Interleukin-6 induced "Acute" phenotypic microenvironment promotes Th1 anti-tumor immunity in cryo-thermal therapy revealed by shotgun and parallel reaction monitoring proteomics

Theranostics

Volumn 6, Issue 6, 2016, Pages 773-794

  Xue, Ting ^a   Liu, Ping ^a   Zhou, Yong ^b   Liu, Kun ^a   Yang, Li ^b   Moritz, Robert L ^b   Yan, Wei ^a   Xu, Lisa X ^a  

^a Chinese National Human Genome Center at Shanghai   (China)

^b INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

Author keywords

"Acute" phase response; Cryo thermal therapy; Interleukin 6; Parallel reaction monitoring; Th1 anti tumor immunity

Indexed keywords

ACUTE PHASE PROTEIN; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 4; INTERLEUKIN 6; PROTEIN ICOSL; UNCLASSIFIED DRUG; INTERLEUKIN-6, MOUSE; PROTEOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CANCER GROWTH; CELL MATURATION; CHRONIC INFLAMMATION; COMPLEMENT SYSTEM; CONTROLLED STUDY; CRYO THERMAL THERAPY; CRYOTHERAPY; CYTOKINE PRODUCTION; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GEL ELECTROPHORESIS; LIQUID CHROMATOGRAPHY; LUNG METASTASIS; LYMPHOCYTE PROLIFERATION; MASS SPECTROMETRY; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEOMICS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TH1 CELL; THERMOTHERAPY; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; UPREGULATION; WESTERN BLOTTING; ANIMAL; BREAST NEOPLASMS; DISEASE MODEL; IMMUNOLOGY; METABOLISM; PATHOLOGY;

ANIMALS; BREAST NEOPLASMS; CRYOTHERAPY; DISEASE MODELS, ANIMAL; HYPERTHERMIA, INDUCED; INTERLEUKIN-6; MICE; PROTEOME; TH1 CELLS; TUMOR MICROENVIRONMENT;

EID: 84984850878     PISSN: None     EISSN: 18387640     Source Type: Journal    
DOI: 10.7150/thno.14394     Document Type: Article

References (91)

1. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA: a cancer journal for clinicians. 2015; 65: 87-108.
2. Hall-Craggs MA, Vaidya JS. Minimally invasive therapy for the treatment of breast tumours. European journal of radiology. 2002; 42: 52-7.
3. Vogl TJ, Farshid P, Naguib NN, Zangos S. Thermal ablation therapies in patients with breast cancer liver metastases: a review. European radiology. 2013; 23: 797-804.
4. Gage AM, Montes M, Gage AA. Destruction of hepatic and splenic tissue by freezing and heating. Cryobiology. 1982; 19: 172-9.
5. Hines-Peralta A, Hollander CY, Solazzo S, Horkan C, Liu ZJ, Goldberg SN. Hybrid radiofrequency and cryoablation device: preliminary results in an animal model. Journal of vascular and interventional radiology: JVIR. 2004; 15: 1111-20.
6. Kuz'menko A, Todor I, Mosienko V. The effect of the combined use of cryosurgery and hyperthermia on an experimental tumor process. Eksperimental'naia onkologiia. 1989; 12: 60-1.
7. Osinsky SP, Rikberg AB, Bubnovskaja LN, Trushina VA. Tumour pH drop after cryotreatment and enhancement of hyperthermia antitumour effect. Int J Hyperthermia. 1993; 9: 297-301.
8. Sun J, Zhang A, Xu LX. Evaluation of alternate cooling and heating for tumor treatment. Int J Heat Mass Transf. 2008; 51: 5478-85.
9. Cai Z, Song M, Zhang A, Sun J, Xu LX. Numerical simulation of a new probe for the alternate cooling and heating of a subcutaneous mouse tumor model. Numerical Heat Transfer, Part A: Applications. 2013; 63: 534-48.
10. Liu J, Ren X, Liu P. Study of Anti-tumor Immunity Induced by Local Thermal Stimulation Using 4T1 Murine Breast Cancer Model. 2013 International Conference on Biological, Medical and Chemical Engineering. 2013: 57-62.
11. Sun J, Xu C, Wei G, Sun X, Liu P, Zhang A, et al. Tumor treatment system with alternate cooling and heating-preliminary results in an animal model. World Congress on Medical Physics and Biomedical Engineering, September 7-12, 2009, Munich, Germany: Springer; 2009: 337-40.
12. Wei C, Shen E, Sun D, Zhang A, Sun J, Hu B. Assessment of alternated cooling and heating treatment by US combined CEUS in the VX2 rabbit liver tumor model. Chinese Sci Bull. 2014; 59: 865-73.
13. Webb H, Lubner MG, Hinshaw JL. Thermal ablation. Seminars in roentgenology. 2011; 46: 133-41.
14. Skitzki JJ, Repasky EA, Evans SS. Hyperthermia as an immunotherapy strategy for cancer. Current opinion in investigational drugs. 2009; 10: 550-8.
15. Sabel MS, Nehs MA, Su G, Lowler KP, Ferrara JL, Chang AE. Immunologic response to cryoablation of breast cancer. Breast cancer research and treatment. 2005; 90: 97-104.
16. Shen Y, Liu P, Zhang A, Xu LX. Study on tumor microvasculature damage induced by alternate cooling and heating. Ann Biomed Eng. 2008; 36: 1409-19.
17. Dong J, Liu P, Xu LX. Immunologic response induced by synergistic effect of alternating cooling and heating of breast cancer. Int J Hyperthermia. 2009; 25: 25-33.
18. Liu P, Ren X, Xu LX. Alternate Cooling and Heating Thermal Physical Treatment: An Effective Strategy Against MDSCs in 4T1 Mouse Mammary Carcinoma. ASME 2012 Summer Bioengineering Conference: American Society of Mechanical Engineers; 2012: 937-8.
19. Aebersold R, Mann M. Mass spectrometry-based proteomics. Nature. 2003; 422: 198-207.
20. Li XJ, Hayward C, Fong PY, Dominguez M, Hunsucker SW, Lee LW, et al. A blood-based proteomic classifier for the molecular characterization of pulmonary nodules. Science translational medicine. 2013; 5: 207ra142.
21. Gallien S, Bourmaud A, Kim SY, Domon B. Technical considerations for large-scale parallel reaction monitoring analysis. J Proteomics. 2014; 100: 147-59.
22. Ronsein GE, Pamir N, von Haller PD, Kim DS, Oda MN, Jarvik GP, et al. Parallel reaction monitoring (PRM) and selected reaction monitoring (SRM) exhibit comparable linearity, dynamic range and precision for targeted quantitative HDL proteomics. Journal of proteomics. 2015; 113: 388-99.
23. Peterson AC, Russell JD, Bailey DJ, Westphall MS, Coon JJ. Parallel reaction monitoring for high resolution and high mass accuracy quantitative, targeted proteomics. Mol Cell Proteomics. 2012; 11: 1475-88.
24. Anderson NL, Anderson NG. The human plasma proteome: history, character, and diagnostic prospects. Mol Cell Proteomics. 2002; 1: 845-67.
25. Zhang H, Li XJ, Martin DB, Aebersold R. Identification and quantification of N-linked glycoproteins using hydrazide chemistry, stable isotope labeling and mass spectrometry. Nature biotechnology. 2003; 21: 660-6.
26. Dennis JW, Granovsky M, Warren CE. Glycoprotein glycosylation and cancer progression. Biochim Biophys Acta. 1999; 1473: 21-34.
27. Gornik O, Royle L, Harvey DJ, Radcliffe CM, Saldova R, Dwek RA, et al. Changes of serum glycans during sepsis and acute pancreatitis. Glycobiology. 2007; 17: 1321-32.
28. Saldova R, Royle L, Radcliffe CM, Abd Hamid UM, Evans R, Arnold JN, et al. Ovarian cancer is associated with changes in glycosylation in both acute-phase proteins and IgG. Glycobiology. 2007; 17: 1344-56.
29. [Internet] A combined UniProtKB/Swiss-Prot and UniProtKB/VarSplic mouse database. ftp://ftp.uniprot.org/pub/databases/uniprot/ current_release/knowledgebase/complete/.
30. [Internet] cRAP. ftp://ftp.thegpm.org/fasta/cRAP.
31. Vizcaino JA, Deutsch EW, Wang R, Csordas A, Reisinger F, Rios D, et al. ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nature biotechnology. 2014; 32: 223-6.
32. MacLean B, Tomazela DM, Shulman N, Chambers M, Finney GL, Frewen B, et al. Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics. 2010; 26: 966-8.
33. Zien A, Aigner T, Zimmer R, Lengauer T. Centralization: a new method for the normalization of gene expression data. Bioinformatics. 2001; 17 Suppl 1: S323-31.
34. Farrah T, Deutsch EW, Omenn GS, Campbell DS, Sun Z, Bletz JA, et al. A high-confidence human plasma proteome reference set with estimated concentrations in PeptideAtlas. Mol Cell Proteomics. 2011; 10: M110 006353.
35. Harel M, Oren-Giladi P, Kaidar-Person O, Shaked Y, Geiger T. Proteomics of microparticles with SILAC Quantification (PROMIS-Quan): a novel proteomic method for plasma biomarker quantification. Mol Cell Proteomics. 2015; 14: 1127-36.
36. Gruys E, Toussaint MJ, Niewold TA, Koopmans SJ. Acute phase reaction and acute phase proteins. J Zhejiang Univ Sci B. 2005; 6: 1045-56.
37. Landskron G, De la Fuente M, Thuwajit P, Thuwajit C, Hermoso MA. Chronic inflammation and cytokines in the tumor microenvironment. Journal of immunology research. 2014; 2014: 149185.
38. Rosen SD. Ligands for L-selectin: homing, inflammation, and beyond. Annual review of immunology. 2004; 22: 129-56.
39. Arbones ML, Ord DC, Ley K, Ratech H, Maynard-Curry C, Otten G, et al. Lymphocyte homing and leukocyte rolling and migration are impaired in L-selectin-deficient mice. Immunity. 1994; 1: 247-60.
40. Libert C, Hochepied T, Berger FG, Baumann H, Fiers W, Brouckaert P. High-level constitutive expression of alpha 1-acid glycoprotein and lack of protection against tumor necrosis factor-induced lethal shock in transgenic mice. Transgenic research. 1998; 7: 429-35.
41. Ngure RM, Eckersall PD, Jennings FW, Burke JM, Stear MJ, Kennedy PG, et al. Major acute phase response of haptoglobin and serum amyloid-P following experimental infection of mice with Trypanosoma brucei brucei. Parasitology International. 1997; 46: 247-54.
42. Mortensen RF, Beisel K, Zeleznik NJ, Le PT. Acute-phase reactants of mice. II. Strain dependence of serum amyloid P-component (SAP) levels and response to inflammation. J Immunol. 1983; 130: 885-9.
43. Baniyash M, Sade-Feldman M, Kanterman J. Chronic inflammation and cancer: suppressing the suppressors. Cancer Immunol Immunother. 2014; 63: 11-20.
44. Curiel TJ. Tregs and rethinking cancer immunotherapy. The Journal of clinical investigation. 2007; 117: 1167-74.
45. Martin-Orozco N, Li Y, Wang Y, Liu S, Hwu P, Liu YJ, et al. Melanoma cells express ICOS ligand to promote the activation and expansion of T-regulatory cells. Cancer Res. 2010; 70: 9581-90.
46. Ito T, Yang M, Wang YH, Lande R, Gregorio J, Perng OA, et al. Plasmacytoid dendritic cells prime IL-10-producing T regulatory cells by inducible costimulator ligand. The Journal of experimental medicine. 2007; 204: 105-15.
47. Faget J, Bendriss-Vermare N, Gobert M, Durand I, Olive D, Biota C, et al. ICOS-ligand expression on plasmacytoid dendritic cells supports breast cancer progression by promoting the accumulation of immunosuppressive CD4+ T cells. Cancer Res. 2012; 72: 6130-41.
48. Aspord C, Leccia MT, Charles J, Plumas J. Plasmacytoid dendritic cells support melanoma progression by promoting Th2 and regulatory immunity through OX40L and ICOSL. Cancer immunology research. 2013; 1: 402-15.
49. Kadkhoda K, Wang S, Joyee AG, Fan Y, Yang J, Yang X. Th1 cytokine responses fail to effectively control Chlamydia lung infection in ICOS ligand knockout mice. J Immunol. 2010; 184: 3780-8.
50. Manches O, Lui G, Chaperot L, Gressin R, Molens JP, Jacob MC, et al. In vitro mechanisms of action of rituximab on primary non-Hodgkin lymphomas. Blood. 2003; 101: 949-54.
51. Weiner LM, Surana R, Wang S. Monoclonal antibodies: versatile platforms for cancer immunotherapy. Nat Rev Immunol. 2010; 10: 317-27.
52. Nakagawa T, Roth W, Wong P, Nelson A, Farr A, Deussing J, et al. Cathepsin L: critical role in Ii degradation and CD4 T cell selection in the thymus. Science. 1998; 280: 450-3.
53. Yu DM, Slaitini L, Gysbers V, Riekhoff AG, Kahne T, Knott HM, et al. Soluble CD26 / dipeptidyl peptidase IV enhances human lymphocyte proliferation in vitro independent of dipeptidyl peptidase enzyme activity and adenosine deaminase binding. Scand J Immunol. 2011; 73: 102-11.
54. De Meester I, Korom S, Van Damme J, Scharpe S. CD26, let it cut or cut it down. Immunol Today. 1999; 20: 367-75.
55. Hatano R, Ohnuma K, Yamamoto J, Dang NH, Morimoto C. CD26-mediated co-stimulation in human CD8(+) T cells provokes effector function via pro-inflammatory cytokine production. Immunology. 2013; 138: 165-72.
56. Krakauer M, Sorensen PS, Sellebjerg F. CD4(+) memory T cells with high CD26 surface expression are enriched for Th1 markers and correlate with clinical severity of multiple sclerosis. J Neuroimmunol. 2006; 181: 157-64.
57. Kalinski P, Hilkens CM, Snijders A, Snijdewint FG, Kapsenberg ML. IL-12-deficient dendritic cells, generated in the presence of prostaglandin E2, promote type 2 cytokine production in maturing human naive T helper cells. J Immunol. 1997; 159: 28-35.
58. Schoenborn JR, Wilson CB. Regulation of interferon-gamma during innate and adaptive immune responses. Advances in immunology. 2007; 96: 41-101.
59. Pulukuri SM, Gorantla B, Knost JA, Rao JS. Frequent loss of cystatin E/M expression implicated in the progression of prostate cancer. Oncogene. 2009; 28: 2829-38.
60. Tan GJ, Peng ZK, Lu JP, Tang FQ. Cathepsins mediate tumor metastasis. World J Biol Chem. 2013; 4: 91-101.
61. Qiu J, Ai L, Ramachandran C, Yao B, Gopalakrishnan S, Fields CR, et al. Invasion suppressor cystatin E/M (CST6): high-level cell type-specific expression in normal brain and epigenetic silencing in gliomas. Lab Invest. 2008; 88: 910-25.
62. Jin L, Zhang Y, Li H, Yao L, Fu D, Yao X, et al. Differential secretome analysis reveals CST6 as a suppressor of breast cancer bone metastasis. Cell Res. 2012; 22: 1356-73.
63. Kloten V, Becker B, Winner K, Schrauder MG, Fasching PA, Anzeneder T, et al. Promoter hypermethylation of the tumor-suppressor genes ITIH5, DKK3, and RASSF1A as novel biomarkers for blood-based breast cancer screening. Breast Cancer Res. 2013; 15: R4.
64. Ueno T, Elmberger G, Weaver TE, Toi M, Linder S. The aspartic protease napsin A suppresses tumor growth independent of its catalytic activity. Lab Invest. 2008; 88: 256-63.
65. Chen Y, Azman SN, Kerishnan JP, Zain RB, Chen YN, Wong YL, et al. Identification of host-immune response protein candidates in the sera of human oral squamous cell carcinoma patients. PLoS One. 2014; 9: e109012.
66. Li C, Zolotarevsky E, Thompson I, Anderson MA, Simeone DM, Casper JM, et al. A multiplexed bead assay for profiling glycosylation patterns on serum protein biomarkers of pancreatic cancer. Electrophoresis. 2011; 32: 2028-35.
67. Tian M, Cui YZ, Song GH, Zong MJ, Zhou XY, Chen Y, et al. Proteomic analysis identifies MMP-9, DJ-1 and A1BG as overexpressed proteins in pancreatic juice from pancreatic ductal adenocarcinoma patients. BMC Cancer. 2008; 8: 241.
68. Kreunin P, Zhao J, Rosser C, Urquidi V, Lubman DM, Goodison S. Bladder cancer associated glycoprotein signatures revealed by urinary proteomic profiling. J Proteome Res. 2007; 6: 2631-9.
69. Holm AT, Wulf-Johansson H, Hvidsten S, Jorgensen PT, Schlosser A, Pilecki B, et al. Characterization of spontaneous airspace enlargement in mice lacking microfibrillar-associated protein 4. Am J Physiol Lung Cell Mol Physiol. 2015: ajplung 00351.2014.
70. Johansson SL, Roberts NB, Schlosser A, Andersen CB, Carlsen J, Wulf-Johansson H, et al. Microfibrillar-associated protein 4: a potential biomarker of chronic obstructive pulmonary disease. Respir Med. 2014; 108: 1336-44.
71. Gabay C, Kushner I. Acute-phase proteins and other systemic responses to inflammation. The New England journal of medicine. 1999; 340: 448-54.
72. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol. 2009; 9: 162-74.
73. Trinchieri G. Cancer Immunity: Lessons From Infectious Diseases. The Journal of infectious diseases. 2015; 212 Suppl 1: S67-73.
74. Zhang S, Danchuk SD, Bonvillain RW, Xu B, Scruggs BA, Strong AL, et al. Interleukin 6 Mediates the Therapeutic Effects of Adipose-Derived Stromal/Stem Cells in Lipopolysaccharide-Induced Acute Lung Injury. Stem Cells. 2014; 32: 1616-28.
75. Chen Q, Fisher DT, Kucinska SA, Wang WC, Evans SS. Dynamic control of lymphocyte trafficking by fever-range thermal stress. Cancer Immunol Immunother. 2006; 55: 299-311.
76. 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.
77. Wang WC, Goldman LM, Schleider DM, Appenheimer MM, Subjeck JR, Repasky EA, et al. Fever-range hyperthermia enhances L-selectin-dependent adhesion of lymphocytes to vascular endothelium. J Immunol. 1998; 160: 961-9.
78. 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. The Journal of clinical investigation. 2011; 121: 3846-59.
79. Ljungberg B, Grankvist K, Rasmuson T. Serum interleukin-6 in relation to acute-phase reactants and survival in patients with renal cell carcinoma. Eur J Cancer. 1997; 33: 1794-8.
80. Martin F, Santolaria F, Batista N, Milena A, Gonzalez-Reimers E, Brito MJ, et al. Cytokine levels (IL-6 and IFN-gamma), acute phase response and nutritional status as prognostic factors in lung cancer. Cytokine. 1999; 11: 80-6.
81. Lippitz BE. Cytokine patterns in patients with cancer: a systematic review. The Lancet Oncology. 2013; 14: e218-28.
82. Mold C, Baca R, Du Clos TW. Serum amyloid P component and C-reactive protein opsonize apoptotic cells for phagocytosis through Fcgamma receptors. Journal of autoimmunity. 2002; 19: 147-54.
83. Le Friec G, Kemper C. Complement: coming full circle. Arch Immunol Ther Exp (Warsz). 2009; 57: 393-407.
84. Peng Q, Li K, Anderson K, Farrar CA, Lu B, Smith RA, et al. Local production and activation of complement up-regulates the allostimulatory function of dendritic cells through C3a-C3aR interaction. Blood. 2008; 111: 2452-61.
85. Strainic MG, Liu J, Huang D, An F, Lalli PN, Muqim N, et al. Locally produced complement fragments C5a and C3a provide both costimulatory and survival signals to naive CD4+ T cells. Immunity. 2008; 28: 425-35.
86. Papp K, Vegh P, Prechl J, Kerekes K, Kovacs J, Csikos G, et al. B lymphocytes and macrophages release cell membrane deposited C3-fragments on exosomes with T cell response-enhancing capacity. Mol Immunol. 2008; 45: 2343-51.
87. van Montfoort N, de Jong JM, Schuurhuis DH, van der Voort EI, Camps MG, Huizinga TW, et al. A novel role of complement factor C1q in augmenting the presentation of antigen captured in immune complexes to CD8+ T lymphocytes. J Immunol. 2007; 178: 7581-6.
88. Jiang K, Chen Y, Xu CS, Jarvis JN. T cell activation by soluble C1q-bearing immune complexes: implications for the pathogenesis of rheumatoid arthritis. Clinical and experimental immunology. 2003; 131: 61-7.
89. Longhi MP, Wright K, Lauder SN, Nowell MA, Jones GW, Godkin AJ, et al. Interleukin-6 is crucial for recall of influenza-specific memory CD4 T cells. PLoS Pathog. 2008; 4: e1000006.
90. Sallusto F, Geginat J, Lanzavecchia A. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annual review of immunology. 2004; 22: 745-63.
91. Newson J, Stables M, Karra E, Arce-Vargas F, Quezada S, Motwani M, et al. Resolution of acute inflammation bridges the gap between innate and adaptive immunity. Blood. 2014: blood-2014-03-562710.