Photodynamic ablation of lymphatic vessels and intralymphatic cancer cells prevents metastasis

Science Translational Medicine

Volumn 3, Issue 69, 2011, Pages

  Tammela, Tuomas ^a   Saaristo, Anne ^a,b   Holopainen, Tanja ^a   Ylä Herttuala, Seppo ^c   Andersson, Leif C ^d   Virolainen, Susanna ^a,d   Immonen, Ilkka ^a   Alitalo, Kari ^a  

^a HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^b TURKU UNIVERSITY HOSPITAL   (Finland)

^c UNIVERSITY OF EASTERN FINLAND   (Finland)

^d UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

VERTEPORFIN; PHOTOSENSITIZING AGENT; PORPHYRIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER RELAPSE; CARCINOMA CELL; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; LUNG CARCINOMA; LYMPH NODE BIOPSY; LYMPH NODE METASTASIS; LYMPH VESSEL; MELANOMA; MELANOMA CELL; MOUSE; NONHUMAN; PHOTODYNAMIC THERAPY; PRIORITY JOURNAL; SWINE; VIRAL GENE DELIVERY SYSTEM; ANIMAL; DRUG EFFECT; METHODOLOGY; NEOPLASM; PHOTOCHEMOTHERAPY;

ANIMALS; HUMANS; LYMPHATIC METASTASIS; LYMPHATIC VESSELS; MELANOMA; MICE; NEOPLASMS; PHOTOCHEMOTHERAPY; PHOTOSENSITIZING AGENTS; PORPHYRINS; SWINE;

EID: 79851483971     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3001699     Document Type: Article

References (36)

1. T. P. Padera, A. Kadambi, E. di Tomaso, C. M. Carreira, E. B. Brown, Y. Boucher, N. C. Choi, D. Mathisen, J. Wain, E. J. Mark, L. L. Munn, R. K. Jain, Lymphatic metastasis in the absence of functional intratumor lymphatics. Science 296, 1883-1886 (2002).
2. K. Alitalo, T. Tammela, T. V. Petrova, Lymphangiogenesis in development and human disease. Nature 438, 946-953 (2005).
3. Y. Moroi, Significance of sentinel lymph node biopsy in malignant melanoma: Overview of international data. Int. J. Clin. Oncol. 14, 485-489 (2009).
4. C. R. Scoggins, R. C. Martin, M. I. Ross, M. J. Edwards, D. S. Reintgen, M. M. Urist, J. E. Gershenwald, J. J. Sussman, R. Dirk Noyes, J. S. Goydos, P. D. Beitsch, S. Ariyan, A. J. Stromberg, L. J. Hagendoorn, K. M. McMasters, Factors associated with false-negative sentinel lymph node biopsy in melanoma patients. Ann. Surg. Oncol. 17, 709-717 (2010).
5. B. Zbytek, J. A. Carlson, J. Granese, J. Ross, M. C. Mihm, A. Slominski, Current concepts of metastasis in melanoma. Expert Rev. Dermatol. 3, 569-585 (2008).
6. M. M. Guggenheim, U. Hug, F. J. Jung, V. Rousson, M. C. Aust, M. Calcagni, W. Künzi, P. Giovanoli, Morbidity and recurrence after completion lymph node dissection following sentinel lymph node biopsy in cutaneous malignant melanoma. Ann. Surg. 247, 687-693 (2008).
7. N. Ferrara, H. P. Gerber, J. LeCouter, The biology of VEGF and its receptors. Nat. Med. 9, 669-676 (2003).
8. T. Tammela, K. Alitalo, Lymphangiogenesis: Molecular mechanisms and future promise. Cell 140, 460-476 (2010).
9. M. Jeltsch, A. Kaipainen, V. Joukov, X. Meng, M. Lakso, H. Rauvala, M. Swartz, D. Fukumura, R. K. Jain, K. Alitalo, Hyperplasia of lymphatic vessels in VEGF-C transgenic mice. Science 276, 1423-1425 (1997).
10. T. Veikkola, L. Jussila, T. Makinen, T. Karpanen, M. Jeltsch, T. V. Petrova, H. Kubo, G. Thurston, D. M. McDonald, M. G. Achen, S. A. Stacker, K. Alitalo, Signalling via vascular endothelial growth factor receptor-3 is sufficient for lymphangiogenesis in transgenic mice. EMBO J. 20, 1223-1231 (2001).
11. T. V. Byzova, C. K. Goldman, J. Jankau, J. Chen, G. Cabrera, M. G. Achen, S. A. Stacker, K. A. Carnevale, M. Siemionow, S. R. Deitcher, P. E. DiCorleto, Adenovirus encoding vascular endothelial growth factor-D induces tissue-specific vascular patterns in vivo. Blood 99, 4434-4442 (2002).
12. J. Lin, A. S. Lalani, T. C. Harding, M. Gonzalez, W. W. Wu, B. Luan, G. H. Tu, K. Koprivnikar, M. J. VanRoey, Y. He, K. Alitalo, K. Jooss, Inhibition of lymphogenous metastasis using adeno-associated virus-mediated gene transfer of a soluble VEGFR-3 decoy receptor. Cancer Res. 65, 6901-6909 (2005).
13. N. Roberts, B. Kloos, M. Cassella, S. Podgrabinska, K. Persaud, Y. Wu, B. Pytowski, M. Skobe, Inhibition of VEGFR-3 activation with the antagonistic antibody more potently suppresses lymph node and distant metastases than inactivation of VEGFR-2. Cancer Res. 66, 2650-2657 (2006).
14. Y. He, I. Rajantie, K. Pajusola, M. Jeltsch, T. Holopainen, S. Yla-Herttuala, T. Harding, K. Jooss, T. Takahashi, K. Alitalo, Vascular endothelial cell growth factor receptor 3-mediated activation of lymphatic endothelium is crucial for tumor cell entry and spread via lymphatic vessels. Cancer Res. 65, 4739-4746 (2005).
15. T. Karpanen, M. Egeblad, M. J. Karkkainen, H. Kubo, S. Ylä-Herttuala, M. Jäättelä, K. Alitalo, Vascular endothelial growth factor C promotes tumor lymphangiogenesis and intralymphatic tumor growth. Cancer Res. 61, 1786-1790 (2001).
16. C. M. Balch, S. J. Soong, M. B. Atkins, A. C. Buzaid, N. Cascinelli, D. G. Coit, I. D. Fleming, J. E. Gershenwald, A. Houghton Jr., J. M. Kirkwood, K. M. McMasters, M. F. Mihm, D. L. Morton, D. S. Reintgen, M. I. Ross, A. Sober, J. A. Thompson, J. F. Thompson, An evidence-based staging system for cutaneous melanoma. CA Cancer J. Clin. 54, 131-149 (2004).
17. C. H. van Deurzen, M. de Boer, E. M. Monninkhof, P. Bult, E. van der Wall, V. C. Tjan-Heijnen, P. J. van Diest, Non-sentinel lymph node metastases associated with isolated breast cancer cells in the sentinel node. J. Natl. Cancer Inst. 100, 1574-1580 (2008).
18. G. Cserni, Commentary on in-transit lymph node metastases in breast cancer: A possible source of local recurrence after sentinel node procedure. J. Clin. Pathol. 61, 1233-1235 (2008).
19. M. Rothen, E. Jablon, G. Monares, M. R. Fontal, D. V. Alfaro III, Anti-macular degeneration agents. Ophthalmol. Clin. North Am. 18, 561-567 (2005).
20. U. Schlötzer-Schrehardt, A. Viestenz, G. O. Naumann, H. Laqua, S. Michels, U. Schmidt-Erfurth, Dose-related structural effects of photodynamic therapy on choroidal and retinal structures of human eyes. Graefes Arch. Clin. Exp. Ophthalmol. 240, 748-757 (2002).
21. S. A. Slavin, A. D. Van den Abbeele, A. Losken, M. A. Swartz, R. K. Jain, Return of lymphatic function after flap transfer for acute lymphedema. Ann. Surg. 229, 421-427 (1999).
22. T. Tammela, A. Saaristo, T. Holopainen, J. Lyytikkä, A. Kotronen, M. Pitkonen, U. Abo-Ramadan, S. Ylä-Herttuala, T. V. Petrova, K. Alitalo, Therapeutic differentiation and maturation of lymphatic vessels after lymph node dissection and transplantation. Nat. Med. 13, 1458-1466 (2007).
23. J. B. Burton, M. Johnson, M. Sato, S. B. Koh, D. J. Mulholland, D. Stout, A. F. Chatziioannou, M. E. Phelps, H. Wu, L. Wu, Adenovirus-mediated gene expression imaging to directly detect sentinel lymph node metastasis of prostate cancer. Nat. Med. 14, 882-888 (2008).
24. P. Baluk, J. Fuxe, H. Hashizume, T. Romano, E. Lashnits, S. Butz, D. Vestweber, M. Corada, C. Molendini, E. Dejana, D. M. McDonald, Functionally specialized junctions between endothelial cells of lymphatic vessels. J. Exp. Med. 204, 2349-2362 (2007).
25. T. Hoshida, N. Isaka, J. Hagendoorn, E. di Tomaso, Y. L. Chen, B. Pytowski, D. Fukumura, T. P. Padera, R. K. Jain, 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. 66, 8065-8075 (2006).
26. D. E. Dolmans, D. Fukumura, R. K. Jain, Photodynamic therapy for cancer. Nat. Rev. Cancer 3, 380-387 (2003).
27. B. Chen, B. W. Pogue, X. Zhou, J. A. O'Hara, N. Solban, E. Demidenko, P. J. Hoopes, T. Hasan, Effect of tumor host microenvironment on photodynamic therapy in a rat prostate tumor model. Clin. Cancer Res. 11, 720-727 (2005).
28. M. Alexiades-Armenakas, Laser-mediated photodynamic therapy. Clin. Dermatol. 24, 16-25 (2006).
29. P. Page, L. X. Yang, Novel chemoradiosensitizers for cancer therapy. Anticancer Res. 30, 3675-3682 (2010).
30. O. Catalano, C. Caracò, N. Mozzillo, A. Siani, Locoregional spread of cutaneous melanoma: Sonography findings. AJR Am. J. Roentgenol. 194, 735-745 (2010).
31. B. Enholm, T. Karpanen, M. Jeltsch, H. Kubo, F. Stenback, R. Prevo, D. G. Jackson, S. Yla-Herttuala, K. Alitalo, Adenoviral expression of vascular endothelial growth factor-C induces lymphangiogenesis in the skin. Circ. Res. 88, 623-629 (2001).
32. P. Baluk, T. Tammela, E. Ator, N. Lyubynska, M. G. Achen, D. J. Hicklin, M. Jeltsch, T. V. Petrova, B. Pytowski, S. A. Stacker, S. Ylä-Herttuala, D. G. Jackson, K. Alitalo, D. M. McDonald, Pathogenesis of persistent lymphatic vessel hyperplasia in chronic airway inflammation. J. Clin. Invest. 115, 247-257 (2005).
33. T. Tammela, A. Saaristo, M. Lohela, T. Morisada, J. Tornberg, C. Norrmén, Y. Oike, K. Pajusola, G. Thurston, T. Suda, S. Yla-Herttuala, K. Alitalo, Angiopoietin-1 promotes lymphatic sprouting and hyperplasia. Blood 105, 4642-4648 (2005).
34. T. V. Petrova, T. Karpanen, C. Norrmén, R. Mellor, T. Tamakoshi, D. Finegold, R. Ferrell, D. Kerjaschki, P. Mortimer, S. Ylä-Herttuala, N. Miura, K. Alitalo, Defective valves and abnormal mural cell recruitment underlie lymphatic vascular failure in lymphedema distichiasis. Nat. Med. 10, 974-981 (2004).
35. E. Kriehuber, S. Breiteneder-Geleff, M. Groeger, A. Soleiman, S. F. Schoppmann, G. Stingl, D. Kerjaschki, D. Maurer, Isolation and characterization of dermal lymphatic and blood endothelial cells reveal stable and functionally specialized cell lineages. J. Exp. Med. 194, 797-808 (2001).
36. Acknowledgments: We thank T. Takahashi for the NCI-H460-LNM35 cells; D. Kerjaschki for podoplanin antibodies; K. Honkonen for help with experiments; and P. Bono, H. Joensuu, and M. Tenhunen for helpful discussions. We are grateful to N. Ihalainen, T. Laakkonen, K. Salo, T. Tainola, S. Wallin, and K. Viita-Aho for excellent technical assistance, as well as A. Lehtonen and H. Karhunen for expert animal husbandry. The Biomedicum Molecular Imaging Unit is acknowledged for microscopy services. We acknowledge E. Viherkoski at Duallaser Ltd. for fruitful collaborations with the laser equipment. Funding: This work was supported by grants from the Association for International Cancer Research, the Finnish Cancer Organizations, the Finnish Academy, the Helsinki University Research Fund, NIH (5 R01 HL075183-02), the Sigrid Juselius Foundation, and the European Union (Tumor Host Genomics, LSHC-CT-2005-518198). T.T. was supported by personal grants from the Finnish Cancer Organizations, the Emil Aaltonen Foundation, the K. Albin Johansson Foundation, the Maud Kuistila Memorial Foundation, the Orion-Farmos Research Foundation, and the Paulo Foundation. Author contributions: T.T. developed the PDT concept, designed and performed the experiments and data analysis, prepared the figures, obtained personal funding, and wrote the paper; A.S. performed adenovirus and tumor experiments; T.H. performed tumor experiments and immunohistochemistry; S.Y.-H. developed and generated adenovirus vectors; L.C.A. provided expertise in pathology and reviewed the paper; S.V. provided human melanoma tissues and expertise in pathology and reviewed the paper; I.I. helped to perform initial experiments, contributed reagents and PDT methodology, and reviewed the paper; and K.A. directed the studies, provided funding, and helped to write the paper. Competing interests: K.A. is the Chairman of the Scientific Advisory Council of Circadian Technologies. A.S. and T.T. consult for LxTherapies Ltd. The other authors declare that they have no competing interests.