLASMS; MAMMARY NEOPLASMS, EXPERIMENTAL; MEMBRANE PROTEINS; METALLOENDOPEPTIDASES; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; NEOPLASM TRANSPLANTATION; PHENOTYPE; SIGNAL TRANSDUCTION; TISSUE INHIBITOR OF METALLOPROTEINASES; TUMOR BURDEN;

EID: 84906899235     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3021     Document Type: Article

References (64)

1. Kalluri, R. & Zeisberg, M. Fibroblasts in cancer. Nat. Rev. Cancer 6, 392-401 (2006).
2. Luga, V. et al. Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell 151, 1542-1556 (2012).
3. Thery, C., Ostrowski, M. & Segura, E. Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 9, 581-593 (2009).
4. Shimoda, M. & Khokha, R. Proteolytic factors in exosomes. Proteomics 13, 1624-1636 (2013).
5. Addadi, Y. et al. p53 status in stromal fibroblasts modulates tumor growth in an SDF1-dependent manner. Cancer Res. 70, 9650-9658 (2010).
6. Trimis, G., Chatzistamou, I., Politi, K., Kiaris, H. & Papavassiliou, A. G. Expression of p21waf1/Cip1 in stromal fibroblasts of primary breast tumors. Hum. Mol. Genet. 17, 3596-3600 (2008).
7. Al-Ansari, M. M., Hendrayani, S. F., Shehata, A. I. & Aboussekhra, A. p16(INK4A) represses the paracrine tumor-promoting effects of breast stromal fibroblasts. Oncogene 32, 2356-2364 (2013).
8. Trimboli, A. J. et al. Pten in stromal fibroblasts suppresses mammary epithelial tumours. Nature 461, 1084-1091 (2009).
9. Sotgia, F. et al. Caveolin-1-/-null mammary stromal fibroblasts share characteristics with human breast cancer-associated fibroblasts. Am. J. Pathol. 174, 746-761 (2009).
10. Bhowmick, N. A. et al. TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 303, 848-851 (2004).
11. Khokha, R., Murthy, A. & Weiss, A. Metalloproteinases and their natural inhibitors in inflammation and immunity. Nat. Rev. Immunol. 13, 649-665 (2013).
12. Cruz-Munoz, W. & Khokha, R. The role of tissue inhibitors of metalloproteinases in tumorigenesis and metastasis. Crit. Rev. Clin. Lab. Sci. 45, 291-338 (2008).
13. English, J. L. et al. Individual Timp deficiencies differentially impact pro-MMP-2 activation. J. Biol. Chem. 281, 10337-10346 (2006).
14. Casey, T. M. et al. Cancer associated fibroblasts stimulated by transforming growth factor beta1 (TGF-β 1) increase invasion rate of tumor cells: a population study. Breast Cancer Res. Treat. 110, 39-49 (2008).
15. Sato, H. et al. A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature 370, 61-65 (1994).
16. Pruessmeyer, J. et al. A disintegrin and metalloproteinase 17 (ADAM17) mediates inflammation-induced shedding of syndecan-1 and-4 by lung epithelial cells. J. Biol. Chem. 285, 555-564 (2010).
17. Murthy, A. et al. Ectodomain shedding of EGFR ligands and TNFR1 dictates hepatocyte apoptosis during fulminant hepatitis in mice. J. Clin. Invest. 120, 2731-2744 (2010).
18. Hundhausen, C. et al. The disintegrin-like metalloproteinase ADAM10 is involved in constitutive cleavage of CX3CL1 (fractalkine) and regulates CX3CL1-mediated cell-cell adhesion. Blood 102, 1186-1195 (2003).
19. Shannon, B. A., Cohen, R. J., Segal, A., Baker, E. G. & Murch, A. R. Clear cell renal cell carcinoma with smooth muscle stroma. Hum. Pathol. 40, 425-429 (2009).
20. Shimoda, M., Mellody, K. T. & Orimo, A. Carcinoma-associated fibroblasts are a rate-limiting determinant for tumour progression. Semin. Cell Dev. Biol. 21, 19-25 (2010).
21. Filipazzi, P., Burdek, M., Villa, A., Rivoltini, L. & Huber, V. Recent advances on the role of tumor exosomes in immunosuppression and disease progression. Semin. Cancer Biol. 22, 342-349 (2012).
22. Al-Nedawi, K. et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat. Cell Biol. 10, 619-624 (2008).
23. True, L. D. et al. CD90/THY1 is overexpressed in prostate cancer-associated fibroblasts and could serve as a cancer biomarker. Mod. Pathol. 23, 1346-1356 (2010).
24. Baker, A. M. et al. The role of lysyl oxidase in SRC-dependent proliferation and metastasis of colorectal cancer. J. Natl Cancer Inst. 103, 407-424 (2011).
25. Oskarsson, T. et al. Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat. Med. 17, 867-874 (2011).
26. Mochizuki, S. & Okada, Y. ADAMs in cancer cell proliferation and progression. Cancer Sci. 98, 621-628 (2007).
27. Stoeck, A. et al. A role for exosomes in the constitutive and stimulus-induced ectodomain cleavage of L1 and CD44. Biochem. J. 393, 609-618 (2006).
28. Gutwein, P. et al. Cleavage of L1 in exosomes and apoptotic membrane vesicles released from ovarian carcinoma cells. Clin. Cancer Res. 11, 2492-2501 (2005).
29. Blanpain, C., Horsley, V. & Fuchs, E. Epithelial stem cells: turning over new leaves. Cell 128, 445-458 (2007).
30. Groot, A. J. & Vooijs, M. A. The role of Adams in Notch signaling. Adv. Exp. Med. Biol. 727, 15-36 (2012).
31. Androutsellis-Theotokis, A. et al. Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 442, 823-826 (2006).
32. Sullivan, J. P. et al. Aldehyde dehydrogenase activity selects for lung adenocarcinoma stem cells dependent on notch signaling. Cancer Res. 70, 9937-9948 (2010).
33. Grudzien, P. et al. Inhibition of Notch signaling reduces the stem-like population of breast cancer cells and prevents mammosphere formation. Anticancer Res. 30, 3853-3867 (2010).
34. Marcato, P. et al. Aldehyde dehydrogenase activity of breast cancer stem cells is primarily due to isoform ALDH1A3 and its expression is predictive of metastasis. Stem Cells 29, 32-45 (2011).
35. Nobes, C. D. & Hall, A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81, 53-62 (1995).
36. Narumiya, S., Tanji, M. & Ishizaki, T. Rho signaling, ROCK and mDia1, in transformation, metastasis and invasion. Cancer Metastasis Rev. 28, 65-76 (2009).
37. Nagumo, H. et al. Rho kinase inhibitor HA-1077 prevents Rho-mediated myosin phosphatase inhibition in smooth muscle cells. Am. J. Physiol. Cell Physiol. 278, C57-65 (2000).
38. Finak, G. et al. Stromal gene expression predicts clinical outcome in breast cancer. Nat. Med. 14, 518-527 (2008).
39. Erez, N., Truitt, M., Olson, P., Arron, S. T. & Hanahan, D. Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-κB-dependent manner. Cancer cell 17, 135-147 (2010).
40. Kojima, Y. et al. Autocrine TGF-β and stromal cell-derived factor-1 (SDF-1) signaling drives the evolution of tumor-promoting mammary stromal myofibroblasts. Proc. Natl Acad. Sci. USA 107, 20009-20014 (2010).
41. Orimo, A. et al. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 121, 335-348 (2005).
42. Yang, C. & Robbins, P. D. The roles of tumor-derived exosomes in cancer pathogenesis. Clin. Dev. Immunol. 2011, 842849.
43. Malanchi, I. et al. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature 481, 85-89 (2012).
44. Meriane, M., Duhamel, S., Lejeune, L., Galipeau, J. & Annabi, B. Cooperation of matrix metalloproteinases with the RhoA/Rho kinase and mitogen-activated protein kinase kinase-1/extracellular signal-regulated kinase signaling pathways is required for the sphingosine-1-phosphate-induced mobilization of marrow-derived stromal cells. Stem Cells 24, 2557-2565 (2006).
45. Sugimoto, K. et al. LOX-1-MT1-MMP axis is crucial for RhoA and Rac1 activation induced by oxidized low-density lipoprotein in endothelial cells. Cardiovasc. Res. 84, 127-136 (2009).
46. Guiet, R. et al. The process of macrophage migration promotes matrix metalloproteinase-independent invasion by tumor cells. J. Immunol. 187, 3806-3814 (2011).
47. Giannoni, E. et al. EphA2-mediated mesenchymal-amoeboid transition induced by endothelial progenitor cells enhances metastatic spread due to cancer-associated fibroblasts. J. Mol. Med. 91, 103-115 (2013).
48. Koskivirta, I. et al. Mice with tissue inhibitor of metalloproteinases 4 (Timp4) deletion succumb to induced myocardial infarction but not to cardiac pressure overload. J. Biol. Chem. 285, 24487-24493 (2010).
49. Leco, K. J. et al. Spontaneous air space enlargement in the lungs of mice lacking tissue inhibitor of metalloproteinases-3 (TIMP-3). J. Clin. Invest. 108, 817-829 (2001).
50. Wang, Z., Juttermann, R. & Soloway, P. D. TIMP-2 is required for efficient activation of proMMP-2 in vivo. J. Biol. Chem. 275, 26411-26415 (2000).
51. Soloway, P. D., Alexander, C. M., Werb, Z. & Jaenisch, R. Targeted mutagenesis of Timp-1 reveals that lung tumor invasion is influenced by Timp-1 genotype of the tumor but not by that of the host. Oncogene 13, 2307-2314 (1996).
52. Ngo, P., Ramalingam, P., Phillips, J. A. & Furuta, G. T. Collagen gel contraction assay. Methods Mol. Biol. 341, 103-109 (2006).
53. Kelavkar, U. P., Hutzley, J., McHugh, K., Allen, K. G. & Parwani, A. Prostate tumor growth can be modulated by dietarily targeting the 15-lipoxygenase-1 and cyclooxygenase-2 enzymes. Neoplasia 11, 692-699 (2009).
54. Cruz-Munoz, W., Kim, I. & Khokha, R. TIMP-3 deficiency in the host, but not in the tumor, enhances tumor growth and angiogenesis. Oncogene 25, 650-655 (2006).
55. Thery, C., Amigorena, S., Raposo, G. & Clayton, A. Isolation and Characterization of Exosomes from Cell Culture Supernatants and Biological Fluids. Ch. 8, Unit 3.22 (Curr. Protec. Cell Biol., 2006).
56. Sokolova, V. et al. Characterisation of exosomes derived from human cells by nanoparticle tracking analysis and scanning electron microscopy. Colloids Surfaces B 87, 146-150 (2011).
57. Fitzner, D. et al. Selective transfer of exosomes from oligodendrocytes to microglia by macropinocytosis. J. Cell Sci. 124, 447-458 (2011).
58. Elschenbroich, S. et al. Peptide separations by on-line MudPIT compared to isoelectric focusing in an off-gel format: application to a membrane-enriched fraction from C2C12 mouse skeletal muscle cells. J. Proteome Res. 8, 4860-4869 (2009).
59. Sodek, K. L. et al. Identification of pathways associated with invasive behavior by ovarian cancer cells using multidimensional protein identification technology (MudPIT). Mol. Biosyst. 4, 762-773 (2008).
60. Cox, J. & Mann, M. MaxQuant enables high peptide identification rates, individualized ppb-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372 (2008).
61. Shaw, F. L. et al. A detailed mammosphere assay protocol for the quantification of breast stem cell activity. J. Mammary Gland Biol. Neoplasia 17, 111-117 (2012).
62. Singh, J. K. et al. Targeting CXCR1/2 significantly reduces breast cancer stem cell activity and increases the efficacy of inhibiting HER2 via HER2-dependent and-independent mechanisms. Clin. Cancer Res. 19, 643-656 (2013).
63. Scholz, F. et al. Constitutive expression and regulated release of the transmembrane chemokine CXCL16 in human and murine skin. J. Invest. Dermatol. 127, 1444-1455 (2007).
64. Prince, M. E. et al. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc. Natl Acad. Sci. USA 104, 973-978 (2007).