Lymph node biophysical remodeling is associated with melanoma lymphatic drainage

FASEB Journal

Volumn 29, Issue 11, 2015, Pages 4512-4522

  Rohner, Nathan Andrew ^a,b   McClain, Jacob ^a,b   Tuell, Sara Lydia ^a,b   Warner, Alex ^a,b   Smith, Blair ^a,b   Yun, Youngho ^a,b   Mohan, Abhinav ^a,b   Sushnitha, Manuela ^a,b   Thomas, Susan Napier ^a,b  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b EMORY UNIVERSITY   (United States)

Author keywords

Cancer; Sentinel lymph node; Tissue mechanical properties

Indexed keywords

COLLAGEN; HYALURONIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOPHYSICS; C57BL 6 MOUSE; CELL ADHESION; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE COURSE; ELASTICITY; FUNCTIONS OF THE HEMIC, LYMPHATIC AND RETICULOENDOTHELIAL SYSTEMS; IMMUNOCOMPETENCE; INOCULATION; LYMPH NODE; LYMPH NODE BIOPHYSICAL REMODELING; LYMPH NODE METASTASIS; LYMPHADENOPATHY; LYMPHATIC DRAINAGE; MELANOMA; MELANOMA B16; MOUSE; NONHUMAN; PRESSURE MEASUREMENT; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; VISCOELASTICITY; ANIMAL; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; CELL ADHESION; CELL LINE, TUMOR; CELL PROLIFERATION; LYMPH NODES; MELANOMA; MICE; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

EID: 84949035397     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.15-274761     Document Type: Article

References (87)

1. Marzo, A. L., Lake, R. A., Lo, D., Sherman, L., McWilliam, A., Nelson, D., Robinson, B. W., and Scott, B. (1999) Tumor antigens are constitutively presented in the draining lymph nodes. J. Immunol. 162, 5838-5845
2. Badwe, R.A., Thorat, M.A., and Parmar, V. V. (2003) Sentinel-node biopsy in breast cancer. N. Engl. J. Med. 349, 1968-1971
3. Veronesi, U., Paganelli, G., Viale, G., Luini, A., Zurrida, S., Galimberti, V., Intra, M., Veronesi, P., Robertson, C., Maisonneuve, P., Renne, G., De Cicco, C., De Lucia, F., and Gennari, R. (2003) A randomized comparison of sentinel-node biopsy with routine axillary dissection in breast cancer. N. Engl. J. Med. 349, 546-553
4. Phan, G. Q., Messina, J. L., Sondak, V. K., and Zager, J. S. (2009) Sentinel lymph node biopsy for melanoma: indications and rationale. Cancer Control 16, 234-239
5. Minamiya, Y., and Ogawa, J. (2006) Benefit of sentinel lymph node mapping in non-small cell lung cancer.Ann.Thorac.Cardiovasc. Surg. 12, 381-382
6. Kumar, S., and Weaver, V. M. (2009)Mechanics, malignancy, and metastasis: the force journey of a tumor cell. Cancer Metastasis Rev. 28, 113-127
7. Helmlinger, G., Netti, P. A., Lichtenbeld, H. C., Melder, R. J., and Jain, R. K. (1997) Solid stress inhibits the growth of multicellular tumor spheroids. Nat. Biotechnol. 15, 778-783
8. Stylianopoulos, T., Martin, J. D., Snuderl, M., Mpekris, F., Jain, S. R., and Jain, R. K. (2013)Coevolution of solid stress and interstitial fluid pressure in tumors during progression: implications for vascular collapse. Cancer Res. 73, 3833-3841
9. Paszek, M. J., Zahir, N., Johnson, K. R., Lakins, J.N., Rozenberg, G. I., Gefen, A., Reinhart-King, C. A., Margulies, S. S., Dembo, M., Boettiger, D., Hammer, D. A., and Weaver, V. M. (2005) Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241-254
10. Fukumura, D., Gohongi, T., Kadambi, A., Izumi, Y., Ang, J., Yun, C.O., Buerk, D. G., Huang, P. L., and Jain, R.K. (2001) Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proc. Natl. Acad. Sci. USA 98, 2604-2609
11. Gutmann, R., Leunig, M., Feyh, J., Goetz, A.E., Messmer, K., Kastenbauer, E., and Jain, R. K. (1992) Interstitial hypertension in head and neck tumors in patients: correlation with tumor size. Cancer Res. 52, 1993-1995
12. Boucher, Y., Leunig, M., and Jain, R. K. (1996) Tumor angiogenesis and interstitial hypertension. Cancer Res. 56, 4264-4266
13. Thomas, S. N., Vokali, E., Lund, A. W., Hubbell, J. A., and Swartz, M. A. (2014) Targeting the tumor-draining lymph node with adjuvanted nanoparticles reshapes the anti-tumor immune response. Biomaterials 35, 814-824
14. Thomas, S. N., and Schudel, A. (2015) Overcoming transport barriers for interstitial-, lymphatic-, and lymph node-targeted drug delivery. Curr. Opin. Chem. Eng. 7, 65-74
15. Shields, J. D., Fleury, M. E., Yong, C., Tomei, A. A., Randolph, G. J., and Swartz, M. A. (2007) Autologous chemotaxis as amechanism of tumor cell homing to lymphatics via interstitial flow and autocrine CCR7 signaling. Cancer Cell 11, 526-538
16. Shieh, A. C., Rozansky, H. A., Hinz, B., and Swartz, M. A. (2011) Tumor cell invasion is promoted by interstitial flow-induced matrix priming by stromal fibroblasts. Cancer Res. 71, 790-800
17. Barcus, C.E., Keely, P. J., Eliceiri, K.W., and Schuler, L.A. (2013) Stiffcollagenmatrices increase tumorigenic prolactin signaling in breast cancer cells. J. Biol. Chem. 288, 12722-12732
18. Lund, A.W., Duraes, F.V., Hirosue, S., Raghavan, V. R., Nembrini, C., Thomas, S. N., Issa, A., Hugues, S., and Swartz, M. A. (2012) VEGF-C promotes immunetolerance inB16melanomas and cross-presentation of tumor antigen by lymph node lymphatics. Cell Reports 1, 191-199
19. Egger, M.E., Bower, M.R., Czyszczon, I.A., Farghaly, H., Noyes, R. D., Reintgen, D. S., Martin II, R.C., Scoggins, C. R., Stromberg, A. J., and McMasters, K. M. (2014) Comparison of sentinel lymph node micrometastatic tumor burden measurements in melanoma. J. Am. Coll. Surg. 218, 519-528
20. Mu, W., Rana, S., and Zöller, M. (2013) Host matrix modulation by tumor exosomes promotes motility and invasiveness. Neoplasia 15, 875-887
21. Lu, P., Weaver, V.M., and Werb, Z. (2012) The extracellularmatrix: a dynamic niche in cancer progression. J. Cell Biol. 196, 395-406
22. Insana, M. F., Pellot-Barakat, C., Sridhar, M., and Lindfors, K. K. (2004) Viscoelastic imaging of breast tumor microenvironment with ultrasound. J. Mammary Gland Biol. Neoplasia 9, 393-404
23. Swartz, M.A., andLund, A.W. (2012)Lymphatic and interstitial flow in the tumour microenvironment: linking mechanobiology with immunity. Nat. Rev. Cancer 12, 210-219
24. DuFort, C. C., Paszek, M. J., and Weaver, V. M. (2011) Balancing forces: architectural control ofmechanotransduction. Nat. Rev.Mol. Cell Biol. 12, 308-319
25. Nathanson, S. D., Shah, R., and Rosso, K. (2015) Sentinel lymph nodemetastases in cancer: causes, detection and their role in disease progression. Semin. Cell Dev. Biol. 38, 106-116
26. Reintgen, M., Murray, L., Akman, K., Giuliano, R., Lozicki, A., Shivers, S., and Reintgen, D. (2013) Evidence for a better nodal staging system formelanoma: the clinical relevance ofmetastatic disease confined to the sentinel lymph nodes. Ann. Surg. Oncol. 20, 668-674
27. Yi, M., Meric-Bernstam, F., Ross, M. I., Akins, J. S., Hwang, R. F., Lucci, A., Kuerer, H. M., Babiera, G. V., Gilcrease, M. Z., and Hunt, K. K. (2008)Howmany sentinel lymph nodes are enough during sentinel lymph node dissection for breast cancer? Cancer 113, 30-37
28. Bobek, V., Kolostova, K., Pinterova, D., Kacprzak, G., Adamiak, J., Kolodziej, J., Boubelik, M., Kubecova, M., andHoffman, R.M. (2010) A clinically relevant, syngeneic model of spontaneous, highly metastatic B16 mouse melanoma. Anticancer Res. 30, 4799-4803
29. Winkelmann, C. T., Figueroa, S. D., Rold, T. L., Volkert, W. A., and Hoffman, T. J. (2006) Microimaging characterization of a B16-F10 melanoma metastasis mouse model. Mol. Imaging 5, 105-114
30. Yang, M., Baranov, E., Jiang, P., Sun, F.X., Li, X.M., Li, L., Hasegawa, S., Bouvet, M., Al-Tuwaijri, M., Chishima, T., Shimada, H., Moossa, A. R., Penman, S., and Hoffman, R. M. (2000) Whole-body optical imaging of green fluorescent protein-expressing tumors and metastases. Proc. Natl. Acad. Sci. USA 97, 1206-1211
31. Jung, J. I., Cho, H. J., Jung, Y. J., Kwon, S.H., Her, S., Choi, S. S., Shin, S.H., Lee, K.W., and Park, J.H. (2015)High-fat diet-induced obesity increases lymphangiogenesis and lymph node metastasis in the B16F10 melanoma allograft model: roles of adipocytes and M2-macrophages. Int. J. Cancer 136, 258-270
32. Miteva, D.O., Rutkowski, J. M., Dixon, J.B., Kilarski, W., Shields, J.D., and Swartz, M. A. (2010) Transmural flow modulates cell and fluid transport functions of lymphatic endothelium. Circ. Res. 106, 920-931
33. Weiler, M., andDixon, J. B. (2013) Differential transport function of lymphatic vessels in the rat tail model and the long-term effects of Indocyanine Green as assessed with near-infrared imaging. Front. Physiol. 4, 215
34. Thomas, S.N., van der Vlies, A. J., O'Neil, C. P., Reddy, S.T., Yu, S.S., Giorgio, T. D., Swartz, M. A., and Hubbell, J. A. (2011) Engineering complement activation on polypropylene sulfide vaccine nanoparticles. Biomaterials 32, 2194-2203
35. Thomas, S.N., Rutkowski, J.M., Pasquier, M., Kuan, E. L., Alitalo, K., Randolph, G. J., and Swartz, M. A. (2012) Impaired humoral immunity and tolerance in K14-VEGFR-3-Ig mice that lack dermal lymphatic drainage. J. Immunol. 189, 2181-2190
36. Johnson, K. L. (1985) ContactMechanics, CambridgeUniversity Press, Cambridge, NY, USA
37. Goel, S., Duda, D. G., Xu, L., Munn, L.L., Boucher, Y., Fukumura, D., and Jain, R.K. (2011)Normalization of the vasculature for treatment of cancer and other diseases. Physiol. Rev. 91, 1071-1121
38. Kornuta, J. A., and Brandon Dixon, J. (2014) Ex vivo lymphatic perfusion system for independently controlling pressure gradient and transmural pressure in isolated vessels. Ann. Biomed. Eng. 42, 1691-1704
39. Koh, Y. X., Chok, A. Y., Zheng, H., Xu, S., and Teo, M. C. (2014) Cloquet's node trumps imaging modalities in the prediction of pelvic nodal involvement in patients with lower limb melanomas in Asian patients with palpable groin nodes. Eur. J. Surg.Oncol. 40, 1263-1270
40. Bastiaannet, E., Wobbes, T., Hoekstra, O. S., van der Jagt, E. J., Brouwers, A.H., Koelemij, R., de Klerk, J.M., Oyen, W. J., Meijer, S., and Hoekstra, H. J. (2009) Prospective comparison of [18F] fluorodeoxyglucose positron emission tomography and computed tomography in patients with melanoma with palpable lymph node metastases: diagnostic accuracy and impact on treatment. J. Clin. Oncol. 27, 4774-4780
41. Maroudas, A. (1975) Biophysical chemistry of cartilaginous tissues with special reference to solute and fluid transport. Biorheology 12, 233-248
42. Fung, Y. C. (1993) Biomechanics: Mechanical Properties of Living Tissues, Springer-Verlag, New York
43. Rudrabhatla, S. R., Mahaffey, C. L., and Mummert, M. E. (2006) Tumor microenvironment modulates hyaluronan expression: the lactate effect. J. Invest. Dermatol. 126, 1378-1387
44. Dunn, M. G., and Silver, F.H. (1983) Viscoelastic behavior of human connective tissues: relative contribution of viscous and elastic components. Connect. Tissue Res. 12, 59-70
45. Faffe, D. S., and Zin, W. A. (2009) Lung parenchymal mechanics in health and disease. Physiol. Rev. 89, 759-775
46. Stylianopoulos, T., Martin, J. D., Chauhan, V. P., Jain, S. R., Diop-Frimpong, B., Bardeesy, N., Smith, B. L., Ferrone, C. R., Hornicek, F. J., Boucher, Y., Munn, L. L., and Jain, R. K. (2012) Causes, consequences, and remedies for growth-induced solid stress in murine and human tumors. Proc. Natl. Acad. Sci. USA 109, 15101-15108
47. Tanter, M., Bercoff, J., Athanasiou, A., Deffieux, T., Gennisson, J.L., Montaldo, G., Muller, M., Tardivon, A., and Fink, M. (2008) Quantitative assessment of breast lesion viscoelasticity: initial clinical results using supersonic shear imaging. Ultrasound Med. Biol. 34, 1373-1386
48. Sloothaak, D. A., Grewal, S., Doornewaard, H., van Duijvendijk, P., Tanis, P. J., Bemelman, W. A., van der Zaag, E. S., and Buskens, C. J. (2014) Lymph node size as a predictor of lymphatic staging in colonic cancer. Br. J. Surg. 101, 701-706
49. Miyaji, K., Furuse, A., Nakajima, J., Kohno, T., Ohtsuka, T., Yagyu, K., Oka, T., and Omata, S. (1997) The stiffness of lymph nodes containing lung carcinoma metastases: a new diagnostic parameter measured by a tactile sensor. Cancer 80, 1920-1925
50. Rutkowski, J. M., Moya, M., Johannes, J., Goldman, J., and Swartz, M. A. (2006) Secondary lymphedema in the mouse tail: Lymphatic hyperplasia, VEGF-C upregulation, and the protective role ofMMP-9. Microvasc. Res. 72, 161-171
51. Rutkowski, J. M., Markhus, C. E., Gyenge, C.C., Alitalo, K., Wiig, H., and Swartz, M. A. (2010) Dermal collagen and lipid deposition correlate with tissue swelling and hydraulic conductivity in murine primary lymphedema. Am. J. Pathol. 176, 1122-1129
52. Shieh, A. C. (2011) Biomechanical forces shape the tumor microenvironment. Ann. Biomed. Eng. 39, 1379-1389
53. Aukland, K., and Reed, R. K. (1993) Interstitial-lymphatic mechanisms in the control of extracellular fluid volume. Physiol. Rev. 73, 1-78
54. Miserocchi, G., Negrini, D., Passi, A., and De Luca, G. (2001) Development of lung edema: interstitial fluid dynamics and molecular structure. News Physiol. Sci. 16, 66-71
55. Wiig, H., Rubin, K., and Reed, R.K. (2003)New and active role of the interstitium in control of interstitial fluid pressure: potential therapeutic consequences. Acta Anaesthesiol. Scand. 47, 111-121
56. Korhonen, R. K., Laasanen, M. S., Töyräs, J., Lappalainen, R., Helminen, H. J., and Jurvelin, J. S. (2003) Fibril reinforced poroelastic model predicts specifically mechanical behavior of normal, proteoglycan depleted and collagen degraded articular cartilage. J. Biomech. 36, 1373-1379
57. Hautmann, S. H., Lokeshwar, V. B., Schroeder, G. L., Civantos, F., Duncan, R.C., Gnann, R., Friedrich, M.G., andSoloway, M. S. (2001) Elevated tissue expression of hyaluronic acid and hyaluronidase validates the HA-HAase urine test for bladder cancer. J. Urol. 165, 2068-2074
58. Lokeshwar, V. B., Rubinowicz, D., Schroeder, G. L., Forgacs, E., Minna, J. D., Block, N. L., Nadji, M., and Lokeshwar, B. L. (2001) Stromal and epithelial expression of tumormarkers hyaluronic acid and HYAL1 hyaluronidase in prostate cancer. J. Biol. Chem. 276, 11922-11932
59. Voutouri, C., and Stylianopoulos, T. (2014) Evolution of osmotic pressure in solid tumors. J. Biomech. 47, 3441-3447
60. Wiig, H., and Swartz, M. A. (2012) Interstitial fluid and lymph formation and transport: physiological regulation and roles in inflammation and cancer. Physiol. Rev. 92, 1005-1060
61. Levick, J. R. (1987) Flow through interstitium and other fibrous matrices. Q. J. Exp. Physiol. 72, 409-437
62. Tilghman, R.W., Blais, E.M., Cowan, C. R., Sherman, N.E., Grigera, P. R., Jeffery, E. D., Fox, J.W., Blackman, B. R., Tschumperlin, D. J., Papin, J.A., and Parsons, J.T. (2012)Matrix rigidity regulates cancer cell growth bymodulating cellularmetabolismand proteinsynthesis. PLoS One 7, e37231
63. O'Connor, R. S., Hao, X., Shen, K., Bashour, K., Akimova, T., Hancock, W. W., Kam, L. C., and Milone, M. C. (2012) Substrate rigidity regulates human T cell activation and proliferation. J. Immunol. 189, 1330-1339
64. Shrestha, B., Hashiguchi, T., Ito, T., Miura, N., Takenouchi, K., Oyama, Y., Kawahara, K., Tancharoen, S., Ki-I, Y., Arimura, N., Yoshinaga, N., Noma, S., Shrestha, C., Nitanda, T., Kitajima, S., Arimura, K., Sato, M., Sakamoto, T., andMaruyama, I. (2010) B cellderived vascular endothelial growth factor A promotes lymphangiogenesis and high endothelial venule expansion in lymph nodes. J. Immunol. 184, 4819-4826
65. Angeli, V., Ginhoux, F., Llodrà, J., Quemeneur, L., Frenette, P. S., Skobe, M., Jessberger, R., Merad, M., and Randolph, G. J. (2006) B cell-driven lymphangiogenesis in inflamed lymph nodes enhances dendritic cell mobilization. Immunity 24, 203-215
66. Tomei, A. A., Siegert, S., Britschgi, M. R., Luther, S. A., and Swartz, M. A. (2009) Fluid flow regulates stromal cell organization and CCL21 expression in a tissue-engineered lymph node microenvironment. J. Immunol. 183, 4273-4283
67. Peinado, H., Lavotshkin, S., and Lyden, D. (2011) The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts. Semin. Cancer Biol. 21, 139-146
68. Harrell, M. I., Iritani, B. M., and Ruddell, A. (2007) Tumor-induced sentinel lymph node lymphangiogenesis and increased lymph flow precede melanoma metastasis. Am. J. Pathol. 170, 774-786
69. Chung, M.K., Do, I.G., Jung, E., Son, Y. I., Jeong, H. S., andBaek, C. H. (2012)Lymphatic vesselsandhighendothelial venules are increasedin the sentinel lymphnodesofpatientswithoral squamouscell carcinoma before the arrival of tumor cells. Ann. Surg. Oncol. 19, 1595-1601
70. Fidler, I. J. (1973) Selection of successive tumour lines formetastasis. Nat. New Biol. 242, 148-149
71. Nathanson, S. D., and Mahan, M. (2011) Sentinel lymph node pressure in breast cancer. Ann. Surg. Oncol. 18, 3791-3796
72. Nathanson, S. D., Shah, R., Chitale, D. A., and Mahan, M. (2014) Intraoperative clinical assessment and pressure measurements of sentinel lymph nodes in breast cancer. Ann. Surg. Oncol. 21, 81-85
73. Hagendoorn, J., Tong, R., Fukumura, D., Lin, Q., Lobo, J., Padera, T. P., Xu, L., Kucherlapati, R., and Jain, R. K. (2006) Onset of abnormal blood and lymphatic vessel function and interstitial hypertension in early stages of carcinogenesis. Cancer Res. 66, 3360-3364
74. Qian, C.N., Berghuis, B., Tsarfaty, G., Bruch, M., Kort, E. J., Ditlev, J., Tsarfaty, I., Hudson, E., Jackson, D. G., Petillo, D., Chen, J., Resau, J. H., and Teh, B. T. (2006) Preparing the "soil": the primary tumor induces vasculature reorganization in the sentinel lymph node before the arrival of metastatic cancer cells. Cancer Res. 66, 10365-10376
75. Webster, B., Ekland, E. H., Agle, L. M., Chyou, S., Ruggieri, R., and Lu, T. T. (2006) Regulation of lymph node vascular growth by dendritic cells. J. Exp. Med. 203, 1903-1913
76. Provenzano, P. P., Inman, D. R., Eliceiri, K. W., Knittel, J.G., Yan, L., Rueden, C. T., White, J. G., and Keely, P. J. (2008) Collagen density promotes mammary tumor initiation and progression. BMC Med. 6, 11
77. Deed, R., Rooney, P., Kumar, P., Norton, J. D., Smith, J., Freemont, A. J., and Kumar, S. (1997) Early-response gene signalling is induced by angiogenic oligosaccharides of hyaluronan in endothelial cells.
78. Fieber, C., Baumann, P., Vallon, R., Termeer, C., Simon, J. C., Hofmann, M., Angel, P., Herrlich, P., and Sleeman, J. P. (2004) Hyaluronan-oligosaccharide-induced transcription of metalloproteases. J. Cell Sci. 117, 359-367
79. Ichikawa, T., Itano, N., Sawai, T., Kimata, K., Koganehira, Y., Saida, T., and Taniguchi, S. (1999) Increased synthesis of hyaluronate enhances motility of human melanoma cells. J. Invest. Dermatol. 113, 935-939
80. Kosaki, R., Watanabe, K., and Yamaguchi, Y. (1999)Overproduction of hyaluronan by expression of the hyaluronan synthase Has2 enhances anchorage-independent growth and tumorigenicity. Cancer Res. 59, 1141-1145
81. Levental, K. R., Yu, H., Kass, L., Lakins, J. N., Egeblad, M., Erler, J. T., Fong, S. F., Csiszar, K., Giaccia, A., Weninger, W., Yamauchi, M., Gasser, D. L., and Weaver, V. M. (2009) Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891-906
82. Mummert, M. E., Mummert, D. I., Ellinger, L., and Takashima, A. (2003) Functional roles of hyaluronan in B16-F10 melanoma growth and experimental metastasis in mice. Mol. Cancer Ther. 2, 295-300
83. Savani, R. C., Cao, G., Pooler, P. M., Zaman, A., Zhou, Z., and DeLisser, H. M. (2001) Differential involvement of the hyaluronan (HA) receptors CD44 and receptor for HA-mediated motility in endothelial cell function and angiogenesis. J. Biol. Chem. 276, 36770-36778
84. Trochon, V., Mabilat-Pragnon, C., Bertrand, P., Legrand, Y., Soria, J., Soria, C., Delpech, B., and Lu, H. (1997) Hyaluronectin blocks the stimulatory effect of hyaluronan-derived fragments on endothelial cells during angiogenesis in vitro. FEBS Lett. 418, 6-10
85. Xu, X. M., Chen, Y., Chen, J., Yang, S., Gao, F., Underhill, C. B., Creswell, K., and Zhang, L. (2003) A peptide with three hyaluronan binding motifs inhibits tumor growth and induces apoptosis. Cancer Res. 63, 5685-5690
86. Yang, B. G., Tanaka, T., Jang, M. H., Bai, Z., Hayasaka, H., and Miyasaka, M. (2007) Binding of lymphoid chemokines to collagen IV that accumulates in the basal lamina of high endothelial venules: its implications in lymphocyte trafficking. J. Immunol. 179, 4376-4382
87. Stylianopoulos, T., and Jain, R. K. (2013) Combining two strategies to improve perfusion and drug delivery in solid tumors. Proc.Natl. Acad. Sci. USA 110, 18632-18637