Synergistic proinflammatory interactions of microbial toxins and structural components characteristic to moisture-damaged buildings

Indoor Air

Volumn 27, Issue 1, 2017, Pages 13-23

  Korkalainen, M ^a   Taubel M ^a   Naarala, J ^b   Kirjavainen, P ^a   Koistinen, A ^b   Hyvarinen A ^a   Komulainen, H ^a   Viluksela, M ^a,b  

^a NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

Co exposure; lipopolysaccharide; microbial toxins; proinflammatory cytokines; synergistic interaction; glucan

Indexed keywords

GENE EXPRESSION; METABOLITES; POLYMERASE CHAIN REACTION;

CO-EXPOSURE; COMPONENT CHARACTERISTICS; GLUCANS; LIPOPOLYSACCHARIDES; MICROBIAL TOXIN; PROINFLAMMATORY; PROINFLAMMATORY CYTOKINES; STRUCTURAL COMPONENT; SYNERGISTIC INTERACTION; Β-GLUCAN;

MOISTURE;

BETA GLUCAN; DEPSIPEPTIDE; EMODIN; ENNIATINS; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; PHYSCION; STERIGMATOCYSTIN; TUMOR NECROSIS FACTOR; VALINOMYCIN;

ANALOGS AND DERIVATIVES; ANALYSIS; BACTERIUM; ENZYME LINKED IMMUNOSORBENT ASSAY; FUNGUS; HUMAN; INDOOR AIR POLLUTION; MACROPHAGE; METABOLISM; MICROBIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; THP-1 CELL LINE;

AIR POLLUTION, INDOOR; BACTERIA; BETA-GLUCANS; DEPSIPEPTIDES; EMODIN; ENZYME-LINKED IMMUNOSORBENT ASSAY; FUNGI; HUMANS; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; MACROPHAGES; REAL-TIME POLYMERASE CHAIN REACTION; STERIGMATOCYSTIN; THP-1 CELLS; TUMOR NECROSIS FACTOR-ALPHA; VALINOMYCIN;

EID: 84959017796     PISSN: 09056947     EISSN: 16000668     Source Type: Journal    
DOI: 10.1111/ina.12282     Document Type: Article

References (47)

1. Alassane-Kpembi, I., Kolf-Clauw, M., Gauthier, T., Abrami, R., Abiola, F.A., Oswald, I.P. and Puel, O. (2013) New insights into mycotoxin mixtures: the toxicity of low doses of Type B trichothecenes on intestinal epithelial cells is synergistic, Toxicol. Appl. Pharmacol., 272, 191–198.
2. Behm, C., Follmann, W. and Degen, G.H. (2012) Cytotoxic potency of mycotoxins in cultures of V79 lung fibroblast cells, J. Toxicol. Environ. Health A, 75, 1226–1231.
3. Bennett, J.W. and Klich, M. (2003) Mycotoxins, Clin. Microbiol. Rev., 16, 497–516.
4. Cai, G.H., Hashim, J.H., Hashim, Z., Ali, F., Bloom, E., Larsson, L., Lampa, E. and Norback, D. (2011) Fungal DNA, allergens, mycotoxins and associations with asthmatic symptoms among pupils in schools from Johor Bahru, Malaysia, Pediatr. Allergy Immunol., 22, 290–297.
5. Carey, S.A., Plopper, C.G., Hyde, D.M., Islam, Z., Pestka, J.J. and Harkema, J.R. (2012) Satratoxin-G from the black mold Stachybotrys chartarum induces rhinitis and apoptosis of olfactory sensory neurons in the nasal airways of rhesus monkeys, Toxicol. Pathol., 40, 887–898.
6. Chanput, W., Mes, J.J. and Wichers, H.J. (2014) THP-1 cell line: an in vitro cell model for immune modulation approach, Int. Immunopharmacol., 23, 37–45.
7. Council for Agricultural Science and Technology (CAST) (2003) Mycotoxins: Risk in Plant, Animal, and Human Systems. Ames, Iowa, USA, Task force report 139, 13–15.
8. Creasia, D.A., Thurman, J.D., Jones, L.J. 3rd, Nealley, M.L., York, C.G., Wannemacher, R.W. Jr and Bunner, D.L. (1987) Acute inhalation toxicity of T-2 mycotoxin in mice, Fundam. Appl. Toxicol., 8, 230–235.
9. Dearborn, D.G., Yike, I., Sorenson, W.G., Miller, M.J. and Etzel, R.A. (1999) Overview of investigations into pulmonary hemorrhage among infants in Cleveland, Ohio, Environ. Health Perspect., 107, 495–499.
10. Etzel, R.A., Montana, E., Sorenson, W.G., Kullman, G.J., Allan, T.M., Dearborn, D.G., Olson, D.R., Jarvis, B.B. and Miller, J.D. (1998) Acute pulmonary hemorrhage in infants associated with exposure to Stachybotrys atra and other fungi, Arch. Pediatr. Adolesc. Med., 152, 757–762.
11. Flappan, S.M., Portnoy, J., Jones, P. and Barnes, C. (1999) Infant pulmonary hemorrhage in a suburban home with water damage and mold (Stachybotrys atra), Environ. Health Perspect., 107, 927–930.
12. Gammelsrud, A., Solhaug, A., Dendele, B., Sandberg, W.J., Ivanova, L., Kocbach Bolling, A., Lagadic-Gossmann, D., Refsnes, M., Becher, R., Eriksen, G. and Holme, J.A. (2012) Enniatin B-induced cell death and inflammatory responses in RAW 267.4 murine macrophages, Toxicol. Appl. Pharmacol., 261, 74–87.
13. Huttunen, K., Pelkonen, J., Nielsen, K.F., Nuutinen, U., Jussila, J. and Hirvonen, M.-R. (2004) Synergistic interaction in simultaneous exposure to Streptomyces californicus and Stachybotrys chartarum, Environ. Health Perspect., 112, 659–665.
14. Huttunen, K., Tirkkonen, J., Täubel, M., Krop, E., Mikkonen, S., Pekkanen, J., Heederik, D., Zock, J.P., Hyvärinen, A. and Hirvonen, M.-R. (2015) Inflammatory potential in relation to the microbial content of settled dust samples collected from moisture-damaged and reference schools: results of HITEA study, Indoor Air, doi: 10.1111/ina.12223 [Epub ahead of print].
15. Islam, Z. and Pestka, J.J. (2006) LPS priming potentiates and prolongs proinflammatory cytokine response to the trichothecene deoxynivalenol in the mouse, Toxicol. Appl. Pharmacol., 211, 53–63.
16. Islam, Z., Amuzie, C.J., Harkema, J.R. and Pestka, J.J. (2007) Neurotoxicity and inflammation in the nasal airways of mice exposed to the macrocyclic trichothecene mycotoxin roridin a: kinetics and potentiation by bacterial lipopolysaccharide coexposure, Toxicol. Sci., 98, 526–541.
17. Jarvis, B.B., Sorenson, W.G., Hintikka, E.L., Nikulin, M., Zhou, Y., Jiang, J., Wang, S., Hinkley, S., Etzel, R.A. and Dearborn, D. (1998) Study of toxin production by isolates of Stachybotrys chartarum and Memnoniella echinata isolated during a study of pulmonary hemosiderosis in infants, Appl. Environ. Microbiol., 64, 3620–3625.
18. Johannessen, L., Lovik, M., Lydersen, S. and Nilsen, A.M. (2009) Combined cell wall polysaccharide, mycotoxin and bacterial lipopolysaccharide exposure and inflammatory cytokine responses, APMIS, 117, 507–517.
19. Johanning, E., Biagini, R., Hull, D., Morey, P., Jarvis, B. and Landsbergis, P. (1996) Health and immunology study following exposure to toxigenic fungi (Stachybotrys chartarum) in a water-damaged office environment, Int. Arch. Occup. Environ. Health, 68, 207–218.
20. Kamyar, M., Rawnduzi, P., Studenik, C.R., Kouri, K. and Lemmens-Gruber, R. (2004) Investigation of the electrophysiological properties of enniatins, Arch. Biochem. Biophys., 429, 215–223.
21. Kanchongkittiphon, W., Mendell, M.J., Gaffin, J.M., Wang, G. and Phipatanakul, W. (2015) Indoor environmental exposures and exacerbation of asthma: an update to the 2000 review by the institute of medicine, Environ. Health Perspect., 123, 6–20.
22. Kankkunen, P., Rintahaka, J., Aalto, A., Leino, M., Majuri, M.L., Alenius, H., Wolff, H. and Matikainen, S. (2009) Trichothecene mycotoxins activate inflammatory response in human macrophages, J. Immunol., 182, 6418–6425.
23. Kankkunen, P., Välimäki, E., Rintahaka, J., Palomäki, J., Nyman, T., Alenius, H., Wolff, H. and Matikainen, S. (2014) Trichothecene mycotoxins activate NLRP3 inflammasome through a P2X7 receptor and Src tyrosine kinase dependent pathway, Hum. Immunol., 75, 134–140.
24. Kirjavainen, P.V., Täubel, M., Karvonen, A.M., Sulyok, M., Tiittanen, P., Krska, R., Hyvärinen, A. and Pekkanen, J. (2015) Microbial secondary metabolites in homes in association with moisture damage and asthma, Indoor Air, doi: 10.1111/ina.12213 [Epub ahead of print].
25. Koskela, A., Viluksela, M., Keinänen, M., Tuukkanen, J. and Korkalainen, M. (2012) Synergistic effects of tributyltin and 2,3,7,8-tetrachlorodibenzo-p-dioxin on differentiating osteoblasts and osteoclasts, Toxicol. Appl. Pharmacol., 263, 210–217.
26. Mendell, M.J., Mirer, A.G., Cheung, K., Tong, M. and Douwes, J. (2011) Respiratory and allergic health effects of dampness, mold, and dampness-related agents: a review of the epidemiologic evidence, Environ. Health Perspect., 119, 748–756.
27. Miller, J.D. and McMullin, D.R. (2014) Fungal secondary metabolites as harmful indoor air contaminants: 10 years on, Appl. Microbiol. Biotechnol., 98, 9953–9966.
28. Morris, M. and Li, L. (2012) Molecular mechanisms and pathological consequences of endotoxin tolerance and priming, Arch. Immunol. Ther. Exp., 60, 13–18.
29. Mueller, A., Schlink, U., Wichmann, G., Bauer, M., Graebsch, C., Schüürmann, G. and Herbarth, O. (2013) Individual and combined effects of mycotoxins from typical indoor moulds, Toxicol. In Vitro, 27, 1970–1978.
30. Munford, R.S. (2010) Murine responses to endotoxin: another dirty little secret? J. Infect. Dis., 201, 175–177.
31. Murtoniemi, T., Penttinen, P., Nevalainen, A. and Hirvonen, M.-.R. (2005) Effects of microbial cocultivation on inflammatory and cytotoxic potential of spores, Inhal. Toxicol., 17, 681–693.
32. Nevalainen, A., Täubel, M. and Hyvärinen, A. (2015) Indoor fungi: companions and contaminants, Indoor Air, 25, 125–156.
33. Nielsen, K.F. (2003) Mycotoxin production by indoor molds, Fungal Genet. Biol., 39, 103–117.
34. Paananen, A., Mikkola, R., Sareneva, T., Matikainen, S., Andersson, M., Julkunen, I., Salkinoja-Salonen, M.S. and Timonen, T. (2000) Inhibition of human NK cell function by valinomycin, a toxin from Streptomyces griseus in indoor air, Infect. Immun., 68, 165–169.
35. Peitzsch, M., Sulyok, M., Täubel, M., Vishwanath, V., Krop, E., Borras-Santos, A., Hyvärinen, A., Nevalainen, A., Krska, R. and Larsson, L. (2012) Microbial secondary metabolites in school buildings inspected for moisture damage in Finland, The Netherlands and Spain, J. Environ. Monit., 14, 2044–2053.
36. Penttinen, P., Huttunen, K., Pelkonen, J. and Hirvonen, M.-R. (2005) The proportions of Streptomyces californicus and Stachybotrys chartarum in simultaneous exposure affect inflammatory responses in mouse RAW264.7 macrophages, Inhal. Toxicol., 17, 79–85.
37. Pestka, J. and Zhou, H.R. (2006) Toll-like receptor priming sensitizes macrophages to proinflammatory cytokine gene induction by deoxynivalenol and other toxicants, Toxicol. Sci., 92, 445–455.
38. Prosperini, A., Font, G. and Ruiz, M.J. (2014) Interaction effects of Fusarium enniatins (A, A1, B and B1) combinations on in vitro cytotoxicity of Caco-2 cells, Toxicol. In Vitro, 28, 88–94.
39. Ruiz, M.J., Macakova, P., Juan-Garcia, A. and Font, G. (2011) Cytotoxic effects of mycotoxin combinations in mammalian kidney cells, Food Chem. Toxicol., 49, 2718–2724.
40. Slob, W. (2002) Dose-response modeling of continuous endpoints, Toxicol. Sci., 66, 298–312.
41. Täubel, M. and Hyvärinen, A. (2015) Occurrence of mycotoxins in indoor environments. In: Viegas C, Pinheiro AC, Sabino R, Viegas S, Brandao J and Verissimo C (eds). Environmental Mycology in Public Health, Amsterdam, Elsevier Academic Press. 299–323.
42. Täubel, M., Sulyok, M., Vishwanath, V., Bloom, E., Turunen, M., Järvi, K., Kauhanen, E., Krska, R., Hyvärinen, A., Larsson, L. and Nevalainen, A. (2011) Co-occurrence of toxic bacterial and fungal secondary metabolites in moisture-damaged indoor environments, Indoor Air, 21, 368–375.
43. Tonshin, A.A., Teplova, V.V., Andersson, M.A. and Salkinoja-Salonen, M.S. (2010) The Fusarium mycotoxins enniatins and beauvericin cause mitochondrial dysfunction by affecting the mitochondrial volume regulation, oxidative phosphorylation and ion homeostasis, Toxicology, 276, 49–57.
44. Wan, L.M., Woo, C.J., Turner, P.C., Wan, J.M. and El-Nezami, H. (2013) Individual and combined effects of Fusarium toxins on the mRNA expression of pro-inflammatory cytokines in swine jejunal epithelial cells, Toxicol. Lett., 220, 238–246.
45. World Health Organization (2009) WHO Guidelines for Indoor Air Quality: Dampness and Mould, Copenhagen, WHO Regional Office for Europe.
46. Zhou, H.R., Harkema, J.R., Yan, D. and Pestka, J.J. (1999) Amplified proinflammatory cytokine expression and toxicity in mice coexposed to lipopolysaccharide and the trichothecene vomitoxin (deoxynivalenol), J. Toxicol. Environ. Health A, 57, 115–136.
47. Zock, J.P., Borras-Santos, A., Jacobs, J., Täubel, M., Espinosa, A., Haverinen-Shaughnessy, U., Peitsch, M., Sulyok, M. and Hyvärinen, A. (2014) Dampness and microbial secondary metabolites in schools and respiratory symptoms in teachers. In: European Respiratory Society Annual Conference, Munich, Abstract 2161.