Cancer Immunology, Immunotherapy

, Volume 52, Issue 11, pp 670–679

Tumor microvasculature as a barrier to antitumor immunity

Symposium in Writing

Keywords

Tumor microvessels Leukocyte recruitment Lymphocyte homing receptors Adhesion molecules Tumor microenvironment 

References

  1. 1.
    Armstrong TD, Jaffee EM (2002) Cytokine modified tumor vaccines. Surg Oncol Clin N Am 11:681–696PubMedGoogle Scholar
  2. 2.
    Davis ID, Jefford M, Parente P, Cebon J (2003) Rational approaches to human cancer immunotherapy. J Leukoc Biol 73, 3–29Google Scholar
  3. 3.
    Mocellin S, Rossi CR, Lise M, Marincola FM (2002) Adjuvant immunotherapy for solid tumors: from promise to clinical application. Cancer Immunol Immunother 51:583–595CrossRefPubMedGoogle Scholar
  4. 4.
    Johnson SK, Kerr KM, Chapman AD, Kennedy MM, King G, Cockburn JS, Jeffrey RR (2000) Immune cell infiltrates and prognosis in primary carcinoma of the lung. Lung Cancer 27:27–35CrossRefPubMedGoogle Scholar
  5. 5.
    Lee TK, Horner RD, Silverman JF, Chen YH, Jenny C, Scarantino CW (1989) Morphometric and morphologic evaluations in stage III non-small cell lung cancers: prognostic significance of quantitative assessment of infiltrating lymphoid cells. Cancer 63:309–316PubMedGoogle Scholar
  6. 6.
    Tosi P, Sforza V, Santopietro R, Lio R, Gotti, G, Paladini, P, Cevenini, G, Barbini, P. (1992) Bronchiolo-alveolar carcinoma: an analysis of survival predictors. Eur J Cancer 28A, 1365–70Google Scholar
  7. 7.
    Clark WH Jr, Elder DE, Guerry DT, Braitman LE, Trock BJ, Schultz D, Synnestvedt M, Halpern AC (1989) Model predicting survival in stage I melanoma based on tumor progression. J Natl Cancer Inst 81:1893–1904PubMedGoogle Scholar
  8. 8.
    Elder DE, Guerry DT, VanHorn M, Hurwitz S, Zehngebot L, Goldman LI, LaRossa D, Hamilton R, Bondi EE, Clark WH Jr (1985) The role of lymph node dissection for clinical stage I malignant melanoma of intermediate thickness (1.51–3.99 mm). Cancer 56:413–418PubMedGoogle Scholar
  9. 9.
    Poppema S, Brocker EB, de Leij L, Terbrack D, Visscher T, Ter Haar A, Macher E, The TH, Sorg C (1983) In situ analysis of the mononuclear cell infiltrate in primary malignant melanoma of the skin. Clin Exp Immunol 51:77–82PubMedGoogle Scholar
  10. 10.
    Dvorak HF (1986) Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N Engl J Med 315:1650–1659Google Scholar
  11. 11.
    Watanabe S, Sato Y, Kodama T, Shimosato Y (1983) Immunohistochemical study with monoclonal antibodies on immune response in human lung cancers. Cancer Res 43:5883–5889PubMedGoogle Scholar
  12. 12.
    An T, Sood U, Pietruk T, Cummings G, Hashimoto K, Crissman JD (1987) In situ quantitation of inflammatory mononuclear cells in ductal infiltrating breast carcinoma: relation to prognostic parameters. Am J Pathol 128:52–60PubMedGoogle Scholar
  13. 13.
    Ioachim HL (1976) The stromal reaction of tumors: an expression of immune surveillance. J Natl Cancer Inst 57:465Google Scholar
  14. 14.
    Freemont AJ (1982) The small blood vessels in areas of lymphocytic infiltration around malignant neoplasms. Br J Cancer 46:283–288PubMedGoogle Scholar
  15. 15.
    Aaltomaa S, Lipponen P, Eskelinen M, Kosma VM, Marin S, Alhava E, Syrjanen K (1992) Lymphocyte infiltrates as a prognostic variable in female breast cancer. Eur J Cancer 28A:859–864PubMedGoogle Scholar
  16. 16.
    Lwin KY, Zuccarini O, Sloane JP, Beverley PC (1985) An immunohistological study of leukocyte localization in benign and malignant breast tissue. Int J Cancer 36:433–438PubMedGoogle Scholar
  17. 17.
    Adams WJ, Morris DL (1997) Pilot study--cimetidine enhances lymphocyte infiltration of human colorectal carcinoma: results of a small randomized control trial. Cancer 80:15–21CrossRefPubMedGoogle Scholar
  18. 18.
    AD E (1980) Assessment of immune responses to tumors using cryostat sections of bronchogenic carcinoma. Cancer Res 40:3598–3601PubMedGoogle Scholar
  19. 19.
    Ben-Hur H, Kossoy G, Schneider DF, Zandbank J, Zusman I (2002) Response of the immune system of mammary tumor-bearing rats to cyclophosphamide and soluble low-molecular mass tumor-associated antigens: the spleen and lymph nodes. Int J Mol Med 9:311–316PubMedGoogle Scholar
  20. 20.
    Menard S, Tomasic G, Casalini P, Balsari A, Pilotti S, Cascinelli N, Salvadori B, Colnaghi MI, Rilke F (1997) Lymphoid infiltration as a prognostic variable for early-onset breast carcinomas. Clin Cancer Res 3:817–819PubMedGoogle Scholar
  21. 21.
    Jass JR, Atkin WS, Cuzick J, Bussey HJ, Morson BC, Northover JM, Todd IP (1986) The grading of rectal cancer: historical perspectives and a multivariate analysis of 447 cases. Histopathology 10:437–459PubMedGoogle Scholar
  22. 22.
    Ueno T, Toi M, Saji H, Muta M, Bando H, Kuroi K, Koike M, Inadera H, Matsushima K (2000) Significance of macrophage chemoattractant protein-1 in macrophage recruitment, angiogenesis, and survival in human breast cancer. Clin Cancer Res 6:3282–3289PubMedGoogle Scholar
  23. 23.
    Nakamura Y, Yasuoka H, Tsujimoto M, Yang Q, Imabun S, Nakahara M, Nakao K, Nakamura M, Mori I, Kakudo K (2003) Prognostic significance of vascular endothelial growth factor D in breast carcinoma with long-term follow-up. Clin Cancer Res 9:716–721PubMedGoogle Scholar
  24. 24.
    Toomey D, Harmey J, Condron C, Kay E, Bouchier-Hayes D (1999) Phenotyping of immune cell infiltrates in breast and colorectal tumours. Immunol Invest 28:29–41PubMedGoogle Scholar
  25. 25.
    Hishii M, Nitta T, Ishida H, Ebato M, Kurosu A, Yagita H, Sato K, Okumura K (1995) Human glioma-derived interleukin-10 inhibits antitumor immune responses in vitro. Neurosurgery 37:1160–1167Google Scholar
  26. 26.
    Harmey JH, Dimitriadis E, Kay E, Redmond HP, Bouchier-Hayes D (1998) Regulation of macrophage production of vascular endothelial growth factor (VEGF) by hypoxia and transforming growth factor beta-1. Ann Surg Oncol 5:271–278PubMedGoogle Scholar
  27. 27.
    Lewis CE, Leek R, Harris A, McGee JO (1995) Cytokine regulation of angiogenesis in breast cancer: the role of tumor-associated macrophages. J Leukoc Biol 57:747–751PubMedGoogle Scholar
  28. 28.
    Mortarini R, Borri A, Tragni G, Bersani I, Vegetti C, Bajetta E, Pilotti S, Cerundolo V, Anichini A (2000) Peripheral burst of tumor-specific cytotoxic T lymphocytes and infiltration of metastatic lesions by memory CD8+ T cells in melanoma patients receiving interleukin 12. Cancer Res 60:3559–3568PubMedGoogle Scholar
  29. 29.
    Piali L, Fichtel A, Terpe HJ, Imhof BA, Gisler RH (1995) Endothelial vascular cell adhesion molecule 1 expression is suppressed by melanoma and carcinoma. J Exp Med 181:811–816PubMedGoogle Scholar
  30. 30.
    Mackensen A, Carcelain G, Viel S, Raynal MC, Michalaki H, Triebel F, Bosq J, Hercend T (1994) Direct evidence to support the immunosurveillance concept in a human regressive melanoma. J Clin Invest 93:1397–1402PubMedGoogle Scholar
  31. 31.
    McGovern VJ (1976) Malignant melanoma, clinical and histological diagnosis. Wiley, New YorkGoogle Scholar
  32. 32.
    Szekeres L, Daroczy J (1981) Electron microscopic investigation on the local cellular reaction to primary malignant melanoma. Dermatologica 163:137–144PubMedGoogle Scholar
  33. 33.
    Dvorak AM, Mihm MC Jr, Osage JE, Dvorak HF (1980) Melanoma: an ultrastructural study of the host inflammatory and vascular responses. J Invest Dermatol 75:388–393PubMedGoogle Scholar
  34. 34.
    Girard JP, Springer TA (1995) High endothelial venules (HEVs): specialized endothelium for lymphocyte migration. Immunol Today 16:449–457CrossRefPubMedGoogle Scholar
  35. 35.
    Butcher EC, Williams M, Youngman K, Rott L, Briskin M (1999) Lymphocyte trafficking and regional immunity. Adv Immunol 72:209–253PubMedGoogle Scholar
  36. 36.
    Kansas GS (1996) Selectins and their ligands: current concepts and controversies. Blood 88:3259–3287PubMedGoogle Scholar
  37. 37.
    Rosen SD, Hwang ST, Giblin PA, Singer MS (1997) High-endothelial-venule ligands for L-selectin: identification and functions. Biochem Soc Trans 25:428–433PubMedGoogle Scholar
  38. 38.
    Butcher EC, Picker LJ (1996) Lymphocyte homing and homeostasis. Science 272:60–66Google Scholar
  39. 39.
    Pober JS, Cotran RS (1990) Cytokines and endothelial cell biology. Physiol Rev 70:427–451PubMedGoogle Scholar
  40. 40.
    Springer TA (1994) Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76:301–314PubMedGoogle Scholar
  41. 41.
    Pober JS (2002) Endothelial activation: intracellular signaling pathways. Arthritis Res 4[Suppl 3]:S109–S116Google Scholar
  42. 42.
    Baggiolini M (1998) Chemokines and leukocyte traffic. Nature 392:565–568PubMedGoogle Scholar
  43. 43.
    Ding Z, Xiong K, Issekutz TB (2001) Chemokines stimulate human T lymphocyte transendothelial migration to utilize VLA-4 in addition to LFA-1. J Leukoc Biol 69:458–466PubMedGoogle Scholar
  44. 44.
    Kunkel EJ, Butcher EC (2002) Chemokines and the tissue-specific migration of lymphocytes. Immunity 16:1–4PubMedGoogle Scholar
  45. 45.
    Sallusto F, Langenkamp A, Geginat J, Lanzavecchia A (2000) Functional subsets of memory T cells identified by CCR7 expression. Curr Top Microbiol Immunol 251:167–171PubMedGoogle Scholar
  46. 46.
    Sallusto F, Lanzavecchia A (2000) Understanding dendritic cell and T-lymphocyte traffic through the analysis of chemokine receptor expression. Immunol Rev 177:134–140PubMedGoogle Scholar
  47. 47.
    Shah A, Unger E, Bain MD, Bruce R, Bodkin J, Ginnetti J, Wang WC, Seon B, Stewart CC, Evans SS (2002) Cytokine and adhesion molecule expression in primary human endothelial cells stimulated with fever-range hyperthermia. Int J Hyperthermia 18:534–551CrossRefPubMedGoogle Scholar
  48. 48.
    Piali L, Albelda SM, Baldwin HS, Hammel P, Gisler RH, Imhof BA (1993) Murine platelet endothelial cell adhesion molecule (PECAM-1)/CD31 modulates beta 2 integrins on lymphokine-activated killer cells. Eur J Immunol 23:2464–2471PubMedGoogle Scholar
  49. 49.
    Melder RJ, Koenig GC, Witwer BP, Safabakhsh N, Munn LL, Jain RK (1996) During angiogenesis, vascular endothelial growth factor and basic fibroblast growth factor regulate natural killer cell adhesion to tumor endothelium. Nat Med 2:992–997PubMedGoogle Scholar
  50. 50.
    Jain RK, Koenig GC, Dellian M, Fukumura D, Munn LL, Melder RJ (1996) Leukocyte-endothelial adhesion and angiogenesis in tumors. Cancer Metastasis Rev 15:195–204PubMedGoogle Scholar
  51. 51.
    Onrust SV, Hartl PM, Rosen SD, Hanahan D (1996) Modulation of L-selectin ligand expression during an immune response accompanying tumorigenesis in transgenic mice. J Clin Invest 97:54–64PubMedGoogle Scholar
  52. 52.
    Ganss R, Hanahan D (1998) Tumor microenvironment can restrict the effectiveness of activated antitumor lymphocytes. Cancer Res 58:4673–4681PubMedGoogle Scholar
  53. 53.
    Chin YH, Ye MW, Cai JP, Xu XM (1996) Differential regulation of tissue-specific lymph node high endothelial venule cell adhesion molecules by tumour necrosis factor and transforming growth factor-beta 1. Immunology 87:559–565PubMedGoogle Scholar
  54. 54.
    Ganss R, Ryschich E, Klar E, Arnold B, Hammerling GJ (2002) Combination of T-cell therapy and trigger of inflammation induces remodeling of the vasculature and tumor eradication. Cancer Res 62:1462–1470PubMedGoogle Scholar
  55. 55.
    Carlos TM (2001) Leukocyte recruitment at sites of tumor: dissonant orchestration. J Leukoc Biol 70:171–184PubMedGoogle Scholar
  56. 56.
    Wu NZ, Klitzman B, Dodge R, Dewhirst MW (1992) Diminished leukocyte-endothelium interaction in tumor microvessels. Cancer Res 52:4265–4268PubMedGoogle Scholar
  57. 57.
    Chen Q, Unger EL, Passanese J, Bangia P, Pritchard M, Wang WC Repasky E, Evans SS (2003) Fever-range thermal stress augments lymphocyte-endothelial adhesion in the tumor microvasculature. 94th annual meeting of American Association for Cancer ResearchGoogle Scholar
  58. 58.
    Ryschich E, Schmidt J, Hammerling GJ, Klar E, Ganss R (2002) Transformation of the microvascular system during multistage tumorigenesis. Int J Cancer 97:719–725CrossRefPubMedGoogle Scholar
  59. 59.
    Schmidt J, Ryschich E, Maksan SM, Werner J, Gebhard MM, Herfarth C, Klar E (1999) Reduced basal and stimulated leukocyte adherence in tumor endothelium of experimental pancreatic cancer. Int J Pancreatol 26, 173–179Google Scholar
  60. 60.
    Irjala H, Salmi M, Alanen K, Grenman R, Jalkanen S (2001) Vascular adhesion protein 1 mediates binding of immunotherapeutic effector cells to tumor endothelium. J Immunol 166:6937–6943PubMedGoogle Scholar
  61. 61.
    Salmi M, Grenman R, Grenman S, Nordman E, Jalkanen S (1995) Tumor endothelium selectively supports binding of IL-2-propagated tumor-infiltrating lymphocytes. J Immunol 154:6002–6012PubMedGoogle Scholar
  62. 62.
    Nelson H, Ramsey PS, Donohue JH, Wold LE (1994) Cell adhesion molecule expression within the microvasculature of human colorectal malignancies. Clin Immunol Immunopathol 72:129–136CrossRefPubMedGoogle Scholar
  63. 63.
    Kunz M, Toksoy A, Goebeler M, Engelhardt E, Brocker E, Gillitzer R (1999) Strong expression of the lymphoattractant C-X-C chemokine Mig is associated with heavy infiltration of T cells in human malignant melanoma. J Pathol 189:552–558CrossRefPubMedGoogle Scholar
  64. 64.
    Griffioen AW, Damen CA, Martinotti S, Blijham GH, Groenewegen G (1996) Endothelial intercellular adhesion molecule-1 expression is suppressed in human malignancies: the role of angiogenic factors. Cancer Res 56:1111–1117PubMedGoogle Scholar
  65. 65.
    Griffioen AW, Damen CA, Blijham GH, Groenewegen G (1996) Tumor angiogenesis is accompanied by a decreased inflammatory response of tumor-associated endothelium. Blood 88:667–673PubMedGoogle Scholar
  66. 66.
    Griffioen AW, Tromp SC, Hillen HF (1998) Angiogenesis modulates the tumour immune response. Int J Exp Pathol 79:363–368CrossRefPubMedGoogle Scholar
  67. 67.
    Tromp SC, oude Egbrink MG, Dings RP, van Velzen S, Slaaf DW, Hillen HF, Tangelder GJ, Reneman RS, Griffioen AW (2000) Tumor angiogenesis factors reduce leukocyte adhesion in vivo. Int Immunol 12:671–676CrossRefPubMedGoogle Scholar
  68. 68.
    Chin YH, Cai JP, Xu XM (1992) Transforming growth factor-beta 1 and IL-4 regulate the adhesiveness of Peyer's patch high endothelial venule cells for lymphocytes. J Immunol 148:1106–1112PubMedGoogle Scholar
  69. 69.
    Gamble JR, Vadas MA (1988) Endothelial adhesiveness for blood neutrophils is inhibited by transforming growth factor-beta. Science 242:97–99PubMedGoogle Scholar
  70. 70.
    Berger R, Albelda SM, Berd D, Ioffreda M, Whitaker D, Murphy GF (1993) Expression of platelet-endothelial cell adhesion molecule-1 (PECAM-1) during melanoma-induced angiogenesis in vivo. J Cutan Pathol 20:399–406PubMedGoogle Scholar
  71. 71.
    Collins T, Read MA, Neish AS, Whitley MZ, Thanos D, Maniatis T (1995) Transcriptional regulation of endothelial cell adhesion molecules: NF-kappa B and cytokine-inducible enhancers. FASEB J 9:899–909PubMedGoogle Scholar
  72. 72.
    Fukumura D, Salehi HA, Witwer B, Tuma RF, Melder RJ, Jain RK (1995) Tumor necrosis factor alpha-induced leukocyte adhesion in normal and tumor vessels: effect of tumor type, transplantation site, and host strain. Cancer Res 55:4824–4829PubMedGoogle Scholar
  73. 73.
    Nooijen PT, Eggermont AM, Verbeek MM, Schalkwijk L, Buurman WA, de Waal RM, Ruiter DJ (1996) Transient induction of E-selectin expression following TNF alpha-based isolated limb perfusion in melanoma and sarcoma patients is not tumor specific. J Immunother Emphasis Tumor Immunol 19:33–44PubMedGoogle Scholar
  74. 74.
    Renard N, Lienard D, Lespagnard L, Eggermont A, Heimann R, Lejeune F (1994) Early endothelium activation and polymorphonuclear cell invasion precede specific necrosis of human melanoma and sarcoma treated by intravascular high-dose tumour necrosis factor alpha (rTNF alpha). Int J Cancer 57:656–663PubMedGoogle Scholar
  75. 75.
    Fujiwara H, Hamaoka T (2001) Coordination of chemokine and adhesion systems in intratumoral T cell migration responsible for the induction of tumor regression. Int Immunopharmacol 1:613–623CrossRefPubMedGoogle Scholar
  76. 76.
    Ogawa M, Tsutsui T, Zou JP, Mu J, Wijesuriya R, Yu WG, Herrmann S, Kubo T, Fujiwara H, Hamaoka T (1997) Enhanced induction of very late antigen 4/lymphocyte function-associated antigen 1-dependent T-cell migration to tumor sites following administration of interleukin 12. Cancer Res 57:2216–2222PubMedGoogle Scholar
  77. 77.
    Ogawa M, Yu WG, Umehara K, Iwasaki M, Wijesuriya R, Tsujimura T, Kubo T, Fujiwara H, Hamaoka T (1998) Multiple roles of interferon-gamma in the mediation of interleukin 12–induced tumor regression. Cancer Res 58:2426–2432PubMedGoogle Scholar
  78. 78.
    Ogawa M, Umehara K, Yu WG, Uekusa Y, Nakajima C, Tsujimura T, Kubo T, Fujiwara H, Hamaoka T (1999) A critical role for a peritumoral stromal reaction in the induction of T-cell migration responsible for interleukin-12-induced tumor regression. Cancer Res 59:1531–1538PubMedGoogle Scholar
  79. 79.
    Nakajima C, Uekusa Y, Iwasaki M, Yamaguchi N, Mukai T, Gao P, Tomura M, Ono S, Tsujimura T, Fujiwara H, Hamaoka T (2001) A role of interferon-gamma (IFN-gamma) in tumor immunity: T cells with the capacity to reject tumor cells are generated but fail to migrate to tumor sites in IFN-gamma-deficient mice. Cancer Res 61:3399–3405PubMedGoogle Scholar
  80. 80.
    Hess SD, Egilmez NK, Bailey N, Anderson TM, Mathiowitz E, Bernstein SH, Bankert RB (2003) Human CD4+ T cells present within the microenvironment of human lung tumors are mobilized by the local and sustained release of IL-12 to kill tumors in situ by indirect effects of IFN-gamma. J Immunol 170:400–412PubMedGoogle Scholar
  81. 81.
    Wang JM, Deng X, Gong W, Su S (1998) Chemokines and their role in tumor growth and metastasis. J Immunol Methods 220:1–17CrossRefPubMedGoogle Scholar
  82. 82.
    Arenberg DA, Zlotnick A, Strom SR, Burdick MD, Strieter RM (2001) The murine CC chemokine, 6C-kine, inhibits tumor growth and angiogenesis in a human lung cancer SCID mouse model. Cancer Immunol Immunother 49:587–592CrossRefPubMedGoogle Scholar
  83. 83.
    Sharma S, Yang SC, Hillinger S, Zhu LX, Huang M, Batra RK, Lin JF, Burdick MD, Strieter RM, Dubinett SM (2003) SLC/CCL21-mediated anti-tumor responses require IFN-gamma, MIG/CXCL9 and IP-10/CXCL10. Mol Cancer 2:22CrossRefPubMedGoogle Scholar
  84. 84.
    White ES, Strieter RM, Arenberg DA (2002) Chemokines as therapeutic targets in non-small cell lung cancer. Curr Med Chem Anti-Cancer Agents 2:403–417Google Scholar
  85. 85.
    Homey B, Muller A, Zlotnik A (2002) Chemokines: agents for the immunotherapy of cancer? Nat Rev Immunol 2:175–184CrossRefPubMedGoogle Scholar
  86. 86.
    Sgadari C, Farber JM, Angiolillo AL, Liao F, Teruya-Feldstein J, Burd PR, Yao L, Gupta G, Kanegane C, Tosato G (1997) Mig, the monokine induced by interferon-gamma, promotes tumor necrosis in vivo. Blood 89:2635–2643PubMedGoogle Scholar
  87. 87.
    Vicari AP, Ait-Yahia S, Chemin K, Mueller A, Zlotnik A, Caux C (2000) Antitumor effects of the mouse chemokine 6Ckine/SLC through angiostatic and immunological mechanisms. J Immunol 165:1992–2000PubMedGoogle Scholar
  88. 88.
    Sharma S, Stolina M, Luo J, Strieter RM, Burdick M, Zhu LX, Batra RK, Dubinett SM(2000) Secondary lymphoid tissue chemokine mediates T cell-dependent antitumor responses in vivo. J Immunol 164, 4558–4563Google Scholar
  89. 89.
    Addison CL, Arenberg DA, Morris SB, Xue YY, Burdick MD, Mulligan MS, Iannettoni MD, Strieter RM (2000) The CXC chemokine, monokine induced by interferon-gamma, inhibits non- small cell lung carcinoma tumor growth and metastasis. Hum Gene Ther 11:247–261Google Scholar
  90. 90.
    Luther SA, Lopez T, Bai W, Hanahan D, Cyster JG (2000) BLC expression in pancreatic islets causes B cell recruitment and lymphotoxin-dependent lymphoid neogenesis. Immunity 12:471–481PubMedGoogle Scholar
  91. 91.
    Fan L, Reilly CR, Luo Y, Dorf ME, Lo D (2000) Cutting edge: ectopic expression of the chemokine TCA4/SLC is sufficient to trigger lymphoid neogenesis. J Immunol 164:3955–3959PubMedGoogle Scholar
  92. 92.
    Gollnick SO, Evans SS, Baumann H, Owczarczak B, Maier P, Vaughan L Wang WC, Unger EL, Henderson BW (2003) The role of cytokines in photodynamic therapy (PDT) induced local and systemic inflammation (in press).Google Scholar
  93. 93.
    Hanahan D (1985) Heritable formation of pancreatic beta-cell tumours in transgenic mice expressing recombinant insulin/simian virus 40 oncogenes. Nature 315:115–122PubMedGoogle Scholar
  94. 94.
    Cao ZA, Daniel D, Hanahan D (2002) Sub-lethal radiation enhances anti-tumor immunotherapy in a transgenic mouse model of pancreatic cancer. BMC Cancer 2:11CrossRefPubMedGoogle Scholar
  95. 95.
    Ganss R, Limmer A, Sacher T, Arnold B, Hammerling GJ (1999) Autoaggression and tumor rejection: it takes more than self-specific T-cell activation. Immunol Rev 169:263–272PubMedGoogle Scholar
  96. 96.
    Burd R, Dziedzic TS, Xu Y, Caligiuri MA, Subjeck JR, Repasky EA (1998) Tumor cell apoptosis, lymphocyte recruitment and tumor vascular changes are induced by low temperature, long duration (fever-like) whole body hyperthermia. J Cell Physiol 177:137–147PubMedGoogle Scholar
  97. 97.
    Di YP, Repasky EA, Subjeck JR (1997) Distribution of HSP70, protein kinase C, and spectrin is altered in lymphocytes during a fever-like hyperthermia exposure. J Cell Physiol 172:44–54CrossRefPubMedGoogle Scholar
  98. 98.
    Ostberg JR, Repasky EA (2000) Use of mild, whole body hyperthermia in cancer therapy. Immunol Invest 29:139–142PubMedGoogle Scholar
  99. 99.
    Repasky EA, Tims E, Pritchard M, Burd R (1999) Characterization of mild whole-body hyperthermia protocols using human breast, ovarian, and colon tumors grown in severe combined immunodeficient mice. Infect Dis Obstet Gynecol 7:91–97CrossRefPubMedGoogle Scholar
  100. 100.
    Wang XY, Kazim L, Repasky EA, Subjeck JR (2001) Characterization of heat shock protein 110 and glucose-regulated protein 170 as cancer vaccines and the effect of fever-range hyperthermia on vaccine activity. J Immunol 166:490–497PubMedGoogle Scholar
  101. 101.
    Evans SS, Wang WC, Bain MD, Burd R, Ostberg JR, Repasky EA (2001) Fever-range hyperthermia dynamically regulates lymphocyte delivery to high endothelial venules. Blood 97:2727–2733CrossRefPubMedGoogle Scholar
  102. 102.
    Kong G, Braun RD, Dewhirst MW (2000) Hyperthermia enables tumor-specific nanoparticle delivery: effect of particle size. Cancer Res 60:4440–4445PubMedGoogle Scholar
  103. 103.
    Kong G, Braun RD, Dewhirst MW (2001) Characterization of the effect of hyperthermia on nanoparticle extravasation from tumor vasculature. Cancer Res 61:3027–3032PubMedGoogle Scholar
  104. 104.
    Moroz P, Jones SK, Gray BN (2001) Status of hyperthermia in the treatment of advanced liver cancer. J Surg Oncol 77:259–269CrossRefPubMedGoogle Scholar
  105. 105.
    Fajardo LF, Prionas SD (1994) Endothelial cells and hyperthermia. Int J Hyperthermia 10:347–353PubMedGoogle Scholar
  106. 106.
    Wust P, Hildebrandt B, Sreenivasa G, Rau B, Gellermann J, Riess H, Felix R, Schlag PM (2002) Hyperthermia in combined treatment of cancer. Lancet Oncol 3:487–497CrossRefPubMedGoogle Scholar
  107. 107.
    Wang WC, Goldman LM, Schleider DM, Appenheimer MM, Subjeck JR, Repasky EA, Evans SS (1998) Fever-range hyperthermia enhances L-selectin-dependent adhesion of lymphocytes to vascular endothelium. J Immunol 160:961–969PubMedGoogle Scholar
  108. 108.
    Evans SS, Schleider DM, Bowman LA, Francis ML, Kansas GS, Black JD (1999) Dynamic association of L-selectin with the lymphocyte cytoskeletal matrix. J Immunol 162:3615–3624PubMedGoogle Scholar
  109. 109.
    Evans SS, Bain MD, Wang WC (2000) Fever-range hyperthermia stimulates alpha4beta7 integrin-dependent lymphocyte-endothelial adhesion. Int J Hyperthermia 16:45–59CrossRefPubMedGoogle Scholar
  110. 110.
    Evans SS, Frey M, Schleider DM, Bruce R, WANG WC, Repasky E, Appenheimer MM (1998) Regulation of leukocyte-endothelail cell interactions in tumor immunity. In: Croce AM (ed) The biology of tumors, Plenum Press, New York, pp 273–286Google Scholar
  111. 111.
    Kraybill WG, Olenki T, Evans SS, Ostberg JR, O'Leary KA, Gibbs JF, Repasky EA (2002) A phase I study of fever-range whole body hyperthermia (FR-WBH) in patients with advanced solid tumours: correlation with mouse models. Int J Hyperthermia 18:253–266CrossRefPubMedGoogle Scholar
  112. 112.
    Ostberg JR, Repasky EA (2000) Comparison of the effects of two different whole body hyperthermia protocols on the distribution of murine leukocyte populations. Int J Hyperthermia 16:29–43CrossRefPubMedGoogle Scholar
  113. 113.
    Demaria S, Volm MD, Shapiro RL, Yee HT, Oratz R, Formenti SC, Muggia F, Symmans WF (2001) Development of tumor-infiltrating lymphocytes in breast cancer after neoadjuvant paclitaxel chemotherapy. Clin Cancer Res 7:3025–3030PubMedGoogle Scholar
  114. 114.
    Parshad R, Kapoor S, Gupta SD, Kumar A, Chattopadhyaya TK (2002) Does famotidine enhance tumor infiltrating lymphocytes in breast cancer? Results of a randomized prospective pilot study. Acta Oncol 41:362–365CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Department of ImmunologyRoswell Park Cancer InstituteBuffaloUSA

Personalised recommendations