Induced lymphatic sinus hyperplasia in sentinel lymph nodes by VEGF-C as the earliest premetastatic indicator

International Journal of Oncology

Volumn 41, Issue 6, 2012, Pages 2073-2078

  Liersch, Ruediger ^a,b,c   Hirakawa, Satoshi ^a   Berdel, Wolfgang E ^b   Mesters, Rolf M ^b   Detmar, Michael ^a,c  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c ETH ZURICH   (Switzerland)

Author keywords

Lymphatic endothelial cells; Lymphatic sinuses; Metastasis; Sentinel lymph node; VEGF C

Indexed keywords

GREEN FLUORESCENT PROTEIN; VASCULOTROPIN C;

ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER CELL; CANCER CELL CULTURE; CANCER PROGNOSIS; CONTROLLED STUDY; ENDOTHELIUM; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; LYMPHANGIOGENESIS; LYMPHOID HYPERPLASIA; MACROPHAGE; MELANOMA; MOUSE; NONHUMAN; ORGAN SIZE; PREDICTIVE VALUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENTINEL LYMPH NODE METASTASIS;

ANIMALS; BIOLOGICAL MARKERS; CELL LINE, TUMOR; ENDOTHELIAL CELLS; FEMALE; HUMANS; HYPERPLASIA; LYMPH NODES; LYMPHANGIOGENESIS; LYMPHATIC METASTASIS; MICE; MICE, NUDE; VASCULAR ENDOTHELIAL GROWTH FACTOR C;

EID: 84869826591     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2012.1665     Document Type: Article

References (47)

1. Skobe M, Hawighorst T, Jackson DG, et al: Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nat Med 7: 192-198, 2001. (Pubitemid 32148486)
2. Stacker SA, Caesar C, Baldwin ME, et al: VEGF-D promotes the metastatic spread of tumor cells via the lymphatics. Nat Med 7: 186-191, 2001. (Pubitemid 32148485)
3. Mandriota SJ, Jussila L, Jeltsch M, et al: Vascular endothelial growth factor-C-mediated lymphangiogenesis promotes tumour metastasis. EMBO J 20: 672-682, 2001. (Pubitemid 32167632)
4. Dadras SS, Paul T, Bertoncini J, et al: Tumor lymphangiogenesis: a novel prognostic indicator for cutaneous melanoma metastasis and survival. Am J Pathol 162: 1951-1960, 2003. (Pubitemid 36613052)
5. Jussila L and Alitalo K: Vascular growth factors and lymphangiogenesis. Physiol Rev 82: 673-700, 2002. (Pubitemid 34743335)
6. Ruddell A, Mezquita P, Brandvold KA, Farr A and Iritani BM: B lymphocyte-specific c-Myc expression stimulates early and functional expansion of the vasculature and lymphatics during lymphomagenesis. Am J Pathol 163: 2233-2245, 2003. (Pubitemid 37466468)
7. Mattila MM, Ruohola JK, Karpanen T, Jackson DG, Alitalo K and Harkonen PL: VEGF-C induced lymphangiogenesis is associated with lymph node metastasis in orthotopic MCF-7 tumors. Int J Cancer 98: 946-951, 2002. (Pubitemid 34286696)
8. Skobe M, Hamberg LM, Hawighorst T, et al: Concurrent induction of lymphangiogenesis, angiogenesis, and macrophage recruitment by vascular endothelial growth factor-C in melanoma. Am J Pathol 159: 893-903, 2001. (Pubitemid 32847180)
9. Karpanen T, Egeblad M, Karkkainen MJ, et al: Vascular endothelial growth factor C promotes tumor lymphangiogenesis and intralymphatic tumor growth. Cancer Res 61: 1786-1790, 2001. (Pubitemid 32691984)
10. Hirakawa S, Brown LF, Kodama S, Paavonen K, Alitalo K and Detmar M: VEGF-C-induced lymphangiogenesis in sentinel lymph nodes promotes tumor metastasis to distant sites. Blood 109: 1010-1017, 2007. (Pubitemid 46220646)
11. Hirakawa S, Kodama S, Kunstfeld R, Kajiya K, Brown LF and Detmar M: VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis. J Exp Med 201: 1089-1099, 2005. (Pubitemid 40524677)
12. Harrell MI, Iritani BM and Ruddell A: Tumor-induced sentinel lymph node lymphangiogenesis and increased lymph flow precede melanoma metastasis. Am J Pathol 170: 774-786, 2007. (Pubitemid 47339411)
13. McGuire WL and Clark GM: Prognostic factors and treatment decisions in axillary-node-negative breast cancer. N Engl J Med 326: 1756-1761, 1992.
14. Shuster TD, Girshovich L, Whitney TM and Hughes KS: Multidisciplinary care for patients with breast cancer. Surg Clin North Am 80: 505-533, 2000. (Pubitemid 30227068)
15. Salama JK, Heimann R, Lin F, et al: Does the number of lymph nodes examined in patients with lymph node-negative breast carcinoma have prognostic significance? Cancer 103: 664-671, 2005. (Pubitemid 40216392)
16. Moorman PG, Hamza A, Marks JR and Olson JA: Prognostic significance of the number of lymph nodes examined in patients with lymph node-negative breast carcinoma. Cancer 91: 2258-2262, 2001. (Pubitemid 32552810)
17. Camp RL, Rimm EB and Rimm DL: A high number of tumor free axillary lymph nodes from patients with lymph node negative breast carcinoma is associated with poor outcome. Cancer 88: 108-113, 2000. (Pubitemid 30027685)
18. Okada S, Albrecht RM, Aharinejad S and Schraufnagel DE: Structural aspects of the lymphocyte traffic in rat submandibular lymph node. Microsc Microanal 8: 116-133, 2002. (Pubitemid 34869824)
19. Hall JG and Morris B: The origin of the cells in the efferent lymph from a single lymph node. J Exp Med 121: 901-910, 1965.
20. Cahill RN, Frost H and Trnka Z: The effects of antigen on the migration of recirculating lymphocytes through single lymph nodes. J Exp Med 143: 870-888, 1976.
21. Lacroix M: MDA-MB-435 cells are from melanoma, not from breast cancer. Cancer Chemother Pharmacol 63: 567, 2009.
22. Ross DT, Scherf U, Eisen MB, et al: Systematic variation in gene expression patterns in human cancer cell lines. Nat Genet 24: 227-235, 2000. (Pubitemid 30132189)
23. Joukov V, Pajusola K, Kaipainen A, et al: 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 15: 1751, 1996. (Pubitemid 26112397)
24. Sato Y, Mukai K, Watanabe S, Goto M and Shimosato Y: The AMeX method. A simplified technique of tissue processing and paraffin embedding with improved preservation of antigens for immunostaining. Am J Pathol 125: 431-435, 1986. (Pubitemid 17208827)
25. Streit M, Stephen AE, Hawighorst T, et al: Systemic inhibition of tumor growth and angiogenesis by thrombospondin-2 using cell-based antiangiogenic gene therapy. Cancer Res 62: 2004-2012, 2002. (Pubitemid 34408444)
26. Hong YK, Shin JW and Detmar M: Development of the lymphatic vascular system: a mystery unravels. Dev Dyn 231: 462-473, 2004. (Pubitemid 39410881)
27. He Y: Scanning electron microscope studies of the rat mesenteric lymph node with special reference to high-endothelial venules and hitherto unknown lymphatic labyrinth. Arch Histol Jpn 48: 1-15, 1985.
28. Ohtani O, Ohtani Y, Carati CJ and Gannon BJ: Fluid and cellular pathways of rat lymph nodes in relation to lymphatic labyrinths and Aquaporin-1 expression. Arch Histol Cytol 66: 261-272, 2003. (Pubitemid 37221578)
29. Belz GT and Heath TJ: Lymph pathways of the medial retropharyngeal lymph node in dogs. J Anat 186: 517-526, 1995.
30. Nicander L, Nafstad P, Landsverk T and Engebretsen RH: A study of modified lymphatics in the deep cortex of ruminant lymph nodes. J Anat 178: 203-212, 1991.
31. Black MM and Zachrau RE: Antitumor immunity in breast cancer patients. Biologic and therapeutic implications. J Reprod Med 23: 21-32, 1979. (Pubitemid 9233735)
32. Tsakraklides V, Anastassiades OT and Kersey JH: Prognostic significance of regional lymph node histology in uterine cervical cancer. Cancer 31: 860-868, 1973.
33. Tsakraklides V, Olson P, Kersey JH and Good RA: Prognostic significance of the regional lymph node histology in cancer of the breast. Cancer 34: 1259-1267, 1974.
34. Oka M, Yoshino S, Hazama S, Shimoda K, Suzuki M and Suzuki T: Prognostic significance of regional lymph node reaction after curative resection of advanced gastric cancer. Br J Surg 79: 1091-1094, 1992.
35. Black MM, Freeman C, Mork T, Harvei S and Cutler SJ: Prognostic significance of microscopic structure of gastric carcinomas and their regional lymph nodes. Cancer 27: 703-711, 1971.
36. Bennett SH, Futrell JW, Roth JA, Hoye RC and Ketcham AS: Prognostic significance of histologic host response in cancer of the larynx or hypopharynx. Cancer 28: 1255-1265, 1971.
37. Malicka K: Attempt at evaluation of defensive activity of lymph nodes on the basis of microscopic and clinical studies in cases of laryngeal cancer. Pol Med J 10: 154-164, 1971.
38. Cassella M and Skobe M: Lymphatic vessel activation in cancer. Ann NY Acad Sci 979: 120-130, 2002. (Pubitemid 36121144)
39. Halin C, Tobler NE, Vigl B, Brown LF and Detmar M: VEGF-A produced by chronically inflamed tissue induces lymphangiogenesis in draining lymph nodes. Blood 110: 3158-3167, 2007. (Pubitemid 350106307)
40. Van Zee KJ, Manasseh DM, Bevilacqua JL, et al: A nomogram for predicting the likelihood of additional nodal metastases in breast cancer patients with a positive sentinel node biopsy. Ann Surg Oncol 10: 1140-1151, 2003. (Pubitemid 40486808)
41. Van den Eynden GG, Vandenberghe MK, van Dam PJ, et al: Increased sentinel lymph node lymphangiogenesis is associated with nonsentinel axillary lymph node involvement in breast cancer patients with a positive sentinel node. Clin Cancer Res 13: 5391-5397, 2007. (Pubitemid 47510365)
42. Studer UE, Scherz S, Scheidegger J, et al: Enlargement of regional lymph nodes in renal cell carcinoma is often not due to metastases. J Urol 144: 243-245, 1990. (Pubitemid 20255089)
43. Van der Auwera I, Van Laere SJ, Van den Eynden GG, et al: Increased angiogenesis and lymphangiogenesis in inflammatory versus noninflammatory breast cancer by real-time reverse transcriptase-PCR gene expression quantification. Clin Cancer Res 10: 7965-7971, 2004. (Pubitemid 39587537)
44. Shirakawa K, Shibuya M, Heike Y, et al: Tumor-infiltrating endothelial cells and endothelial precursor cells in inflammatory breast cancer. Int J Cancer 99: 344-351, 2002. (Pubitemid 34495848)
45. Padera TP, Kadambi A, di Tomaso E, et al: Lymphatic metastasis in the absence of functional intratumor lymphatics. Science 296: 1883-1886, 2002. (Pubitemid 34596277)
46. Schoppmann SF, Birner P, Stockl J, et al: Tumor-associated macrophages express lymphatic endothelial growth factors and are related to peritumoral lymphangiogenesis. Am J Pathol 161: 947-956, 2002. (Pubitemid 34988382)
47. Hattori H: Caution should be taken in using CD31 for distinguishing the vasculature of lymph nodes. J Clin Pathol 56: 638-639, 2003.