Immunotherapeutic approaches to treatment of fungal diseases

The Lancet Infectious Diseases

Volumn 17, Issue 12, 2017, Pages e393-e402

  Armstrong James, Darius ^a   Brown, Gordon D ^b   Netea, Mihai G ^c   Zelante, Teresa ^d   Gresnigt, Mark S ^c   van de Veerdonk, Frank L ^c   Levitz, Stuart M ^e  

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UNIVERSITY OF PERUGIA   (Italy)

^e UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIFUNGAL AGENT; FUNGUS VACCINE; IMMUNOLOGIC FACTOR;

ADOPTIVE IMMUNOTHERAPY; ALLERGIC DISEASE; ANTIFUNGAL THERAPY; ANTIRETROVIRAL THERAPY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; DISEASE ASSOCIATION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE DYSREGULATION; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IMMUNOREACTIVITY; IMMUNOSUPPRESSIVE TREATMENT; IMMUNOTHERAPY; INCIDENCE; INFECTION RISK; INNATE IMMUNITY; MORBIDITY; MORTALITY; MYCOSIS; NONHUMAN; PANDEMIC; PRIORITY JOURNAL; PROGNOSIS; REVIEW; TREATMENT OUTCOME; IMMUNOLOGY;

HUMANS; IMMUNOLOGIC FACTORS; IMMUNOTHERAPY; MYCOSES;

EID: 85026513464     PISSN: 14733099     EISSN: 14744457     Source Type: Journal    
DOI: 10.1016/S1473-3099(17)30442-5     Document Type: Review

References (101)

1. Brown, GD, Denning, DW, Gow, NA, Levitz, SM, Netea, MG, White, TC, Hidden killers: human fungal infections. Sci Transl Med, 4, 2012, 165rv13.
2. Vallabhaneni, S, Mody, RK, Walker, T, Chiller, T, The global burden of fungal diseases. Infect Dis Clin North Am 30 (2016), 1–11.
3. Brown, GD, Innate antifungal immunity: the key role of phagocytes. Annu Rev Immunol 29 (2011), 1–21.
4. Wuthrich, M, Deepe, GS Jr, Klein, B, Adaptive immunity to fungi. Annu Rev Immunol 30 (2012), 115–148.
5. Hardison, SE, Brown, GD, C-type lectin receptors orchestrate antifungal immunity. Nature Immunol 13 (2012), 817–822.
6. Carvalho, A, Cunha, C, Pasqualotto, AC, Pitzurra, L, Denning, DW, Romani, L, Genetic variability of innate immunity impacts human susceptibility to fungal diseases. Int J Infect Dis 14 (2010), e460–e468.
7. Pappas, PG, Bustamante, B, Ticona, E, et al. Recombinant interferon-gamma 1b as adjunctive therapy for AIDS-related acute cryptococcal meningitis. J Infect Dis 189 (2004), 2185–2191.
8. Wuthrich, M, Filutowicz, HI, Warner, T, Deepe, GS Jr, Klein, BS, Vaccine immunity to pathogenic fungi overcomes the requirement for CD4 help in exogenous antigen presentation to CD8+ T cells: implications for vaccine development in immune-deficient hosts. J Exp Med 197 (2003), 1405–1416.
9. Iliev, ID, Funari, VA, Taylor, KD, et al. Interactions between commensal fungi and the C-type lectin receptor dectin-1 influence colitis. Science 336 (2012), 1314–1317.
10. Plantinga, TS, Johnson, MD, Scott, WK, et al. Human genetic susceptibility to candida infections. Med Mycol 50 (2012), 785–794.
11. Lanternier, F, Cypowyj, S, Picard, C, et al. Primary immunodeficiencies underlying fungal infections. Curr Opin Pediatr 25 (2013), 736–747.
12. van de Veerdonk, FL, Netea, MG, Joosten, LA, van der Meer, JW, Kullberg, BJ, Novel strategies for the prevention and treatment of candida infections: the potential of immunotherapy. FEMS Microbiol Rev 34 (2010), 1063–1075.
13. Vazquez, JA, Gupta, S, Villanueva, A, Potential utility of recombinant human GM-CSF as adjunctive treatment of refractory oropharyngeal candidiasis in AIDS patients. Eur J Clin Microbiol Infect Dis 17 (1998), 781–783.
14. Vazquez, JA, Hidalgo, JA, De Bono, S, Use of sargramostim (rh-GM-CSF) as adjunctive treatment of fluconazole-refractory oropharyngeal candidiasis in patients with AIDS: a pilot study. HIV Clin Trials 1 (2000), 23–29.
15. Wan, L, Zhang, Y, Lai, Y, et al. Effect of granulocyte-macrophage colony-stimulating factor on prevention and treatment of invasive fungal disease in recipients of allogeneic stem-cell transplantation: a prospective multicenter randomized phase IV trial. J Clin Oncol 33 (2015), 3999–4006.
16. Bandera, A, Trabattoni, D, Ferrario, G, et al. Interferon-gamma and granulocyte-macrophage colony stimulating factor therapy in three patients with pulmonary aspergillosis. Infection 36 (2008), 368–373.
17. Saijo, T, Chen, J, Chen, SC, et al. Anti-granulocyte-macrophage colony-stimulating factor autoantibodies are a risk factor for central nervous system infection by Cryptococcus gattii in otherwise immunocompetent patients. mBio 5 (2014), e00912–e00914.
18. Kullberg, BJ, Oude Lashof, AM, Netea, MG, Design of efficacy trials of cytokines in combination with antifungal drugs. Clin Infect Dis 39:suppl 4 (2004), S218–S223.
19. Todeschini, G, Murari, C, Bonesi, R, et al. Invasive aspergillosis in neutropenic patients: rapid neutrophil recovery is a risk factor for severe pulmonary complications. Eur J Clin Invest 29 (1999), 453–457.
20. Kullberg, BJ, van 't Wout, JW, Hoogstraten, C, van Furth, R, Recombinant interferon-gamma enhances resistance to acute disseminated Candida albicans infection in mice. J Infect Dis 168 (1993), 436–443.
21. Nagai, H, Guo, J, Choi, H, Kurup, V, Interferon-gamma and tumor necrosis factor-alpha protect mice from invasive aspergillosis. J Infect Dis 172 (1995), 1554–1560.
22. Clemons, KV, Lutz, JE, Stevens, DA, Efficacy of recombinant gamma interferon for treatment of systemic cryptococcosis in SCID mice. Antimicrob Agents Chemother 45 (2001), 686–689.
23. The International Chronic Granulomatous Disease Cooperative Study Group. A controlled trial of interferon gamma to prevent infection in chronic granulomatous disease. N Engl J Med 324 (1991), 509–516.
24. Marciano, BE, Wesley, R, De Carlo, ES, et al. Long-term interferon-gamma therapy for patients with chronic granulomatous disease. Clin Infect Dis 39 (2004), 692–699.
25. Armstrong-James, D, Teo, IA, Shrivastava, S, et al. Exogenous interferon-gamma immunotherapy for invasive fungal infections in kidney transplant patients. Am J Transplant 10 (2010), 1796–1803.
26. Siddiqui, AA, Brouwer, AE, Wuthiekanun, V, et al. IFN-gamma at the site of infection determines rate of clearance of infection in cryptococcal meningitis. J Immunol 174 (2005), 1746–1750.
27. Jarvis, JN, Meintjes, G, Rebe, K, et al. Adjunctive interferon-gamma immunotherapy for the treatment of HIV-associated cryptococcal meningitis: a randomized controlled trial. Aids 26 (2012), 1105–1113.
28. Netea, MG, Brouwer, AE, Hoogendoorn, EH, et al. Two patients with cryptococcal meningitis and idiopathic CD4 lymphopenia: defective cytokine production and reversal by recombinant interferon-gamma therapy. Clin Infect Dis 39 (2004), e83–e87.
29. Delsing, CE, Gresnigt, MS, Leentjens, J, et al. Interferon-gamma as adjunctive immunotherapy for invasive fungal infections: a case series. BMC Infect Dis, 14, 2014, 166.
30. Meintjes, G, Scriven, J, Marais, S, Management of the immune reconstitution inflammatory syndrome. Curr HIV/AIDS Rep 9 (2012), 238–250.
31. Raberg, L, Sim, D, Read, AF, Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318 (2007), 812–814.
32. Zelante, T, Iannitti, R, De Luca, A, Romani, L, IL-22 in antifungal immunity. Eur J Immunol 41 (2011), 270–275.
33. Casadevall, A, Pirofski, LA, The damage-response framework of microbial pathogenesis. Nat Rev Microbiol 1 (2003), 17–24.
34. Montagnoli, C, Bozza, S, Gaziano, R, et al. Immunity and tolerance to Aspergillus fumigatus. Novartis Found Symp 279 (2006), 66–79 216–19.
35. Kisand, K, Lilic, D, Casanova, JL, Peterson, P, Meager, A, Willcox, N, Mucocutaneous candidiasis and autoimmunity against cytokines in APECED and thymoma patients: clinical and pathogenetic implications. Eur J Immunol 41 (2011), 1517–1527.
36. Kisand, K, Boe Wolff, AS, Podkrajsek, KT, et al. Chronic mucocutaneous candidiasis in APECED or thymoma patients correlates with autoimmunity to Th17-associated cytokines. J Exp Med 207 (2010), 299–308.
37. Browne, SK, Anticytokine autoantibody-associated immunodeficiency. Annu Rev Immunol 32 (2014), 635–657.
38. Panackal, AA, Wuest, SC, Lin, YC, et al. Paradoxical immune responses in non-HIV cryptococcal meningitis. PLoS Pathog, 11, 2015, e1004884.
39. Tang, BS, Chan, JF, Chen, M, et al. Disseminated penicilliosis, recurrent bacteremic nontyphoidal salmonellosis, and burkholderiosis associated with acquired immunodeficiency due to autoantibody against gamma interferon. Clin Vaccine Immunol 17 (2010), 1132–1138.
40. Browne, SK, Zaman, R, Sampaio, EP, et al. Anti-CD20 (rituximab) therapy for anti-IFN-gamma autoantibody-associated nontuberculous mycobacterial infection. Blood 119 (2012), 3933–3939.
41. Legrand, F, Lecuit, M, Dupont, B, et al. Adjuvant corticosteroid therapy for chronic disseminated candidiasis. Clin Infect Dis 46 (2008), 696–702.
42. Ferwerda, B, Ferwerda, G, Plantinga, TS, et al. Human dectin-1 deficiency and mucocutaneous fungal infections. N Engl J Med 361 (2009), 1760–1767.
43. Borghi, M, De Luca, A, Puccetti, M, et al. Pathogenic NLRP3 inflammasome activity during candida infection is negatively regulated by IL-22 via activation of NLRC4 and IL-1Ra. Cell Host Microbe 18 (2015), 198–209.
44. Majer, O, Bourgeois, C, Zwolanek, F, et al. Type I interferons promote fatal immunopathology by regulating inflammatory monocytes and neutrophils during candida infections. PLoS Pathog, 8, 2012, e1002811.
45. Ling, Y, Cypowyj, S, Aytekin, C, et al. Inherited IL-17RC deficiency in patients with chronic mucocutaneous candidiasis. J Exp Med 212 (2015), 619–631.
46. Boisson, B, Wang, C, Pedergnana, V, et al. An ACT1 mutation selectively abolishes interleukin-17 responses in humans with chronic mucocutaneous candidiasis. Immunity 39 (2013), 676–686.
47. Milner, JD, Sandler, NG, Douek, DC, Th17 cells, Job's syndrome and HIV: opportunities for bacterial and fungal infections. Curr Opin HIV AIDS 5 (2010), 179–183.
48. Toubiana, J, Okada, S, Hiller, J, et al. Heterozygous STAT1 gain-of-function mutations underlie an unexpectedly broad clinical phenotype. Blood 127 (2016), 3154–3164.
49. Mossner, R, Diering, N, Bader, O, et al. Ruxolitinib induces interleukin 17 and ameliorates chronic mucocutaneous candidiasis caused by STAT1 gain-of-function mutation. Clin Infect Dis 62 (2016), 951–953.
50. Higgins, E, Al Shehri, T, McAleer, MA, et al. Use of ruxolitinib to successfully treat chronic mucocutaneous candidiasis caused by gain-of-function signal transducer and activator of transcription 1 (STAT1) mutation. J Allergy Clin Immunol 135 (2015), 551–553.
51. Kyrmizi, I, Gresnigt, MS, Akoumianaki, T, et al. Corticosteroids block autophagy protein recruitment in Aspergillus fumigatus phagosomes via targeting dectin-1/Syk kinase signaling. J Immunol 191 (2013), 1287–1299.
52. de Luca, A, Smeekens, SP, Casagrande, A, et al. IL-1 receptor blockade restores autophagy and reduces inflammation in chronic granulomatous disease in mice and in humans. Proc Natl Acad Sci USA 111 (2014), 3526–3531.
53. Horvath, R, Rozkova, D, Lastovicka, J, et al. Expansion of T helper type 17 lymphocytes in patients with chronic granulomatous disease. Clin Exp Immunol 166 (2011), 26–33.
54. Romani, L, Fallarino, F, De Luca, A, et al. Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease. Nature 451 (2008), 211–215.
55. Knutsen, AP, Bush, RK, Demain, JG, et al. Fungi and allergic lower respiratory tract diseases. J Allergy Clin Immunol 129 (2012), 280–291.
56. Chishimba, L, Niven, RM, Cooley, J, Denning, DW, Voriconazole and posaconazole improve asthma severity in allergic bronchopulmonary aspergillosis and severe asthma with fungal sensitization. J Asthma 49 (2012), 423–433.
57. Latzin, P, Hartl, D, Regamey, N, Frey, U, Schoeni, MH, Casaulta, C, Comparison of serum markers for allergic bronchopulmonary aspergillosis in cystic fibrosis. Eur Respir J 31 (2008), 36–42.
58. Hartl, D, Buckland, KF, Hogaboam, CM, Chemokines in allergic aspergillosis—from animal models to human lung diseases. Inflamm Allergy Drug Targets 5 (2006), 219–228.
59. Dubey, LK, Moeller, JB, Schlosser, A, Sorensen, GL, Holmskov, U, Induction of innate immunity by Aspergillus fumigatus cell wall polysaccharides is enhanced by the composite presentation of chitin and beta-glucan. Immunobiology 219 (2014), 179–188.
60. Hartl, D, Immunological mechanisms behind the cystic fibrosis-ABPA link. Med Mycol 47:suppl 1 (2009), S183–S191.
61. Nguyen, NL, Chen, K, McAleer, J, Kolls, JK, Vitamin D regulation of OX40 ligand in immune responses to Aspergillus fumigatus. Infect Immun 81 (2013), 1510–1519.
62. Nguyen, NL, Pilewski, JM, Celedon, JC, et al. Vitamin D supplementation decreases specific Th2 responses in CF patients with aspergillus sensitization: a phase one open-label study. Asthma Res Pract, 1, 2015, 3.
63. Wong, R, Wong, M, Robinson, PD, Fitzgerald, DA, Omalizumab in the management of steroid dependent allergic bronchopulmonary aspergillosis (ABPA) complicating cystic fibrosis. Paediatr Respir Rev 14 (2013), 22–24.
64. Homma, T, Kurokawa, M, Matsukura, S, Yamaguchi, M, Adachi, M, Anti-IgE therapy for allergic bronchopulmonary aspergillosis. J Microbiol Immunol Infect 49 (2016), 459–463.
65. Collins, J, Devos, G, Hudes, G, Rosenstreich, D, Allergic bronchopulmonary aspergillosis treated successfully for one year with omalizumab. J Asthma Allergy 5 (2012), 65–70.
66. Aydin, O, Sozener, ZC, Soyyigit, S, et al. Omalizumab in the treatment of allergic bronchopulmonary aspergillosis: one center's experience with 14 cases. Allergy Asthma Proc 36 (2015), 493–500.
67. Becker, KL, Gresnigt, MS, Smeekens, SP, et al. Pattern recognition pathways leading to a Th2 cytokine bias in ABPA patients. Clin Exp Allergy 45 (2015), 423–437.
68. Castanhinha, S, Sherburn, R, Walker, S, et al. Pediatric severe asthma with fungal sensitization is mediated by steroid-resistant IL-33. J Allergy Clin Immunol 136 (2015), 312–322.
69. Fei, M, Bhatia, S, Oriss, TB, et al. TNF-alpha from inflammatory dendritic cells (DCs) regulates lung IL-17A/IL-5 levels and neutrophilia versus eosinophilia during persistent fungal infection. Proc Natl Acad Sci USA 108 (2011), 5360–5365.
70. Levitz, SM, Golenbock, DT, Beyond empiricism: informing vaccine development through innate immunity research. Cell 148 (2012), 1284–1292.
71. Torosantucci, A, Bromuro, C, Chiani, P, et al. A novel glyco-conjugate vaccine against fungal pathogens. J Exp Med 202 (2005), 597–606.
72. Specht, CA, Lee, CK, Huang, H, et al. Protection against experimental cryptococcosis following vaccination with glucan particles containing cryptococcus alkaline extracts. mBio 6 (2015), e01905–e01915.
73. Santos, E, Levitz, SM, Fungal vaccines and immunotherapeutics. Cold Spring Harb Perspect Med, 4, 2014, a019711.
74. Wozniak, KL, Young, ML, Wormley, FL Jr, Protective immunity against experimental pulmonary cryptococcosis in T cell-depleted mice. Clin Vaccine Immunol 18 (2011), 717–723.
75. Pappagianis, D, Group, TVFVS, Evaluation of the protective efficacy of the killed Coccidioides immitis spherule vaccine in humans. Am Rev Respir Dis 148 (1993), 656–660.
76. Schmidt, CS, White, CJ, Ibrahim, AS, et al. NDV-3, a recombinant alum-adjuvanted vaccine for candida and Staphylococcus aureus, is safe and immunogenic in healthy adults. Vaccine 30 (2012), 7594–7600.
77. De Bernardis, F, Amacker, M, Arancia, S, et al. A virosomal vaccine against candidal vaginitis: immunogenicity, efficacy and safety profile in animal models. Vaccine 30 (2012), 4490–4498.
78. McClelland, EE, Nicola, AM, Prados-Rosales, R, Casadevall, A, Ab binding alters gene expression in Cryptococcus neoformans and directly modulates fungal metabolism. J Clin Invest 120 (2010), 1355–1361.
79. Larsen, RA, Pappas, PG, Perfect, J, et al. Phase I evaluation of the safety and pharmacokinetics of murine-derived anticryptococcal antibody 18B7 in subjects with treated cryptococcal meningitis. Antimicrob Agents Chemother 49 (2005), 952–958.
80. Delorme, EJ, Alexander, P, Treatment of primary fibrosarcoma in the rat with immune lymphocytes. Lancet 284 (1964), 117–120.
81. Gross, G, Waks, T, Eshhar, Z, Expression of immunoglobulin-T-cell receptor chimeric molecules as functional receptors with antibody-type specificity. Proc Natl Acad Sci USA 86 (1989), 10024–10028.
82. Rosenberg, SA, Restifo, NP, Adoptive cell transfer as personalized immunotherapy for human cancer. Science 348 (2015), 62–68.
83. Dale, DC, Liles, WC, Price, TH, Renewed interest in granulocyte transfusion therapy. Br J Haematol 98 (1997), 497–501.
84. Beck, O, Koehl, U, Tramsen, L, et al. Enumeration of functionally active anti-aspergillus T-cells in human peripheral blood. J Immunol Methods 335 (2008), 41–45.
85. Perruccio, K, Tosti, A, Burchielli, E, et al. Transferring functional immune responses to pathogens after haploidentical hematopoietic transplantation. Blood 106 (2005), 4397–4406.
86. Papadopoulou, A, Kaloyannidis, P, Yannaki, E, Cruz, CR, Adoptive transfer of aspergillus-specific T cells as a novel anti-fungal therapy for hematopoietic stem cell transplant recipients: progress and challenges. Crit Rev Oncol Hematol 98 (2016), 62–72.
87. Tramsen, L, Schmidt, S, Boenig, H, et al. Clinical-scale generation of multi-specific anti-fungal T cells targeting candida, aspergillus and mucormycetes. Cytotherapy 15 (2013), 344–351.
88. Srivastava, S, Riddell, SR, Engineering CAR-T cells: Design concepts. Trends Immunol 36 (2015), 494–502.
89. Kumaresan, PR, Manuri, PR, Albert, ND, et al. Bioengineering T cells to target carbohydrate to treat opportunistic fungal infection. Proc Natl Acad Sci USA 111 (2014), 10660–10665.
90. Seidel, MG, Peters, C, Wacker, A, et al. Randomized phase III study of granulocyte transfusions in neutropenic patients. Bone Marrow Transplant 42 (2008), 679–684.
91. Price, TH, Boeckh, M, Harrison, RW, et al. Efficacy of transfusion with granulocytes from G-CSF/dexamethasone-treated donors in neutropenic patients with infection. Blood 126 (2015), 2153–2161.
92. Bozza, S, Perruccio, K, Montagnoli, C, et al. A dendritic cell vaccine against invasive aspergillosis in allogeneic hematopoietic transplantation. Blood 102 (2003), 3807–3814.
93. Schmidt, S, Tramsen, L, Hanisch, M, et al. Human natural killer cells exhibit direct activity against Aspergillus fumigatus hyphae, but not against resting conidia. J Infect Dis 203 (2011), 430–435.
94. Schmidt, S, Tramsen, L, Perkhofer, S, et al. Rhizopus oryzae hyphae are damaged by human natural killer (NK) cells, but suppress NK cell mediated immunity. Immunobiology 218 (2013), 939–944.
95. Stern, M, Passweg, JR, Meyer-Monard, S, et al. Pre-emptive immunotherapy with purified natural killer cells after haploidentical SCT: a prospective phase II study in two centers. Bone Marrow Transplant 48 (2013), 433–438.
96. Sousa Mda, G, Reid, DM, Schweighoffer, E, et al. Restoration of pattern recognition receptor costimulation to treat chromoblastomycosis, a chronic fungal infection of the skin. Cell Host Microbe 9 (2011), 436–443.
97. de Sousa Mda, G, Belda, W Jr, Spina, R, et al. Topical application of imiquimod as a treatment for chromoblastomycosis. Clin Infect Dis 58 (2014), 1734–1737.
98. Maskarinec, SA, Johnson, MD, Perfect, JR, Genetic susceptibility to fungal infections: what is in the genes?. Curr Clin Microbiol Rep 3 (2016), 81–91.
99. Wojtowicz, A, Bochud, PY, Host genetics of invasive aspergillus and candida infections. Semin Immunopathol 37 (2015), 173–186.
100. Armstrong-James, D, Teo, I, Herbst, S, et al. Renal allograft recipients fail to increase interferon-gamma during invasive fungal diseases. Am J Transplant 12 (2012), 3437–3440.
101. Netea, MG, Brouwer, AE, Hoogendoorn, EH, et al. Two patients with cryptococcal meningitis and idiopathic CD4 lymphopenia: defective cytokine production and reversal by recombinant interferon-gamma therapy. Clin Infect Dis 39 (2004), e83–e87.