Blockade of hyaluronan inhibits IL-2-induced vascular leak syndrome and maintains effectiveness of IL-2 treatment for metastatic melanoma

Journal of Immunology

Volumn 179, Issue 6, 2007, Pages 3715-3723

  Guan, Hongbing ^a   Nagarkatti, Prakash S ^a   Nagarkatti, Mitzi ^a  

^a UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYALURONIC ACID; HYALURONIC ACID BINDING PROTEIN; INTERLEUKIN 2; PROTEIN PEP 1; UNCLASSIFIED DRUG; C1QBP PROTEIN, MOUSE; CARRIER PROTEIN; HERMES ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CAPILLARY LEAK SYNDROME; CELL KILLING; CONTROLLED STUDY; CYTOTOXICITY; DRUG BINDING; ENDOTHELIUM CELL; FEMALE; HISTOPATHOLOGY; INTERSTITIUM; LUNG METASTASIS; LYMPHOCYTE MIGRATION; LYMPHOKINE ACTIVATED KILLER CELL; MELANOMA; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; VASCULAR LEAK SYNDROME; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL DIFFERENTIATION; CYTOLOGY; DRUG ANTAGONISM; EXPERIMENTAL MELANOMA; IMMUNOLOGY; LUNG TUMOR; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR ASSOCIATED LEUKOCYTE; VASCULAR ENDOTHELIUM; VASCULARIZATION;

ANIMALS; ANTIGENS, CD44; APOPTOSIS; CAPILLARY LEAK SYNDROME; CARRIER PROTEINS; CELL DIFFERENTIATION; CYTOTOXICITY, IMMUNOLOGIC; ENDOTHELIUM, VASCULAR; FEMALE; HYALURONIC ACID; INTERLEUKIN-2; KILLER CELLS, LYMPHOKINE-ACTIVATED; LUNG NEOPLASMS; LYMPHOCYTES, TUMOR-INFILTRATING; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL;

EID: 35748937057     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.6.3715     Document Type: Article

References (45)

1. Rosenberg, S. A., J. C. Yang, S. L. Topalian, D. J. Schwartzentruber, J. S. Weber, D. R. Parkinson, C. A. Seipp, J. H. Einhorn, and D. E. White. 1994. Treatment of 283 consecutive patients with metastatic melanoma or renal cell cancer using high-dose bolus interleukin 2. J. Am. Med. Assoc. 271: 907-913.
2. Baluna, R., and E. S. Vitetta. 1997. Vascular leak syndrome: a side effect of immunotherapy. Immunopharmacology 37: 117-132.
3. Chelstrom, L. M., D. Finnegan, and F. M. Uckun. 1992. Treatment of BCL-1 murine B-cell leukemia with recombinant cytokines: comparative analysis of the anti-leukemic potential of interleukin 1α (IL-1β), interleukin 2 (IL-2), interleukin-6 (IL-6), tumor necrosis factor α (TNF α), granulocyte colony stimulating factor (G-CSF), granulocyte-macrophage colony stimulating factor (GM-CSF), and their combination. Leuk. Lymphoma 7: 79-86.
4. + T cells. Blood 100: 2159-2167.
5. + T cells in vivo after IL-2 treatment of patients with HIV infection. Proc. Natl. Acad. Sci. USA 99: 10712-10717.
6. Jacobson, E. L., F. Pilaro, and K. A. Smith. 1996. Rational interleukin 2 therapy for HIV positive individuals: daily low doses enhance immune function without toxicity. Proc. Natl. Acad. Sci. USA 93: 10405-10410.
7. de Gast, G. C., D. Batchelor, M. J. Kersten, F. A. Vyth-Dreese, J. Sein, W. F. van de Kasteele, W. J. Nooijen, O. E. Nieweg, M. A. de Waal, and W. Boogerd. 2003. Temozolomide followed by combined immunotherapy with GM-CSF, low-dose IL2 and IFN α in patients with metastatic melanoma. Br. J. Cancer 88: 175-180.
8. O'Brien, G. C., R. A. Cahill, D. J. Bouchier-Hayes, and H. P. Redmond. 2006. Co-immunotherapy with interleukin-2 and taurolidine for progressive metastatic melanoma. Ir. J. Med. Sci. 175: 10-14.
9. Cotran, R. S., J. S. Pober, M. A. Gimbrone, Jr., T. A. Springer, E. A. Wiebke, A. A. Gaspari, S. A. Rosenberg, and M. T. Lotze. 1988. Endothelial activation during interleukin 2 immunotherapy: a possible mechanism for the vascular leak syndrome. J. Immunol. 140: 1883-1888.
10. Baluna, R., J. Rizo, B. E. Gordon, V. Ghetie, and E. S. Vitetta. 1999. Evidence for a structural motif in toxins and interleukin-2 that may be responsible for binding to endothelial cells and initiating vascular leak syndrome. Proc. Natl. Acad. Sci. USA 96: 3957-3962.
11. Rosenstein, M., S. E. Ettinghausen, and S. A. Rosenberg. 1986. Extravasation of intravascular fluid mediated by the systemic administration of recombinant interleukin 2. J. Immunol. 137: 1735-1742.
12. Damle, N. K., and L. V. Doyle. 1989. IL-2-activated human killer lymphocytes but not their secreted products mediate increase in albumin flux across cultured endothelial monolayers: implications for vascular leak syndrome. J. Immunol. 142: 2660-2669.
13. Assier, E., V. Jullien, J. Lefort, J. L. Moreau, J. P. Di Santo, B. B. Vargaftig, J. R. Lapa e Silva, and J. Theze. 2004. NK cells and polymorphonuclear neutrophils are both critical for IL-2-induced pulmonary vascular leak syndrome. J. Immunol. 172: 7661-7668.
14. G-methyl-L-arginine, an inhibitor of nitric oxide synthesis, on interleukin-2-induced capillary leakage and antitumor responses in healthy and tumor-bearing mice. Cancer Immunol. Immunother. 42: 38-46.
15. G-nitro-L-arginine methyl ester, an inhibitor of nitric oxide synthesis, ameliorates interleukin 2-induced capillary leakage and reduces tumour growth in adenocarcinoma-bearing mice. Br. J. Cancer 73: 189-196.
16. ω-nitro-L-arginine methyl ester inhibits inflammatory liver injury induced by interleukin-2. J. Leukocyte Biol. 63: 22-30.
17. Rafi, A. Q., A. Zeytun, M. J. Bradley, D. P. Sponenberg, R. L. Grayson, M. Nagarkatti, and P. S. Nagarkatti. 1998. Evidence for the involvement of Fas ligand and perforin in the induction of vascular leak syndrome. J. Immunol. 161: 3077-3086.
18. Lentsch, A. B., F. N. Miller, and M. J. Edwards. 1999. Mechanisms of leukocyte-mediated tissue injury induced by interleukin-2. Cancer Immunol. Immunother. 47: 243-248.
19. Mustafa, A., R. J. McKallip, M. Fisher, R. Duncan, P. S. Nagarkatti, and M. Nagarkatti. 2002. Regulation of interleukin-2-induced vascular leak syndrome by targeting CD44 using hyaluronic acid and anti-CD44 antibodies. J. Immunother. 25: 476-488.
20. Rafi-Janajreh, A. Q., D. Chen, R. Schmits, T. W. Mak, R. L. Grayson, D. P. Sponenberg, M. Nagarkatti, and P. S. Nagarkatti. 1999. Evidence for the involvement of CD44 in endothelial cell injury and induction of vascular leak syndrome by IL-2. J. Immunol. 163: 1619-1627.
21. McKallip, R. J., M. Fisher, Y. Do, A. K. Szakal, U. Gunthert, P. S. Nagarkatti, and M. Nagarkatti. 2003. Targeted deletion of CD44v7 exon leads to decreased endothelial cell injury but not tumor cell killing mediated by interleukin-2-activated cytolytic lymphocytes. J. Biol. Chem. 278: 43818-43830.
22. Mummert, M. E., M. Mohamadzadeh, D. I. Mummert, N. Mizumoto, and A. Takashima. 2000. Development of a peptide inhibitor of hyaluronan-mediated leukocyte trafficking. J. Exp. Med. 192: 769-779.
23. + T regulatory cells in IL-2-induced vascular leak. Int. Immunol. 18: 1461-1471.
24. Mummert, M. E. 2005. Immunologic roles of hyaluronan. Immunol. Res. 31: 189-206.
25. Mummert, M. E., D. I. Mummert, L. Ellinger, and A. Takashima. 2003. Functional roles of hyaluronan in B16-F10 melanoma growth and experimental metastasis in mice. Mol. Cancer Ther. 2: 295-300.
26. Rudrabhatla, S. R., C. L. Mahaffey, and M. E. Mummert. 2006. Tumor microenvironment modulates hyaluronan expression: the lactate effect. J. Invest. Dermatol. 126: 1378-1387.
27. Kawasaki, M., K. Kuwano, N. Hagimoto, T. Matsuba, R. Kunitake, T. Tanaka, T. Maeyama, and N. Hara. 2000. Protection from lethal apoptosis in lipopolysaccharide-induced acute lung injury in mice by a caspase inhibitor. Am. J. Pathol. 157: 597-603.
28. Kuwano, K., R. Kunitake, T. Maeyama, N. Hagimoto, M. Kawasaki, T. Matsuba, M. Yoshimi, I. Inoshima, K. Yoshida, and N. Hara. 2001. Attenuation of bleomycin-induced pneumopathy in mice by a caspase inhibitor. Am. J. Physiol. 280: L316-L325.
29. Jiang, D., J. Liang, J. Fan, S. Yu, S. Chen, Y. Luo, G. D. Prestwich, M. M. Mascarenhas, H. G. Garg, D. A. Quinn, et al. 2005. Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat. Med. 11: 1173-1179.
30. Assier, E., V. Jullien, J. Lefort, J. L. Moreau, B. B. Vargaftig, J. R. Lapa e Silva, and J. Theze. 2005. Constitutive expression of IL-2Rβ chain and its effects on IL-2-induced vascular leak syndrome. Cytokine 32: 280-286.
31. Hammond-McKibben, D. M., A. Seth, P. S. Nagarkatti, and M. Nagarkatti. 1995. Characterization of factors regulating successful immunotherapy using a tumor-specific cytotoxic T lymphocyte clone: role of interleukin-2, cycling pattern of lytic activity and adhesion molecules. Int. J. Cancer 60: 828-836.
32. Estess, P., A. Nandi, M. Mohamadzadeh, and M. H. Siegelman. 1999. Interleukin 15 induces endothelial hyaluronan expression in vitro and promotes activated T cell extravasation through a CD44-dependent pathway in vivo. J. Exp. Med. 190: 9-19.
33. Suzuki, K., T. Yamamoto, T. Usui, K. Suzuki, P. Heldin, and H. Yamashita. 2003. Expression of hyaluronan synthase in intraocular proliferative diseases: regulation of expression in human vascular endothelial cells by transforming growth factor-α. Jpn. J. Ophthalmol. 47: 557-564.
34. Mohamadzadeh, M., H. DeGrendele, H. Arizpe, P. Estess, and M. Siegelman. 1998. Proinflammatory stimuli regulate endothelial hyaluronan expression and CD44/HA-dependent primary adhesion. J. Clin. Invest. 101: 97-108.
35. Seth, A., L. Gote, M. Nagarkatti, and P. S. Nagarkatti. 1991. T-cell-receptor-independent activation of cytolytic activity of cytotoxic T lymphocytes mediated through CD44 and gp90MEL-14. Proc. Natl. Acad. Sci. USA 88: 7877-7881.
36. Mummert, M. E., D. Mummert, D. Edelbaum, F. Hui, H. Matsue, and A. Takashima. 2002. Synthesis and surface expression of hyaluronan by dendritic cells and its potential role in antigen presentation. J. Immunol. 169: 4322-4331.
37. Rockey, D. C., J. J. Chung, C. M. McKee, and P. W. Noble. 1998. Stimulation of inducible nitric oxide synthase in rat liver by hyaluronan fragments. Hepatology 27: 86-92.
38. Taylor, K. R., J. M. Trowbridge, J. A. Rudisill, C. C. Termeer, J. C. Simon, and R. L. Gallo. 2004. Hyaluronan fragments stimulate endothelial recognition of injury through TLR4. J. Biol. Chem. 279: 17079-17084.
39. Locker, G. J., S. Kapiotis, M. Veitl, R. M. Mader, B. Stoiser, J. Kofler, A. E. Sieder, H. Rainer, G. G. Steger, C. Mannhalter, and O. F. Wagner. 1999. Activation of endothelium by immunotherapy with interleukin-2 in patients with malignant disorders. Br. J. Haematol. 105: 912-919.
40. Rodella, L., L. Zamai, R. Rezzani, M. Artico, G. Peri, M. Falconi, A. Facchini, G. Pelusi, and M. Vitale. 2001. Interleukin 2 and interleukin 15 differentially predispose natural killer cells to apoptosis mediated by endothelial and tumour cells. Br. J. Haematol. 115: 442-450.
41. Malyszko, J., J. S. Malyszko, S. Brzosko, S. Wolczynski, and M. Mysliwiec. 2005. Markers of endothelial cell activation/injury: CD146 and thrombomodulin are related to adiponectin in kidney allograft recipients. Am. J. Nephrol. 25: 203-210.
42. + regulatory T cells in cancer patients. Blood 107: 2409-2414.
43. high regulatory T cells. Blood 104: 895-903.
44. + regulatory T cells and for expansion of these cells. J. Immunol. 178: 2018-2027.
45. Atkins, M. B. 2006. Cytokine-based therapy and biochemotherapy for advanced melanoma. Clin. Cancer Res. 12: 2353s-2358s.