1932

Abstract

Metastasis contributes to poor prognosis in many types of cancer and is the leading cause of cancer-related deaths. Tumor cells metastasize to distant sites via the circulatory and lymphatic systems. In this review, we discuss the potential of circulating tumor cells for diagnosis and describe the experimental therapeutics that aim to target these disseminating cancer cells. We discuss the advantages and limitations of such strategies and how they may lead to the development of the next generation of antimetastasis treatments.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-bioeng-062117-120947
2018-06-04
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/20/1/annurev-bioeng-062117-120947.html?itemId=/content/journals/10.1146/annurev-bioeng-062117-120947&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Bednarz-Knoll N, Alix-Panabieres C, Pantel K 2012. Plasticity of disseminating cancer cells in patients with epithelial malignancies. Cancer Metastasis Rev 31:673–87
    [Google Scholar]
  2. 2.  Marshall E 2010. Public health. Brawling over mammography. Science 327:936–38
    [Google Scholar]
  3. 3.  Aberle DR, Adams AM, Berg CD, Black WC, Clapp JD et al.(Natl. Lung Screen. Trial Res. Team). 2011. Reduced lung-cancer mortality with low-dose computed tomographic screening. N. Engl. J. Med. 365:395–409
    [Google Scholar]
  4. 4.  Albert JM 2013. Radiation risk from CT: implications for cancer screening. Am. J. Roentgenol. 201:W81–87
    [Google Scholar]
  5. 5.  Edwards BK, Ward E, Kohler BA, Eheman C, Zauber AG et al. 2010. Annual report to the nation on the status of cancer, 1975–2006, featuring colorectal cancer trends and impact of interventions (risk factors, screening, and treatment) to reduce future rates. Cancer 116:544–73
    [Google Scholar]
  6. 6.  Ashworth TR 1869. A case of cancer in which cells similar to those in the tumors were seen in the blood after death. Aust. Med. J. 14:146–49
    [Google Scholar]
  7. 7.  Allard WJ, Matera J, Miller MC, Repollet M, Connelly MC et al. 2004. Tumor cells circulate in the peripheral blood of all major carcinomas but not in healthy subjects or patients with nonmalignant diseases. Clin. Cancer Res. 10:6897–904
    [Google Scholar]
  8. 8.  Cristofanilli M, Budd GT, Ellis MJ, Stopeck A, Matera J et al. 2004. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N. Engl. J. Med. 351:781–91
    [Google Scholar]
  9. 9.  Cristofanilli M, Hayes DF, Budd GT, Ellis MJ, Stopeck A et al. 2005. Circulating tumor cells: a novel prognostic factor for newly diagnosed metastatic breast cancer. J. Clin. Oncol. 23:1420–30
    [Google Scholar]
  10. 10.  Riethdorf S, Fritsche H, Müller V, Rau T, Schindlbeck C et al. 2007. Detection of circulating tumor cells in peripheral blood of patients with metastatic breast cancer: a validation study of the CellSearch system. Clin. Cancer Res. 13:920–28
    [Google Scholar]
  11. 11.  Yagata H, Nakamura S, Toi M, Bando H, Ohno S, Kataoka A 2008. Evaluation of circulating tumor cells in patients with breast cancer: multi-institutional clinical trial in Japan. Int. J. Clin. Oncol. 13:252–56
    [Google Scholar]
  12. 12.  Kurihara T, Itoi T, Sofuni A, Itokawa F, Tsuchia T et al. 2008. Detection of circulating tumor cells in patients with pancreatic cancer: a preliminary result. J. Hepatobiliary Pancreat. Surg. 15:189–95
    [Google Scholar]
  13. 13.  Khoja L, Backen A, Sloane R, Menasce L, Ryder D et al. 2012. A pilot study to explore circulating tumour cells in pancreatic cancer as a novel biomarker. Br. J. Cancer 106:508–16
    [Google Scholar]
  14. 14.  Maheswaran S, Sequist SV, Nagrath S, Uluks L, Brannigan B et al. 2008. Detection of mutations in EGFR in circulating lung-cancer cells. N. Engl. J. Med. 359:366–77
    [Google Scholar]
  15. 15.  Nagrath S, Sequist SV, Maheswaran S, Bell DW, Irimia D et al. 2007. Isolation of rare circulating tumour cells in cancer patients by microchip technology. Nature 450:1235–39
    [Google Scholar]
  16. 16.  Stott SL, Hsu CH, Tsukrov DI, Yu M, Miyamoto DT et al. 2010. Isolation of circulating tumor cells using a microvortex-generating herringbone chip. PNAS 107:18392–97
    [Google Scholar]
  17. 17.  Stott SL, Lee RJ, Nagrath S, Yu M, Mitamoto DT et al. 2010. Isolation and characterization of circulating tumor cells from patients with localized and metastatic prostate cancer. Sci. Transl. Med. 2:25ra23
    [Google Scholar]
  18. 18.  Cen P, Ni X, Yang J, Graham DY, Li M 2012. Circulating tumor cells in the diagnosis and management of pancreatic cancer. Biochim. Biophys. Acta 1826:350–56
    [Google Scholar]
  19. 19.  Soeth E, Grigoleit U, Moellmann B, Röder C, Schniewind B et al. 2005. Detection of tumor cell dissemination in pancreatic ductal carcinoma patients by CK 20 RT-PCR indicates poor survival. J. Cancer Res. Clin. Oncol. 131:669–76
    [Google Scholar]
  20. 20.  Hoffmann K, Kerner C, Wilfert W, Mueller M, Thiery J et al. 2007. Detection of disseminated pancreatic cells by amplification of cytokeratin-19 with quantitative RT-PCR in blood, bone marrow and peritoneal lavage of pancreatic carcinoma patients. World J. Gastroenterol. 13:257–63
    [Google Scholar]
  21. 21.  de Albuquerque A, Kubisch I, Breier G, Stamminger G, Fersis N et al. 2012. Multimarker gene analysis of circulating tumor cells in pancreatic cancer patients: a feasibility study. Oncology 82:3–10
    [Google Scholar]
  22. 22.  Alix-Panabieres C, Pantel K 2013. Circulating tumor cells: liquid biopsy of cancer. Clin. Chem. 59:110–18
    [Google Scholar]
  23. 23.  Gazzaniga P, Raimondi C, Nicolazzo C, Carletti R, di Gioia C et al. 2015. The rationale for liquid biopsy in colorectal cancer: a focus on circulating tumor cells. Expert Rev. Mol. Diagn. 15:925–32
    [Google Scholar]
  24. 24.  Hüsemann Y, Geigl JB, Schubert F, Musiani P, Meyer M et al. 2008. Systemic spread is an early step in breast cancer. Cancer Cell 13:58–68
    [Google Scholar]
  25. 25.  Zhang Z, Shiratsuchi H, Lin J, Chen G, Reddy RM et al. 2015. Expansion of CTCs from early stage lung cancer patients using a microfluidic co-culture model. Cancer Res 75:12393–97
    [Google Scholar]
  26. 26.  Murlidhar V, Reddy RM, Fouladdel S, Zhao L, Ishikawa MK et al. 2017. Poor prognosis indicated by venous circulating tumor cell clusters in early-stage lung cancers. Cancer Res 77:5194–206
    [Google Scholar]
  27. 27.  Pantel K, Speicher MR 2016. The biology of circulating tumor cells. Oncogene 35:1216–24
    [Google Scholar]
  28. 28.  Smerage JB, Barlow WE, Hortobagyi GN, Winer EP, Leyland-Jones B et al. 2014. Circulating tumor cells and response to chemotherapy in metastatic breast cancer: SWOG S0500. J. Clin. Oncol. 32:3483–89
    [Google Scholar]
  29. 29.  Wan L, Pantel K, Kang Y 2013. Tumor metastasis: moving new biological insights into the clinic. Nat. Med. 19:1450–64
    [Google Scholar]
  30. 30.  Alix-Panabieres C, Pantel K 2014. Challenges in circulating tumour cell research. Nat. Rev. Cancer 14:623–31
    [Google Scholar]
  31. 31.  Gorges TM, Kuske A, Röck K, Mauermann O, Müller V et al. 2016. Accession of tumor heterogeneity by multiplex transcriptome profiling of single circulating tumor cells. Clin. Chem. 62:1504–15
    [Google Scholar]
  32. 32.  Zhang Z, Shiratsuchi H, Palanisamy N, Nagrath S, Ramnath N 2017. Expanded circulating tumor cells from a patient with ALK-positive lung cancer present with EML4-ALK rearrangement along with resistance mutation and enable drug sensitivity testing: a case study. J. Thorac. Oncol. 12:397–402
    [Google Scholar]
  33. 33.  Jordan NV, Bardia A, Wittner BS, Benes C, Ligorio M et al. 2016. HER2 expression identifies dynamic functional states within circulating breast cancer cells. Nature 537:102–6
    [Google Scholar]
  34. 34.  Kaiser J 2010. Cancer's circulation problem. Science 327:1072–74
    [Google Scholar]
  35. 35.  Giuliano M, Giordano A, Hsu L, Handy BC, Ueno NT et al. 2011. Circulating tumor cells as prognostic and predictive markers in metastatic breast cancer patients receiving first-line systemic treatment. Breast Cancer Res 13:R67
    [Google Scholar]
  36. 36.  Cohen SJ, Punt CJ, Iannotti N, Saidman BH, Sabbath KD et al. 2008. Relationship of circulating tumor cells to tumor response, progression-free survival, and overall survival in patients with metastatic colorectal cancer. J. Clin. Oncol. 26:3213–21
    [Google Scholar]
  37. 37.  Ignatiadis M, Lee M, Jeffrey SS 2015. Circulating tumor cells and circulating tumor DNA: challenges and opportunities on the path to clinical utility. Clin. Cancer Res. 21:4786–800
    [Google Scholar]
  38. 38.  Mostert B, Kraan J, Bolt-de Vries J, van der Spoel P, Sieuwerts AM et al. 2011. Detection of circulating tumor cells in breast cancer may improve through enrichment with anti-CD146. Breast Cancer Res. Treat. 127:33–41
    [Google Scholar]
  39. 39.  Zhang T, Boominathan R, Foulk B, Rao C, Kemeny G et al. 2016. Development of a novel c-MET-based CTC detection platform. Mol. Cancer Res. 14:539–47
    [Google Scholar]
  40. 40.  Bitting RL, Boominathan R, Rao C, Kemeny G, Foulk B et al. 2013. Development of a method to isolate circulating tumor cells using mesenchymal-based capture. Methods 64:129–36
    [Google Scholar]
  41. 41.  Andree KC, van Dalum G, Terstappen LW 2016. Challenges in circulating tumor cell detection by the CellSearch system. Mol. Oncol. 10:395–407
    [Google Scholar]
  42. 42.  Yoon HJ, Kim TH, Zhang Z, Azizi E, Pham TM et al. 2013. Sensitive capture of circulating tumour cells by functionalized graphene oxide nanosheets. Nat. Nanotechnol. 8:735–41
    [Google Scholar]
  43. 43.  Vona G, Sabile A, Louha M, Sitruk V, Romana S et al. 2000. Isolation by size of epithelial tumor cells: a new method for the immunomorphological and molecular characterization of circulating tumor cells. Am. J. Pathol. 156:57–63
    [Google Scholar]
  44. 44.  Farace F, Massard C, Vimond N, Drusch F, Jacques N et al. 2011. A direct comparison of CellSearch and ISET for circulating tumour-cell detection in patients with metastatic carcinomas. Br. J. Cancer 105:847–53
    [Google Scholar]
  45. 45.  Zheng S, Lin HK, Lu B, Williams A, Datar R et al. 2011. 3D microfilter device for viable circulating tumor cell (CTC) enrichment from blood. Biomed. Microdevices 13:203–13
    [Google Scholar]
  46. 46.  Zheng S, Lin H, Liu JQ, Balic M, Datar R et al. 2007. Membrane microfilter device for selective capture, electrolysis and genomic analysis of human circulating tumor cells. J. Chromatogr. A 1162:154–61
    [Google Scholar]
  47. 47.  Di Carlo D, Irimia D, Tompkins RG, Toner M 2007. Continuous inertial focusing, ordering, and separation of particles in microchannels. PNAS 104:18892–97
    [Google Scholar]
  48. 48.  Hur SC, Mach AJ, Di Carlo D 2011. High-throughput size-based rare cell enrichment using microscale vortices. Biomicrofluidics 5:22206
    [Google Scholar]
  49. 49.  Sollier E, Go DE, Che J, Gossett DR, O'Byrne S et al. 2014. Size-selective collection of circulating tumor cells using Vortex technology. Lab Chip 14:63–77
    [Google Scholar]
  50. 50.  Che J, Yu V, Dhar M, Renier C, Matsumoto M et al. 2016. Classification of large circulating tumor cells isolated with ultra-high throughput microfluidic Vortex technology. Oncotarget 7:12748–60
    [Google Scholar]
  51. 51.  Hyun KA, Kwon K, Han H, Kim SI, Jung HI 2013. Microfluidic flow fractionation device for label-free isolation of circulating tumor cells (CTCs) from breast cancer patients. Biosens. Bioelectron. 40:206–12
    [Google Scholar]
  52. 52.  Hou HW, Warkiani ME, Khoo BL, Li ZR, Soo RA et al. 2013. Isolation and retrieval of circulating tumor cells using centrifugal forces. Sci. Rep. 3:1259
    [Google Scholar]
  53. 53.  Warkiani ME, Guan G, Luan KB, Lee WC, Bhagat AA et al. 2014. Slanted spiral microfluidics for the ultra-fast, label-free isolation of circulating tumor cells. Lab Chip 14:128–37
    [Google Scholar]
  54. 54.  Warkiani ME, Khoo BL, Tan DSW, Bahag AAS, Lim WT et al. 2014. An ultra-high-throughput spiral microfluidic biochip for the enrichment of circulating tumor cells. Analyst 139:3245–55
    [Google Scholar]
  55. 55.  Lin E, Rivera-Báez L, Fouladdel S, Yoon HJ, Guthrie S et al. 2017. High-throughput microfluidic Labyrinth for the label-free isolation of circulating tumor cells. Cell Syst 5:295–304
    [Google Scholar]
  56. 56.  Becker FF, Wang SB, Huang Y, Pethig R, Vykoual J, Gascoyne PR 1995. Separation of human breast cancer cells from blood by differential dielectric affinity. PNAS 92:860–64
    [Google Scholar]
  57. 57.  Jackson JM, Witek MA, Kamande JW, Soper SA 2017. Materials and microfluidics: enabling the efficient isolation and analysis of circulating tumour cells. Chem. Soc. Rev. 46:4245–80
    [Google Scholar]
  58. 58.  Gascoyne PR, Shim S 2014. Isolation of circulating tumor cells by dielectrophoresis. Cancers 6:545–79
    [Google Scholar]
  59. 59.  Manaresi N, Romani A, Medoro G, Altomare L, Leonardi A et al. 2003. A CMOS chip for individual cell manipulation and detection. IEEE J. Solid-State Circuits 38:2297–305
    [Google Scholar]
  60. 60.  Peeters DJ, De Laere B, Van den Eynden GG, Van Laere SJ, Rothé F et al. 2013. Semiautomated isolation and molecular characterisation of single or highly purified tumour cells from CellSearch enriched blood samples using dielectrophoretic cell sorting. Br. J. Cancer 108:1358–67
    [Google Scholar]
  61. 61.  Ozkumur E, Shah AM, Ciciliano JC, Emmink BL, Miyamoto DT et al. 2013. Inertial focusing for tumor antigen-dependent and -independent sorting of rare circulating tumor cells. Sci. Transl. Med. 5:179ra47
    [Google Scholar]
  62. 62.  Jack RM, Grafton MMG, Rodrigues D, Giraldez MD, Griffith C et al. 2016. Ultra-specific isolation of circulating tumor cells enables rare-cell RNA profiling. Adv. Sci. 3:1600063
    [Google Scholar]
  63. 63.  Greene BT, Hughes AD, King MR 2012. Circulating tumor cells: the substrate of personalized medicine?. Front. Oncol. 2:69
    [Google Scholar]
  64. 64.  Maheswaran S, Haber DA 2010. Circulating tumor cells: a window into cancer biology and metastasis. Curr. Opin. Genet. Dev. 20:96–99
    [Google Scholar]
  65. 65.  Riethdorf S, Wikman H, Pantel K 2008. Biological relevance of disseminated tumor cells in cancer patients. Int. J. Cancer 123:1991–2006
    [Google Scholar]
  66. 66.  Chambers AF, MacDonald IC, Schmidt EE, Koop S, Morris VL et al. 1995. Steps in tumor metastasis: new concepts from intravital videomicroscopy. Cancer Metastasis Rev 14:279–301
    [Google Scholar]
  67. 67.  Steeg PS 2006. Tumor metastasis: mechanistic insights and clinical challenges. Nat. Med. 12:895–904
    [Google Scholar]
  68. 68.  Chandrasekaran S, King M 2014. Microenvironment of tumor-draining lymph nodes: opportunities for liposome-based targeted therapy. Int. J. Mol. Sci. 15:20209–39
    [Google Scholar]
  69. 69.  Chaffer CL, Weinberg RA 2011. A perspective on cancer cell metastasis. Science 331:1559–64
    [Google Scholar]
  70. 70.  Allard WJ 2004. Tumor cells circulate in the peripheral blood of all major carcinomas but not in healthy subjects or patients with nonmalignant diseases. Clin. Cancer Res. 10:6897–904
    [Google Scholar]
  71. 71.  Franklin WA, Glaspy J, Pflaumer SM, Jones RB, Hami L et al. 1999. Incidence of tumor-cell contamination in leukapheresis products of breast cancer patients mobilized with stem cell factor and granulocyte colony-stimulating factor (G-CSF) or with G-CSF alone. Blood 94:340–47
    [Google Scholar]
  72. 72.  Gertler R, Rosenberg R, Fuehrer K, Dahm M, Nekarda H, Siewert JR 2003. Detection of circulating tumor cells in blood using an optimized density gradient centrifugation. Recent Results Cancer Res 162:149–55
    [Google Scholar]
  73. 73.  Baker MK, Mikhitarian K, Osta W, Callahan K, Hoda R et al. 2003. Molecular detection of breast cancer cells in the peripheral blood of advanced-stage breast cancer patients using multimarker real-time reverse transcription–polymerase chain reaction and a novel porous barrier density gradient centrifugation technology. Clin. Cancer Res. 9:4865–71
    [Google Scholar]
  74. 74.  Vona G, Estepa L, Béroud C, Damotte D, Capron F et al. 2004. Impact of cytomorphological detection of circulating tumor cells in patients with liver cancer. Hepatology 39:792–97
    [Google Scholar]
  75. 75.  Eifler RL, Lind J, Falkenhagen D, Weber V, Fischer MB, Zeillinger R 2011. Enrichment of circulating tumor cells from a large blood volume using leukapheresis and elutriation: proof of concept. Cytometry B 80:100–11
    [Google Scholar]
  76. 76.  Fischer JC, Niederacher D, Topp SA, Honisch E, Schumacher S et al. 2013. Diagnostic leukapheresis enables reliable detection of circulating tumor cells of nonmetastatic cancer patients. PNAS 110:16580–85
    [Google Scholar]
  77. 77.  Ross AA, Cooper BW, Lazarus HM, Mackay W, Moss TJ et al. 1993. Detection and viability of tumor cells in peripheral blood stem cell collections from breast cancer patients using immunocytochemical and clonogenic assay techniques. Blood 82:2605–10
    [Google Scholar]
  78. 78.  Mazzolini G, Alfaro C, Sangro B, Feijoó E, Ruiz J et al. 2005. Intratumoral injection of dendritic cells engineered to secrete interleukin-12 by recombinant adenovirus in patients with metastatic gastrointestinal carcinomas. J. Clin. Oncol. 23:999–1010
    [Google Scholar]
  79. 79.  Dohnal AM, Graffi S, Witt V, Eichstill C, Wagner D et al. 2009. Comparative evaluation of techniques for the manufacturing of dendritic cell–based cancer vaccines. J. Cell. Mol. Med. 13:125–35
    [Google Scholar]
  80. 80.  Warkiani ME, Wu L, Tay AKP, Han J 2015. Large-volume microfluidic cell sorting for biomedical applications. Annu. Rev. Biomed. Eng. 17:1–34
    [Google Scholar]
  81. 81.  Gorges TM, Pantel K 2013. Circulating tumor cells as therapy-related biomarkers in cancer patients. Cancer Immunol. Immunother. 62:931–39
    [Google Scholar]
  82. 82.  Nedosekin DA, Sarimollaoglu M, Ye J-H, Galanzha EI, Zharov VP 2011. In vivo ultra-fast photoacoustic flow cytometry of circulating human melanoma cells using near-infrared high-pulse rate lasers. Cytometry A 79:825–33
    [Google Scholar]
  83. 83.  Kim J-W, Galanzha EI, Zaharoff DA, Griffin RJ, Zharov VP 2013. Nanotheranostics of circulating tumor cells, infections and other pathological features in vivo. Mol. Pharm. 10:813–30
    [Google Scholar]
  84. 84.  Wei X 2016. Monitoring circulating tumor cells by in-vivo flow cytometry Presented at Asia Commun. Photonics Conf., Wuhan, China, Nov. 2–5
  85. 85.  Zharov VP, Galanzha EI, Shashkov EV, Khlebtsov NG, Tuchin VV 2006. In vivo photoacoustic flow cytometry for monitoring of circulating single cancer cells and contrast agents. Opt. Lett 31:3623–25
    [Google Scholar]
  86. 86.  Novak J, Georgakoudi I, Wei X, Prossin A, Lin CP 2004. In vivo flow cytometer for real-time detection and quantification of circulating cells. Opt. Lett 29:77–79
    [Google Scholar]
  87. 87.  Galanzha EI, Kim J-W, Zharov VP 2009. Nanotechnology-based molecular photoacoustic and photothermal flow cytometry platform for in-vivo detection and killing of circulating cancer stem cells. J. Biophotonics 2:725–35
    [Google Scholar]
  88. 88.  Chambers AF, Naumov GN, Vantyghem SA, Tuck AB 2000. Molecular biology of breast cancer metastasis: clinical implications of experimental studies on metastatic inefficiency. Breast Cancer Res 2:18
    [Google Scholar]
  89. 89.  MacDonald IC, Groom AC, Chambers AF 2002. Cancer spread and micrometastasis development: quantitative approaches for in vivo models. BioEssays 24:885–93
    [Google Scholar]
  90. 90.  Gakhar G, Navarro VN, Jurish M, Lee GY, Tagawa ST et al. 2013. Circulating tumor cells from prostate cancer patients interact with E-selectin under physiologic blood flow. PLOS ONE 8:e85143
    [Google Scholar]
  91. 91.  Rana K, Liesveld JL, King MR 2009. Delivery of apoptotic signal to rolling cancer cells: a novel biomimetic technique using immobilized TRAIL and E-selectin. Biotechnol. Bioeng. 102:1692–702
    [Google Scholar]
  92. 92.  Wang S, El-Deiry WS 2003. TRAIL and apoptosis induction by TNF-family death receptors. Oncogene 22:8628–33
    [Google Scholar]
  93. 93.  Phipps LE, Hino S, Muschel RJ 2011. Targeting cell spreading: a method of sensitizing metastatic tumor cells to TRAIL-induced apoptosis. Mol. Cancer Res. 9:249–58
    [Google Scholar]
  94. 94.  Mitchell MJ, King MR 2013. Fluid shear stress sensitizes cancer cells to receptor-mediated apoptosis via trimeric death receptors. New J. Phys. 15:015008
    [Google Scholar]
  95. 95.  Turitto VT 1982. Blood viscosity, mass transport, and thrombogenesis. Prog. Hemost. Thromb. 6:139–77
    [Google Scholar]
  96. 96.  Mitchell MJ, King MR 2013. Computational and experimental models of cancer cell response to fluid shear stress. Front. Oncol. 3:44
    [Google Scholar]
  97. 97.  Luo C-W, Wu C-C, Chang H-J 2014. Radiation sensitization of tumor cells induced by shear stress: the roles of integrins and FAK. Biochim. Biophys. Acta 1843:2129–37
    [Google Scholar]
  98. 98.  Mitchell MJ, Wayne E, Rana K, Schaffer CB, King MR 2014. TRAIL-coated leukocytes that kill cancer cells in the circulation. PNAS 111:930–35
    [Google Scholar]
  99. 99.  Wayne EC, Chandrasekaran S, Mitchell MJ, Chan MF, Lee RE et al. 2016. TRAIL-coated leukocytes that prevent the bloodborne metastasis of prostate cancer. J. Control. Release 223:215–23
    [Google Scholar]
  100. 100.  Labelle M, Hynes RO 2012. The initial hours of metastasis: the importance of cooperative host–tumor cell interactions during hematogenous dissemination. Cancer Discov 2:1091–99
    [Google Scholar]
  101. 101.  Gay LJ, Felding-Habermann B 2011. Contribution of platelets to tumour metastasis. Nat. Rev. Cancer 11:123–34
    [Google Scholar]
  102. 102.  Gay LJ, Felding-Habermann B 2011. Platelets alter tumor cell attributes to propel metastasis: programming in transit. Cancer Cell 20:553–54
    [Google Scholar]
  103. 103.  Nieswandt B, Hafner M, Echtenacher B, Männel DN 1999. Lysis of tumor cells by natural killer cells in mice is impeded by platelets. Cancer Res 59:1295–300
    [Google Scholar]
  104. 104.  Bambace NM, Holmes CE 2011. The platelet contribution to cancer progression. J. Thromb. Haemost. 9:237–49
    [Google Scholar]
  105. 105.  Weber MR, Zuka M, Lorger M, Tschan M, Torbett BE et al. 2016. Activated tumor cell integrin αvβ3 cooperates with platelets to promote extravasation and metastasis from the blood stream. Thromb. Res. 140:S27–36
    [Google Scholar]
  106. 106.  Labelle M, Begum S, Hynes RO 2011. Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer Cell 20:576–90
    [Google Scholar]
  107. 107.  Wenzel J, Zeisig R, Fichtner I 2009. Inhibition of metastasis in a murine 4T1 breast cancer model by liposomes preventing tumor cell–platelet interactions. Clin. Exp. Metastasis 27:25–34
    [Google Scholar]
  108. 108.  Zhang Y, Wei J, Liu S, Wang J, Han X et al. 2017. Inhibition of platelet function using liposomal nanoparticles blocks tumor metastasis. Theranostics 7:1062–71
    [Google Scholar]
  109. 109.  Zhang W, Dang S, Hong T, Tang J, Fan J et al. 2012. A humanized single-chain antibody against β3 integrin inhibits pulmonary metastasis by preferentially fragmenting activated platelets in the tumor microenvironment. Blood 120:2889–98 Erratum. 2014 Blood 123:302
    [Google Scholar]
  110. 110.  Li J, Sharkey CC, Wun B, Liesveld JL, King MR 2016. Genetic engineering of platelets to neutralize circulating tumor cells. J. Control. Release 228:38–47
    [Google Scholar]
  111. 111.  Li J, Ai Y, Wang L, Bu P, Sharkey CC et al. 2016. Targeted drug delivery to circulating tumor cells via platelet membrane-functionalized particles. Biomaterials 76:52–65
    [Google Scholar]
  112. 112.  Best MG, Sol N, Kooi I, Tannous J, Westerman BA et al. 2015. RNA-seq of tumor-educated platelets enables blood-based pan-cancer, multiclass, and molecular pathway cancer diagnostics. Cancer Cell 28:666–76
    [Google Scholar]
  113. 113.  Morton DL 1992. Technical details of intraoperative lymphatic mapping for early stage melanoma. Arch. Surg. 127:392–99
    [Google Scholar]
  114. 114.  Ross MI 1997. Lymphatic mapping and sentinel node biopsy for early stage melanoma: how we do it at the M.D. Anderson Cancer Center. J. Surg. Oncol. 66:273–76
    [Google Scholar]
  115. 115.  Ariel IM 1988. Incidence of metastases to lymph nodes from soft-tissue sarcomas. Semin. Surg. Oncol. 4:27–29
    [Google Scholar]
  116. 116.  Van Trappen PO, Pepper MS 2002. Lymphatic dissemination of tumour cells and the formation of micrometastases. Lancet Oncol 3:44–52
    [Google Scholar]
  117. 117.  Leong SPL, Nakakura EK, Pollock R, Choti MA, Morton DL et al. 2011. Unique patterns of metastases in common and rare types of malignancy. J. Surg. Oncol. 103:607–14
    [Google Scholar]
  118. 118.  Massucco P, Ribero D, Sgotto E, Mellano A, Muratore A, Capussotti L 2009. Prognostic significance of lymph node metastases in pancreatic head cancer treated with extended lymphadenectomy: not just a matter of numbers. Ann. Surg. Oncol. 16:3323–32
    [Google Scholar]
  119. 119.  Murakami Y, Uemura K, Sudo T, Hayashidani Y, Hashimoto Y et al. 2010. Number of metastatic lymph nodes, but not lymph node ratio, is an independent prognostic factor after resection of pancreatic carcinoma. J. Am. Coll. Surg. 211:196–204
    [Google Scholar]
  120. 120.  Gugliemetti G, Sukhu R, Conca Baenas MA, Meeks J, Sjoberg DD et al. 2016. Number of metastatic lymph nodes as determinant of outcome after salvage radical prostatectomy for radiation-recurrent prostate cancer. Actas Urol. Esp. 40:434–39
    [Google Scholar]
  121. 121.  Maccio L, Barresi V, Domati F, Martorana E, Cesinaro AM et al. 2016. Clinical significance of pelvic lymph node status in prostate cancer: review of 1,690 cases. Intern. Emerg. Med. 11:399–404
    [Google Scholar]
  122. 122.  Andrian von UH, Mempel TR 2003. Homing and cellular traffic in lymph nodes. Nat. Rev. Immunol. 3:867–78
    [Google Scholar]
  123. 123.  Weiden J, Tel J, Figdor CG 2017. Synthetic immune niches for cancer immunotherapy. Nat. Rev. Immunol. 11:107
    [Google Scholar]
  124. 124.  Munn DH, Mellor AL 2006. The tumor‐draining lymph node as an immune‐privileged site. Immunol. Rev. 213:146–58
    [Google Scholar]
  125. 125.  Bhatia A, Kumar Y 2014. Cellular and molecular mechanisms in cancer immune escape: a comprehensive review. Expert Rev. Clin. Immunol. 10:41–62
    [Google Scholar]
  126. 126.  Zamai L, Ahmad M, Bennett IM, Azzoni L, Alnemri ES, Perussia B 1998. Natural killer (NK) cell-mediated cytotoxicity: differential use of TRAIL and Fas ligand by immature and mature primary human NK cells. J. Exp. Med. 188:2375–80
    [Google Scholar]
  127. 127.  Smyth MJ, Cretney E, Takeda K, Wiltrout RH, Sedger LM et al. 2001. Tumor necrosis factor–related apoptosis-inducing ligand (TRAIL) contributes to interferon γ–dependent natural killer cell protection from tumor metastasis. J. Exp. Med. 193:6661–70
    [Google Scholar]
  128. 128.  Schuster IS, Wikstrom ME, Brizard G, Coudert JD, Estcourt MJ et al. 2014. TRAIL+ NK cells control CD4+ T cell responses during chronic viral infection to limit autoimmunity. Immunity 41:646–56
    [Google Scholar]
  129. 129.  Wu JD, Higgins LM, Steinle A, Cosman D, Haugk K, Plymate SR 2004. Prevalent expression of the immunostimulatory MHC class I chain–related molecule is counteracted by shedding in prostate cancer. J. Clin. Investig. 114:560–68
    [Google Scholar]
  130. 130.  Garcia Lora A, Algarra I, Garrido F 2003. MHC class I antigens, immune surveillance, and tumor immune escape. J. Cell. Physiol. 195:346–55
    [Google Scholar]
  131. 131.  Groh V, Wu J, Yee C, Spies T 2002. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 419:734–38
    [Google Scholar]
  132. 132.  Lee J-C, Lee K-M, Kim D-W, Heo DS 2004. Elevated TGF-β1 secretion and down-modulation of NKG2D underlies impaired NK cytotoxicity in cancer patients. J. Immunol. 172:7335–40
    [Google Scholar]
  133. 133.  Ruggeri L, Capanni M, Urbani E, Perruccio K, Shlomchik WD et al. 2002. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 295:2097–100
    [Google Scholar]
  134. 134.  Ishikawa E, Tsuboi K, Saijo K, Harada H, Takano S et al. 2004. Autologous natural killer cell therapy for human recurrent malignant glioma. Anticancer Res 24:1861–71
    [Google Scholar]
  135. 135.  Lundqvist A, McCoy JP, Samsel L, Childs R 2007. Reduction of GVHD and enhanced antitumor effects after adoptive infusion of alloreactive Ly49-mismatched NK cells from MHC-matched donors. Blood 109:3603–6
    [Google Scholar]
  136. 136.  Cheng M, Chen Y, Xiao W, Sun R, Tian Z 2013. NK cell–based immunotherapy for malignant diseases. Cell. Mol. Immunol. 10:230–52
    [Google Scholar]
  137. 137.  Chandrasekaran S, McGuire MJ, King MR 2014. Sweeping lymph node micrometastases off their feet: an engineered model to evaluate natural killer cell mediated therapeutic intervention of circulating tumor cells that disseminate to the lymph nodes. Lab Chip 14:118–27
    [Google Scholar]
  138. 138.  Chandrasekaran S, Chan MF, Li J, King MR 2016. Super natural killer cells that target metastases in the tumor draining lymph nodes. Biomaterials 77:66–76
    [Google Scholar]
  139. 139.  Banchereau J, Steinman RM 1998. Dendritic cells and the control of immunity. Nature 392:245–52
    [Google Scholar]
  140. 140.  Ma Y, Shurin GV, Peiyuan Z, Shurin MR 2013. Dendritic cells in the cancer microenvironment. J. Cancer 4:36–44
    [Google Scholar]
  141. 141.  Fridman WH, Pagès F, Sautès-Fridman C, Galon J 2012. The immune contexture in human tumours: impact on clinical outcome. Nat. Rev. Cancer 12:298–306
    [Google Scholar]
  142. 142.  Azuma M, Ebihara T, Oshiumi H, Matsumoto M, Seya T 2014. Cross-priming for antitumor CTL induced by soluble Ag+ polyI:C depends on the TICAM-1 pathway in mouse CD11c+/CD8α+ dendritic cells. OncoImmunology 1:581–92
    [Google Scholar]
  143. 143.  Wu A, Oh S, Gharagozlou S, Vedi RN, Ericson K et al. 2007. In vivo vaccination with tumor cell lysate plus CpG oligodeoxynucleotides eradicates murine glioblastoma. J. Immunother. 30:789–97
    [Google Scholar]
  144. 144.  Pinzon-Charry A, Maxwell T 2005. Dendritic cell dysfunction in cancer: a mechanism for immunosuppression. Immunol. Cell 83:451–61
    [Google Scholar]
  145. 145.  Banchereau J, Palucka AK, Dhodapkar M, Burkeholder S, Taquet N et al. 2001. Immune and clinical responses in patients with metastatic melanoma to CD34+ progenitor–derived dendritic cell vaccine. Cancer Res 61:6451–58
    [Google Scholar]
  146. 146.  Jeanbart L, Ballester M, de Titta A, Corthésy P, Romero P et al. 2014. Enhancing efficacy of anticancer vaccines by targeted delivery to tumor-draining lymph nodes. Cancer Immunol. Res. 2:436–47
    [Google Scholar]
  147. 147.  Thomas SN, Vokali E, Lund AW, Hubbell JA, Swartz MA 2014. Targeting the tumor-draining lymph node with adjuvanted nanoparticles reshapes the anti-tumor immune response. Biomaterials 35:814–24
    [Google Scholar]
  148. 148.  Liu Y, Xiao L, Joo K-I, Hu B, Fang J, Wang P 2014. In situ modulation of dendritic cells by injectable thermosensitive hydrogels for cancer vaccines in mice. Biomacromolecules 15:3836–45
    [Google Scholar]
  149. 149.  Ali OA, Huebsch N, Cao L, Dranoff G, Mooney DJ 2009. Infection-mimicking materials to program dendritic cells in situ. Nat. Mater. 8:151–58
    [Google Scholar]
  150. 150.  Ali OA, Lewin SA, Dranoff G, Mooney DJ 2016. Vaccines combined with immune checkpoint antibodies promote cytotoxic T-cell activity and tumor eradication. Cancer Immunol. Res. 4:95–100
    [Google Scholar]
/content/journals/10.1146/annurev-bioeng-062117-120947
Loading
/content/journals/10.1146/annurev-bioeng-062117-120947
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error