1932

Abstract

Metastases are responsible for the vast majority of cancer-related deaths, but, despite intense efforts to understand their underlying mechanisms with the goal of uncovering effective therapeutic targets, treatment of metastatic cancer has progressed minimally. In this review, we examine the biological programs currently proposed to be key drivers of metastasis. On the basis of evidence from a growing body of research, we discuss to what extent the cellular and molecular mechanisms that are suggested to underlie cancer cell dissemination are specific to the metastatic process, as opposed to representing natural primary tumor progression. Our review highlights the contrast between the abundance of insight gained into the events that constitute the metastatic cascade and the paucity of therapeutic options.

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2018-01-24
2024-03-29
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Literature Cited

  1. Fidler IJ. 1.  2003. The pathogenesis of cancer metastasis: the ‘seed and soil’ hypothesis revisited. Nat. Rev. Cancer 3:6453–58 [Google Scholar]
  2. Oskarsson T, Batlle E, Massague J. 2.  2014. Metastatic stem cells: sources, niches, and vital pathways. Cell Stem Cell 14:3306–21 [Google Scholar]
  3. Lambert AW, Pattabiraman DR, Weinberg RA. 3.  2017. Emerging biological principles of metastasis. Cell 168:4670–91 [Google Scholar]
  4. Nowell PC. 4.  1976. The clonal evolution of tumor cell populations. Science 194:426023–28 [Google Scholar]
  5. Cairns J. 5.  1975. Mutation selection and the natural history of cancer. Nature 255:5505197–200 [Google Scholar]
  6. Talmadge JE. 6.  2007. Clonal selection of metastasis within the life history of a tumor. Cancer Res 67:2411471–75 [Google Scholar]
  7. Gupta GP, Massague J. 7.  2006. Cancer metastasis: building a framework. Cell 127:4679–95 [Google Scholar]
  8. Talmadge JE, Fidler IJ. 8.  2010. AACR centennial series: the biology of cancer metastasis: historical perspective. Cancer Res 70:145649–69 [Google Scholar]
  9. Fidler IJ. 9.  1973. Selection of successive tumour lines for metastasis. Nat. New Biol. 242:118148–49 [Google Scholar]
  10. Talmadge JE, Wolman SR, Fidler IJ. 10.  1982. Evidence for the clonal origin of spontaneous metastases. Science 217:4557361–63 [Google Scholar]
  11. Kozlowski JM, Hart IR, Fidler IJ, Hanna N. 11.  1984. A human melanoma line heterogeneous with respect to metastatic capacity in athymic nude mice. J. Natl. Cancer Inst. 72:4913–17 [Google Scholar]
  12. Clark EA, Golub TR, Lander ES, Hynes RO. 12.  2000. Genomic analysis of metastasis reveals an essential role for RhoC. Nature 406:6795532–35 [Google Scholar]
  13. Ramaswamy S, Ross KN, Lander ES, Golub TR. 13.  2003. A molecular signature of metastasis in primary solid tumors. Nat. Genet. 33:149–54 [Google Scholar]
  14. van 't Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AA. 14.  et al. 2003. Expression profiling predicts outcome in breast cancer. Breast Cancer Res 5:157–58 [Google Scholar]
  15. van 't Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AA. 15.  et al. 2002. Gene expression profiling predicts clinical outcome of breast cancer. Nature 415:6871530–36 [Google Scholar]
  16. Chang HY, Sneddon JB, Alizadeh AA, Sood R, West RB. 16.  et al. 2004. Gene expression signature of fibroblast serum response predicts human cancer progression: similarities between tumors and wounds. PLOS Biol 2:2E7 [Google Scholar]
  17. Huang E, Cheng SH, Dressman H, Pittman J, Tsou MH. 17.  et al. 2003. Gene expression predictors of breast cancer outcomes. Lancet 361:93691590–96 [Google Scholar]
  18. Wang Y, Klijn JG, Zhang Y, Sieuwerts AM, Look MP. 18.  et al. 2005. Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet 365:9460671–79 [Google Scholar]
  19. Fan C, Oh DS, Wessels L, Weigelt B, Nuyten DS. 19.  et al. 2006. Concordance among gene-expression-based predictors for breast cancer. N. Engl. J. Med. 355:6560–69 [Google Scholar]
  20. Bernards R, Weinberg RA. 20.  2002. A progression puzzle. Nature 418:6900823 [Google Scholar]
  21. Kang Y, Siegel PM, Shu W, Drobnjak M, Kakonen SM. 21.  et al. 2003. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3:6537–49 [Google Scholar]
  22. Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W. 22.  et al. 2005. Genes that mediate breast cancer metastasis to lung. Nature 436:7050518–24 [Google Scholar]
  23. Hynes RO. 23.  2002. Integrins: bidirectional, allosteric signaling machines. Cell 110:6673–87 [Google Scholar]
  24. Mitra SK, Hanson DA, Schlaepfer DD. 24.  2005. Focal adhesion kinase: in command and control of cell motility. Nat. Rev. Mol. Cell Biol. 6:156–68 [Google Scholar]
  25. Schlaepfer DD, Mitra SK. 25.  2004. Multiple connections link FAK to cell motility and invasion. Curr. Opin. Genet. Dev. 14:192–101 [Google Scholar]
  26. Sulzmaier FJ, Jean C, Schlaepfer DD. 26.  2014. FAK in cancer: mechanistic findings and clinical applications. Nat. Rev. Cancer 14:9598–610 [Google Scholar]
  27. Sahai E, Marshall CJ. 27.  2002. RHO-GTPases and cancer. Nat. Rev. Cancer 2:2133–42 [Google Scholar]
  28. Mayor R, Etienne-Manneville S. 28.  2016. The front and rear of collective cell migration. Nat. Rev. Mol. Cell Biol. 17:297–109 [Google Scholar]
  29. Stamenkovic I. 29.  2003. Extracellular matrix remodelling: the role of matrix metalloproteinases. J. Pathol. 200:4448–64 [Google Scholar]
  30. Egeblad M, Werb Z. 30.  2002. New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2:3161–74 [Google Scholar]
  31. Affara NI, Andreu P, Coussens LM. 31.  2009. Delineating protease functions during cancer development. Methods Mol. Biol. 539:1–32 [Google Scholar]
  32. Podsypanina K, Du YC, Jechlinger M, Beverly LJ, Hambardzumyan D, Varmus H. 32.  2008. Seeding and propagation of untransformed mouse mammary cells in the lung. Science 321:58971841–44 [Google Scholar]
  33. Naxerova K, Jain RK. 33.  2015. Using tumour phylogenetics to identify the roots of metastasis in humans. Nat. Rev. Clin. Oncol. 12:5258–72 [Google Scholar]
  34. Garraway LA, Lander ES. 34.  2013. Lessons from the cancer genome. Cell 153:117–37 [Google Scholar]
  35. Vogelstein B, Papadopoulos N, Velculescu VE, Zhou S, Diaz LA Jr., Kinzler KW. 35.  2013. Cancer genome landscapes. Science 339:61271546–58 [Google Scholar]
  36. Yachida S, Jones S, Bozic I, Antal T, Leary R. 36.  et al. 2010. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature 467:73191114–17 [Google Scholar]
  37. Bozic I, Antal T, Ohtsuki H, Carter H, Kim D. 37.  et al. 2010. Accumulation of driver and passenger mutations during tumor progression. PNAS 107:4318545–50 [Google Scholar]
  38. Magee JA, Piskounova E, Morrison SJ. 38.  2012. Cancer stem cells: impact, heterogeneity, and uncertainty. Cancer Cell 21:3283–96 [Google Scholar]
  39. Kreso A, Dick JE. 39.  2014. Evolution of the cancer stem cell model. Cell Stem Cell 14:3275–91 [Google Scholar]
  40. Visvader JE, Lindeman GJ. 40.  2012. Cancer stem cells: current status and evolving complexities. Cell Stem Cell 10:6717–28 [Google Scholar]
  41. Celià-Terrassa T, Kang Y. 41.  2016. Distinctive properties of metastasis-initiating cells. Genes Dev 30:8892–908 [Google Scholar]
  42. Quintana E, Shackleton M, Foster HR, Fullen DR, Sabel MS. 42.  et al. 2010. Phenotypic heterogeneity among tumorigenic melanoma cells from patients that is reversible and not hierarchically organized. Cancer Cell 18:5510–23 [Google Scholar]
  43. Quintana E, Shackleton M, Sabel MS, Fullen DR, Johnson TM, Morrison SJ. 43.  2008. Efficient tumour formation by single human melanoma cells. Nature 456:7222593–98 [Google Scholar]
  44. Meacham CE, Morrison SJ. 44.  2013. Tumour heterogeneity and cancer cell plasticity. Nature 501:7467328–37 [Google Scholar]
  45. Tlsty TD, Coussens LM. 45.  2006. Tumor stroma and regulation of cancer development. Annu. Rev. Pathol. 1:119–50 [Google Scholar]
  46. Nieto MA, Huang RY, Jackson RA, Thiery JP. 46.  2016. EMT: 2016. Cell 166:121–45 [Google Scholar]
  47. Lamouille S, Xu J, Derynck R. 47.  2014. Molecular mechanisms of epithelial-mesenchymal transition. Nat. Rev. Mol. Cell Biol. 15:3178–96 [Google Scholar]
  48. Jordan NV, Johnson GL, Abell AN. 48.  2011. Tracking the intermediate stages of epithelial-mesenchymal transition in epithelial stem cells and cancer. Cell Cycle 10:172865–73 [Google Scholar]
  49. Huang RY, Wong MK, Tan TZ, Kuay KT, Ng AH. 49.  et al. 2013. An EMT spectrum defines an anoikis-resistant and spheroidogenic intermediate mesenchymal state that is sensitive to e-cadherin restoration by a src-kinase inhibitor, saracatinib (AZD0530). Cell Death Dis 4:e915 [Google Scholar]
  50. Grigore AD, Jolly MK, Jia D, Farach-Carson MC, Levine H. 50.  2016. Tumor budding: The name is EMT. Partial EMT. J. Clin. Med. 5:551 [Google Scholar]
  51. Lovisa S, LeBleu VS, Tampe B, Sugimoto H, Vadnagara K. 51.  et al. 2015. Epithelial-to-mesenchymal transition induces cell cycle arrest and parenchymal damage in renal fibrosis. Nat. Med. 21:9998–1009 [Google Scholar]
  52. Thiery JP, Acloque H, Huang RY, Nieto MA. 52.  2009. Epithelial-mesenchymal transitions in development and disease. Cell 139:5871–90 [Google Scholar]
  53. Peinado H, Olmeda D, Cano A. 53.  2007. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype?. Nat. Rev. Cancer 7:6415–28 [Google Scholar]
  54. Lamouille S, Subramanyam D, Blelloch R, Derynck R. 54.  2013. Regulation of epithelial-mesenchymal and mesenchymal-epithelial transitions by microRNAs. Curr. Opin. Cell Biol. 25:2200–7 [Google Scholar]
  55. Diaz-Lopez A, Moreno-Bueno G, Cano A. 55.  2014. Role of microRNA in epithelial to mesenchymal transition and metastasis and clinical perspectives. Cancer Manag. Res. 6:205–16 [Google Scholar]
  56. Friedl P, Locker J, Sahai E, Segall JE. 56.  2012. Classifying collective cancer cell invasion. Nat. Cell Biol. 14:8777–83 [Google Scholar]
  57. Veracini L, Grall D, Schaub S, Beghelli-de la Forest Divonne S, Etienne-Grimaldi MC. 57.  et al. 2015. Elevated Src family kinase activity stabilizes E-cadherin-based junctions and collective movement of head and neck squamous cell carcinomas. Oncotarget 6:107570–83 [Google Scholar]
  58. Chung YC, Wei WC, Hung CN, Kuo JF, Hsu CP. 58.  et al. 2016. Rab11 collaborates E-cadherin to promote collective cell migration and indicates a poor prognosis in colorectal carcinoma. Eur. J. Clin. Investig. 46:121002–11 [Google Scholar]
  59. Gaggioli C, Hooper S, Hidalgo-Carcedo C, Grosse R, Marshall JF. 59.  et al. 2007. Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat. Cell Biol. 9:121392–400 [Google Scholar]
  60. Revenu C, Gilmour D. 60.  2009. EMT 2.0: shaping epithelia through collective migration. Curr. Opin. Genet. Dev. 19:4338–42 [Google Scholar]
  61. Westcott JM, Prechtl AM, Maine EA, Dang TT, Esparza MA. 61.  et al. 2015. An epigenetically distinct breast cancer cell subpopulation promotes collective invasion. J. Clin. Investig. 125:51927–43 [Google Scholar]
  62. Yu M, Bardia A, Wittner BS, Stott SL, Smas ME. 62.  et al. 2013. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science 339:6119580–84 [Google Scholar]
  63. Khoo BL, Lee SC, Kumar P, Tan TZ, Warkiani ME. 63.  et al. 2015. Short-term expansion of breast circulating cancer cells predicts response to anti-cancer therapy. Oncotarget 6:1715578–93 [Google Scholar]
  64. Ocana OH, Corcoles R, Fabra A, Moreno-Bueno G, Acloque H. 64.  et al. 2012. Metastatic colonization requires the repression of the epithelial-mesenchymal transition inducer Prrx1. Cancer Cell 22:6709–24 [Google Scholar]
  65. Tsai JH, Donaher JL, Murphy DA, Chau S, Yang J. 65.  2012. Spatiotemporal regulation of epithelial-mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer Cell 22:6725–36 [Google Scholar]
  66. Del Pozo Martin Y, Park D, Ramachandran A, Ombrato L, Calvo F. 66.  et al. 2015. Mesenchymal cancer cell-stroma crosstalk promotes niche activation, epithelial reversion, and metastatic colonization. Cell Rep 13:112456–69 [Google Scholar]
  67. Fischer KR, Durrans A, Lee S, Sheng J, Li F. 67.  et al. 2015. Epithelial-to-mesenchymal transition is not required for lung metastasis but contributes to chemoresistance. Nature 527:7579472–76 [Google Scholar]
  68. Zheng X, Carstens JL, Kim J, Scheible M, Kaye J. 68.  et al. 2015. Epithelial-to-mesenchymal transition is dispensable for metastasis but induces chemoresistance in pancreatic cancer. Nature 527:7579525–30 [Google Scholar]
  69. Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. 69.  2005. Opinion: migrating cancer stem cells—an integrated concept of malignant tumour progression. Nat. Rev. Cancer 5:9744–49 [Google Scholar]
  70. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A. 70.  et al. 2008. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133:4704–15 [Google Scholar]
  71. Wellner U, Schubert J, Burk UC, Schmalhofer O, Zhu F. 71.  et al. 2009. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat. Cell Biol. 11:121487–95 [Google Scholar]
  72. Hwang WL, Jiang JK, Yang SH, Huang TS, Lan HY. 72.  et al. 2014. MicroRNA-146a directs the symmetric division of Snail-dominant colorectal cancer stem cells. Nat. Cell Biol. 16:3268–80 [Google Scholar]
  73. Yu M, Smolen GA, Zhang J, Wittner B, Schott BJ. 73.  et al. 2009. A developmentally regulated inducer of EMT, LBX1, contributes to breast cancer progression. Genes Dev 23:151737–42 [Google Scholar]
  74. Nieto MA. 74.  2013. Epithelial plasticity: a common theme in embryonic and cancer cells. Science 342:61591234850 [Google Scholar]
  75. Chang CC, Hsu WH, Wang CC, Chou CH, Kuo MY. 75.  et al. 2013. Connective tissue growth factor activates pluripotency genes and mesenchymal-epithelial transition in head and neck cancer cells. Cancer Res 73:134147–57 [Google Scholar]
  76. Stankic M, Pavlovic S, Chin Y, Brogi E, Padua D. 76.  et al. 2013. TGF-β-Id1 signaling opposes Twist1 and promotes metastatic colonization via a mesenchymal-to-epithelial transition. Cell Rep 5:51228–42 [Google Scholar]
  77. Voon DC, Wang H, Koo JK, Chai JH, Hor YT. 77.  et al. 2013. EMT-induced stemness and tumorigenicity are fueled by the EGFR/Ras pathway. PLOS ONE 8:8e70427 [Google Scholar]
  78. Drasin DJ, Guarnieri AL, Neelakantan D, Kim J, Cabrera JH. 78.  et al. 2015. TWIST1-induced miR-424 reversibly drives mesenchymal programming while inhibiting tumor initiation. Cancer Res 75:91908–21 [Google Scholar]
  79. Celià-Terrassa T, Meca-Cortes O, Mateo F, Martinez de Paz A, Rubio N. 79.  et al. 2012. Epithelial-mesenchymal transition can suppress major attributes of human epithelial tumor-initiating cells. J. Clin. Investig. 122:51849–68 [Google Scholar]
  80. Beck B, Lapouge G, Rorive S, Drogat B, Desaedelaere K. 80.  et al. 2015. Different levels of Twist1 regulate skin tumor initiation, stemness, and progression. Cell Stem Cell 16:167–79 [Google Scholar]
  81. Schmidt JM, Panzilius E, Bartsch HS, Irmler M, Beckers J. 81.  et al. 2015. Stem-cell-like properties and epithelial plasticity arise as stable traits after transient Twist1 activation. Cell Rep 10:2131–39 [Google Scholar]
  82. Coffelt SB, Wellenstein MD, de Visser KE. 82.  2016. Neutrophils in cancer: neutral no more. Nat. Rev. Cancer 16:7431–46 [Google Scholar]
  83. Dvorak HF. 83.  1986. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N. Engl. J. Med. 315:261650–59 [Google Scholar]
  84. Maheswaran S, Haber DA. 84.  2015. Ex vivo culture of CTCs: an emerging resource to guide cancer therapy. Cancer Res 75:122411–15 [Google Scholar]
  85. Joosse SA, Gorges TM, Pantel K. 85.  2015. Biology, detection, and clinical implications of circulating tumor cells. EMBO Mol. Med. 7:11–11 [Google Scholar]
  86. Haber DA, Velculescu VE. 86.  2014. Blood-based analyses of cancer: circulating tumor cells and circulating tumor DNA. Cancer Discov 4:6650–61 [Google Scholar]
  87. Yu M, Stott S, Toner M, Maheswaran S, Haber DA. 87.  2011. Circulating tumor cells: approaches to isolation and characterization. J. Cell Biol. 192:3373–82 [Google Scholar]
  88. Cristofanilli M, Budd GT, Ellis MJ, Stopeck A, Matera J. 88.  et al. 2004. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N. Engl. J. Med. 351:8781–91 [Google Scholar]
  89. Bidard FC, Peeters DJ, Fehm T, Nole F, Gisbert-Criado R. 89.  et al. 2014. Clinical validity of circulating tumour cells in patients with metastatic breast cancer: a pooled analysis of individual patient data. Lancet Oncol 15:4406–14 [Google Scholar]
  90. Baccelli I, Schneeweiss A, Riethdorf S, Stenzinger A, Schillert A. 90.  et al. 2013. Identification of a population of blood circulating tumor cells from breast cancer patients that initiates metastasis in a xenograft assay. Nat. Biotechnol. 31:6539–44 [Google Scholar]
  91. Zhang L, Ridgway LD, Wetzel MD, Ngo J, Yin W. 91.  et al. 2013. The identification and characterization of breast cancer CTCs competent for brain metastasis. Sci. Transl. Med. 5:180180ra48 [Google Scholar]
  92. Hodgkinson CL, Morrow CJ, Li Y, Metcalf RL, Rothwell DG. 92.  et al. 2014. Tumorigenicity and genetic profiling of circulating tumor cells in small-cell lung cancer. Nat. Med. 20:8897–903 [Google Scholar]
  93. Aceto N, Bardia A, Miyamoto DT, Donaldson MC, Wittner BS. 93.  et al. 2014. Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis. Cell 158:51110–22 [Google Scholar]
  94. Labelle M, Begum S, Hynes RO. 94.  2011. Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer Cell 20:5576–90 [Google Scholar]
  95. Labelle M, Hynes RO. 95.  2012. The initial hours of metastasis: the importance of cooperative host-tumor cell interactions during hematogenous dissemination. Cancer Discov 2:121091–99 [Google Scholar]
  96. Gong L, Cai Y, Zhou X, Yang H. 96.  2012. Activated platelets interact with lung cancer cells through P-selectin glycoprotein ligand-1. Pathol. Oncol. Res. 18:4989–96 [Google Scholar]
  97. Gay LJ, Felding-Habermann B. 97.  2011. Contribution of platelets to tumour metastasis. Nat. Rev. Cancer 11:2123–34 [Google Scholar]
  98. Palumbo JS, Talmage KE, Massari JV, La Jeunesse CM, Flick MJ. 98.  et al. 2005. Platelets and fibrin(ogen) increase metastatic potential by impeding natural killer cell-mediated elimination of tumor cells. Blood 105:1178–85 [Google Scholar]
  99. Kopp HG, Placke T, Salih HR. 99.  2009. Platelet-derived transforming growth factor-β down-regulates NKG2D thereby inhibiting natural killer cell antitumor reactivity. Cancer Res 69:197775–83 [Google Scholar]
  100. Cedervall J, Zhang Y, Olsson AK. 100.  2016. Tumor-induced NETosis as a risk factor for metastasis and organ failure. Cancer Res 76:154311–15 [Google Scholar]
  101. Reymond N, d'Agua BB, Ridley AJ. 101.  2013. Crossing the endothelial barrier during metastasis. Nat. Rev. Cancer 13:12858–70 [Google Scholar]
  102. Butcher EC, Picker LJ. 102.  1996. Lymphocyte homing and homeostasis. Science 272:525860–66 [Google Scholar]
  103. Hiratsuka S, Goel S, Kamoun WS, Maru Y, Fukumura D. 103.  et al. 2011. Endothelial focal adhesion kinase mediates cancer cell homing to discrete regions of the lungs via E-selectin up-regulation. PNAS 108:93725–30 [Google Scholar]
  104. Kohler S, Ullrich S, Richter U, Schumacher U. 104.  2010. E-/P-selectins and colon carcinoma metastasis: first in vivo evidence for their crucial role in a clinically relevant model of spontaneous metastasis formation in the lung. Br. J. Cancer 102:3602–9 [Google Scholar]
  105. Biancone L, Araki M, Araki K, Vassalli P, Stamenkovic I. 105.  1996. Redirection of tumor metastasis by expression of E-selectin in vivo. J. Exp. Med. 183:2581–87 [Google Scholar]
  106. Kunkel EJ, Butcher EC. 106.  2002. Chemokines and the tissue-specific migration of lymphocytes. Immunity 16:11–4 [Google Scholar]
  107. Balkwill FR. 107.  2012. The chemokine system and cancer. J. Pathol. 226:2148–57 [Google Scholar]
  108. Ben-Baruch A. 108.  2008. Organ selectivity in metastasis: regulation by chemokines and their receptors. Clin. Exp. Metastasis 25:4345–56 [Google Scholar]
  109. Teicher BA, Fricker SP. 109.  2010. CXCL12 (SDF-1)/CXCR4 pathway in cancer. Clin. Cancer Res. 16:112927–31 [Google Scholar]
  110. Wu QD, Wang JH, Condron C, Bouchier-Hayes D, Redmond HP. 110.  2001. Human neutrophils facilitate tumor cell transendothelial migration. Am. J. Physiol. Cell Physiol. 280:4C814–22 [Google Scholar]
  111. Huh SJ, Liang S, Sharma A, Dong C, Robertson GP. 111.  2010. Transiently entrapped circulating tumor cells interact with neutrophils to facilitate lung metastasis development. Cancer Res 70:146071–82 [Google Scholar]
  112. Al-Mehdi AB, Tozawa K, Fisher AB, Shientag L, Lee A, Muschel RJ. 112.  2000. Intravascular origin of metastasis from the proliferation of endothelium-attached tumor cells: a new model for metastasis. Nat. Med. 6:1100–2 [Google Scholar]
  113. Karrison TG, Ferguson DJ, Meier P. 113.  1999. Dormancy of mammary carcinoma after mastectomy. J. Natl. Cancer Inst. 91:180–85 [Google Scholar]
  114. Aguirre-Ghiso JA. 114.  2007. Models, mechanisms and clinical evidence for cancer dormancy. Nat. Rev. Cancer 7:11834–46 [Google Scholar]
  115. Giancotti FG. 115.  2013. Mechanisms governing metastatic dormancy and reactivation. Cell 155:4750–64 [Google Scholar]
  116. Croucher PI, McDonald MM, Martin TJ. 116.  2016. Bone metastasis: the importance of the neighbourhood. Nat. Rev. Cancer 16:6373–86 [Google Scholar]
  117. Lawson MA, McDonald MM, Kovacic N, Hua Khoo W, Terry RL. 117.  et al. 2015. Osteoclasts control reactivation of dormant myeloma cells by remodelling the endosteal niche. Nat. Commun. 6:8983 [Google Scholar]
  118. Karadag A, Oyajobi BO, Apperley JF, Russell RG, Croucher PI. 118.  2000. Human myeloma cells promote the production of interleukin 6 by primary human osteoblasts. Br. J. Haematol. 108:2383–90 [Google Scholar]
  119. Li X, Pennisi A, Yaccoby S. 119.  2008. Role of decorin in the antimyeloma effects of osteoblasts. Blood 112:1159–68 [Google Scholar]
  120. Ro TB, Holt RU, Brenne AT, Hjorth-Hansen H, Waage A. 120.  et al. 2004. Bone morphogenetic protein-5, -6 and -7 inhibit growth and induce apoptosis in human myeloma cells. Oncogene 23:173024–32 [Google Scholar]
  121. Holien T, Sundan A. 121.  2014. The role of bone morphogenetic proteins in myeloma cell survival. Cytokine Growth Factor Rev 25:3343–50 [Google Scholar]
  122. Ghajar CM, Peinado H, Mori H, Matei IR, Evason KJ. 122.  et al. 2013. The perivascular niche regulates breast tumour dormancy. Nat. Cell Biol. 15:7807–17 [Google Scholar]
  123. Guise TA, Yin JJ, Taylor SD, Kumagai Y, Dallas M. 123.  et al. 1996. Evidence for a causal role of parathyroid hormone-related protein in the pathogenesis of human breast cancer-mediated osteolysis. J. Clin. Investig. 98:71544–49 [Google Scholar]
  124. Zheng Y, Zhou H, Fong-Yee C, Modzelewski JR, Seibel MJ, Dunstan CR. 124.  2008. Bone resorption increases tumour growth in a mouse model of osteosclerotic breast cancer metastasis. Clin. Exp. Metastasis 25:5559–67 [Google Scholar]
  125. Zheng Y, Zhou H, Ooi LL, Snir AD, Dunstan CR, Seibel MJ. 125.  2011. Vitamin D deficiency promotes prostate cancer growth in bone. Prostate 71:91012–21 [Google Scholar]
  126. Ooi LL, Zhou H, Kalak R, Zheng Y, Conigrave AD. 126.  et al. 2010. Vitamin D deficiency promotes human breast cancer growth in a murine model of bone metastasis. Cancer Res 70:51835–44 [Google Scholar]
  127. Corey E, Brown LG, Kiefer JA, Quinn JE, Pitts TE. 127.  et al. 2005. Osteoprotegerin in prostate cancer bone metastasis. Cancer Res 65:51710–18 [Google Scholar]
  128. Corey E, Brown LG, Quinn JE, Poot M, Roudier MP. 128.  et al. 2003. Zoledronic acid exhibits inhibitory effects on osteoblastic and osteolytic metastases of prostate cancer. Clin. Cancer Res. 9:1295–306 [Google Scholar]
  129. Lowe SW, Cepero E, Evan G. 129.  2004. Intrinsic tumour suppression. Nature 432:7015307–15 [Google Scholar]
  130. Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L. 130.  et al. 2005. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 438:7069820–27 [Google Scholar]
  131. Minciacchi VR, Freeman MR, Di Vizio D. 131.  2015. Extracellular vesicles in cancer: exosomes, microvesicles and the emerging role of large oncosomes. Semin. Cell Dev. Biol. 40:41–51 [Google Scholar]
  132. Liu Y, Gu Y, Han Y, Zhang Q, Jiang Z. 132.  et al. 2016. Tumor exosomal RNAs promote lung pre-metastatic niche formation by activating alveolar epithelial TLR3 to recruit neutrophils. Cancer Cell 30:2243–56 [Google Scholar]
  133. Liu Y, Cao X. 133.  2016. Characteristics and significance of the pre-metastatic niche. Cancer Cell 30:5668–81 [Google Scholar]
  134. Hiratsuka S, Watanabe A, Aburatani H, Maru Y. 134.  2006. Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat. Cell Biol. 8:121369–75 [Google Scholar]
  135. Hiratsuka S, Watanabe A, Sakurai Y, Akashi-Takamura S, Ishibashi S. 135.  et al. 2008. The S100A8-serum amyloid A3-TLR4 paracrine cascade establishes a pre-metastatic phase. Nat. Cell Biol. 10:111349–55 [Google Scholar]
  136. Kowanetz M, Wu X, Lee J, Tan M, Hagenbeek T. 136.  et al. 2010. Granulocyte-colony stimulating factor promotes lung metastasis through mobilization of Ly6G+Ly6C+ granulocytes. PNAS 107:5021248–55 [Google Scholar]
  137. Kim S, Takahashi H, Lin WW, Descargues P, Grivennikov S. 137.  et al. 2009. Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature 457:7225102–6 [Google Scholar]
  138. Erler JT, Bennewith KL, Cox TR, Lang G, Bird D. 138.  et al. 2009. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 15:135–44 [Google Scholar]
  139. Granot Z, Henke E, Comen EA, King TA, Norton L, Benezra R. 139.  2011. Tumor entrained neutrophils inhibit seeding in the premetastatic lung. Cancer Cell 20:3300–14 [Google Scholar]
  140. Wong CC, Gilkes DM, Zhang H, Chen J, Wei H. 140.  et al. 2011. Hypoxia-inducible factor 1 is a master regulator of breast cancer metastatic niche formation. PNAS 108:3916369–74 [Google Scholar]
  141. Mauti LA, Le Bitoux MA, Baumer K, Stehle JC, Golshayan D. 141.  et al. 2011. Myeloid-derived suppressor cells are implicated in regulating permissiveness for tumor metastasis during mouse gestation. J. Clin. Investig. 121:72794–807 [Google Scholar]
  142. Hosseini H, Obradovic MM, Hoffmann M, Harper KL, Sosa MS. 142.  et al. 2016. Early dissemination seeds metastasis in breast cancer. Nature 540:552–58 [Google Scholar]
  143. Harper KL, Sosa MS, Entenberg D, Hosseini H, Cheung JF. 143.  et al. 2016. Mechanism of early dissemination and metastasis in Her2+ mammary cancer. Nature 540:588–92 [Google Scholar]
  144. Yakushiji S, Ando M, Yonemori K, Kohno T, Shimizu C. 144.  et al. 2006. Cancer of unknown primary site: review of consecutive cases at the National Cancer Center Hospital of Japan. Int. J. Clin. Oncol. 11:6421–25 [Google Scholar]
  145. Turajlic S, Swanton C. 145.  2016. Metastasis as an evolutionary process. Science 352:6282169–75 [Google Scholar]
  146. Steeg PS. 146.  2016. Targeting metastasis. Nat. Rev. Cancer 16:4201–18 [Google Scholar]
  147. Straussman R, Morikawa T, Shee K, Barzily-Rokni M, Qian ZR. 147.  et al. 2012. Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 487:7408500–4 [Google Scholar]
  148. Gilbert LA, Hemann MT. 148.  2010. DNA damage-mediated induction of a chemoresistant niche. Cell 143:3355–66 [Google Scholar]
  149. Acharyya S, Oskarsson T, Vanharanta S, Malladi S, Kim J. 149.  et al. 2012. A CXCL1 paracrine network links cancer chemoresistance and metastasis. Cell 150:1165–78 [Google Scholar]
  150. Obenauf AC, Zou Y, Ji AL, Vanharanta S, Shu W. 150.  et al. 2015. Therapy-induced tumour secretomes promote resistance and tumour progression. Nature 520:7547368–72 [Google Scholar]
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