3D functional and perfusable microvascular networks for organotypic microfluidic models

Journal of Materials Science: Materials in Medicine

Volumn 26, Issue 5, 2015, Pages

  Bersini, Simone ^a   Moretti, Matteo ^a  

^a IRCCS ISTITUTO ORTOPEDICO GALEAZZI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD VESSELS; COMPLEX NETWORKS; DISEASES; MICROFLUIDICS; PATHOLOGY; PHYSIOLOGY; TUMORS;

CANCER METASTASIS; CAPILLARY NETWORK; MICRO ARCHITECTURES; MICROENVIRONMENTS; MICROVASCULAR NETWORK; MOLECULAR PATHWAYS; MULTISTEP PROCESS; PERSONALIZED MEDICINES;

PHYSIOLOGICAL MODELS;

ANTIBODY SPECIFICITY; ARTICLE; CANCER MODEL; CAPILLARY FLOW; CELL ADHESION; CELL MIGRATION; CELL VIABILITY; EXTRAVASATION; HUMAN; IN VITRO STUDY; METASTASIS; MICROFLUIDICS; MICROVASCULARIZATION; MICROVASCULATURE; PRIORITY JOURNAL; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; CAPILLARY; CELL CULTURE; ENDOTHELIUM CELL; LAB ON A CHIP; MALE; NEOVASCULARIZATION (PATHOLOGY); ORGANOGENESIS; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; THREE DIMENSIONAL PRINTING;

CAPILLARIES; CELLS, CULTURED; ENDOTHELIAL CELLS; HUMANS; LAB-ON-A-CHIP DEVICES; MALE; MICROVESSELS; NEOPLASM METASTASIS; NEOVASCULARIZATION, PATHOLOGIC; ORGANOGENESIS; PRINTING, THREE-DIMENSIONAL;

EID: 84928412002     PISSN: 09574530     EISSN: 15734838     Source Type: Journal    
DOI: 10.1007/s10856-015-5520-5     Document Type: Article

References (80)

1. International Agency for Research on Cancer. GLOBOCAN 2012: estimated Cancer Incidence, Mortality and Prevalence Worldwide in 2012. http://globocan.iarc.fr/Pages/fact_sheets_cancer.aspx.
2. Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science. 2011;331:1559–64.
3. Leung CT, Brugge JS. Outgrowth of single oncogene-expressing cells from suppressive epithelial environments. Nature. 2012;482:410–3.
4. Kaplon J, Zheng L, Meissl K, Chaneton B, Selivanov VA, Mackay G, et al. A key role for mitochondrial gatekeeper pyruvate dehydrogenase in oncogene-induced senescence. Nature. 2013;498:109–12.
5. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000;100:57–70.
6. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646–74.
7. Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat Rev Cancer. 2009;9:239–52.
8. Valastyan S, Weinberg RA. Tumor metastasis: molecular insights and evolving paradigms. Cell. 2011;147:275–92.
9. Cao Y. Opinion: emerging mechanisms of tumour lymphangiogenesis and lymphatic metastasis. Nat Rev Cancer. 2005;5:735–43.
10. Stacker SA, Achen MG, Jussila L, Baldwin ME, Alitalo K. Lymphangiogenesis and cancer metastasis. Nat Rev Cancer. 2002;2:573–83.
11. Chambers AF, Groom AC, MacDonald IC. Dissemination and growth of cancer cells in metastatic sites. Nat Rev Cancer. 2002;2:563–72.
12. Paget S. The distribution of secondary growths in cancer of the breast. Cancer Metastasis Rev. 1989;8:98–101.
13. Fidler IJ. The pathogenesis of cancer metastasis: the ‘seed and soil’ hypothesis revisited. Nat Rev Cancer. 2003;3:453–8.
14. Bos PD, Zhang XH, Nadal C, Shu W, Gomis RR, Nguyen DX, et al. Genes that mediate breast cancer metastasis to the brain. Nature. 2009;459:1005–9.
15. Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, Giri DD, et al. Genes that mediate breast cancer metastasis to lung. Nature. 2005;436:518–24.
16. Crissman JD, Hatfield JS, Menter DG, Sloane B, Honn KV. Morphological study of the interaction of intravascular tumor cells with endothelial cells and subendothelial matrix. Cancer Res. 1988;48:4065–72.
17. Miles FL, Pruitt FL, van Golen KL, Cooper CR. Stepping out of the flow: capillary extravasation in cancer metastasis. Clin Exp Metastasis. 2008;25:305–24.
18. Fukuda M, Hiraoka N, Yeh JC. C-type lectins and sialyl Lewis X oligosaccharides. Versatile roles in cell-cell interaction. J Cell Biol. 1999;147:467–70.
19. Khatib AM, Auguste P, Fallavollita L, Wang N, Samani A, Kontogiannea M, et al. Characterization of the host proinflammatory response to tumor cells during the initial stages of liver metastasis. Am J Pathol. 2005;167:749–59.
20. Reymond N, Borda d’Agua B, Ridley AJ. Crossing the endothelial barrier during metastasis. Nat Rev Cancer. 2013;13:858–70.
21. Shibue T, Brooks MW, Weinberg RA. An integrin-linked machinery of cytoskeletal regulation that enables experimental tumor initiation and metastatic colonization. Cancer Cell. 2013;24(4):481–98.
22. Giancotti FG. Mechanisms governing metastatic dormancy and reactivation. Cell. 2013;155:15.
23. Kuperwasser C, Dessain S, Bierbaum BE, Garnet D, Sperandio K, Gauvin GP, et al. A mouse model of human breast cancer metastasis to human bone. Cancer Res. 2005;65:6130–8.
24. Stoletov K, Kato H, Zardouzian E, Kelber J, Yang J, Shattil S, et al. Visualizing extravasation dynamics of metastatic tumor cells. J Cell Sci. 2010;123:2332–41.
25. Hendrix MJ, Seftor EA, Seftor RE, Fidler IJ. A simple quantitative assay for studying the invasive potential of high and low human metastatic variants. Cancer Lett. 1987;38:137–47.
26. Sagnella SM, Kligman F, Anderson EH, King JE, Murugesan G, Marchant RE, et al. Human microvascular endothelial cell growth and migration on biomimetic surfactant polymers. Biomaterials. 2004;25:1249–59.
27. Shin Y, Han S, Jeon JS, Yamamoto K, Zervantonakis IK, Sudo R, et al. Microfluidic assay for simultaneous culture of multiple cell types on surfaces or within hydrogels. Nat Protoc. 2012;7:1247–59.
28. Chaw KC, Manimaran M, Tay EH, Swaminathan S. Multi-step microfluidic device for studying cancer metastasis. Lab Chip. 2007;7:1041–7.
29. Jeon JS, Zervantonakis IK, Chung S, Kamm RD, Charest JL. In vitro model of tumor cell extravasation. PLoS One. 2013;8:e56910.
30. Zhang Q, Liu T, Qin J. A microfluidic-based device for study of transendothelial invasion of tumor aggregates in realtime. Lab Chip. 2012;12:2837–42.
31. Gout S, Tremblay PL, Huot J. Selectins and selectin ligands in extravasation of cancer cells and organ selectivity of metastasis. Clin Exp Metastasis. 2008;25:335–44.
32. Jain RK. Molecular regulation of vessel maturation. Nat Med. 2003;9:685–93.
33. Yancopoulos GD, Davis S, Gale NW, Rudge JS, Wiegand SJ, Holash J. Vascular-specific growth factors and blood vessel formation. Nature. 2000;407:242–8.
34. Olofsson B, Jeltsch M, Eriksson U, Alitalo K. Current biology of VEGF-B and VEGF-C. Curr Opin Biotechnol. 1999;10:528–35.
35. Lee HJ, Cho CH, Hwang SJ, Choi HH, Kim KT, Ahn SY, et al. Biological characterization of angiopoietin-3 and angiopoietin-4. FASEB J. 2004;18:1200–8.
36. Gohongi T, Fukumura D, Boucher Y, Yun CO, Soff GA, Compton C, et al. Tumor-host interactions in the gallbladder suppress distal angiogenesis and tumor growth: involvement of transforming growth factor beta1. Nat Med. 1999;5:1203–8.
37. Pepper MS. Transforming growth factor-beta: vasculogenesis, angiogenesis, and vessel wall integrity. Cytokine Growth Factor Rev. 1997;8:21–43.
38. Armulik A, Abramsson A, Betsholtz C. Endothelial/pericyte interactions. Circ Res. 2005;97:512–23.
39. Goerke SM, Plaha J, Hager S, Strassburg S, Torio-Padron N, Stark GB, et al. Human endothelial progenitor cells induce extracellular signal-regulated kinase-dependent differentiation of mesenchymal stem cells into smooth muscle cells upon cocultivation. Tissue Eng Part A. 2012;18:2395–405.
40. Guo X, Stice SL, Boyd NL, Chen SY. A novel in vitro model system for smooth muscle differentiation from human embryonic stem cell-derived mesenchymal cells. Am J Physiol Cell Physiol. 2013;304:C289–98.
41. Gavard J, Gutkind JS. VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin. Nat Cell Biol. 2006;8:1223–34.
42. Griffith LG, Swartz MA. Capturing complex 3D tissue physiology in vitro. Nat Rev Mol Cell Biol. 2006;7:211–24.
43. Schwartz MA, Chen CS. Cell biology. Deconstructing dimensionality. Science. 2013;339:402–4.
44. McLeod C, Higgins J, Miroshnikova Y, Liu R, Garrett A, Sarang-Sieminski AL. Microscopic matrix remodeling precedes endothelial morphological changes during capillary morphogenesis. J Biomech Eng. 2013;135:71002.
45. Helm CL, Zisch A, Swartz MA. Engineered blood and lymphatic capillaries in 3-D VEGF-fibrin-collagen matrices with interstitial flow. Biotechnol Bioeng. 2007;96:167–76.
46. Ng CP, Helm CL, Swartz MA. Interstitial flow differentially stimulates blood and lymphatic endothelial cell morphogenesis in vitro. Microvasc Res. 2004;68:258–64.
47. Miteva DO, Rutkowski JM, Dixon JB, Kilarski W, Shields JD, Swartz MA. Transmural flow modulates cell and fluid transport functions of lymphatic endothelium. Circ Res. 2010;106:920–31.
48. Bischel LL, Young EW, Mader BR, Beebe DJ. Tubeless microfluidic angiogenesis assay with three-dimensional endothelial-lined microvessels. Biomaterials. 2013;34:1471–7.
49. Vickerman V, Kamm RD. Mechanism of a flow-gated angiogenesis switch: early signaling events at cell-matrix and cell-cell junctions. Integr Biol (Camb). 2012;4:863–74.
50. Song JW, Bazou D, Munn LL. Anastomosis of endothelial sprouts forms new vessels in a tissue analogue of angiogenesis. Integr Biol (Camb). 2012;4:857–62.
51. Yeon JH, Ryu HR, Chung M, Hu QP, Jeon NL. In vitro formation and characterization of a perfusable three-dimensional tubular capillary network in microfluidic devices. Lab Chip. 2012;12:2815–22.
52. Golden AP, Tien J. Fabrication of microfluidic hydrogels using molded gelatin as a sacrificial element. Lab Chip. 2007;7:720–5.
53. Wang XY, Jin ZH, Gan BW, Lv SW, Xie M, Huang WH. Engineering interconnected 3D vascular networks in hydrogels using molded sodium alginate lattice as the sacrificial template. Lab Chip. 2014;14:2709–16.
54. Zheng Y, Chen J, Craven M, Choi NW, Totorica S, Diaz-Santana A, et al. In vitro microvessels for the study of angiogenesis and thrombosis. Proc Natl Acad Sci USA. 2012;109:9342–7.
55. Hsu YH, Moya ML, Hughes CC, George SC, Lee AP. A microfluidic platform for generating large-scale nearly identical human microphysiological vascularized tissue arrays. Lab Chip. 2013;13:2990–8.
56. Kim S, Lee H, Chung M, Jeon NL. Engineering of functional, perfusable 3D microvascular networks on a chip. Lab Chip. 2013;13:1489–500.
57. Whisler JA, Chen MB, Kamm RD. Control of perfusable microvascular network morphology using a multiculture microfluidic system. Tissue Eng Part C Methods. 2014;20:543–52.
58. Jeon JS, Bersini S, Whisler JA, Chen MB, Dubini G, Charest JL, et al. Generation of 3D functional microvascular networks with human mesenchymal stem cells in microfluidic systems. Integr Biol (Camb). 2014;6:555–63.
59. Shin MK, Kim SK, Jung H. Integration of intra- and extravasation in one cell-based microfluidic chip for the study of cancer metastasis. Lab Chip. 2011;11:3880–7.
60. Song JW, Cavnar SP, Walker AC, Luker KE, Gupta M, Tung YC, et al. Microfluidic endothelium for studying the intravascular adhesion of metastatic breast cancer cells. PLoS One. 2009;4:e5756.
61. Bersini S, Jeon JS, Dubini G, Arrigoni C, Chung S, Charest JL, et al. A microfluidic 3D in vitro model for specificity of breast cancer metastasis to bone. Biomaterials. 2014;35:2454–61.
62. Bhatia SN, Ingber DE. Microfluidic organs-on-chips. Nat Biotechnol. 2014;32:760–72.
63. Shin Y, Yang K, Han S, Park HJ, Seok Heo Y, Cho SW, et al. Reconstituting vascular microenvironment of neural stem cell niche in three-dimensional extracellular matrix. Adv Healthc Mater. 2014;3:1457–64.
64. Huh D, Leslie DC, Matthews BD, Fraser JP, Jurek S, Hamilton GA, et al. A human disease model of drug toxicity-induced pulmonary edema in a lung-on-a-chip microdevice. Sci Transl Med. 2012;4:159.
65. Torisawa YS, Spina CS, Mammoto T, Mammoto A, Weaver JC, Tat T, et al. Bone marrow-on-a-chip replicates hematopoietic niche physiology in vitro. Nat Methods. 2014;11:663–9.
66. Lee PJ, Hung PJ, Lee LP. An artificial liver sinusoid with a microfluidic endothelial-like barrier for primary hepatocyte culture. Biotechnol Bioeng. 2007;97:1340–6.
67. Li CY, Stevens KR, Schwartz RE, Alejandro BS, Huang JH, Bhatia SN. Micropatterned cell-cell interactions enable functional encapsulation of primary hepatocytes in hydrogel microtissues. Tissue Eng Part A. 2014;20:2200–12.
68. Jang KJ, Mehr AP, Hamilton GA, McPartlin LA, Chung S, Suh KY, et al. Human kidney proximal tubule-on-a-chip for drug transport and nephrotoxicity assessment. Integr Biol (Camb). 2013;5:1119–29.
69. Kim HJ, Huh D, Hamilton G, Ingber DE. Human gut-on-a-chip inhabited by microbial flora that experiences intestinal peristalsis-like motions and flow. Lab Chip. 2012;12:2165–74.
70. Kim HJ, Ingber DE. Gut-on-a-Chip microenvironment induces human intestinal cells to undergo villus differentiation. Integr Biol (Camb). 2013;5:1130–40.
71. Booth R, Kim H. Characterization of a microfluidic in vitro model of the blood-brain barrier (muBBB). Lab Chip. 2012;12:1784–92.
72. Achyuta AK, Conway AJ, Crouse RB, Bannister EC, Lee RN, Katnik CP, et al. A modular approach to create a neurovascular unit-on-a-chip. Lab Chip. 2013;13:542–53.
73. Bersini S, Jeon JS, Moretti M, Kamm RD. In vitro models of the metastatic cascade: from local invasion to extravasation. Drug Discov Today. 2014;19:735–42.
74. Garcia-Roman J, Zentella-Dehesa A. Vascular permeability changes involved in tumor metastasis. Cancer Lett. 2013;335:259–69.
75. Mierke CT. Cancer cells regulate biomechanical properties of human microvascular endothelial cells. J Biol Chem. 2011;286:40025–37.
76. Weis S, Cui J, Barnes L, Cheresh D. Endothelial barrier disruption by VEGF-mediated Src activity potentiates tumor cell extravasation and metastasis. J Cell Biol. 2004;167:223–9.
77. Jeon JS, Bersini S, Gilardi M, Dubini G, Charest JL, Moretti M, et al. Human 3D vascularized organotypic microfluidic assays to study breast cancer cell extravasation. Proc Natl Acad Sci USA. 2015;112:214–9.
78. Sung JH, Shuler ML. A micro cell culture analog (microCCA) with 3-D hydrogel culture of multiple cell lines to assess metabolism-dependent cytotoxicity of anti-cancer drugs. Lab Chip. 2009;9:1385–94.
79. Tatosian DA, Shuler ML. A novel system for evaluation of drug mixtures for potential efficacy in treating multidrug resistant cancers. Biotechnol Bioeng. 2009;103:187–98.
80. Chu X, Bleasby K, Evers R. Species differences in drug transporters and implications for translating preclinical findings to humans. Expert Opin Drug Metab Toxicol. 2013;9:237–52.