Preconditioning thermal therapy: Flipping the switch on IL-6 for anti-tumour immunity

International Journal of Hyperthermia

Volumn 29, Issue 5, 2013, Pages 464-473

  Mikucki, Maryann E ^a   Fisher, Daniel T ^a   Ku, Amy W ^a   Appenheimer, Michelle M ^a   Muhitch, Jason B ^a   Evans, Sharon S ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

Immunotherapy; Interleukin 6; Lymphocyte trafficking; Systemic thermal therapy; Tumour vasculature

Indexed keywords

INTERLEUKIN 6;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNOTHERAPY; HUMAN; HYPERTHERMIC THERAPY; LYMPHOCYTE MIGRATION; NONHUMAN; T LYMPHOCYTE; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; WARMING;

EID: 84881146048     PISSN: 02656736     EISSN: 14645157     Source Type: Journal    
DOI: 10.3109/02656736.2013.807440     Document Type: Article

References (96)

1. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006;313:1960-4. (Pubitemid 44498003)
2. Fridman WH, Galon J, Pages F, Tartour E, Sautes-Fridman C, Kroemer G. Prognostic and predictive impact of intra- and peritumoral immune infiltrates. Cancer Res 2011;71:5601-5.
3. Fridman WH, Pages F, Sautes-Fridman C, Galon J. The immune contexture in human tumours: Impact on clinical outcome. Nat Rev Cancer 2012;12:298-306.
4. Gajewski TF, Woo SR, Zha Y, Spaapen R, Zheng Y, Corrales L, et al. Cancer immunotherapy strategies based on overcoming barriers within the tumor microenvironment. Curr Opin Immunol 2013;25:268-76.
5. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell 2010;140:883-99.
6. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008;454:436-44.
7. Coussens LM, Zitvogel L, Palucka AK. Neutralizing tumorpromoting chronic inflammation: A magic bullet? Science 2013; 339:286-91.
8. Sato E, Olson SH, Ahn J, Bundy B, Nishikawa H, Qian F, et al. Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc Natl Acad Sci USA 2005;102:18538-43. (Pubitemid 43011261)
9. Fisher DT, Chen Q, Appenheimer MM, Skitzki J, Wang WC, Odunsi K, et al. Hurdles to lymphocyte trafficking in the tumor microenvironment: Implications for effective immunotherapy. Immunol Invest 2006;35:251-77. (Pubitemid 44266776)
10. Rosenberg SA, Restifo NP, Yang JC, Morgan RA, Dudley ME. Adoptive cell transfer: A clinical path to effective cancer immunotherapy. Nat Rev Cancer 2008;8:299-308. (Pubitemid 351430867)
11. Zitvogel L, Kepp O, Kroemer G. Immune parameters affecting the efficacy of chemotherapeutic regimens. Nat Rev Clin Oncol 2011; 8:151-60.
12. Mattarollo SR, Loi S, Duret H, Ma Y, Zitvogel L, Smyth MJ. Pivotal role of innate and adaptive immunity in anthracycline chemotherapy of established tumors. Cancer Res 2011;71:4809-20.
13. Lee Y, Auh SL, Wang Y, Burnette B, Meng Y, Beckett M, et al. Therapeutic effects of ablative radiation on local tumor require CD8+ T cells: Changing strategies for cancer treatment. Blood 2009;114:589-95.
14. Boon T, Coulie PG, Eynde BJ, Bruggen PV. Human T cell responses against melanoma. Annu Rev Immunol 2006;24: 175-208.
15. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010;363:711-23.
16. Culver ME, Gatesman ML, Mancl EE, Lowe DK. Ipilimumab: A novel treatment for metastatic melanoma. Ann Pharmacother 2011;45:510-19.
17. Sondak VK, Smalley KS, Kudchadkar R, Grippon S, Kirkpatrick P. Ipilimumab. Nat Rev Drug Discov 2011;10:411-12.
18. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012;366:2443-54.
19. Turnis ME, Korman AJ, Drake CG, Vignali DA. Combinatorial Immunotherapy: PD-1 may not be LAG-ing behind any more. Oncoimmunology 2012;1:1172-4.
20. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: Integrating immunity's roles in cancer suppression and promotion. Science 2011;331:1565-70.
21. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 2012; 12:253-68.
22. Vardam TD, Zhou L, Appenheimer MM, Chen Q, Wang WC, Baumann H, et al. Regulation of a lymphocyte-endothelial-IL-6 trans-signaling axis by fever-range thermal stress: Hot spot of immune surveillance. Cytokine 2007;39:84-96. (Pubitemid 47454713)
23. Evans SS, Fisher DT, Skitzki JJ, Chen Q. Targeted regulation of a lymphocyte-endothelial-interleukin-6 axis by thermal stress. Int J Hyperthermia 2008;24:67-78. (Pubitemid 351167620)
24. Luster AD, Alon R, von Andrian UH. Immune cell migration in inflammation: Present and future therapeutic targets. Nat Immunol 2005;6:1182-90. (Pubitemid 43045626)
25. Girard JP, Moussion C, Forster R. HEVs, lymphatics and homeostatic immune cell trafficking in lymph nodes. Nat Rev Immunol 2012;12:762-73.
26. Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: The leukocyte adhesion cascade updated. Nat Rev Immunol 2007;7:678-89. (Pubitemid 47327397)
27. Silver JS, Hunter CA. gp130 at the nexus of inflammation, autoimmunity, and cancer. J Leukoc Biol 2010;88:1145-56.
28. Chen Q, Evans SS. Thermal regulation of lymphocyte trafficking: Hot spots of the immune response. Int J Hyperthermia 2005;21: 723-9. (Pubitemid 41807099)
29. Chen Q, Wang WC, Evans SS. Tumor microvasculature as a barrier to antitumor immunity. Cancer Immunol Immunother 2003;52: 670-9. (Pubitemid 37363637)
30. Griffioen AW. Anti-angiogenesis: Making the tumor vulnerable to the immune system. Cancer Immunol Immunother 2008;57: 1553-8.
31. Boissonnas A, Fetler L, Zeelenberg IS, Hugues S, Amigorena S. In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor. J Exp Med 2007;204:345-56. (Pubitemid 46294550)
32. Wu NZ, Klitzman B, Dodge R, Dewhirst MW. Diminished leukocyte-endothelium interaction in tumor microvessels. Cancer Res 1992;52:4265-8.
33. Bessa X, Elizalde JI, Mitjans F, Pinol V, Miquel R, Panes J, et al. Leukocyte recruitment in colon cancer: Role of cell adhesion molecules, nitric oxide, and transforming growth factor beta1. Gastroenterology 2002;122:1122-32. (Pubitemid 34267293)
34. Dirkx AE, oude Egbrink MG, Castermans K, van der Schaft DW, Thijssen VL, Dings RP, et al. Anti-angiogenesis therapy can overcome endothelial cell anergy and promote leukocyteendothelium interactions and infiltration in tumors. FASEB J 2006;20:621-30. (Pubitemid 44933306)
35. Fisher DT, Chen Q, Skitzki JJ, Muhitch JB, Zhou L, Appenheimer MM, et al. IL-6 trans-signaling licenses mouse and human tumor microvascular gateways for trafficking of cytotoxic T cells. J Clin Invest 2011;121:3846-59.
36. Yuan F, Dellian M, Fukumura D, Leunig M, Berk DA, Torchilin VP, et al. Vascular permeability in a human tumor xenograft: Molecular size dependence and cutoff size. Cancer Res 1995;55: 3752-6.
37. Kong G, Braun RD, Dewhirst MW. Hyperthermia enables tumorspecific nanoparticle delivery: effect of particle size. Cancer Res 2000;60:4440-5. (Pubitemid 32103623)
38. Rowe-Horwege RW. Hyperthermia, Systemic. Encyclopedia of Medical Devices and Instrumentation. Wiley online, 2006. doi: 10.1002/0471732877.emd138.
39. Burd R, Dziedzic TS, Xu Y, Caligiuri MA, Subjeck JR, Repasky EA. Tumor cell apoptosis, lymphocyte recruitment and tumor vascular changes are induced by low temperature, long duration (fever-like) whole body hyperthermia. J Cell Physiol 1998;177: 137-47. (Pubitemid 28421530)
40. Jones EL, Oleson JR, Prosnitz LR, Samulski TV, Vujaskovic Z, Yu D, et al. Randomized trial of hyperthermia and radiation for superficial tumors. J Clin Oncol 2005;23:3079-85. (Pubitemid 46224131)
41. van der Zee J, Gonzalez Gonzalez D, van Rhoon GC, van Dijk JD, van Putten WL, Hart AA. Comparison of radiotherapy alone with radiotherapy plus hyperthermia in locally advanced pelvic tumours: A prospective, randomised, multicentre trial. Dutch Deep Hyperthermia Group. Lancet 2000;355:1119-25. (Pubitemid 30172932)
42. Issels RD, Lindner LH, Verweij J, Wust P, Reichardt P, Schem BC, et al. Neo-adjuvant chemotherapy alone or with regional hyperthermia for localised high-risk soft-tissue sarcoma: A randomised phase 3 multicentre study. Lancet Oncol 2010;11: 561-70.
43. Sen A, Capitano ML, Spernyak JA, Schueckler JT, Thomas S, Singh AK, et al. Mild elevation of body temperature reduces tumor interstitial fluid pressure and hypoxia and enhances efficacy of radiotherapy in murine tumor models. Cancer Res 2011;71: 3872-80.
44. Sumiyoshi K, Strebel FR, Rowe RW, Bull JM. The effect of wholebody hyperthermia combined with 'metronomic' chemotherapy on rat mammary adenocarcinoma metastases. Int J Hyperthermia 2003;19:103-18. (Pubitemid 36304680)
45. Kraybill WG, Olenki T, Evans SS, Ostberg JR, O'Leary KA, Gibbs JF, et al. 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 2002;18:253-66. (Pubitemid 34618582)
46. Ostberg JR, Dayanc BE, Yuan M, Oflazoglu E, Repasky EA. Enhancement of natural killer (NK) cell cytotoxicity by fever-range thermal stress is dependent on NKG2D function and is associated with plasma membrane NKG2D clustering and increased expression of MICA on target cells. J Leukoc Biol 2007;82:1322-31. (Pubitemid 350133530)
47. Ostberg JR, Ertel BR, Lanphere JA. An important role for granulocytes in the thermal regulation of colon tumor growth. Immunol Invest 2005;34:259-72. (Pubitemid 41176818)
48. Thrall DE, Prescott DM, Samulski TV, Rosner GL, Denman DL, Legorreta RL, et al. Radiation plus local hyperthermia versus radiation plus the combination of local and whole-body hyperthermia in canine sarcomas. Int J Radiat Oncol Biol Phys 1996;34: 1087-96. (Pubitemid 26105446)
49. Evans SS, Wang WC, Bain MD, Burd R, Ostberg JR, Repasky EA. Fever-range hyperthermia dynamically regulates lymphocyte delivery to high endothelial venules. Blood 2001;97:2727-33.
50. Chen Q, Fisher DT, Clancy KA, Gauguet JM, Wang WC, Unger E, et al. Fever-range thermal stress promotes lymphocyte trafficking across high endothelial venules via an interleukin 6 trans-signaling mechanism. Nat Immunol 2006;7:1299-308. (Pubitemid 46111251)
51. Chen Q, Clancy KA, Wang WC, Evans SS. Inflammatory cues controlling lymphocyte-endothelial interactions during fever-range thermal stress. In: Aird W, editor Endothelial Biomedicine. New York: Cambridge University Press, 2007, pp 471-9.
52. Skitzki JJ, Chen Q, Wang WC, Evans SS. Primary immune surveillance: Some like it hot. J Mol Med 2007;85:1361-7. (Pubitemid 350234095)
53. Evans SS, Bain MD, Wang WC. Fever-range hyperthermia stimulates alpha4beta7 integrin-dependent lymphocyte-endothelial adhesion. Int J Hyperthermia 2000;16:45-59. (Pubitemid 30050260)
54. Chen Q, Appenheimer MM, Muhitch JB, Fisher DT, Clancy KA, Miecznikowski JC, et al. Thermal facilitation of lymphocyte trafficking involves temporal induction of intravascular ICAM-1. Microcirculation 2009;16:143-58.
55. von Andrian UH, Mempel TR. Homing and cellular traffic in lymph nodes. Nat Rev Immunol 2003;3:867-78. (Pubitemid 37411716)
56. Carman CV, Springer TA. A transmigratory cup in leukocyte diapedesis both through individual vascular endothelial cells and between them. J Cell Biol 2004;167:377-88. (Pubitemid 39435079)
57. Karin M. Nuclear factor-kappaB in cancer development and progression. Nature 2006;441:431-6. (Pubitemid 44050137)
58. Tu B, Du L, Fan QM, Tang Z, Tang TT. STAT3 activation by IL-6 from mesenchymal stem cells promotes the proliferation and metastasis of osteosarcoma. Cancer Lett 2012;325:80-8.
59. Bromberg JF, Wrzeszczynska MH, Devgan G, Zhao Y, Pestell RG, Albanese C, et al. Stat3 as an oncogene. Cell 1999;98:295-303. (Pubitemid 29380565)
60. Yu H, Kortylewski M, Pardoll D. Crosstalk between cancer and immune cells: Role of STAT3 in the tumour microenvironment. Nat Rev Immunol 2007;7:41-51. (Pubitemid 46020826)
61. Wang Y, Niu XL, Qu Y, Wu J, Zhu YQ, Sun WJ, et al. Autocrine production of interleukin-6 confers cisplatin and paclitaxel resistance in ovarian cancer cells. Cancer Lett 2010;295:110-23.
62. Kim MY, Oskarsson T, Acharyya S, Nguyen DX, Zhang XH, Norton L, et al. Tumor self-seeding by circulating cancer cells. Cell 2009;139:1315-26.
63. Chen CC, Chen WC, Lu CH, Wang WH, Lin PY, Lee KD, et al. Significance of interleukin-6 signaling in the resistance of pharyngeal cancer to irradiation and the epidermal growth factor receptor inhibitor. Int J Radiat Oncol Biol Phys 2010;76:1214-24.
64. Gilbert LA, Hemann MT. DNA damage-mediated induction of a chemoresistant niche. Cell 2010;143:355-66.
65. Rose-John S, Scheller J, Elson G, Jones SA. Interleukin-6 biology is coordinated by membrane-bound and soluble receptors: role in inflammation and cancer. J Leukoc Biol 2006;80:227-36. (Pubitemid 44835496)
66. Fischer M, Goldschmitt J, Peschel C, Brakenhoff JP, Kallen KJ, Wollmer A, et al. I. A bioactive designer cytokine for human hematopoietic progenitor cell expansion. Nat Biotechnol 1997; 15:142-5. (Pubitemid 27081778)
67. Schooltink H, Rose-John S. Cytokines as therapeutic drugs. J Interferon Cytokine Res 2002;22:505-16. (Pubitemid 34639141)
68. Seinen JM, Hoekstra HJ. Isolated limb perfusion of soft tissue sarcomas: A comprehensive review of literature. Cancer Treat Rev 2013;39:569-77.
69. Chan DL, Morris DL, Rao A, Chua TC. Intraperitoneal chemotherapy in ovarian cancer: a review of tolerance and efficacy. Cancer Manag Res 2012;4:413-22.
70. Haen SP, Pereira PL, Salih HR, Rammensee HG, Gouttefangeas C. More than just tumor destruction: Immunomodulation by thermal ablation of cancer. Clin Dev Immunol 2011;2011:160250-69.
71. Herzog TJ. The role of heated intraperitoneal chemotherapy (HIPEC) in ovarian cancer: hope or hoax? Ann Surg Oncol 2012; 19:3998-4000.
72. Dewhirst MW, Vujaskovic Z, Jones E, Thrall D. Re-setting the biologic rationale for thermal therapy. Int J Hyperthermia 2005;21: 779-90. (Pubitemid 41818597)
73. Skitzki J, Craig RA, Okuyama R, Knibbs RN, McDonagh K, Chang AE, et al. Donor cell cycling, trafficking, and accumulation during adoptive immunotherapy for murine lung metastases. Cancer Res 2004;64:2183-91. (Pubitemid 38339471)
74. Bromley SK, Mempel TR, Luster AD. Orchestrating the orchestrators: Chemokines in control of T cell traffic. Nat Immunol 2008; 9:970-80.
75. Rot A, von Andrian UH. Chemokines in innate and adaptive host defense: Basic chemokinese grammar for immune cells. Annu Rev Immunol 2004;22:891-928. (Pubitemid 38680444)
76. Rossi D, Zlotnik A. The biology of chemokines and their receptors. Annu Rev Immunol 2000;18:217-42.
77. Mlecnik B, Tosolini M, Charoentong P, Kirilovsky A, Bindea G, Berger A, et al. Biomolecular network reconstruction identifies T-cell homing factors associated with survival in colorectal cancer. Gastroenterology 2010;138:1429-40.
78. Harlin H, Meng Y, Peterson AC, Zha Y, Tretiakova M, Slingluff C, et al. Chemokine expression in melanoma metastases associated with CD8+ T-cell recruitment. Cancer Res 2009;69:3077-85.
79. McLoughlin RM, Jenkins BJ, Grail D, Williams AS, Fielding CA, Parker CR, et al. IL-6 trans-signaling via STAT3 directs T cell infiltration in acute inflammation. Proc Natl Acad Sci USA 2005; 102:9589-94. (Pubitemid 40981725)
80. Romano M, Sironi M, Toniatti C, Polentarutti N, Fruscella P, Ghezzi P, et al. Role of IL-6 and its soluble receptor in induction of chemokines and leukocyte recruitment. Immunity 1997;6: 315-25. (Pubitemid 27148598)
81. Biswas P, Delfanti F, Bernasconi S, Mengozzi M, Cota M, Polentarutti N, et al. Interleukin-6 induces monocyte chemotactic protein-1 in peripheral blood mononuclear cells and in the U937 cell line. Blood 1998;91:258-65. (Pubitemid 28018753)
82. Coward J, Kulbe H, Chakravarty P, Leader D, Vassileva V, Leinster DA, et al. Interleukin-6 as a therapeutic target in human ovarian cancer. Clin Cancer Res 2011;17:6083-96.
83. Acharyya S, Oskarsson T, Vanharanta S, Malladi S, Kim J, Morris PG, et al. A CXCL1 paracrine network links cancer chemoresistance and metastasis. Cell 2012;150:165-78.
84. Ahn GO, Tseng D, Liao CH, Dorie MJ, Czechowicz A, Brown JM. Inhibition of Mac-1 (CD11b/CD18) enhances tumor response to radiation by reducing myeloid cell recruitment. Proc Natl Acad Sci USA 2010;107:8363-8.
85. Bouma-ter Steege JC, Baeten CI, Thijssen VL, Satijn SA, Verhoeven IC, Hillen HF, et al. Angiogenic profile of breast carcinoma determines leukocyte infiltration. Clin Cancer Res 2004; 10:7171-8. (Pubitemid 39487702)
86. Huet O, Laemmel E, Fu Y, Dupic L, Aprico A, Andrews KL, et al. Interleukin 10 antioxidant effect decreases leukocytes/endothelial interaction induced by tumor necrosis factor alpha. Shock 2013;39: 83-8.
87. Walia B, Wang L, Merlin D, Sitaraman SV. TGF-beta downregulates IL-6 signaling in intestinal epithelial cells: Critical role of SMAD-2. Faseb J 2003;17:2130-2.
88. Niemand C, Nimmesgern A, Haan S, Fischer P, Schaper F, Rossaint R, et al. Activation of STAT3 by IL-6 and IL-10 in primary human macrophages is differentially modulated by suppressor of cytokine signaling 3. J Immunol 2003;170:3263-72. (Pubitemid 36302204)
89. Josefowicz SZ, Lu LF, Rudensky AY. Regulatory T cells: Mechanisms of differentiation and function. Annu Rev Immunol 2012;30:531-64.
90. Manzoor AA, Lindner LH, Landon CD, Park JY, Simnick AJ, Dreher MR, et al. Overcoming limitations in nanoparticle drug delivery: Triggered, intravascular release to improve drug penetration into tumors. Cancer Res 2012;72:5566-75.
91. Li L, Ten Hagen TL, Hossann M, Suss R, van Rhoon GC, Eggermont AM, et al. Mild hyperthermia triggered doxorubicin release from optimized stealth thermosensitive liposomes improves intratumoral drug delivery and efficacy. J Control Release 2013; 168:142-50.
92. Urosevic M, Maier T, Benninghoff B, Slade H, Burg G, Dummer R. Mechanisms underlying imiquimod-induced regression of basal cell carcinoma in vivo. Arch Dermatol 2003;139:1325-32. (Pubitemid 37248283)
93. Prins RM, Craft N, Bruhn KW, Khan-Farooqi H, Koya RC, Stripecke R, et al. The TLR-7 agonist, imiquimod, enhances dendritic cell survival and promotes tumor antigen-specific T cell priming: Relation to central nervous system antitumor immunity. J Immunol 2006;176:157-64. (Pubitemid 43023259)
94. Lugade AA, Sorensen EW, Gerber SA, Moran JP, Frelinger JG, Lord EM. Radiation-induced IFN-gamma production within the tumor microenvironment influences antitumor immunity. J Immunol 2008;180:3132-9.
95. Cao ZA, Daniel D, Hanahan D. Sub-lethal radiation enhances antitumor immunotherapy in a transgenic mouse model of pancreatic cancer. BMC Cancer 2002;2:11-21.
96. Ganss R, Ryschich E, Klar E, Arnold B, Hammerling GJ. Combination of T-cell therapy and trigger of inflammation induces remodeling of the vasculature and tumor eradication. Cancer Res 2002;62:1462-70. (Pubitemid 34407808)