Lymphatics in nanophysiology

Advanced Drug Delivery Reviews

Volumn 74, Issue , 2014, Pages 12-18

  Hirakawa, Satoshi ^a   Detmar, Michael ^b   Karaman, Sinem ^b  

^a HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b ETH ZURICH   (Switzerland)

Author keywords

Cancer; Endothelial cells; Inflammation; Lymphangiogenesis; VEGF C

Indexed keywords

DRUG DELIVERY; ENDOTHELIAL CELLS; NANOTECHNOLOGY; PATHOLOGY; TISSUE HOMEOSTASIS; PHYSIOLOGY;

CANCER; DIFFERENTIAL STRUCTURE; INFLAMMATION; LYMPHANGIOGENESIS; MORPHOLOGICAL STRUCTURES; PATHOLOGICAL CONDITIONS; PHYSIOLOGICAL CONDITION; PHYSIOLOGICAL FUNCTIONS; FUNDAMENTAL STRUCTURES;

TRANSPORT PROPERTIES;

BEVACIZUMAB; INDOCYANINE GREEN; NANOCARRIER; NANOPARTICLE; VASCULOTROPIN A; VASCULOTROPIN C;

CHRONIC INFLAMMATION; DRUG DELIVERY SYSTEM; FLUID TRANSPORT; FLUORESCENCE IMAGING; HUMAN; LYMPH FLOW; LYMPH VESSEL; LYMPHANGIOGENESIS; LYMPHATIC SYSTEM DISEASE; METASTASIS; NANOTECHNOLOGY; NONHUMAN; PERMEABILITY; PHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SKIN BLOOD VESSEL; TUMOR VASCULARIZATION; ANIMAL; FUNCTIONS OF THE SKIN AND ITS APPENDAGES; NANOMEDICINE; NEOPLASM; PATHOLOGY; PATHOPHYSIOLOGY; SKIN; VASCULARIZATION; BLOOD VESSEL; LYMPHATIC DRAINAGE; MEDICAL RESEARCH; MEMBRANE PERMEABILITY;

ANIMALS; HUMANS; LYMPHANGIOGENESIS; LYMPHATIC DISEASES; LYMPHATIC VESSELS; NANOMEDICINE; NEOPLASMS; SKIN; SKIN PHYSIOLOGICAL PHENOMENA; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84906054729     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2014.01.011     Document Type: Review

References (50)

1. Tammela T., Alitalo K. Lymphangiogenesis: molecular mechanisms and future promise. Cell 2010, 140:460-476.
2. Huggenberger R., Ullmann S., Proulx S.T., Pytowski B., Alitalo K., Detmar M. Stimulation of lymphangiogenesis via VEGFR-3 inhibits chronic skin inflammation. J. Exp. Med. 2010, 207:2255-2269.
3. Skobe M., Hawighorst T., Jackson D.G., Prevo R., Janes L., Velasco P., Riccardi L., Alitalo K., Claffey K., Detmar M. Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nat. Med. 2001, 7:192-198.
4. Mandriota S.J., Jussila L., Jeltsch M., Compagni A., Baetens D., Prevo R., Banerji S., Huarte J., Montesano R., Jackson D.G., Orci L., Alitalo K., Christofori G., Pepper M.S. Vascular endothelial growth factor-C-mediated lymphangiogenesis promotes tumour metastasis. EMBO J. 2001, 20:672-682.
5. Stacker S.A., Caesar C., Baldwin M.E., Thornton G.E., Williams R.A., Prevo R., Jackson D.G., Nishikawa S., Kubo H., Achen M.G. VEGF-D promotes the metastatic spread of tumor cells via the lymphatics. Nat. Med. 2001, 7:186-191.
6. 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.
7. Hirakawa S., Brown L.F., Kodama S., Paavonen K., Alitalo K., Detmar M. VEGF-C-induced lymphangiogenesis in sentinel lymph nodes promotes tumor metastasis to distant sites. Blood 2007, 109:1010-1017.
8. Dadras S.S., Paul T., Bertoncini J., Brown L.F., Muzikansky A., Jackson D.G., Ellwanger U., Garbe C., Mihm M.C., Detmar M. Tumor lymphangiogenesis: a novel prognostic indicator for cutaneous melanoma metastasis and survival. Am. J. Pathol. 2003, 162:1951-1960.
9. Dadras S.S., Lange-Asschenfeldt B., Velasco P., Nguyen L., Vora A., Muzikansky A., Jahnke K., Hauschild A., Hirakawa S., Mihm M.C., Detmar M. Tumor lymphangiogenesis predicts melanoma metastasis to sentinel lymph nodes. Mod. Pathol. 2005, 18:1232-1242.
10. Hirakawa S., Detmar M., Kerjaschki D., Nagamatsu S., Matsuo K., Tanemura A., Kamata N., Higashikawa K., Okazaki H., Kameda K., Nishida-Fukuda H., Mori H., Hanakawa Y., Sayama K., Shirakata Y., Tohyama M., Tokumaru S., Katayama I., Hashimoto K. Nodal lymphangiogenesis and metastasis: role of tumor-induced lymphatic vessel activation in extramammary Paget's disease. Am. J. Pathol. 2009, 175:2235-2248.
11. Alitalo A., Detmar M. Interaction of tumor cells and lymphatic vessels in cancer progression. Oncogene 2012, 31:4499-4508.
12. Schoppmann S.F., Birner P., Stockl J., Kalt R., Ullrich R., Caucig C., Kriehuber E., Nagy K., Alitalo K., Kerjaschki D. Tumor-associated macrophages express lymphatic endothelial growth factors and are related to peritumoral lymphangiogenesis. Am. J. Pathol. 2002, 161:947-956.
13. Kerjaschki D. The crucial role of macrophages in lymphangiogenesis. J. Clin. Invest. 2005, 115:2316-2319.
14. Karkkainen M.J., Haiko P., Sainio K., Partanen J., Taipale J., Petrova T.V., Jeltsch M., Jackson D.G., Talikka M., Rauvala H., Betsholtz C., Alitalo K. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat. Immunol. 2004, 5:74-80.
15. Oliver G., Sosa-Pineda B., Geisendorf S., Spana E.P., Doe C.Q., Gruss P. Prox 1, a prospero-related homeobox gene expressed during mouse development. Mech. Dev. 1993, 44:3-16.
16. Joukov V., Pajusola K., Kaipainen A., Chilov D., Lahtinen I., Kukk E., Saksela O., Kalkkinen N., Alitalo K. A novel vascular endothelial growth factor, VEGF-C, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases. EMBO J. 1996, 15:1751.
17. Makinen T., Jussila L., Veikkola T., Karpanen T., Kettunen M.I., Pulkkanen K.J., Kauppinen R., Jackson D.G., Kubo H., Nishikawa S., Yla H.S., Alitalo K. Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor-3. Nat. Med. 2001, 7:199-205.
18. Wigle J.T., Oliver G. Prox1 function is required for the development of the murine lymphatic system. Cell 1999, 98:769-778.
19. Dellinger M.T., Hunter R.J., Bernas M.J., Witte M.H., Erickson R.P. Chy-3 mice are Vegfc haploinsufficient and exhibit defective dermal superficial to deep lymphatic transition and dermal lymphatic hypoplasia. Dev. Dyn. 2007, 236:2346-2355.
20. Harvey N.L., Srinivasan R.S., Dillard M.E., Johnson N.C., Witte M.H., Boyd K., Sleeman M.W., Oliver G. Lymphatic vascular defects promoted by Prox1 haploinsufficiency cause adult-onset obesity. Nat. Genet. 2005, 37:1072-1081.
21. Baluk P., Fuxe J., Hashizume H., Romano T., Lashnits E., Butz S., Vestweber D., Corada M., Molendini C., Dejana E., McDonald D.M. Functionally specialized junctions between endothelial cells of lymphatic vessels. J. Exp. Med. 2007, 204:2349-2362.
22. Banerji S., Ni J., Wang S.X., Clasper S., Su J., Tammi R., Jones M., Jackson D.G. LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J. Cell Biol. 1999, 144:789-801.
23. Petrova T.V., Karpanen T., Norrmen C., Mellor R., Tamakoshi T., Finegold D., Ferrell R., Kerjaschki D., Mortimer P., Yla-Herttuala S., Miura N., Alitalo K. Defective valves and abnormal mural cell recruitment underlie lymphatic vascular failure in lymphedema distichiasis. Nat. Med. 2004, 10:974-981.
24. Fang J., Dagenais S.L., Erickson R.P., Arlt M.F., Glynn M.W., Gorski J.L., Seaver L.H., Glover T.W. Mutations in FOXC2 (MFH-1), a forkhead family transcription factor, are responsible for the hereditary lymphedema-distichiasis syndrome. Am. J. Hum. Genet. 2000, 67:1382-1388.
25. Mellor R.H., Tate N., Stanton A.W., Hubert C., Makinen T., Smith A., Burnand K.G., Jeffery S., Levick J.R., Mortimer P.S. Mutations in FOXC2 in humans (lymphoedema distichiasis syndrome) cause lymphatic dysfunction on dependency. J. Vasc. Res. 2011, 48:397-407.
26. Hirakawa S. Regulation of pathological lymphangiogenesis requires factors distinct from those governing physiological lymphangiogenesis. J. Dermatol. Sci. 2011, 61:85-93.
27. Detmar M., Brown L.F., Schön M.P., Elicker B.M., Velasco P., Richard L., Fukumura D., Monsky W., Claffey K.P., Jain R.K. Increased microvascular density and enhanced leukocyte rolling and adhesion in the skin of VEGF transgenic mice. J. Invest. Dermatol. 1998, 111:1-6.
28. Kunstfeld R., Hirakawa S., Hong Y.K., Schacht V., Lange-Asschenfeldt B., Velasco P., Lin C., Fiebiger E., Wei X., Wu Y., Hicklin D., Bohlen P., Detmar M. VEGF-A plays a key role in the induction of chronic inflammation and the associated lymphangiogenic response. Blood 2004, 104:1048-1057.
29. Pflicke H., Sixt M. Preformed portals facilitate dendritic cell entry into afferent lymphatic vessels. J. Exp. Med. 2009, 206:2925-2935.
30. Balch C.M., Gershenwald J.E., Soong S.J., Thompson J.F., Atkins M.B., Byrd D.R., Buzaid A.C., Cochran A.J., Coit D.G., Ding S., Eggermont A.M., Flaherty K.T., Gimotty P.A., Kirkwood J.M., McMasters K.M., Mihm M.C., Morton D.L., Ross M.I., Sober A.J., Sondak V.K. Final version of 2009 AJCC melanoma staging and classification. J. Clin. Oncol. 2009, 27:6199-6206.
31. Karpanen T., Egeblad M., Karkkainen M.J., Kubo H., Yla-Herttuala S., Jaattela M., Alitalo K. Vascular endothelial growth factor C promotes tumor lymphangiogenesis and intralymphatic tumor growth. Cancer Res. 2001, 61:1786-1790.
32. He Y., Kozaki K., Karpanen T., Koshikawa K., Yla-Herttuala S., Takahashi T., Alitalo K. Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling. J. Natl. Cancer Inst. 2002, 94:819-825.
33. Shimizu K., Kubo H., Yamaguchi K., Kawashima K., Ueda Y., Matsuo K., Awane M., Shimahara Y., Takabayashi A., Yamaoka Y., Satoh S. Suppression of VEGFR-3 signaling inhibits lymph node metastasis in gastric cancer. Cancer Sci. 2004, 95:328-333.
34. Roberts N., Kloos B., Cassella M., Podgrabinska S., Persaud K., Wu Y., Pytowski B., Skobe M. Inhibition of VEGFR-3 activation with the antagonistic antibody more potently suppresses lymph node and distant metastases than inactivation of VEGFR-2. Cancer Res. 2006, 66:2650-2657.
35. M. Rinderknecht, A. Villa, K. Ballmer-Hofer, D. Neri, M. Detmar, Phage-derived fully human monoclonal antibody fragments to human vascular endothelial growth factor-C block its interaction with VEGF receptor-2 and 3, PLoS One, 5 e11941.
36. 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., Teh B.T. Preparing the "soil": the primary tumor induces vasculature reorganization in the sentinel lymph node before the arrival of metastatic cancer cells. Cancer Res. 2006, 66:10365-10376.
37. Kerjaschki D., Bago-Horvath Z., Rudas M., Sexl V., Schneckenleithner C., Wolbank S., Bartel G., Krieger S., Kalt R., Hantusch B., Keller T., Nagy-Bojarszky K., Huttary N., Raab I., Lackner K., Krautgasser K., Schachner H., Kaserer K., Rezar S., Madlener S., Vonach C., Davidovits A., Nosaka H., Hammerle M., Viola K., Dolznig H., Schreiber M., Nader A., Mikulits W., Gnant M., Hirakawa S., Detmar M., Alitalo K., Nijman S., Offner F., Maier T.J., Steinhilber D., Krupitza G. Lipoxygenase mediates invasion of intrametastatic lymphatic vessels and propagates lymph node metastasis of human mammary carcinoma xenografts in mouse. J. Clin. Invest. 2011, 121:2000-2012.
38. Proulx S.T., Luciani P., Dieterich L.C., Karaman S., Leroux J.C., Detmar M. Expansion of the lymphatic vasculature in cancer and inflammation: new opportunities for in vivo imaging and drug delivery. J. Control. Release 2013, 172:550-557.
39. Proulx S.T., Luciani P., Derzsi S., Rinderknecht M., Mumprecht V., Leroux J.C., Detmar M. Quantitative imaging of lymphatic function with liposomal indocyanine green. Cancer Res. 2010, 70:7053-7062.
40. Kataru R.P., Jung K., Jang C., Yang H., Schwendener R.A., Baik J.E., Han S.H., Alitalo K., Koh G.Y. Critical role of CD11b+ macrophages and VEGF in inflammatory lymphangiogenesis, antigen clearance, and inflammation resolution. Blood 2009, 113:5650-5659.
41. Matsumura Y., Maeda H. A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs. Cancer Res. 1986, 46:6387-6392.
42. Matsumura Y. Preclinical and clinical studies of NK012, an SN-38-incorporating polymeric micelles, which is designed based on EPR effect. Adv. Drug Deliv. Rev. 2011, 63:184-192.
43. Prabhakar U., Maeda H., Jain R.K., Sevick-Muraca E.M., Zamboni W., Farokhzad O.C., Barry S.T., Gabizon A., Grodzinski P., Blakey D.C. Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology. Cancer Res. 2013, 73:2412-2417.
44. Hurwitz H.I., Fehrenbacher L., Hainsworth J.D., Heim W., Berlin J., Holmgren E., Hambleton J., Novotny W.F., Kabbinavar F. Bevacizumab in combination with fluorouracil and leucovorin: an active regimen for first-line metastatic colorectal cancer. J. Clin. Oncol. 2005, 23:3502-3508.
45. Hurwitz H., Fehrenbacher L., Novotny W., Cartwright T., Hainsworth J., Heim W., Berlin J., Baron A., Griffing S., Holmgren E., Ferrara N., Fyfe G., Rogers B., Ross R., Kabbinavar F. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N. Engl. J. Med. 2004, 350:2335-2342.
46. Reddy S.T., Rehor A., Schmoekel H.G., Hubbell J.A., Swartz M.A. In vivo targeting of dendritic cells in lymph nodes with poly(propylene sulfide) nanoparticles. J. Control. Release 2006, 112:26-34.
47. G. Asellius, De lactibus sive lacteis venis, quarto vasorum mesarai corum genere nova invento, Mediolani, Milan, 1627.
48. Kriehuber E., Breiteneder G.S., Groeger M., Soleiman A., Schoppmann S.F., Stingl G., Kerjaschki D., Maurer D. Isolation and characterization of dermal lymphatic and blood endothelial cells reveal stable and functionally specialized cell lineages. J. Exp. Med. 2001, 194:797-808.
49. Petrova T.V., Makinen T., Makela T.P., Saarela J., Virtanen I., Ferrell R.E., Finegold D.N., Kerjaschki D., Yla-Herttuala S., Alitalo K. Lymphatic endothelial reprogramming of vascular endothelial cells by the Prox-1 homeobox transcription factor. EMBO J. 2002, 21:4593-4599.
50. Hirakawa S., Hong Y.K., Harvey N., Schacht V., Matsuda K., Libermann T., Detmar M. Identification of vascular lineage-specific genes by transcriptional profiling of isolated blood vascular and lymphatic endothelial cells. Am. J. Pathol. 2003, 162:575-586.