The effects of monocytes on tumor cell extravasation in a 3D vascularized microfluidic model

Biomaterials

Volumn 198, Issue , 2019, Pages 180-193

  Boussommier Calleja, A ^a   Atiyas, Y ^a   Haase, K ^a   Headley, M ^b,c   Lewis, C ^d   Kamm, R D ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Fred Hutchinson Cancer Research Center   (United States)

^d UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Cancer cell extravasation; Cancer immunotherapy; Cancer metastasis; Microfluidic models; Monocyte extravasation; Monocyte to macrophage differentiation

Indexed keywords

CYTOLOGY; LIFE CYCLE; MACROPHAGES; MICROFLUIDICS; PATHOLOGY; PHYSIOLOGICAL MODELS; TUMORS;

CANCER CELLS; CANCER IMMUNOTHERAPY; CANCER METASTASIS; MACROPHAGE DIFFERENTIATIONS; MONOCYTE EXTRAVASATION;

DISEASES;

MYOSIN ADENOSINE TRIPHOSPHATASE;

ARTICLE; CANCER GROWTH; CANCER IMMUNOTHERAPY; CELL DIFFERENTIATION; CELL FUNCTION; CELL INTERACTION; CELL ISOLATION; CELL MEMBRANE PERMEABILITY; CELL MIGRATION; CONTROLLED STUDY; EVIDENCE BASED PRACTICE; HUMAN; HUMAN CELL; IN VITRO STUDY; LIFE CYCLE STAGE; MACROPHAGE; MICROFLUIDICS; MICROTECHNOLOGY; MONOCYTE; PRIORITY JOURNAL; TUMOR CELL; TUMOR MICROENVIRONMENT; VASCULARIZATION; CELL COMMUNICATION; CELL MOTION; DEVICES; EQUIPMENT DESIGN; INFLAMMATION; MICROFLUIDIC ANALYSIS; MICROVASCULATURE; NEOPLASM; PATHOLOGY; PROCEDURES; TUMOR CELL LINE; UMBILICAL VEIN ENDOTHELIAL CELL;

CELL COMMUNICATION; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL MOVEMENT; EQUIPMENT DESIGN; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INFLAMMATION; MACROPHAGES; MICROFLUIDIC ANALYTICAL TECHNIQUES; MICROVESSELS; MONOCYTES; NEOPLASMS;

EID: 85043480176     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2018.03.005     Document Type: Article

References (79)

1. Hanna, R.N., et al. Patrolling monocytes control tumor metastasis to the lung., 350(6263), 2015, 985–991.
2. Brempelis, K.J., Crispe, I.N., Infiltrating monocytes in liver injury and repair. Clin. Transl. Immunol., 5(11), Nov. 2016, e113.
3. Grubczak, K., Monjuszko, M., The role of different monocyte subsets and macrophages in asthma pathogenesis. Prog Heal. Sci 5:1 (2015), 176–184.
4. Ginhoux, F., Jung, S., Monocytes and macrophages: developmental pathways and tissue homeostasis. Nat. Rev. Immunol. 14:6 (Jun. 2014), 392–404.
5. Yang, J., Zhang, L., Yu, C., Yang, X.-F., Wang, H., Monocyte and macrophage differentiation: circulation inflammatory monocyte as biomarker for inflammatory diseases. Biomark. Res., 2(1), 2014, 1.
6. Gordon, S., Taylor, P.R., Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5:12 (Dec. 2005), 953–964.
7. Patel, A.A., et al. The fate and lifespan of human monocyte subsets in steady state and systemic inflammation. J. Exp. Med. 214:7 (Jul. 2017), 1913–1923.
8. Grage-Griebenow, G., Flad, H., Ernst, M., Heterogeneity of human peripheral blood monocyte subsets. J. Leukoc. Biol. 69:1 (2001), 11–20.
9. Carlin, L.M., et al. Nr4a1-dependent Ly6Clow monocytes monitor endothelial cells and orchestrate their disposal. Cell 153:2 (2013), 362–375.
10. Fesnak, A.D., June, C.H., Levine, B.L., Engineered T cells: the promise and challenges of cancer immunotherapy. Nat. Rev. Cancer 16:9 (Aug. 2016), 566–581.
11. Mantovani, A., Vecchi, A., Allavena, P., Pharmacological modulation of monocytes and macrophages. Curr. Opin. Pharmacol. 17:1 (2014), 38–44.
12. Kitamura, T., Qian, B.-Z., Pollard, J.W., Immune cell promotion of metastasis. Nat. Rev. Immunol. 15:2 (2015), 73–86.
13. Wyckoff, J.B., Jones, J.G., Condeelis, J.S., Segall, J.E., A critical step in metastasis: in vivo analysis of intravasation at the primary tumor. Cancer Res 60:9 (2000), 2504–2511.
14. Condeelis, J., Pollard, J.W., “Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 124:2 (Jan. 2006), 263–266.
15. Qian, B., et al. A distinct macrophage population mediates metastatic breast cancer cell extravasation, establishment and growth. PLoS One, 4(8), Jan. 2009, e6562.
16. Wyckoff, J., et al. A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Res. 64:19 (Oct. 2004), 7022–7029.
17. Qian, B.-Z., Pollard, J.W., Macrophage diversity enhances tumor progression and metastasis. Cell 141:1 (Apr. 2010), 39–51.
18. Kitamura, T., et al. CCL2-induced chemokine cascade promotes breast cancer metastasis by enhancing retention of metastasis-associated macrophages. J. Exp. Med. 212:7 (2015), 1043–1059.
19. Chen, Q., Zhang, X.H.-F., Massagué, J., Macrophage binding to receptor VCAM-1 transmits survival signals in breast cancer cells that invade the lungs. Canc. Cell 20:4 (Oct. 2011), 538–549.
20. Qian, B.-Z., et al. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 475:7355, (Jul. 2011), 222–225.
21. Butler, K.L., Clancy-Thompson, E., Mullins, D.W., CXCR3+ monocytes/macrophages are required for establishment of pulmonary metastases. Sci. Rep., 7, Mar. 2017, 45593.
22. Sahai, E., Illuminating the metastatic process. Nat. Rev. Cancer 7:10 (Oct. 2007), 737–749.
23. Boussommier-calleja, A., Li, R., Chen, M.B., Wong, S.C., Kamm, R.D., Microfluidics: a new tool for modeling cancer – immune interactions. Trends Cancer 2:1 (2016), 6–19.
24. Whitesides, G.M., “The origins and the future of microfluidics. Nature 442:7101 (2006), 368–373.
25. Junkin, M., Tay, S., Microfluidic single-cell analysis for systems immunology. Lab a Chip 14:7 (2014), 1246–1260.
26. Whisler, J.A., Chen, M.B., Kamm, R.D., Control of perfusable microvascular network morphology using a multiculture microfluidic system. Tissue Eng. Part C Methods 20:7 (Jul. 2014), 543–552.
27. Yeon, J.H., Ryu, H.R., Chung, M., Hu, Q.P., Jeon, N.L., In vitro formation and characterization of a perfusable three-dimensional tubular capillary network in microfluidic devices. Lab a Chip 12:16 (Aug. 2012), 2815–2822.
28. Chen, M.B., Whisler, J.A., Fröse, J., Yu, C., Shin, Y., Kamm, R.D., On-chip human microvasculature assay for visualization and quantification of tumor cell extravasation dynamics. Nat. Protoc. 12:5 (2017), 865–880.
29. Carrion, B., Janson, I.A., Kong, Y.P., Putnam, A.J., A safe and efficient method to retrieve mesenchymal stem cells from three-dimensional fibrin gels. Tissue Eng. Part C Methods 20:3 (Mar. 2014), 252–263.
30. Kim, S., Lee, H., Chung, M., Jeon, N.L., “Engineering of functional, perfusable 3D microvascular networks on a chip. Lab. Chip. 13:8 (2013), 1489–1500.
31. Silzle, T., Kreutz, M., Dobler, M.A., Brockhoff, G., Knuechel, R., Kunz-Schughart, L.A., “Tumor-associated fibroblasts recruit blood monocytes into tumor tissue. Eur. J. Immunol. 33:5 (2003), 1311–1320.
32. Shi, C., Pamer, E.G., “Monocyte recruitment during infection and inflammation. Nat. Rev. Immunol. 11:11 (2011), 762–774.
33. Stroka, K.M., Hayenga, H.N., Aranda-Espinoza, H., Human neutrophil cytoskeletal dynamics and contractility actively contribute to trans-endothelial migration. PLoS One, 8(no. 4), 2013.
34. Chan, C.J., et al. Myosin II activity softens cells in suspension. Biophys. J. 108:8 (2015), 1856–1869.
35. Hind, L.E., Dembo, M., Hammer, D.A., Macrophage motility is driven by frontal-towing with a force magnitude dependent on substrate stiffness. Integr. Biol. Camb. 7:4 (Apr. 2015), 447–453.
36. Jacobelli, J., et al. Confinement-optimized three-dimensional T cell amoeboid motility is modulated via myosin IIA–regulated adhesions. Nat. Immunol. 11:10 (Oct. 2010), 953–961.
37. Chen, M.B., Whisler, J.A., Jeon, J.S., Kamm, R.D., Mechanisms of tumor cell extravasation in an in vitro microvascular network platform. Integr. Biol. Camb 5:10 (Oct. 2013), 1262–1271.
38. Waugh, D.J.J., Wilson, C., The interleukin-8 pathway in cancer. Clin. Cancer Res. 14:21 (Nov. 2008), 6735–6741.
39. Lian, S., et al. Elevated expression of growth-regulated oncogene-alpha in tumor and stromal cells predicts unfavorable prognosis in pancreatic cancer. Med. Baltimore., 95(30), Jul. 2016, e4328.
40. Desurmont, T., et al. Overexpression of chemokine receptor CXCR2 and ligand CXCL7 in liver metastases from colon cancer is correlated to shorter disease-free and overall survival. Cancer Sci. 106:3 (Mar. 2015), 262–269.
41. Jin, L., et al. CCL24 contributes to HCC malignancy via RhoB- VEGFA-VEGFR2 angiogenesis pathway and indicates poor prognosis. Oncotarget 8:3 (Jan. 2017), 402–406.
42. Auffray, C., et al. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior., 317(August), 2007, 666–671.
43. Wyckoff, J.B., et al. Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. Cancer Res. 67:6 (Mar. 2007), 2649–2656.
44. Schenkel, A.R., Mamdouh, Z., Muller, W.A., Locomotion of monocytes on endothelium is a critical step during extravasation. Nat. Immunol. 5:4 (2004), 393–400.
45. Schenkel, A.R., Mamdouh, Z., Chen, X., Liebman, R.M., Muller, W.A., CD99 plays a major role in the migration of monocytes through endothelial junctions. Nat. Immunol. 3:2 (Feb. 2002), 143–150.
46. Haase, K., Kamm, R.D., Advances in on-chip vascularization. Regen. Med. 12:3 (Apr. 2017), 285–302.
47. Collison, J.L., Carlin, L.M., Eichmann, M., Geissmann, F., Peakman, M., Heterogeneity in the locomotory behavior of human monocyte subsets over human vascular endothelium in vitro. J. Immunol. 195:3 (2015), 1162–1170.
48. Gerhardt, T., Ley, K., Monocyte trafficking across the vessel wall. Cardiovasc. Res. 107:3 (2015), 321–330.
49. Cros, J., et al. Human CD14dim monocytes patrol and sense nucleic acids and viruses via TLR7 and TLR8 receptors. Immunity 33:3 (2010), 375–386.
50. Tsou, C.-L., et al. Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J. Clin. Invest. 117:4 (Apr. 2007), 902–909.
51. Thomas, G., Tacke, R., Hedrick, C.C., Hanna, R.N., Nonclassical patrolling monocyte function in the vasculature. Arterioscler. Thromb. Vasc. Biol. 35:6 (2015), 1306–1316.
52. Jacobelli, J., Estin Matthews, M., Chen, S., Krummel, M.F., Activated T cell trans-endothelial migration relies on myosin-IIA contractility for squeezing the cell nucleus through endothelial cell barriers. PLoS One 8:9 (2013), 1–13.
53. Si, J., Ge, Y., Zhuang, S., Gong, R., Inhibiting nonmuscle myosin II impedes inflammatory infiltration and ameliorates progressive renal disease. Lab. Invest. 90:3 (2010), 448–458.
54. Bzymek, R., et al. Real-time two- and three-dimensional imaging of monocyte motility and navigation on planar surfaces and in collagen matrices: roles of Rho. Sci. Rep., 6(February), 2016, 25016.
55. Barros, M.H.M., Hauck, F., Dreyer, J.H., Kempkes, B., Niedobitek, G., Macrophage polarisation: an immunohistochemical approach for identifying M1 and M2 macrophages. PLoS One, 8(11), Nov. 2013 e80908.
56. Williams, M.R., Sakurai, Y., Zughaier, S.M., Eskin, S.G., McIntire, L.V., Transmigration across activated endothelium induces transcriptional changes, inhibits apoptosis, and decreases antimicrobial protein expression in human monocytes. J. Leukoc. Biol. 86:6 (Dec. 2009), 1331–1343.
57. Ghavampour, S., Lange, C., Bottino, C., Gerke, V., Transcriptional profiling of human monocytes identifies the inhibitory receptor CD300a as regulator of transendothelial migration. PLoS One, 8(9), 2013.
58. Italiani, P., Boraschi, D., From monocytes to m1/m2 macrophages: phenotypical vs. Functional differentiation. Front. Immunol., 5, Oct. 2014.
59. He, H., et al. Endothelial cells provide an instructive niche for the differentiation and functional polarization of M2-like macrophages. Blood 120:15 (Oct. 2012), 3152–3162.
60. Sánchez-Martín, L., Estecha, A., Samaniego, R., Sánchez-Ramón, S., Vega, M.Á., Sánchez-Mateos, P., The chemokine CXCL12 regulates monocyte-macrophage differentiation and RUNX3 expression. Blood 117:1 (2011), 88–97.
61. Previtera, M.L., Sengupta, A., Substrate stiffness regulates proinflammatory mediator production through TLR4 activity in macrophages. PLoS One, 10(12), Dec. 2015 e0145813.
62. McWhorter, F.Y., Wang, T., Nguyen, P., Chung, T., Liu, W.F., Modulation of macrophage phenotype by cell shape. Proc. Natl. Acad. Sci. Unit. States Am. 110:43 (2013), 17253–17258.
63. Charafe-Jauffret, E., et al. Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res 69:4 (Feb. 2009), 1302–1313.
64. Sheridan, C., et al. CD44+/CD24- breast cancer cells exhibit enhanced invasive properties: an early step necessary for metastasis. Breast Cancer Res., 8(5), 2006, R59.
65. Hiraga, T., Ito, S., Nakamura, H., Side population in MDA-MB-231 human breast cancer cells exhibits cancer stem cell-like properties without higher bone-metastatic potential. Oncol. Rep. 25:1 (Jan. 2011), 289–296.
66. Cavallaro, S., CXCR4/CXCL12 in non-small-cell lung cancer metastasis to the brain. Int. J. Mol. Sci. 14:1 (Jan. 2013), 1713–1727.
67. Sierra-Filardi, E., et al. CCL2 shapes macrophage polarization by GM-CSF and M-CSF: identification of CCL2/CCR2-dependent gene expression profile. J. Immunol. 192:8 (2014), 3858–3867.
68. Lee, Y.S., et al. Interleukin-8 and its receptor CXCR2 in the tumour microenvironment promote colon cancer growth, progression and metastasis. Br. J. Cancer 106:11 (May 2012), 1833–1841.
69. Wolf, M.J., et al. Endothelial CCR2 signaling induced by colon carcinoma cells enables extravasation via the JAK2-Stat5 and p38MAPK pathway. Canc. Cell 22:1 (Jul. 2012), 91–105.
70. Kawamata, H., Kawai, K., Kameyama, S., Johnson, M.D., Stetler-Stevenson, W.G., Oyasu, R., Over-expression of tissue inhibitor of matrix metalloproteinases (TIMP1 and TIMP2) suppresses extravasation of pulmonary metastasis of a rat bladder carcinoma. Int. J. Cancer 63:5 (1995), 680–687.
71. Koop, S., et al. Overexpression of Metalloproteinase Inhibitor in B16F10 Cells Does Not Affect Extravasation but Reduces Tumor Growth Overexpression of Metalloproteinase Inhibitor in B16F10 Cells Does Not Affect Extravasation but Reduces Tumor Growth1. 1994, 4791–4797.
72. Stoletov, K., Montel, V., Lester, R.D., Gonias, S.L., Klemke, R., High-resolution imaging of the dynamic tumor cell vascular interface in transparent zebrafish. Proc. Natl. Acad. Sci. Unit. States Am. 104:44 (Oct. 2007), 17406–17411.
73. Leong, H.S., et al. Invadopodia are required for cancer cell extravasation and are a therapeutic target for metastasis. Cell Rep. 8:5 (2014), 1558–1570.
74. Mierke, C.T., “Role of the endothelium during tumor cell metastasis: is the endothelium a barrier or a promoter for cell invasion and metastasis?. J. Biophys., 2008, 2008, 183516.
75. Mohana, T., Navin, A.V., Jamuna, S., Sakeena Sadullah, M.S., Niranjali Devaraj, S., Inhibition of differentiation of monocyte to macrophages in atherosclerosis by oligomeric proanthocyanidins -In-vivo and in-vitro study. Food Chem. Toxicol. 82 (Aug. 2015), 96–105.
76. Weiss, R., et al. Nicotinamide: a vitamin able to shift macrophage differentiation toward macrophages with restricted inflammatory features. Innate Immun. 21:8 (Nov. 2015), 813–826.
77. Dijkgraaf, E.M., et al. Chemotherapy alters monocyte differentiation to favor generation of cancer-supporting M2 macrophages in the tumor microenvironment. Cancer Res 73:8 (Apr. 2013), 2480–2492.
78. Kral, J.B., Schrottmaier, W.C., Salzmann, M., Assinger, A., Platelet interaction with innate immune cells. Transfus. Med. Hemotherapy 43:2 (Mar. 2016), 78–88.
79. Labelle, M., Begum, S., Hynes, R.O., Platelets guide the formation of early metastatic niches. Proc. Natl. Acad. Sci. U. S. A. 111:30 (2014), 3053–3061.