nature.com

The metastatic niche: adapting the foreign soil - Nature Reviews Cancer

  • ️Lyden, David
  • ️Wed Apr 01 2009
  • Paget, S. The distribution of secondary growths in cancer of the breast. Lancet 1, 571–573 (1889).

    Google Scholar 

  • Paget, S. The distribution of secondary growths in cancer of the breast. 1889. Cancer Metastasis Rev. 8, 98–101 (1989).

    CAS  PubMed  Google Scholar 

  • Virchow, R. Cellularpathologie 1st edn (ed. Hirschwalkd, A.) (Berlin, 1858).

    Google Scholar 

  • Ewing, J. Neoplastic diseases 6th edn (ed. Saunders, W.) (W. B. Saunders Co., Philadelphia, 1928).

    Google Scholar 

  • Fidler, I. J. & Kripke, M. L. Metastasis results from preexisting variant cells within a malignant tumor. Science 197, 893–895 (1977).

    CAS  PubMed  Google Scholar 

  • Hart, I. R. & Fidler, I. J. Role of organ selectivity in the determination of metastatic patterns of B16 melanoma. Cancer Res. 40, 2281–2287 (1980).

    CAS  PubMed  Google Scholar 

  • Li, L. & Neaves, W. B. Normal stem cells and cancer stem cells: the niche matters. Cancer Res. 66, 4553–4557 (2006).

    CAS  PubMed  Google Scholar 

  • Yin, T. & Li, L. The stem cell niches in bone. J. Clin. Invest. 116, 1195–1201 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, J. & Li, L. Stem cell niche: microenvironment and beyond. J. Biol. Chem. 283, 9499–9503 (2008).

    CAS  PubMed  Google Scholar 

  • Scadden, D. T. The stem-cell niche as an entity of action. Nature 441, 1075–1079 (2006).

    CAS  PubMed  Google Scholar 

  • Sneddon, J. B. & Werb, Z. Location, location, location: the cancer stem cell niche. Cell Stem Cell 1, 607–611 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Psaila, B., Kaplan, R. N., Port, E. R. & Lyden, D. Priming the 'soil' for breast cancer metastasis: the pre-metastatic niche. Breast Dis. 26, 65–74 (2006).

    CAS  PubMed  Google Scholar 

  • Folkman, J. Role of angiogenesis in tumor growth and metastasis. Semin. Oncol. 29, 15–18 (2002).

    CAS  PubMed  Google Scholar 

  • Weigelt, B. & Bissell, M. J. Unraveling the microenvironmental influences on the normal mammary gland and breast cancer. Semin. Cancer Biol. 18, 311–321 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Joyce, J. A. & Hanahan, D. Multiple roles for cysteine cathepsins in cancer. Cell Cycle 3, 1516–1619 (2004).

    CAS  PubMed  Google Scholar 

  • Mantovani, A., Allavena, P., Sica, A. & Balkwill, F. Cancer-related inflammation. Nature 454, 436–444 (2008).

    CAS  PubMed  Google Scholar 

  • Chambers, A. F., Groom, A. C. & MacDonald, I. C. Dissemination and growth of cancer cells in metastatic sites. Nature Rev. Cancer 2, 563–572 (2002).

    CAS  Google Scholar 

  • Weiss, L. & Ward, P. M. Arrest and retention of circulating cancer cells in the lungs of animals with defined metastatic status. Cancer Res. 42, 1898–1903 (1982).

    CAS  PubMed  Google Scholar 

  • Kaplan, R. N. et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 438, 820–827 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Weiss, L., Mayhew, E., Rapp, D. G. & Holmes, J. C. Metastatic inefficiency in mice bearing B16 melanomas. Br. J. Cancer 45, 44–53 (1982).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hiratsuka, S., Watanabe, A., Aburatani, H. & Maru, Y. Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nature Cell Biol. 8, 1369–1375 (2006).

    CAS  PubMed  Google Scholar 

  • Hiratsuka, S. et al. The S100A8–serum amyloid A3–TLR4 paracrine cascade establishes a pre-metastatic phase. Nature Cell Biol. 10, 1349–1355 (2008).

    CAS  PubMed  Google Scholar 

  • Wels, J., Kaplan, R. N., Rafii, S. & Lyden, D. Migratory neighbors and distant invaders: tumor-associated niche cells. Genes Dev. 22, 559–574 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peinado, H., Rafii, S. & Lyden, D. Inflammation joins the “niche”. Cancer Cell 14, 347–349 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lyden, D. et al. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nature Med. 7, 1194–1201 (2001).

    CAS  PubMed  Google Scholar 

  • Karnoub, A. E. et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 449, 557–563 (2007).

    CAS  PubMed  Google Scholar 

  • Nilsson, S. K., Johnston, H. M. & Coverdale, J. A. Spatial localization of transplanted hemopoietic stem cells: inferences for the localization of stem cell niches. Blood 97, 2293–2299 (2001).

    CAS  PubMed  Google Scholar 

  • Calvi, L. M. et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425, 841–846 (2003).

    CAS  PubMed  Google Scholar 

  • Kiel, M. J., Yilmaz, O. H., Iwashita, T., Terhorst, C. & Morrison, S. J. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121, 1109–1121 (2005).

    CAS  PubMed  Google Scholar 

  • Kiel, M. J. & Morrison, S. J. Uncertainty in the niches that maintain haematopoietic stem cells. Nature Rev. Immunol. 8, 290–301 (2008).

    CAS  Google Scholar 

  • Kaplan, R. N., Psaila, B. & Lyden, D. Niche-to-niche migration of bone-marrow-derived cells. Trends Mol. Med. 13, 72–81 (2007).

    CAS  PubMed  Google Scholar 

  • Alix-Panabieres, C., Riethdorf, S. & Pantel, K. Circulating tumor cells and bone marrow micrometastasis. Clin. Cancer Res. 14, 5013–5021 (2008).

    CAS  PubMed  Google Scholar 

  • Jones, D. H. et al. Regulation of cancer cell migration and bone metastasis by RANKL. Nature 440, 692–696 (2006).

    CAS  PubMed  Google Scholar 

  • Mantovani, A. Cancer: Inflaming metastasis. Nature 457, 36–37 (2009).

    CAS  PubMed  Google Scholar 

  • Giavazzi, R. et al. Interleukin 1-induced augmentation of experimental metastases from a human melanoma in nude mice. Cancer Res. 50, 4771–4775 (1990).

    CAS  PubMed  Google Scholar 

  • Kim, S. et al. Carcinoma produced factors activate myeloid cells via TLR2 to stimulate metastasis. Nature 457, 102–106 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hiratsuka, S. et al. MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Cancer Cell 2, 289–300 (2002).

    CAS  PubMed  Google Scholar 

  • Page-McCaw, A., Ewald, A. J. & Werb, Z. Matrix metalloproteinases and the regulation of tissue remodelling. Nature Rev. Mol. Cell Biol. 8, 221–233 (2007).

    CAS  Google Scholar 

  • Lopez-Otin, C. & Matrisian, L. M. Emerging roles of proteases in tumour suppression. Nature Rev. Cancer 7, 800–808 (2007).

    CAS  Google Scholar 

  • Yang, L. & Moses, H. L. Transforming growth factor b: tumor suppressor or promoter? Are host immune cells the answer? Cancer Res. 68, 9107–9111 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wai, P. Y. & Kuo, P. C. Osteopontin: regulation in tumor metastasis. Cancer Metastasis Rev. 27, 103–118 (2008).

    CAS  PubMed  Google Scholar 

  • Bellahcene, A., Castronovo, V., Ogbureke, K. U., Fisher, L. W. & Fedarko, N. S. Small integrin-binding ligand N-linked glycoproteins (SIBLINGs): multifunctional proteins in cancer. Nature Rev. Cancer 8, 212–226 (2008).

    CAS  Google Scholar 

  • Pollard, J. W. Tumour-educated macrophages promote tumour progression and metastasis. Nature Rev. Cancer 4, 71–78 (2004).

    CAS  Google Scholar 

  • Yang, L. et al. Abrogation of TGFb signaling in mammary carcinomas recruits Gr-1+CD11b+ myeloid cells that promote metastasis. Cancer Cell 13, 23–35 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lin, E. Y. & Pollard, J. W. Tumor-associated macrophages press the angiogenic switch in breast cancer. Cancer Res. 67, 5064–5066 (2007).

    CAS  PubMed  Google Scholar 

  • Jin, D. K. et al. Cytokine-mediated deployment of SDF-1 induces revascularization through recruitment of CXCR4+ hemangiocytes. Nature Med. 12, 557–567 (2006).

    CAS  PubMed  Google Scholar 

  • Italiano, J. E. Jr et al. Angiogenesis is regulated by a novel mechanism: pro- and antiangiogenic proteins are organized into separate platelet alpha granules and differentially released. Blood 111, 1227–1233 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rafii, D. C., Psaila, B., Butler, J., Jin, D. K. & Lyden, D. Regulation of vasculogenesis by platelet-mediated recruitment of bone marrow-derived cells. Arterioscler. Thromb. Vasc. Biol. 28, 217–222 (2008).

    CAS  PubMed  Google Scholar 

  • Jain, S. et al. Platelet glycoprotein Iba supports experimental lung metastasis. Proc. Natl Acad. Sci. USA 104, 9024–9028 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kucia, M. et al. Trafficking of normal stem cells and metastasis of cancer stem cells involve similar mechanisms: pivotal role of the SDF-1–CXCR4 axis. Stem Cells 23, 879–894 (2005).

    CAS  PubMed  Google Scholar 

  • 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).

    CAS  PubMed  Google Scholar 

  • Kalluri, R. & Zeisberg, M. Fibroblasts in cancer. Nature Rev. Cancer 6, 392–401 (2006).

    CAS  Google Scholar 

  • Erler, J. T. et al. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow-derived cell recruitment to form the pre-metastatic niche. Cancer Cell 15, 35–44 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  • van Deventer, H. W. et al. C-C chemokine receptor 5 on pulmonary fibrocytes facilitates migration and promotes metastasis via matrix metalloproteinase 9. Am. J. Pathol. 173, 253–264 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Erler, J. T. et al. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 15, 35–44 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng, J. D. & Weiner, L. M. Tumors and their microenvironments: tilling the soil. Commentary re: A. M. Scott. et al. A Phase I dose-escalation study of sibrotuzumab in patients with advanced or metastatic fibroblast activation protein-positive cancer. Clin. Cancer Res. 9, 1590–1595 (2003).

    CAS  PubMed  Google Scholar 

  • Olaso, E. et al. Tumor-dependent activation of rodent hepatic stellate cells during experimental melanoma metastasis. Hepatology 26, 634–642 (1997).

    CAS  PubMed  Google Scholar 

  • Olaso, E. et al. Proangiogenic role of tumor-activated hepatic stellate cells in experimental melanoma metastasis. Hepatology 37, 674–685 (2003).

    CAS  PubMed  Google Scholar 

  • Zeisberg, E. M., Potenta, S. E., Sugimoto, H., Zeisberg, M. & Kalluri, R. Fibroblasts in kidney fibrosis emerge via endothelial-to-mesenchymal transition. J. Am. Soc. Nephrol 19, 2282–2287 (2008).

    PubMed  PubMed Central  Google Scholar 

  • Ghajar, C. M. & Bissell, M. J. Extracellular matrix control of mammary gland morphogenesis and tumorigenesis: insights from imaging. Histochem. Cell Biol. 130, 1105–1118 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Du, R. et al. HIF1α induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 13, 206–220 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Denko, N. C. et al. Investigating hypoxic tumor physiology through gene expression patterns. Oncogene 22, 5907–5914 (2003).

    CAS  PubMed  Google Scholar 

  • Erler, J. T. et al. Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 440, 1222–1226 (2006).

    CAS  PubMed  Google Scholar 

  • Astrof, S. et al. Direct test of potential roles of EIIIA and EIIIB alternatively spliced segments of fibronectin in physiological and tumor angiogenesis. Mol. Cell. Biol. 24, 8662–8670 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Alcaraz, J. et al. Laminin and biomimetic extracellular elasticity enhance functional differentiation in mammary epithelia. EMBO J. 27, 2829–2838 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  • McDonbald, D. M. & Baluk, P. Significance of blood vessel leakiness in cancer. Cancer Res, 62, 5381–5385 (2002).

    Google Scholar 

  • Dvorak, H. F., Nagy, J. A., Dvorak, J. T. & Dvorak, A. M. Identification and characterization of the blood vessels of solid tumors that are leaky to circulating macromolecules. Am. J. Pathol. 133, 95–109 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Padua, D. et al. TGFβ primes breast tumors for lung metastasis seeding through angiopoietin-like 4. Cell 133, 66–77 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ribatti, D., Nico, B., Vacca, A., Roncali, L. & Dammacco, F. Endothelial cell heterogeneity and organ specificity. J. Hematother. Stem Cell Res. 11, 81–90 (2002).

    PubMed  Google Scholar 

  • LeCouter, J. et al. Identification of an angiogenic mitogen selective for endocrine gland endothelium. Nature 412, 877–884 (2001).

    CAS  PubMed  Google Scholar 

  • LeCouter, J., Lin, R. & Ferrara, N. Endocrine gland-derived VEGF and the emerging hypothesis of organ-specific regulation of angiogenesis. Nature Med. 8, 913–917 (2002).

    CAS  PubMed  Google Scholar 

  • Minn, A. J. et al. Genes that mediate breast cancer metastasis to lung. Nature 436, 518–524 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ding, L. et al. In vivo evaluation of the early events associated with liver metastasis of circulating cancer cells. Br. J. Cancer 85, 431–438 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Biancone, L., Araki, M., Araki, K., Vassalli, P. & Stamenkovic, I. Redirection of tumor metastasis by expression of E-selectin in vivo. J. Exp. Med. 183, 581–587 (1996).

    CAS  PubMed  Google Scholar 

  • Hirakawa, S. et al. VEGF-C-induced lymphangiogenesis in sentinel lymph nodes promotes tumor metastasis to distant sites. Blood 109, 1010–1017 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hirakawa, S. et al. VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis. J. Exp. Med. 201, 1089–1099 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rinderknecht, M. & Detmar, M. Tumor lymphangiogenesis and melanoma metastasis. J. Cell Physiol. 216, 347–354 (2008).

    CAS  PubMed  Google Scholar 

  • Podsypanina, K. et al. Seeding and propagation of untransformed mouse mammary cells in the lung. Science 321, 1841–1844 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chin, L. The genetics of malignant melanoma: lessons from mouse and man. Nature Rev. Cancer 3, 559–570 (2003).

    CAS  Google Scholar 

  • Bidard, F. C., Pierga, J. Y., Vincent-Salomon, A. & Poupon, M. F. A “class action” against the microenvironment: do cancer cells cooperate in metastasis? Cancer Metastasis Rev. 27, 5–10 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Weiss, L. Metastatic inefficiency. Adv. Cancer Res. 54, 159–211 (1990).

    CAS  PubMed  Google Scholar 

  • Weiss, L. Cancer cell traffic from the lungs to the liver: an example of metastatic inefficiency. Int. J. Cancer 25, 385–392 (1980).

    CAS  PubMed  Google Scholar 

  • Langley, R. R. & Fidler, I. J. Tumor cell-organ microenvironment interactions in the pathogenesis of cancer metastasis. Endocr. Rev. 28, 297–321 (2007).

    CAS  PubMed  Google Scholar 

  • Minn., A. J. et al. Distinct organ-specific metastatic potential of individual breast cancer cells and primary tumors. J. Clin. Invest. 115, 44–55 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Minn., A. J. et al. Lung metastasis genes couple breast tumor size and metastatic spread. Proc. Natl Acad. Sci. USA 104, 6740–6745 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lyden, D. et al. Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 401, 670–677 (1999).

    CAS  PubMed  Google Scholar 

  • Gupta, G. P. et al. ID genes mediate tumor reinitiation during breast cancer lung metastasis. Proc. Natl Acad. Sci. USA 104, 19506–19511 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Steeg, P. S. Metastasis suppressors alter the signal transduction of cancer cells. Nature Rev. Cancer 3, 55–63 (2003).

    CAS  Google Scholar 

  • Vaida, K. S. et al. Breast cancer metastasis suppressor-1 differentially modulates growth factor signaling. J. Biol. Chem 283, 28354–28360 (2008).

    Google Scholar 

  • Lapidot, T. et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367, 645–648 (1994).

    CAS  PubMed  Google Scholar 

  • Al-Hajj, M., Wicha, M. S., Benito-Hernandez, A., Morrison, S. J. & Clarke, M. F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl Acad. Sci. USA 100, 3983–3988 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mani, S. A. et al. The epithelial–mesenchymal transition generates cells with properties of stem cells. Cell 133, 704–715 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Larizza, L. et al. Suggestive evidence that the highly metastatic variant ESb of the T-cell lymphoma Eb is derived from spontaneous fusion with a host macrophage. Int. J. Cancer 34, 699–707 (1984).

    CAS  PubMed  Google Scholar 

  • Pawelek, J. M. & Chakraborty, A. K. The cancer cell–leukocyte fusion theory of metastasis. Adv. Cancer Res. 101, 397–444 (2008).

    CAS  PubMed  Google Scholar 

  • Pawelek, J. M. & Chakraborty, A. K. Fusion of tumour cells with bone marrow-derived cells: a unifying explanation for metastasis. Nature Rev. Cancer 8, 377–386 (2008).

    CAS  Google Scholar 

  • Mehlen, P. & Puisieux, A. Metastasis: a question of life or death. Nature Rev. Cancer 6, 449–458 (2006).

    CAS  Google Scholar 

  • Yu, Q., Toole, B. P. & Stamenkovic, I. Induction of apoptosis of metastatic mammary carcinoma cells in vivo by disruption of tumor cell surface CD44 function. J. Exp. Med. 186, 1985–1996 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Holmgren, L., O'Reilly, M. S. & Folkman, J. Dormancy of micrometastases: balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nature Med. 1, 149–153 (1995).

    CAS  PubMed  Google Scholar 

  • Naumov, G. N., Akslen, L. A. & Folkman, J. Role of angiogenesis in human tumor dormancy: animal models of the angiogenic switch. Cell Cycle 5, 1779–1787 (2006).

    CAS  PubMed  Google Scholar 

  • Gao, D. et al. Endothelial progenitor cells control the angiogenic switch in mouse lung metastasis. Science 319, 195–198 (2008).

    CAS  PubMed  Google Scholar 

  • Yamamoto, M. et al. TSU68 prevents liver metastasis of colon cancer xenografts by modulating the premetastatic niche. Cancer Res. 68, 9754–9762 (2008).

    CAS  PubMed  Google Scholar 

  • Wang, J. & Armant, D. R. Integrin-mediated adhesion and signaling during blastocyst implantation. Cells Tissues Organs 172, 190–201 (2002).

    CAS  PubMed  Google Scholar 

  • Wang, J., Mayernik, L. & Armant, D. R. Integrin signaling regulates blastocyst adhesion to fibronectin at implantation: intracellular calcium transients and vesicle trafficking in primary trophoblast cells. Dev. Biol. 245, 270–279 (2002).

    CAS  PubMed  Google Scholar 

  • Hess, R. A., Cooke, P. S., Hofmann, M. C. & Murphy, K. M. Mechanistic insights into the regulation of the spermatogonial stem cell niche. Cell Cycle 5, 1164–1170 (2006).

    CAS  PubMed  Google Scholar 

  • Taupin, P. Adult neural stem cells, neurogenic niches, and cellular therapy. Stem Cell Rev. 2, 213–219 (2006).

    PubMed  Google Scholar 

  • Steinman, L. Nuanced roles of cytokines in three major human brain disorders. J. Clin. Invest. 118, 3557–3563 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Libby, P. Role of inflammation in atherosclerosis associated with rheumatoid arthritis. Am. J. Med. 121, S21–S31 (2008).

    CAS  PubMed  Google Scholar 

  • Weber, C., Zernecke, A. & Libby, P. The multifaceted contributions of leukocyte subsets to atherosclerosis: lessons from mouse models. Nature Rev. Immunol. 8, 802–815 (2008).

    CAS  Google Scholar 

  • Szekanecz, Z. & Koch, A. E. Mechanisms of disease: angiogenesis in inflammatory diseases. Nature Clin. Pract. Rheumatol. 3, 635–643 (2007).

    CAS  Google Scholar