Immune-promoted tumor cell invasion and metastasis: New considerations in cancer therapy

Advances in Experimental Medicine and Biology

Volumn 532, Issue , 2003, Pages 153-173

  Barberá Guillem, Emilio ^a   Sampsel, James W ^a  

^a NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER ANTIBODY; VASCULOTROPIN;

B LYMPHOCYTE; CELL DAMAGE; CELL MOTILITY; CONFERENCE PAPER; GENE TRANSLOCATION; GRANULOCYTE; HUMAN; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; TUMOR CELL; TUMOR GROWTH; TUMOR IMMUNITY;

ANIMALS; ANTIGENS, NEOPLASM; CELL LINE, TUMOR; GRANULOCYTES; HUMANS; IMMUNOTHERAPY; MICE; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM TRANSPLANTATION; NEOPLASMS; NEUTROPHILS; TIME FACTORS;

EID: 0141645491     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: None     Document Type: Conference Paper

References (99)

1. Hellstrom I, Hellstrom KE, Pierce GE, Yang JP. Cellular and humoral immunity to different types of human neoplasms. Nature. 220(174): 1352-4. 1968.
2. Hellstrom I, Hellstrom KE, Sjogren HO, Warner GA. Demonstration of cell-mediated immunity to human neoplasms of various histological types. Int J Cancer. 7(1): 1-16. 1971.
3. Sjogren HO, Hellstrom I, Bansal SC, Hellstrom KE. Suggestive evidence that the "blocking antibodies" of tumor-bearing individuals may be antigen-antibody complexes. Proc Natl Acad Sci U S A. 68(6): 1372-5. 1971.
4. Sjogren HO, Hellstrom I, Bansal SC, Warner GA, Hellstrom KE. Elution of "blocking factors" from human tumors, capable of abrogating tumor-cell destruction by specifically immune lymphocytes. Int J Cancer. 9(2): 274-83. 1972.
5. Tamerius J, Nepom J, Hellstrom I, Hellstrom KE. Tumor-associated blocking factors: isolation from sera of tumor-bearing mice. J Immunol. 116(3): 724-30. 1976.
6. Nepom JT, Hellstrom I, Hellstrom KE. Antigen-specific purification of blocking factors from sera of mice with chemically induced tumors. Proc Natl Acad Sci U S A. 74(10): 4605-9. 1977.
7. Prehn RT, Lappe MA. An immunostimulation theory of tumor development. Transplant Rev. 7:26-54. 1971.
8. Prehn RT. The immune reaction as a stimulator of tumor growth. Science. 176(31): 170-1. 1972.
9. Prehn RT. Immunomodulation of tumor growth. Am J Pathol. 77(1): 119-122. 1974.
10. Murasko DM, Prehn RT. Stimulatory effect of immunization on tumor induction by Moloney murine sarcoma virus. J Natl Cancer Inst. 61(5): 1323-7. 1978.
11. Lawler EM, Prehn RT. Influence of immune status of host on immunogenicity of tumors induced with two doses of methylcholanthrene. Cancer Immunol Immunother. 13(3): 194-7. 1982.
12. Hewitt HB, Blake ER, Walder AS. A critique of the evidence for active host defense against cancer, based on personal studies of 27 murine tumors of spontaneous origin. Br J Cancer. 33(3): 241-59. 1976.
13. Prehn RT. Stimulatory effects of immune reactions upon the growths of untransplanted tumors. Cancer Res. 54(4): 908-14. 1994.
14. Manson LA. Anti-tumor immune responses of the tumor-bearing host: the case for antibody-mediated immunologic enhancement. Clin Immunol Immunopathol. 72(1): 1-8. 1994.
15. Manson LA. The role of anti-tumor antibody in progressive tumor growth. Transplant Proc. 16(2): 524-7. 1984.
16. Monach PA, Schreiber H, Rowley DA. CD4+ and B lymphocytes in transplantation immunity. II. Augmented rejection of tumor allografts by mice lacking B cells. Transplantation. 55(6): 1356-61. 1993.
17. Barbera-Guillem E, Nelson MB, Barr B, Nyhus JK, May KF Jr, Feng L, Sampsel JW. B lymphocyte pathology in human colorectal cancer. Experimental and clinical therapeutic effects of partial B cell depletion. Cancer Immunol Immunother 48(10): 541-9. 2000.
18. Quan N, Zhang Z, Demetrikopoulos MK, Kitson RP, Chambers WH, Goldfarb RH, Weiss JM. Evidence for involvement of B lymphocytes in the surveillance of lung metastasis in the rat. Cancer Res. 59(5): 1080-9. 1999.
19. Shingu K, Helfritz A, Kuhlmann S, Zielinska-Skowronek M, Jacobs R, Schmidt RE, Pabst R, von Horsten S. Kinetics of the early recruitment of leukocyte subsets at the sites of tumor cells in the lungs: natural killer (NK) cells rapidly attract monocytes but not lymphocytes in the surveillance of micrometastasis. Int J Cancer. 99(1): 74-81. 2002.
20. Qin Z, Richter G, Schuler T, Ibe S, Cao X, Blankenstein T. B cells inhibit induction of T cell-dependent tumor immunity. Nat Med. 4(5): 627-30. 1998.
21. Mandelboim O, Vadai E, Fridkin M, Katz-Hillel A, Feldman M, Berke G, Eisenbach L. Regression of established murine carcinoma metastases following vaccination with tumour-associated antigen peptides. Nat Med. 1(11): 1179-83. 1995.
22. Wang R, Taniguchi M. Limited T cell antigen receptor repertoire in tumor-infiltrating lymphocyte and inhibition of experimental lung metastasis of murine melanoma by anti-TCR antibody. J Immunol. 154(4): 1797-803. 1995.
23. Emilio Barbera-Guillem, Julie K. Nyhus, Chris C. Wolford, Chad R. Friece, and James W. Sampsel, Vascular endothelial growth factor secretion by tumor infiltrating macrophages essentially supports tumor angiogenesis, and IgG immune-complexes potentiate the process. Cancer Res. In publication. 2002
24. Koeppen HK, Singh S, Stauss HJ, Park BH, Rowley DA, Schreiber H. CD4-positive and B lymphocytes in transplantation immunity. I. Promotion of tumor allograft rejection through elimination of CD4-positive lymphocytes. Transplantation. 55(6): 1349-55. 1993.
25. O'Boyle KP, Goya V, Zuckier LS, Chun S, Bhargava K. Expression of human tumor mucin-associated carbohydrate epitopes, including sialylated Tn, and localization of murine monoclonal antibodies CC49 and B72.3 in a syngeneic rat colon carcinoma model. J Immunother Emphasis Tumor Immunol. 16(4): 251-61. 1994.
26. Nelson MB, Nyhus JK, Oravecz-Wilson KI, Barbera-Guillem E. Tumor cells express FcgammaRI which contributes to tumor cell growth and a metastatic phenotype. Neoplasia. 3(2): 115-24 2001.
27. Horst HA, Horny HP Tumor-infiltrating lymphoreticular cells. Histologic and immunohistologic investigations performed on metastasizing squamous cell carcinomas of the head and neck. Cancer. 1991 Dec 1;68(11):2397-402.
28. Tjiong MY, Zumbach K, Schegget JT, van der Vange N, Out TA, Pawlita M, Struyk L. Antibodies against human papillomavirus type 16 and 18 E6 and E7 proteins in cervicovaginal washings and serum of patients with cervical neoplasia. Viral Immunol. 14(4): 415-24. 2001.
29. Behrends U, Jandl T, Golbeck A, Lechner B, Muller-Weihrich S, Schmid I, Till H, Berthold F, Voltz R, Mautner JM. Novel products of the HUD, HUC, NNP-1 and alpha-internexin genes identified by autologous antibody screening of a pediatric neuroblastoma library. Int J Cancer. 100(6): 669-77. 2002.
30. Sofen H, O'Toole C. Anti-squamous tumor antibodies in patients with squamous cell carcinoma. Cancer Res. 38(1): 199-203. 1978.
31. Brichory F, Beer D, Le Naour F, Giordano T, Hanash S. Proteomics-based identification of protein gene product 9.5 as a tumor antigen that induces a humoral immune response in lung cancer. Cancer Res. 61(21): 7908-12. 2001.
32. Berczi I, McMorris LS, Thoriakson TK, Thoriakson RH, Kellen JA, Sehon AH. Detection of tumor antibodies in patients with gastrointestinal carcinomas by a solid-phase radioimmunoassay. J Natl Cancer Inst. 63(3): 553-66. 1979.
33. Knuth A, Lloyd KO, Lipkin M, Oettgen HF, Old LJ. Natural antibodies in human sera directed against blood-group-related determinants expressed on colon cancer cells. Int J Cancer. 32(2): 199-204. 1983.
34. Butschak G, Karsten U. Isolation and characterization of thomsen-friedenreich-specific antibodies from human serum. Tumour Biol. 23(3): 113-22. 2002.
35. von Mensdorff-Pouilly S, Gourevitch MM, Kenemans P, Verstraeten AA, van Kamp GJ, Kok A, van Uffelen K, Snijdewint FG, Paul MA, Meijer S, Hilgers J. An enzyme-linked immunosorbent assay for the measurement of circulating antibodies to polymorphic epithelial mucin (MUC1). Tumour Biol. 19(3): 186-95. 1998.
36. von Mensdorff-Pouilly S, Verstraeten AA, Kenemans P, Snijdewint FG, Kok A, Van Kamp GJ, Paul MA, Van Diest PJ, Meijer S, Hilgers J. Survival in early breast cancer patients is favorably influenced by a natural humoral immune response to polymorphic epithelial mucin. J Clin Oncol. 18(3): 574-83. 2000.
37. Scanlan MJ, Welt S, Gordon CM, Chen YT, Gure AO, Stockert E, Jungbluth AA, Ritter G, Jager D, Jager E, Knuth A, Old LJ. Cancer-related serological recognition of human colon cancer: identification of potential diagnostic and immunotherapeutic targets. Cancer Res. 62(14): 4041-7. 2002.
38. Lee YT, Sheikh KM, Quismorio FP Jr, Friou GJ. Circulating anti-tumor and autoantibodies in breast carcinoma: relationship to stage and prognosis. Breast Cancer Res Treat. 6(1): 57-65 1985.
39. Meyer EM, Grundmann E. Lymph node reactions to cancer. Kiln Wochenschr 60(21): 1329-38. 1982.
40. Mariani-Costantini R, Muraro R, Ficari F, Valli C, Bei R, Tonelli F, Caramia F, Frati L. Immunohistochemical evidence of immune responses to tumor-associated antigens in lymph nodes of colon carcinoma patients. Cancer. 67(11): 2880-6. 1991.
41. Michalak T, Krawczynski K, Harlozinska A, Potomski J, Albert Z. Localization of carcinoembryonic antigen in mesenteric lymph nodes of patients with gastrointestinal cancer. Neoplasma. 30(1): 67-72. 1983.
42. Triozzi PL, Kim JA, Aldrich W, Young DC, Sampsel JW, Martin EW Jr. Localization of tumor-reactive lymph node lymphocytes in vivo using radiolabeled monoclonal antibody. Cancer. 73(3): 580-9. 1994.
43. Arnold MW, Young DC, Hitchcock CL, Schneebaum S, Martin EW Jr. Radioimmunoguided surgery in primary colorectal carcinoma: an intraoperative prognostic tool and adjuvant to traditional staging. Am J Surg. 170(4): 315-8. 1995.
44. Potomski J, Harlozinska A, Starzky H, Richter R, Wozniewski A. Correlation between immunohistochemical localization of carcinoembryonic antigen (CEA) and histological estimation of carcinomas, normal mucosae and lymph nodes of the digestive tract in humans. Arch Immunol Ther Exp (Warsz). 27(1-2): 177-86 1979.
45. Loy TS, Haege DD. B72.3 immunoreactivity in benign abdominal lymph nodes associated with gastrointestinal disease. Dis Colon Rectum. 38(9): 983-7. 1995.
46. Cernea C, Montenegro F, Castro I, Cordeiro A, Gayotto L, Ferraz A, de Carlucci D Jr. Prognostic significance of lymph node reactivity in the control of pathologic negative node squamous cell carcinomas of the oral cavity. Am J Surg. 174(5): 548-51. 1997.
47. Herr HW, Bean MA, Whitmore WF. Jr. Prognostic significance of regional lymph node histology in cancer of the bladder. J Urol. 115(3): 264-7. 1976.
48. Riegrova D, Jansa P. Prognostic significance of reactive changes in regional lymph nodes in gastric and mammary carcinomas. Neoplasma. 29(4): 481-6. 1982.
49. Barbera-Guillem E, Arnold MW, Nelson MB, Martin EW Jr. First results for resetting the antitumor immune response by immune corrective surgery in colon cancer. Am J Surg. 176(4): 339-43. 1998.
50. Hitchcock CL, Arnold MW, Young DC, Schneebaum S, Martin EW Jr. TAG-72 expression in lymph nodes and RIGS. Dis Colon Rectum. 39(4): 473-5. 1996.
51. Fu YX, Huang G, Wang Y, Chaplin DD. Lymphotoxin-alpha-dependent spleen microenvironment supports the generation of memory B cells and is required for their subsequent antigen-induced activation. J Immunol. 164(5): 2508-14. 2000.
52. Wang J, Foster A, Chin R, Yu P, Sun Y, Wang Y, Pfeffer K, Fu YX. The complementation of lymphotoxin deficiency with LIGHT, a newly discovered TNF family member, for the restoration of secondary lymphoid structure and function. Eur J Immunol. 32(7): 1969-79. 2002.
53. Ryffel B, Di Padova F, Schreier MH, Le Hir M, Eugster HP, Quesniaux VF. Lack of type 2 T cell-independent B cell responses and defect in isotype switching in TNF-lymphotoxin alpha-deficient mice. J Immunol 1997 Mar 1;158(5):2126-33)
54. Fu YX, Huang G, Wang Y, Chaplin DD. B lymphocytes induce the formation of follicular dendritic cell clusters in a lymphotoxin alpha-dependent fashion. J Exp Med. 187(7): 1009-18. 1998.
55. De Togni P, Goellner J, Ruddle NH, Streeter PR, Fick A, Mariathasan S, Smith SC, Carlson R, Shornick LP, Strauss-Schoenberger J, et al. Abnormal development of peripheral lymphoid organs in mice deficient in lymphotoxin. Science. 264(5159): 703-7. 1994.
56. Kumaraguru U, Davis IA, Deshpande S, Tevethia SS, Rouse BT. Lymphotoxin alpha-/- mice develop functionally impaired CD8+ T cell responses and fail to contain virus infection of the central nervous system. J Immunol. 166(2): 1066-74. 2001.
57. Eo SK, Kumaraguru U, Rouse BT. Plasmid DNA encoding CCR7 ligands compensate for dysfunctional CD8+ T cell responses by effects on dendritic cells. J Immunol. 167(7): 3592-9. 2001.
58. Elewaut D, Brossay L, Santee SM, Naidenko OV, Burdin N, De Winter H, Matsuda J, Ware CF, Cheroutre H, Kronenberg M. Membrane lymphotoxin is required for the development of different subpopulations of NK T cells. J Immunol 2000 Jul 15;165(2):671-9.
59. Ito D, Back TC, Shakhov AN, Wiltrout RH, Nedospasov SA. Mice with a targeted mutation in lymphotoxin-alpha exhibit enhanced tumor growth and metastasis: impaired NK cell development and recruitment. J Immunol. 163(5): 2809-15. 1999.
60. Ruddle NH. Lymphoid neo-organogenesis: lymphotoxin's role in inflammation and development. Immunol Res. 19(2-3): 119-25. 1999.
61. Bevilacqua MP, Nelson RM Endothelial-leukocyte adhesion molecules in inflammation and metastasis. Thromb Haemost. 70(1): 152-4. 1993.
62. Chen WS, Wei SJ, Liu JM, Hsiao M, Kou-Lin J, Yang WK. Tumor invasiveness and liver metastasis of colon cancer cells correlated with cyclooxygenase-2 (COX-2) expression and inhibited by a COX-2-selective inhibitor, etodolac. Int J Cancer. 2001 Mar 15;91(6):894-9.
63. Wang Y, Huang G, Wang J, Molina H, Chaplin DD, Fu YX. Antigen persistence is required for somatic mutation and affinity maturation of immunoglobulin. Eur J Immunol. 30(8): 2226-34. 2000.
64. Anderson F, Game BA, Atchley D, Xu M, Lopes-Virella MF, Huang Y. IFN-gamma pretreatment augments immune complex-induced matrix metalloproteinase-1 expression in U937 histiocytes. Clin Immunol. 102(2): 200-7. 2002.
65. Warner RL, Lewis CS, Beltran L, Younkin EM, Varani J, Johnson KJ. The role of metalloelastase in immune complex-induced acute lung injury. Am J Pathol. 158(6): 2139-44. 2001.
66. Anderson CF, Mosser DM. A novel phenotype for an activated macrophage: the type 2 activated macrophage. J Leukoc Biol. 72(1): 101-6. 2002.
67. van Ravenswaay Claasen, H.H., Kluin, P.M., and Fleuren, G.J. Tumor infiltrating cells in human cancer. On the possible role of CD16+ macrophages in antitumor cytotoxicity. Lab. Invest. 67(2): 166-174. 1992.
68. Wang ZQ, Bapat AS, Rayanade RJ, Dagtas AS, Hoffmann MK. Interleukin-10 induces macrophage apoptosis and expression of CD16 (FcgammaRIII) whose engagement blocks the cell death programme and facilitates differentiation. Immunology. 102(3): 331-7. 2001.
69. Cameron AJ, McDonald KJ, Harnett MM, Allen JM. Differentiation of the human monocyte cell line, U937, with dibutyryl cyclicAMP induces the expression of the inhibitory Fc receptor, FcgammaRIIb. Immunol Lett. 83(3): 171-9. 2002.
70. Tridandapani S, Siefker K, Teillaud JL, Carter JE, Wewers MD, Anderson CL. Regulated expression and inhibitory function of Fcgamma RIIb in human monocytic cells. J Biol Chem. 277(7): 5082-9. 2002.
71. Guo RF, Ward PA. Mediators and regulation of neutrophil accumulation in inflammatory responses in lung: insights from the IgG immune complex model (1,2). Free Radic Biol Med. 33(3): 303-10. 2002.
72. Anderson CF, Mosser DM. Cutting edge: biasing immune responses by directing antigen to macrophage Fc gamma receptors. J Immunol. 168(8): 3697-701. 2002.
73. Coxon A, Cullere X, Knight S, Sethi S, Wakelin MW, Stavrakis G, Luscinskas FW, Mayadas TN. Fc gamma RIII mediates neutrophil recruitment to immune complexes. A mechanism for neutrophil accumulation in immune-mediated inflammation. Immunity. 14(6): 693-704. 2001.
74. Fossati G, Bucknall RC, Edwards SW. Insoluble and soluble immune complexes activate neutrophils by distinct activation mechanisms: changes in functional responses induced by priming with cytokines. Ann Rheum Dis. 61(1): 13-9. 2002.
75. Nyhus JK, Wolford CC, Friece CR, Nelson MB, Sampsel JW, Barbera-Guillem E. IgG-recognizing shed tumor-associated antigens can promote tumor invasion and metastasis. Cancer Immunol Immunother. 50(7): 361-72. 2001.
76. Barbera-Guillem E, May KF Jr, Nyhus JK, Nelson MB. Promotion of tumor invasion by cooperation of granulocytes and macrophages activated by anti-tumor antibodies. Neoplasia. 1(5): 453-60. 1999.
77. Swift, M.E., Kleinman, H.K., and DiPietro, L.A. Impaired wound repair and delayed angiogenesis in aged mice. Lab. Invest. 79(12): 1479-1487. 1999.
78. Presta, L.G., Chen, H., O'Connor, S.J., Chisholm, V., Meng, Y.G., Krummen, L., Winkler, M., and Ferrara, N. Humanization of an anti-vascular endothelial growth factor monoclonal antibody for the therapy of solid tumors and other disorders. Cancer Res., 57(20): 4593-4599. 1997.
79. Saleh, M., Stacker, S.A., and Wilks, A.F. Inhibition of growth of C6 glioma cells in vivo by expression of antisense vascular endothelial growth factor sequence. Cancer Res., 56(2): 393-401. 1996.
80. Borgstrom, P., Hillan, K.J., Sriramarao, P., and Ferrara, N. Complete inhibition of angiogenesis and growth of microtumors by anti-vascular endothelial growth factor neutralizing antibody: novel concepts of angiostatic therapy from intravital videomicroscopy. Cancer Res., 56(17): 4032-4039. 1996.
81. Rak, J., Mitsuhashi, Y., Bayko, L., Filmus, J., Shirasawa, S., Sasazuki, T., and Kerbel, R.S. Mutant ras oncogenes up regulate VEGF/VPF expression: implications for induction and inhibition of tumor angiogenesis. Cancer Res., 55(20): 4575-4580. 1995.
82. Yoshiji, H., Gomez, D.E., Shibuya, M., and Thorgeirsson, U.P. Expression of vascular endothelial growth factor, its receptor, and other angiogenic factors in human breast cancer. Cancer Res., 56(9): 2013-2016. 1996.
83. Detmar, M., Velasco, P., Richard, L., Claffey, K.P., Streit, M., Riccardi, L., Skobe, M., Brown, L.F. Expression of vascular endothelial growth factor induces an invasive phenotype in human squamous cell carcinomas. Am. J. Pathol., 156(1): 159-167. 2000.
84. Kondo, Y., Arii, S., Mori, A., Furutani, M., Chiba, T. and Imamura, M. Enhancement of angiogenesis, tumor growth, and metastasis by transfection of vascular endothelial growth factor into LoVo human colon cancer cell line. Clin. Cancer Res., 6(2): 622-630. 2000.
85. Aonuma, M., Saeki, Y., Akimoto, T., Nakayama, Y., Hattori, C., Yoshitake, Y., Nishikawa, K., Shibuya, M., and Tanaka, N.G. Vascular endothelial growth factor overproduced by tumour cells acts predominantly as a potent angiogenic factor contributing to malignant progression. Int. J. Exp. Pathol., 80(5): 271-281. 1999.
86. Verheul, H.M., Hoekman, K., Luykx-de Bakker, S., Eekman, C.A., Folman, C.C., Broxterman, H.J., and Pinedo, H.M. Platelet: transporter of vascular endothelial growth factor. Clin. Cancer Res., 3(12 Pt 1): 2187-2190. 1997.
87. Wartiovaara, U., Salven, P., Mikkola, H., Lassila, R., Kaukonen, J., Joukov, V., Orpana, A., Ristimaki, A., Heikinheimo, M., Joensuu, H., Alitalo, K., and Palotie, A. Peripheral blood platelets express VEGF-C and VEGF, which are released during platelet activation. Thromb. Haemost., 80(1): 171-175. 1998.
88. Salven, P., Orpana, A., and Joensuu, H. Leukocytes and platelets of patients with cancer contain high levels of vascular endothelial growth factor. Clin. Cancer Res., 5(3): 487-491. 1999.
89. Huang YQ, Li JJ, Hu L, Lee M, Karpatkin S. Thrombin induces increased expression and secretion of VEGF from human FS4 fibroblasts, DU145 prostate cells and CHRF megakaryocytes. Thromb Haemost. 86(4): 1094-8. 2001.
90. Xiong, M., Elson, G., Legarda, D., and Leibovich, S.J. Production of vascular endothelial growth factor by routine macrophages: regulation by hypoxia, lactate, and the inducible nitric oxide synthase pathway. Am. J. Pathol., 153(2): 587-598. 1998.
91. Lu, B., Rutledge, B. J., and Gu, L. Abnormalities in monocyte recruitment and cytokine expression in monocyte chemoattractant protein 1-deficient mice. J. Exp. Med., 187: 601-608. 1998.
92. Takayuki Ueno, Masakazu Toi, I Hisashi Saji, Mariko Muta, Hiroko Bando, Katsumasa Kuroi, Morio Koike, Hidekuni Inadera, and Kouji Matsushima. Significance of Macrophage Chemoattractant Protein-1 in Macrophage Recruitment, Angiogenesis, and Survival in Human Breast Cancer. Clin. Cancer Res., 6: 3282-3289. 2000.
93. Shanley, T.P., Schmal, H., Warner, R.L., Schmid, E., Friedl, H.P., and Ward, P.A. Requirement for C-X-C chemokines (macrophage inflammatory protein-2 and cytokine-induced neutrophil chemoattractant) in IgG immune complex-induced lung injury. J. Immunol., 158(7): 3439-3448. 1997.
94. Kranz, A., Mattfeldt, T., and Waltenberger, J. Molecular mediators of tumor angiogenesis: enhanced expression and activation of vascular endothelial growth factor receptor KDR in primary breast cancer. Int. J. Cancer, 84(3): 293-298. 1999.
95. Goede, V., Brogelli, L., Ziche, M., and Augustin, H.G. Induction of inflammatory angiogenesis by monocyte chemoattractant protein-1. Int. J. Cancer, 82(5): 765-770. 1999.
96. Brunda, M.J., Sulich, V., Wright, R.B., and Palleroni, A.V. Tumoricidal activity and cytokine secretion by tumor-infiltrating macrophages. Int. J. Cancer, 48(5): 704-708. 1991.
97. Barbera-Guillem, E., Nyhus, J.K., Wolford, C.C., Friece C.R., and Sampsel J.W. Vascular endothelial growth factor secretion by tumor infiltrating macrophages essentially supports tumor angiogenesis, and IgG immune-complexes potentiate the process. Cancer Res. (In press). 2002.
98. Jeltsch, M., Kaipainen, A., Joukov, V., Meng, X., Lakso, M., Rauvala, H., Swartz, M., Fukumura, D., Jain, R.K., and Alitalo, K. Hyperplasia of lymphatic vessels in VEGF-C transgenic mice. Science, 276(5317): 1423-1425. 1997.
99. Skobe, M., Hawighorst, T., Jackson, D.G., Prevo, R., Janes, L., Velasco, P., Riccardi, L., Alitalo, K., Claffey, K., and Detmar, M. Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nat. Med., 7(2): 192-198. 2001.