Three-dimensional biomimetic model to reconstitute sprouting lymphangiogenesis in vitro

Biomaterials

Volumn 78, Issue , 2016, Pages 115-128

  Kim, Sudong ^a   Chung, Minhwan ^a   Jeon, Noo Li ^a  

^a Seoul National University   (South Korea)

Author keywords

3D in vitro model; Interstitial flow; Lymphangiogenesis; Microfluidics; Tumor microenvironment

Indexed keywords

BIOMIMETICS; DIAGNOSIS; ENDOTHELIAL CELLS; ENZYME ACTIVITY; PATHOLOGY; TUMORS;

ENVIRONMENTAL FACTORS; EXTRACELLULAR MATRICES; IN-VITRO MODELS; INTERSTITIAL FLOW; LYMPHANGIOGENESIS; MICROFLUIDIC PLATFORMS; MOLECULAR SIGNATURES; TUMOR MICROENVIRONMENT;

MICROFLUIDICS;

MITOGEN ACTIVATED PROTEIN KINASE;

BIOLOGICAL MODEL; BIOMIMETICS; CELL PROLIFERATION; ENZYME ACTIVATION; HUMAN; IN VITRO STUDY; LYMPHANGIOGENESIS; METABOLISM; MICROFLUIDICS;

BIOMIMETICS; CELL PROLIFERATION; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; IN VITRO TECHNIQUES; LYMPHANGIOGENESIS; MICROFLUIDICS; MODELS, BIOLOGICAL;

EID: 84949961394     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.11.019     Document Type: Article

References (72)

1. Alitalo K., Tammela T., Petrova T.V. Lymphangiogenesis in development and human disease. Nature 2005, 438:946-953.
2. Tammela T., Alitalo K. Lymphangiogenesis: molecular mechanisms and future promise. Cell 2010, 140:460-476.
3. Cao R., Ji H., Feng N., Zhang Y., Yang X., Andersson P., et al. Collaborative interplay between FGF-2 and VEGF-C promotes lymphangiogenesis and metastasis. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:15894-15899.
4. Bruyère F., Noël A. Lymphangiogenesis: in vitro and in vivo models. FASEB J. 2010, 24:8-21.
5. Bruyère F., Melen-Lamalle L., Blacher S., Roland G., Thiry M., Moons L., et al. Modeling lymphangiogenesis in a three-dimensional culture system. Nat. Methods 2008, 5:431-437.
6. Cao R., Lim S., Ji H., Zhang Y., Yang Y., Honek J., et al. Mouse corneal lymphangiogenesis model. Nat. Protoc. 2011, 6:817-826.
7. Swartz M.A., Lund A.W. Lymphatic and interstitial flow in the tumour microenvironment: linking mechanobiology with immunity. Nat. Rev. Cancer 2012, 12:210-219.
8. Hoshida T., Isaka N., Hagendoorn J., di Tomaso E., Chen Y.-L., Pytowski B., et al. Imaging steps of lymphatic metastasis reveals that vascular endothelial growth factor-C increases metastasis by increasing delivery of cancer cells to lymph nodes: therapeutic implications. Cancer Res. 2006, 66:8065-8075.
9. Harrell M.I., Iritani B.M., Ruddell A. Tumor-induced sentinel lymph node lymphangiogenesis and increased lymph flow precede melanoma metastasis. Am. J. Pathol. 2007, 170:774-786.
10. Rofstad E.K., Galappathi K., Mathiesen B.S. Tumor interstitial fluid pressure-a link between tumor hypoxia, microvascular density, and lymph node metastasis. Neoplasia 2014, 16:586-594.
11. Boardman K.C., Swartz M.A. Interstitial flow as a guide for lymphangiogenesis. Circ. Res. 2003, 92:801-808.
12. Goldman J., Conley K.A., Raehl A., Bondy D.M., Pytowski B., Swartz M.A., et al. Regulation of lymphatic capillary regeneration by interstitial flow in skin. Am. J. Physiol. Heart Circ. Physiol. 2007, 292:H2176-H2183.
13. Helm C.-L.E., Fleury M.E., Zisch A.H., Boschetti F., Swartz M.A. Synergy between interstitial flow and VEGF directs capillary morphogenesis in vitro through a gradient amplification mechanism. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:15779-15784.
14. Miteva D.O., Rutkowski J.M., Dixon J.B., Kilarski W., Shields J.D., Swartz M.A. Transmural flow modulates cell and fluid transport functions of lymphatic endothelium. Circ. Res. 2010, 106:920-931.
15. Shin J.W., Huggenberger R., Detmar M. Transcriptional profiling of VEGF-A and VEGF-C target genes in lymphatic endothelium reveals endothelial-specific molecule-1 as a novel mediator of lymphangiogenesis. Blood 2008, 112:2318-2326.
16. Chary S.R., Jain R.K. Direct measurement of interstitial convection and diffusion of albumin in normal and neoplastic tissues by fluorescence photobleaching. Proc. Natl. Acad. Sci. U. S. A. 1989, 86:5385-5389.
17. Munson J.M., Shieh A., Munson J.M., Shieh A.C. Interstitial fluid flow in cancer: implications for disease progression and treatment. Cancer Manag. Res. 2014, 6:317-328.
18. Kim S., Lee H., Chung M., Jeon N.L. Engineering of functional, perfusable 3D microvascular networks on a chip. Lab. Chip 2013, 13:1489-1500.
19. Fukumura D., Jain R.K. Tumor microenvironment abnormalities: causes, consequences, and strategies to normalize. J. Cell Biochem. 2007, 101:937-949.
20. Kalluri R., Zeisberg M. Fibroblasts in cancer. Nat. Rev. Cancer 2006, 6:392-401.
21. Chyou S., Ekland E.H., Carpenter A.C., Tzeng T.-C.J., Tian S., Michaud M., et al. Fibroblast-type reticular stromal cells regulate the lymph node vasculature. J. Immunol. 2008, 181:3887-3896.
22. Marino D., Luginbühl J., Scola S., Meuli M., Reichmann E. Bioengineering dermo-epidermal skin grafts with blood and lymphatic capillaries. Sci. Transl. Med. 2014, 6. 221ra14-ra14.
23. Zheng W., Tammela T., Yamamoto M., Anisimov A., Holopainen T., Kaijalainen S., et al. Notch restricts lymphatic vessel sprouting induced by vascular endothelial growth factor. Blood 2011, 118:1154-1162.
24. Trzewik J., Mallipattu S., Artmann G.M., Delano F., Schmid-Schönbein G.W. Evidence for a second valve system in lymphatics: endothelial microvalves. FASEB J. 2001, 15:1711-1717.
25. Mäkinen T., Veikkola T., Mustjoki S., Karpanen T., Catimel B., Nice E.C., et al. Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF-C/D receptor VEGFR-3. EMBO J. 2001, 20:4762-4773.
26. Liu N., He Q. The regulatory effects of cytokines on lymphatic angiogenesis. Lymphology 1997, 30:3-12.
27. Podgrabinska S., Braun P., Velasco P., Kloos B., Pepper M.S., Jackson D.G., et al. Molecular characterization of lymphatic endothelial cells. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:16069-16074.
28. Yoon C.M., Hong B.S., Moon H.G., Lim S., Suh P.-G., Kim Y.-K., et al. Sphingosine-1-phosphate promotes lymphangiogenesis by stimulating S1P1/Gi/PLC/Ca2+ signaling pathways. Blood 2008, 112:1129-1138.
29. Skobe M., Hawighorst T., Jackson D.G., Prevo R., Janes L., Velasco P., et al. Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nat. Med. 2001, 7:192-198.
30. Karkkainen M.J., Haiko P., Sainio K., Partanen J., Taipale J., Petrova T.V., et al. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat. Immunol. 2003, 5:74-80.
31. Chang L.K., Garcia-Cardeña G., Farnebo F., Fannon M., Chen E.J., Butterfield C., et al. Dose-dependent response of FGF-2 for lymphangiogenesis. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:11658-11663.
32. Hirakawa S., Kodama S., Kunstfeld R., Kajiya K., Brown L.F., Detmar M. VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis. J. Exp. Med. 2005, 201:1089-1099.
33. Kajiya K., Hirakawa S., Ma B., Drinnenberg I., Detmar M. Hepatocyte growth factor promotes lymphatic vessel formation and function. EMBO J. 2005, 24:2885-2895.
34. Björndahl M., Cao R., Nissen L.J., Clasper S., Johnson L.A., Xue Y., et al. Insulin-like growth factors 1 and 2 induce lymphangiogenesis in vivo. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:15593-15598.
35. Cao R., Björndahl M.A., Religa P., Clasper S., Garvin S., Galter D., et al. PDGF-BB induces intratumoral lymphangiogenesis and promotes lymphatic metastasis. Cancer Cell 2004, 6:333-345.
36. Benest A.V., Harper S.J., Herttuala S.Y., Alitalo K., Bates D.O. VEGF-C induced angiogenesis preferentially occurs at a distance from lymphangiogenesis. Cardiovasc. Res. 2008, 78:315-323.
37. Gerhardt H., Golding M., Fruttiger M., Ruhrberg C., Lundkvist A., Abramsson A., et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 2003, 161:1163-1177.
38. Baluk P., Fuxe J., Hashizume H., Romano T., Lashnits E., Butz S., et al. Functionally specialized junctions between endothelial cells of lymphatic vessels. J. Exp. Med. 2007, 204:2349-2362.
39. Pflicke H., Sixt M. Preformed portals facilitate dendritic cell entry into afferent lymphatic vessels. J. Exp. Med. 2009, 206:2925-2935.
40. Munson J.M., Bellamkonda R.V., Swartz M.A. Interstitial flow in a 3D microenvironment increases glioma invasion by a CXCR4-dependent mechanism. Cancer Res. 2013, 73:1536-1546.
41. Polacheck W.J., Charest J.L., Kamm R.D. Interstitial flow influences direction of tumor cell migration through competing mechanisms. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:11115-11120.
42. Polacheck W.J., German A.E., Mammoto A., Ingber D.E., Kamm R.D. Mechanotransduction of fluid stresses governs 3D cell migration. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:2447-2452.
43. Shieh A.C., Rozansky H.A., Hinz B., Swartz M.A. Tumor cell invasion is promoted by interstitial flow-induced matrix priming by stromal fibroblasts. Cancer Res. 2011, 71:790-800.
44. Li S., Kim M., Hu Y.-L., Jalali S., Schlaepfer D.D., Hunter T., et al. Fluid shear stress activation of focal adhesion kinase linking to mitogen-activated protein kinases. J. Biol. Chem. 1997, 272:30455-30462.
45. Birukov K.G., Jacobson J.R., Flores A.A., Ye S.Q., Birukova A.A., Verin A.D., et al. Magnitude-dependent regulation of pulmonary endothelial cell barrier function by cyclic stretch. Am. J. Physiol. Lung Cell Mol. Physiol. 2003, 285:L785-L797.
46. Paszek M.J., Zahir N., Johnson K.R., Lakins J.N., Rozenberg G.I., Gefen A., et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 2005, 8:241-254.
47. Deng Y., Atri D., Eichmann A., Simons M. Endothelial ERK signaling controls lymphatic fate specification. J. Clin. Invest 2013, 123:1202.
48. Schulz M.M.P., Reisen F., Zgraggen S., Fischer S., Yuen D., Kang G.J., et al. Phenotype-based high-content chemical library screening identifies statins as inhibitors of in vivo lymphangiogenesis. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E2665-E2674.
49. Hong Y.-K., Detmar M. Prox1, master regulator of the lymphatic vasculature phenotype. Cell Tissue Res. 2003, 314:85-92.
50. Shin K., Kataru R.P., Park H.J., Kwon B.-I., Kim T.W., Hong Y.K., et al. TH2 cells and their cytokines regulate formation and function of lymphatic vessels. Nat. Commun. 2015, 6.
51. Flister M.J., Wilber A., Hall K.L., Iwata C., Miyazono K., Nisato R.E., et al. Inflammation induces lymphangiogenesis through up-regulation of VEGFR-3 mediated by NF-κB and Prox1. Blood 2010, 115:418-429.
52. Shin J.W., Min M., Larrieu-Lahargue F., Canron X., Kunstfeld R., Nguyen L., et al. Prox1 promotes lineage-specific expression of fibroblast growth factor (FGF) receptor-3 in lymphatic endothelium: a role for FGF signaling in lymphangiogenesis. Mole Biol. Cell 2006, 17:576-584.
53. Kataru R.P., Kim H., Jang C., Choi D.K., Koh B.I., Kim M., et al. T lymphocytes negatively regulate lymph node lymphatic vessel formation. Immunity 2011, 34:96-107.
54. Mullershausen F., Zecri F., Cetin C., Billich A., Guerini D., Seuwen K. Persistent signaling induced by FTY720-phosphate is mediated by internalized S1P1 receptors. Nat. Chem. Biol. 2009, 5:428-434.
55. Jung B., Obinata H., Galvani S., Mendelson K., Ding B-s Skoura A., et al. Flow-regulated endothelial S1P receptor-1 signaling sustains vascular development. Dev. Cell 2012, 23:600-610.
56. Daniel C., Mohamad A., Masayuki W., Patrick R., Ashley J.S., Yusuf A.H., et al. Sphingosine 1-phosphate induces filopodia formation through S1PR2 activation of ERM proteins. Biochem. J. 2013, 449:661-672.
57. Song J.W., Munn L.L. Fluid forces control endothelial sprouting. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:15342-15347.
58. Galie P.A., Nguyen D.-H.T., Choi C.K., Cohen D.M., Janmey P.A., Chen C.S. Fluid shear stress threshold regulates angiogenic sprouting. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:7968-7973.
59. Ng C.P., Hinz B., Swartz M.A. Interstitial fluid flow induces myofibroblast differentiation and collagen alignment in vitro. J. Cell Sci. 2005, 118:4731-4739.
60. Shields J.D., Fleury M.E., Yong C., Tomei A.A., Randolph G.J., Swartz M.A. Autologous chemotaxis as a mechanism of tumor cell homing to lymphatics via interstitial flow and autocrine CCR7 signaling. Cancer Cell 2007, 11:526-538.
61. Planas-Paz L., Strilić B., Goedecke A., Breier G., Fässler R., Lammert E. Mechanoinduction of lymph vessel expansion. EMBO J. 2012, 31:788-804.
62. Sabine A., Agalarov Y., Maby-El Hajjami H., Jaquet M., Hägerling R., Pollmann C., et al. Mechanotransduction, PROX1, and FOXC2 cooperate to control connexin37 and calcineurin during lymphatic-valve formation. Dev. Cell 2012, 22:430-445.
63. Sabine A., Bovay E., Demir C.S., Kimura W., Jaquet M., Agalarov Y., et al. FOXC2 and fluid shear stress stabilize postnatal lymphatic vasculature. J. Clin. Invest 2015, 125:3861-3877.
64. Sweet D.T., Jiménez J.M., Chang J., Hess P.R., Mericko-Ishizuka P., Fu J., et al. Lymph flow regulates collecting lymphatic vessel maturation in vivo. J. Clin. Invest 2015, 125:2995-3007.
65. Raju B., Haug S.R., Ibrahim S.O., Heyeraas K.J. High interstitial fluid pressure in rat tongue cancer is related to increased lymph vessel area, tumor size, invasiveness and decreased body weight. J. Oral Pathol. Med. 2008, 37:137-144.
66. Hellström M., Phng L.-K., Hofmann J.J., Wallgard E., Coultas L., Lindblom P., et al. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 2007, 445:776-780.
67. Lu X., Le Noble F., Yuan L., Jiang Q., De Lafarge B., Sugiyama D., et al. The netrin receptor UNC5B mediates guidance events controlling morphogenesis of the vascular system. Nature 2004, 432:179-186.
68. Phng L.-K., Stanchi F., Gerhardt H. Filopodia are dispensable for endothelial tip cell guidance. Development 2013, 140:4031-4040.
69. Pan M.-R., Chang T.-M., Chang H.-C., Su J.-L., Wang H.-W., Hung W.-C. Sumoylation of Prox1 controls its ability to induce VEGFR3 expression and lymphatic phenotypes in endothelial cells. J. Cell Sci. 2009, 122:3358-3364.
70. Lin J., Lalani A.S., Harding T.C., Gonzalez M., Wu W.-W., Luan B., et al. Inhibition of lymphogenous metastasis using adeno-associated virus-mediated gene transfer of a soluble VEGFR-3 decoy receptor. Cancer Res. 2005, 65:6901-6909.
71. Pytowski B., Goldman J., Persaud K., Wu Y., Witte L., Hicklin D.J., et al. Complete and specific inhibition of adult lymphatic regeneration by a novel VEGFR-3 neutralizing antibody. J. Natl. Cancer Inst. 2005, 97:14-21.
72. Karpanen T., Wirzenius M., Mäkinen T., Veikkola T., Haisma H.J., Achen M.G., et al. Lymphangiogenic growth factor responsiveness is modulated by postnatal lymphatic vessel maturation. Am. J. Pathol. 2006, 169:708-718.