The Dynamic Role of the IL-33/ST2 Axis in Chronic Viral-infections: Alarming and Adjuvanting the Immune Response

EBioMedicine

Volumn 9, Issue , 2016, Pages 37-44

  Mehraj, Vikram ^a,b   Ponte, Rosalie ^a,b   Routy, Jean Pierre ^a,b  

^a RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

HBV; HCV; HIV; Interleukin 33 (IL 33); Suppressor of tumorigenicity 2 (ST2); Vaccine adjuvant

Indexed keywords

BIOLOGICAL MARKER; IMMUNOLOGICAL ADJUVANT; IMMUNOMODULATING AGENT; INFLAMMASOME; INTERLEUKIN 33; SUPPRESSION OF TUMORIGENICITY 2; UNCLASSIFIED DRUG; VACCINE; ANTIVIRUS AGENT; ASCOMYCIN; INTERLEUKIN 1 RECEPTOR LIKE 1 PROTEIN; TACROLIMUS;

AUTOIMMUNE DISEASE; CELL DEATH; HEPATITIS B; HEPATITIS C; HERPES SIMPLEX; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; IMMUNOTHERAPY; LIVER FIBROSIS; MIXED INFECTION; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; TH1 TH2 BALANCE; TREATMENT RESPONSE; VIRUS INFECTION; ANALOGS AND DERIVATIVES; ANIMAL; DRUG EFFECTS; IMMUNOLOGY; METABOLISM; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION; VIROLOGY; VIRUS DISEASES;

ANIMALS; ANTIVIRAL AGENTS; COINFECTION; HUMANS; INTERLEUKIN-1 RECEPTOR-LIKE 1 PROTEIN; INTERLEUKIN-33; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS; TACROLIMUS; VIRUS DISEASES;

EID: 84991624725     PISSN: None     EISSN: 23523964     Source Type: Journal    
DOI: 10.1016/j.ebiom.2016.06.047     Document Type: Review

References (81)

1. Ahmad, R., Sindhu, S.T., Toma, E., Morisset, R., Ahmad, A., Elevated levels of circulating interleukin-18 in human immunodeficiency virus-infected individuals: role of peripheral blood mononuclear cells and implications for AIDS pathogenesis. J. Virol. 76 (2002), 12448–12456.
2. Alves-Filho, J.C., Sonego, F., Souto, F.O., Freitas, A., Verri, W.A. JR., Auxiliadora-Martins, M., Basile-Filho, A., Mckenzie, A.N., Xu, D., Cunha, F.Q., Liew, F.Y., Interleukin-33 attenuates sepsis by enhancing neutrophil influx to the site of infection. Nat. Med. 16 (2010), 708–712.
3. Ananworanich, J., Chomont, N., Fletcher, J.L., Pinyakorn, S., Schuetz, A., Sereti, I., Rerknimitr, R., Dewar, R., Kroon, E., Vandergeeten, C., Trichavaroj, R., Chomchey, N., Chalermchai, T., Michael, N.L., Kim, J.H., Phanuphak, P., Phanuphak, N., Markers of HIV reservoir size and immune activation after treatment in acute HIV infection with and without raltegravir and maraviroc intensification. J. Virus. Erad. 1 (2015), 116–122.
4. Anderson, R.J., Tang, C.W., Daniels, N.J., Compton, B.J., Hayman, C.M., Johnston, K.A., Knight, D.A., Gasser, O., Poyntz, H.C., Ferguson, P.M., Larsen, D.S., Ronchese, F., Painter, G.F., Hermans, I.F., A self-adjuvanting vaccine induces cytotoxic T lymphocytes that suppress allergy. Nat. Chem. Biol. 10 (2014), 943–949.
5. Andersson, C., Enserro, D., Sullivan, L., Wang, T.J., Januzzi, J.L., Benjamin, E.J., Vita, J.A., Hamburg, N.M., Larson, M.G., Mitchell, G.F., Vasan, R.S., Relations of circulating GDF-15, soluble ST2, and troponin-I concentrations with vascular function in the community: the Framingham Heart Study. Atherosclerosis 248 (2016), 245–251.
6. Aoki, R., Kawamura, T., Goshima, F., Ogawa, Y., Nakae, S., Nakao, A., Moriishi, K., Nishiyama, Y., Shimada, S., Mast cells play a key role in host defense against herpes simplex virus infection through TNF-alpha and IL-6 production. J. Invest. Dermatol. 133 (2013), 2170–2179.
7. Arshad, M.I., Khan, H.A., Noel, G., Piquet-Pellorce, C., Samson, M., Potential therapeutic aspects of alarmin cytokine interleukin 33 or its inhibitors in various diseases. Clin. Ther. 38 (2016), 1000–1016.
8. Barouch, D.H., Ghneim, K., Bosche, W.J., Li, Y., Berkemeier, B., Hull, M., Bhattacharyya, S., Cameron, M., Liu, J., Smith, K., Borducchi, E., Cabral, C., Peter, L., Brinkman, A., Shetty, M., Li, H., Gittens, C., Baker, C., Wagner, W., Lewis, M.G., Colantonio, A., Kang, H.J., Li, W., Lifson, J.D., Piatak, M. Jr., Sekaly, R.P., Rapid inflammasome activation following mucosal SIV infection of rhesus monkeys. Cell 165 (2016), 656–667.
9. Baumann, C., Bonilla, W.V., Frohlich, A., Helmstetter, C., Peine, M., Hegazy, A.N., Pinschewer, D.D., Lohning, M., T-bet- and STAT4-dependent IL-33 receptor expression directly promotes antiviral Th1 cell responses. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 4056–4061.
10. Becerra, A., Warke, R.V., De Bosch, N., Rothman, A.L., Bosch, I., Elevated levels of soluble ST2 protein in dengue virus infected patients. Cytokine 41 (2008), 114–120.
11. Blom, L., Poulsen, L.K., IL-1 family members IL-18 and IL-33 upregulate the inflammatory potential of differentiated human Th1 and Th2 cultures. J. Immunol. 189 (2012), 4331–4337.
12. Bonilla, W.V., Frohlich, A., Senn, K., Kallert, S., Fernandez, M., Johnson, S., Kreutzfeldt, M., Hegazy, A.N., Schrick, C., Fallon, P.G., Klemenz, R., Nakae, S., Adler, H., Merkler, D., Lohning, M., Pinschewer, D.D., The alarmin interleukin-33 drives protective antiviral CD8(+) T cell responses. Science 335 (2012), 984–989.
13. Cao, W., Mehraj, V., Kaufmann, D.E., Li, T., Routy, J.P., Elevation and persistence of CD8 T-cells in HIV infection: the Achilles heel in the ART era. J. Int. AIDS Soc., 19, 2016, 20697.
14. Cayrol, C., Girard, J.P., The IL-1-like cytokine IL-33 is inactivated after maturation by caspase-1. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 9021–9026.
15. Cayrol, C., Girard, J.P., IL-33: an alarmin cytokine with crucial roles in innate immunity, inflammation and allergy. Curr. Opin. Immunol. 31 (2014), 31–37.
16. Chen, L.Q., De Lemos, J.A., Das, S.R., Ayers, C.R., Rohatgi, A., Soluble ST2 is associated with all-cause and cardiovascular mortality in a population-based cohort: the Dallas Heart Study. Clin. Chem. 59 (2013), 536–546.
17. Fitch, K.V., Defilippi, C., Christenson, R., Srinivasa, S., Lee, H., Lo, J., Lu, M.T., Wong, K., Petrow, E., Sanchez, L., Looby, S.E., Hoffmann, U., Zanni, M., Grinspoon, S.K., Subclinical myocyte injury, fibrosis and strain in relationship to coronary plaque in asymptomatic HIV-infected individuals. AIDS, 2016.
18. Gao, S., Huan, S.L., Han, L.Y., Li, F., Ji, X.F., Li, X.Y., Fan, Y.C., Wang, K., Overexpression of serum sST2 is associated with poor prognosis in acute-on-chronic hepatitis B liver failure. Clin. Res. Hepatol. Gastroenterol. 39 (2015), 315–323.
19. Gao, Y., Liu, Y., Yang, M., Guo, X., Zhang, M., Li, H., Li, J., Zhao, J., IL-33 treatment attenuated diet-induced hepatic steatosis but aggravated hepatic fibrosis. Oncotarget, 2016.
20. Gianella, S., Massanella, M., Wertheim, J.O., Smith, D.M., The sordid affair between human herpesvirus and HIV. J. Infect. Dis. 212 (2015), 845–852.
21. Hayakawa, H., Hayakawa, M., Kume, A., Tominaga, S., Soluble ST2 blocks interleukin-33 signaling in allergic airway inflammation. J. Biol. Chem. 282 (2007), 26369–26380.
22. Hazlett, L.D., Mcclellan, S.A., Barrett, R.P., Huang, X., Zhang, Y., Wu, M., Van Rooijen, N., Szliter, E., IL-33 shifts macrophage polarization, promoting resistance against Pseudomonas aeruginosa keratitis. Invest. Ophthalmol. Vis. Sci. 51 (2010), 1524–1532.
23. Hunt, P.W., Sinclair, E., Rodriguez, B., Shive, C., Clagett, B., Funderburg, N., Robinson, J., Huang, Y., Epling, L., Martin, J.N., Deeks, S.G., Meinert, C.L., Van Natta, M.L., Jabs, D.A., Lederman, M.M., Gut epithelial barrier dysfunction and innate immune activation predict mortality in treated HIV infection. J. Infect. Dis. 210 (2014), 1228–1238.
24. Iannello, A., Samarani, S., Debbeche, O., Ahmad, R., Boulassel, M.R., Tremblay, C., Toma, E., Routy, J.P., Ahmad, A., Potential role of interleukin-18 in the immunopathogenesis of AIDS: involvement in fratricidal killing of NK cells. J. Virol. 83 (2009), 5999–6010.
25. Jenabian, M. A., El-Far, M., Vyboh, K., Kema, I., Costiniuk, C. T., Thomas, R., Baril, J. G., Leblanc, R., Kanagaratham, C., Radzioch, D., Allam, O., Ahmad, A., Lebouche, B., Tremblay, C., Ancuta, P., Routy, J. P., Montreal Primary, I. & Slow Progressor Study, G. 2015. Immunosuppressive tryptophan catabolism and gut mucosal dysfunction following early HIV infection. J. Infect. Dis., 212, 355–66.
26. Jones, L.A., Roberts, F., Nickdel, M.B., Brombacher, F., Mckenzie, A.N., Henriquez, F.L., Alexander, J., Roberts, C.W., IL-33 receptor (T1/ST2) signalling is necessary to prevent the development of encephalitis in mice infected with Toxoplasma gondii. Eur. J. Immunol. 40 (2010), 426–436.
27. Jovanovic, I.P., Pejnovic, N.N., Radosavljevic, G.D., Arsenijevic, N.N., Lukic, M.L., IL-33/ST2 axis in innate and acquired immunity to tumors. Oncoimmunology 1 (2012), 229–231.
28. Kakkar, R., Lee, R.T., The IL-33/ST2 pathway: therapeutic target and novel biomarker. Nat. Rev. Drug Discov. 7 (2008), 827–840.
29. Kayamuro, H., Yoshioka, Y., Abe, Y., Arita, S., Katayama, K., Nomura, T., Yoshikawa, T., Kubota-Koketsu, R., Ikuta, K., Okamoto, S., Mori, Y., Kunisawa, J., Kiyono, H., Itoh, N., Nagano, K., Kamada, H., Tsutsumi, Y., Tsunoda, S., Interleukin-1 family cytokines as mucosal vaccine adjuvants for induction of protective immunity against influenza virus. J. Virol. 84 (2010), 12703–12712.
30. Kerfoot, S.M., Yaari, G., Patel, J.R., Johnson, K.L., Gonzalez, D.G., Kleinstein, S.H., Haberman, A.M., Germinal center B cell and T follicular helper cell development initiates in the interfollicular zone. Immunity 34 (2011), 947–960.
31. Latz, E., Xiao, T.S., Stutz, A., Activation and regulation of the inflammasomes. Nat. Rev. Immunol. 13 (2013), 397–411.
32. Lei, Z., Mo, Z., Zhu, J., Pang, X., Zheng, X., Wu, Z., Wang, K., Li, X., Xie, D., Gao, Z., Soluble ST2 plasma concentrations predict mortality in HBV-related acute-on-chronic liver failure. Mediat. Inflamm., 2015, 2015, 535938.
33. Li, D., Guabiraba, R., Besnard, A.G., Komai-Koma, M., Jabir, M.S., Zhang, L., Graham, G.J., Kurowska-Stolarska, M., Liew, F.Y., Mcsharry, C., Xu, D., IL-33 promotes ST2-dependent lung fibrosis by the induction of alternatively activated macrophages and innate lymphoid cells in mice. J. Allergy Clin. Immunol., 134(1422–1432), 2014, e11.
34. Li, P., Lin, W., Zheng, X., IL-33 neutralization suppresses lupus disease in lupus-prone mice. Inflammation 37 (2014), 824–832.
35. Liang, Y., Jie, Z., Hou, L., Aguilar-Valenzuela, R., Vu, D., Soong, L., Sun, J., IL-33 induces nuocytes and modulates liver injury in viral hepatitis. J. Immunol. 190 (2013), 5666–5675.
36. Liang, Y., Jie, Z., Hou, L., Yi, P., Wang, W., Kwota, Z., Salvato, M., De Waal Malefyt, R., Soong, L., Sun, J., IL-33 promotes innate IFN-gamma production and modulates dendritic cell response in LCMV-induced hepatitis in mice. Eur. J. Immunol. 45 (2015), 3052–3063.
37. Lu, J., Kang, J., Zhang, C., Zhang, X., The role of IL-33/ST2L signals in the immune cells. Immunol. Lett. 164 (2015), 11–17.
38. Martin, N.T., Martin, M.U., Interleukin 33 is a guardian of barriers and a local alarmin. Nat. Immunol. 17 (2016), 122–131.
39. Marvie, P., Lisbonne, M., L'helgoualc'h, A., Rauch, M., Turlin, B., Preisser, L., Bourd-Boittin, K., Theret, N., Gascan, H., Piquet-Pellorce, C., Samson, M., Interleukin-33 overexpression is associated with liver fibrosis in mice and humans. J. Cell. Mol. Med. 14 (2010), 1726–1739.
40. Masubuchi, Y., Sugiyama, S., Horie, T., Th1/Th2 cytokine balance as a determinant of acetaminophen-induced liver injury. Chem. Biol. Interact. 179 (2009), 273–279.
41. Mehraj, V., Jenabian, M.A., Ponte, R., Lebouche, B., Costiniuk, C., Thomas, R., Baril, J.G., Leblanc, R., Cox, J., Tremblay, C., Routy, J.P., Montreal Primary HIV Infection, the Canadian Long-Term Non-Progressors Study Groups. The plasma levels of soluble ST2 as a marker of gutmucosal damage in early HIV infection. AIDS 30 (2016), 1617–1627.
42. Miller, A.M., Role of IL-33 in inflammation and disease. J. Inflamm. (Lond), 8, 2011, 22.
43. Miller, A.M., Xu, D., Asquith, D.L., Denby, L., Li, Y., Sattar, N., Baker, A.H., Mcinnes, I.B., Liew, F.Y., IL-33 reduces the development of atherosclerosis. J. Exp. Med. 205 (2008), 339–346.
44. Miyagaki, T., Sugaya, M., Yokobayashi, H., Kato, T., Ohmatsu, H., Fujita, H., Saeki, H., Kikuchi, Y., Tamaki, T., Sato, S., High levels of soluble ST2 and low levels of IL-33 in sera of patients with HIV infection. J. Invest. Dermatol. 131 (2011), 794–796.
45. Molofsky, A.B., Savage, A.K., Locksley, R.M., Interleukin-33 in tissue homeostasis, injury, and inflammation. Immunity 42 (2015), 1005–1019.
46. Molofsky, A.B., Van Gool, F., Liang, H.E., Van Dyken, S.J., Nussbaum, J.C., Lee, J., Bluestone, J.A., Locksley, R.M., Interleukin-33 and interferon-gamma counter-regulate group 2 innate lymphoid cell activation during immune perturbation. Immunity 43 (2015), 161–174.
47. Monticelli, L.A., Sonnenberg, G.F., Abt, M.C., Alenghat, T., Ziegler, C.G., Doering, T.A., Angelosanto, J.M., Laidlaw, B.J., Yang, C.Y., Sathaliyawala, T., Kubota, M., Turner, D., Diamond, J.M., Goldrath, A.W., Farber, D.L., Collman, R.G., Wherry, E.J., Artis, D., Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat. Immunol. 12 (2011), 1045–1054.
48. Moussion, C., Ortega, N., Girard, J.P., The IL-1-like cytokine IL-33 is constitutively expressed in the nucleus of endothelial cells and epithelial cells in vivo: a novel ‘alarmin’?. PLoS One, 3, 2008, e3331.
49. Nabekura, T., Girard, J.P., Lanier, L.L., IL-33 receptor ST2 amplifies the expansion of NK cells and enhances host defense during mouse cytomegalovirus infection. J. Immunol. 194 (2015), 5948–5952.
50. Nygaard, U., Vestergaard, C., Johansen, C., Deleuran, M., Hvid, M., Measuring serum concentrations of interleukin-33 in atopic dermatitis is associated with potential false positive results. Springerplus, 5, 2016, 33.
51. Oh, J.E., Kim, B.C., Chang, D.H., Kwon, M., Lee, S.Y., Kang, D., Kim, J.Y., Hwang, I., Yu, J.W., Nakae, S., Lee, H.K., Dysbiosis-induced IL-33 contributes to impaired antiviral immunity in the genital mucosa. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), E762–E771.
52. Okragly, A.J., Hamang, M.J., Pena, E.A., Baker, H.E., Bullock, H.A., Lucchesi, J., Martin, A.P., Ma, Y.L., Benschop, R.J., Elevated levels of interleukin (IL)-33 induce bone pathology but absence of IL-33 does not negatively impact normal bone homeostasis. Cytokine 79 (2016), 66–73.
53. Pastorelli, L., Garg, R.R., Hoang, S.B., Spina, L., Mattioli, B., Scarpa, M., Fiocchi, C., Vecchi, M., Pizarro, T.T., Epithelial-derived IL-33 and its receptor ST2 are dysregulated in ulcerative colitis and in experimental Th1/Th2 driven enteritis. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 8017–8022.
54. Peine, M., Marek, R.M., Lohning, M., IL-33 in T cell differentiation, function, and immune homeostasis. Trends Immunol. 37 (2016), 321–333.
55. Petrasek, J., Bala, S., Csak, T., Lippai, D., Kodys, K., Menashy, V., Barrieau, M., Min, S.Y., Kurt-Jones, E.A., Szabo, G., IL-1 receptor antagonist ameliorates inflammasome-dependent alcoholic steatohepatitis in mice. J. Clin. Invest. 122 (2012), 3476–3489.
56. Ponte, R., Mehraj, V., Ghali, P., Couedel-Courteille, A., Cheynier, R., Routy, J.P., Reversing gut damage in HIV infection: using non-human primate models to instruct clinical research. EBioMedicine 4 (2016), 40–49.
57. Reichenbach, D.K., Schwarze, V., Matta, B.M., Tkachev, V., Lieberknecht, E., Liu, Q., Koehn, B.H., Pfeifer, D., Taylor, P.A., Prinz, G., Dierbach, H., Stickel, N., Beck, Y., Warncke, M., Junt, T., Schmitt-Graeff, A., Nakae, S., Follo, M., Wertheimer, T., Schwab, L., Devlin, J., Watkins, S.C., Duyster, J., Ferrara, J.L., Turnquist, H.R., Zeiser, R., Blazar, B.R., The IL-33/ST2 axis augments effector T-cell responses during acute GVHD. Blood 125 (2015), 3183–3192.
58. Rostan, O., Arshad, M.I., Piquet-Pellorce, C., Robert-Gangneux, F., Gangneux, J.P., Samson, M., Crucial and diverse role of the interleukin-33/ST2 axis in infectious diseases. Infect. Immun. 83 (2015), 1738–1748.
59. Roth, G.A., Zimmermann, M., Lubsczyk, B.A., Pilz, J., Faybik, P., Hetz, H., Hacker, S., Mangold, A., Bacher, A., Krenn, C.G., Ankersmit, H.J., Up-regulation of interleukin 33 and soluble ST2 serum levels in liver failure. J. Surg. Res. 163 (2010), e79–e83.
60. Routy, J.P., Mehraj, V., Cao, W., HIV immunotherapy comes of age: implications for prevention, treatment and cure. Expert. Rev. Clin. Immunol. 12 (2016), 91–94.
61. Salter, B.M., Oliveria, J.P., Nusca, G., Smith, S.G., Tworek, D., Mitchell, P.D., Watson, R.M., Sehmi, R., Gauvreau, G.M., IL-25 and IL-33 induce type 2 inflammation in basophils from subjects with allergic asthma. Respir. Res., 17, 2016, 5.
62. Samarani, S., Allam, O., Sagala, P., Aldabah, Z., Jenabian, M.A., Mehraj, V., Tremblay, C., Routy, J.P., Amre, D., Ahmad, A., Imbalanced production of IL-18 and its antagonist in human diseases, and its implications for HIV-1 infection. Cytokine 82 (2016), 38–51.
63. Schacker, T.W., Reilly, C., Beilman, G.J., Taylor, J., Skarda, D., Krason, D., Larson, M., Haase, A.T., Amount of lymphatic tissue fibrosis in HIV infection predicts magnitude of HAART-associated change in peripheral CD4 cell count. AIDS 19 (2005), 2169–2171.
64. Schiering, C., Krausgruber, T., Chomka, A., Frohlich, A., Adelmann, K., Wohlfert, E.A., Pott, J., Griseri, T., Bollrath, J., Hegazy, A.N., Harrison, O.J., Owens, B.M., Lohning, M., Belkaid, Y., Fallon, P.G., Powrie, F., The alarmin IL-33 promotes regulatory T-cell function in the intestine. Nature 513 (2014), 564–568.
65. Schmitz, J., Owyang, A., Oldham, E., Song, Y., Murphy, E., Mcclanahan, T.K., Zurawski, G., Moshrefi, M., Qin, J., Li, X., Gorman, D.M., Bazan, J.F., Kastelein, R.A., IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 23 (2005), 479–490.
66. Secemsky, E.A., Scherzer, R., Nitta, E., Wu, A.H., Lange, D.C., Deeks, S.G., Martin, J.N., Snider, J., Ganz, P., Hsue, P.Y., Novel Biomarkers of Cardiac Stress, Cardiovascular Dysfunction, and Outcomes in HIV-infected Individuals. JACC Heart Fail. 3, 2015, 591–599.
67. Sesti-Costa, R., Silva, G.K., Proenca-Modena, J.L., Carlos, D., Silva, M.L., Alves-Filho, J.C., Arruda, E., Liew, F.Y., Silva, J.S., The IL-33/ST2 pathway controls coxsackievirus B5-induced experimental pancreatitis. J. Immunol. 191 (2013), 283–292.
68. Shang, J., Zhao, J., Wu, X., Xu, Y., Xie, J., Interleukin-33 promotes inflammatory cytokine production in chronic airway inflammation. Biochem. Cell Biol.., 93, 2015, 359–366.
69. Smithgall, M.D., Comeau, M.R., Yoon, B.R., Kaufman, D., Armitage, R., Smith, D.E., IL-33 amplifies both Th1- and Th2-type responses through its activity on human basophils, allergen-reactive Th2 cells, iNKT and NK cells. Int. Immunol. 20 (2008), 1019–1030.
70. Stasi, C., Milani, S., Non-invasive assessment of liver fibrosis: between prediction/prevention of outcomes and cost-effectiveness. World J. Gastroenterol. 22 (2016), 1711–1720.
71. Sun, Y., Zhang, J.Y., Lv, S., Wang, H., Gong, M., Du, N., Liu, H., Zhang, N., Jing, J., Zhou, C., Zhang, F., Wang, Z., Interleukin-33 promotes disease progression in patients with primary biliary cirrhosis. Tohoku J. Exp. Med.., 234, 2014, 255–261.
72. Tang, S., Huang, H., Hu, F., Zhou, W., Guo, J., Jiang, H., Mu, R., Li, Z., Increased IL-33 in synovial fluid and paired serum is associated with disease activity and autoantibodies in rheumatoid arthritis. Clin. Dev. Immunol., 2013, 2013, 985301.
73. Vander Lugt, M.T., Braun, T.M., Hanash, S., Ritz, J., Ho, V.T., Antin, J.H., Zhang, Q., Wong, C.H., Wang, H., Chin, A., Gomez, A., Harris, A.C., Levine, J.E., Choi, S.W., Couriel, D., Reddy, P., Ferrara, J.L., Paczesny, S., ST2 as a marker for risk of therapy-resistant graft-versus-host disease and death. N. Engl. J. Med. 369 (2013), 529–539.
74. Villarreal, D.O., Siefert, R.J., Weiner, D.B., Alarmin IL-33 elicits potent TB-specific cell-mediated responses. Hum. Vaccin. Immunother. 11 (2015), 1954–1960.
75. Villarreal, D.O., Svoronos, N., Wise, M.C., Shedlock, D.J., Morrow, M.P., Conejo-Garcia, J.R., Weiner, D.B., Molecular adjuvant IL-33 enhances the potency of a DNA vaccine in a lethal challenge model. Vaccine 33 (2015), 4313–4320.
76. Villarreal, D.O., Weiner, D.B., IL-33 isoforms: their future as vaccine adjuvants?. Expert Rev. Vaccines 14 (2015), 489–492.
77. Villarreal, D.O., Wise, M.C., Walters, J.N., Reuschel, E.L., Choi, M.J., Obeng-Adjei, N., Yan, J., Morrow, M.P., Weiner, D.B., Alarmin IL-33 acts as an immunoadjuvant to enhance antigen-specific tumor immunity. Cancer Res. 74 (2014), 1789–1800.
78. Volarevic, V., Mitrovic, M., Milovanovic, M., Zelen, I., Nikolic, I., Mitrovic, S., Pejnovic, N., Arsenijevic, N., Lukic, M.L., Protective role of IL-33/ST2 axis in Con A-induced hepatitis. J. Hepatol. 56 (2012), 26–33.
79. WANG, J., CAI, Y., Ji, H., Feng, J., Ayana, D.A., Niu, J., Jiang, Y., Serum IL-33 levels are associated with liver damage in patients with chronic hepatitis B. J. Interf. Cytokine Res. 32 (2012), 248–253.
80. Wang, J., Zhao, P., Guo, H., Sun, X., Jiang, Z., Xu, L., Feng, J., Niu, J., Jiang, Y., Serum IL-33 levels are associated with liver damage in patients with chronic hepatitis C. Mediat. Inflamm., 2012, 2012, 819636.
81. Yndart, A., Kaushik, A., Agudelo, M., Raymond, A., Atluri, V.S., Saxena, S.K., Nair, M., Investigation of neuropathogenesis in HIV-1 clade B and C infection associated with IL-33 and ST2 regulation. ACS Chem. Neurosci. 6 (2015), 1600–1612.