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Inhalation Toxicology
International Forum for Respiratory Research
Volume 36, 2024 - Issue 2
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Research Articles

Crystalline silica-induced pulmonary inflammation and autoimmunity in mature adult NZBW/f1 mice: age-related sensitivity and impact of omega-3 fatty acid intervention

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Pages 106-123 | Received 21 Dec 2023, Accepted 07 Feb 2024, Published online: 13 Mar 2024

References

  • Adamichou C, Bertsias G. 2017. Flares in systemic lupus erythematosus: diagnosis, risk factors and preventive strategies. Mediterr J Rheumatol. 28(1):4–12. doi: 10.31138/mjr.28.1.4.
  • Akbar U, Yang M, Kurian D, Mohan C. 2017. Omega-3 fatty acids in rheumatic diseases: a critical review. J Clin Rheumatol. 23(6):330–339. doi: 10.1097/RHU.0000000000000563.
  • Alexander NJ, Smythe NL, Jokinen MP. 1987. The type of dietary fat affects the severity of autoimmune disease in NZB/NZW mice. Am J Pathol. 127(1):106–121.
  • Arriens C, Hynan LS, Lerman RH, Karp DR, Mohan C. 2015. Placebo-controlled randomized clinical trial of fish oil’s impact on fatigue, quality of life, and disease activity in Systemic Lupus Erythematosus. Nutr J. 14(1):82. doi: 10.1186/s12937-015-0068-2.
  • Basta F, Fasola F, Triantafyllias K, Schwarting A. 2020. Systemic lupus erythematosus (SLE) therapy: the old and the new. Rheumatol Ther. 7(3):433–446. doi: 10.1007/s40744-020-00212-9.
  • Bates MA, Akbari P, Gilley KN, Wagner JG, Li N, Kopec AK, Wierenga KA, Jackson-Humbles D, Brandenberger C, Holian A, et al. 2018. Dietary docosahexaenoic acid prevents silica-induced development of pulmonary ectopic germinal centers and glomerulonephritis in the lupus-prone NZBWF1 mouse. Front Immunol. 9:2002. doi: 10.3389/fimmu.2018.02002.
  • Bates MA, Benninghoff AD, Gilley KN, Holian A, Harkema JR, Pestka JJ. 2019. Mapping of dynamic transcriptome changes associated with silica-triggered autoimmune pathogenesis in the lupus-prone NZBWF1 mouse. Front Immunol. 10:632. doi: 10.3389/fimmu.2019.00632.
  • Bates MA, Brandenberger C, Langohr I, Kumagai K, Harkema JR, Holian A, Pestka JJ. 2015. Silica triggers inflammation and ectopic lymphoid neogenesis in the lungs in parallel with accelerated onset of systemic autoimmunity and glomerulonephritis in the lupus-prone NZBWF1 mouse. PLoS One. 10(5):e0125481. doi: 10.1371/journal.pone.0125481.
  • Bates MA, Brandenberger C, Langohr II, Kumagai K, Lock AL, Harkema JR, Holian A, Pestka JJ. 2016. Silica-triggered autoimmunity in lupus-prone mice blocked by docosahexaenoic acid consumption. PLoS One. 11(8):e0160622. doi: 10.1371/journal.pone.0160622.
  • Benninghoff AD, Bates MA, Chauhan PS, Wierenga KA, Gilley KN, Holian A, Harkema JR, Pestka JJ. 2019. Docosahexaenoic acid consumption impedes early interferon- and chemokine-related gene expression while suppressing silica-triggered flaring of murine lupus. Front Immunol. 10:2851. doi: 10.3389/fimmu.2019.02851.
  • Benninghoff AD, Hintze KJ, Monsanto SP, Rodriguez DM, Hunter AH, Phatak S, Pestka JJ, Wettere AJV, Ward RE. 2020. Consumption of the total western diet promotes colitis and inflammation-associated colorectal cancer in mice. Nutrients. 12(2):544. doi: 10.3390/nu12020544.
  • Bhattacharya A, Lawrence RA, Krishnan A, Zaman K, Sun D, Fernandes G. 2003. Effect of dietary n-3 and n-6 oils with and without food restriction on activity of antioxidant enzymes and lipid peroxidation in livers of cyclophosphamide treated autoimmune-prone NZB/W female mice. J Am Coll Nutr. 22(5):388–399. doi: 10.1080/07315724.2003.10719322.
  • Brown JM, Archer AJ, Pfau JC, Holian A. 2003. Silica accelerated systemic autoimmune disease in lupus-prone New Zealand mixed mice. Clin Exp Immunol. 131(3):415–421. doi: 10.1046/j.1365-2249.2003.02094.x.
  • Brown JM, Pfau JC, Holian A. 2004. Immunoglobulin and lymphocyte responses following silica exposure in New Zealand mixed mice. Inhal Toxicol. 16(3):133–139. doi: 10.1080/08958370490270936.
  • Burnet FM, Holmes MC. 1965. The natural history of the NZB/NZW F1 hybrid mouse: a laboratory model of systemic lupus erythematosus. Australas Ann Med. 14(3):185–191. doi: 10.1111/imj.1965.14.3.185.
  • Calder PC. 2017. Omega-3 fatty acids and inflammatory processes: from molecules to man. Biochem Soc Trans. 45(5):1105–1115. doi: 10.1042/BST20160474.
  • Celhar T, Fairhurst AM. 2017. Modelling clinical systemic lupus erythematosus: similarities, differences and success stories. Rheumatology (Oxford). 56(suppl_1):i88–i99.
  • Chandrasekar B, Troyer DA, Venkatraman JT, Fernandes G. 1995. Dietary omega-3 lipids delay the onset and progression of autoimmune lupus nephritis by inhibiting transforming growth factor beta mRNA and protein expression. J Autoimmun. 8(3):381–393. doi: 10.1006/jaut.1995.0030.
  • Chang HY, Lee HN, Kim W, Surh YJ. 2015. Docosahexaenoic acid induces M2 macrophage polarization through peroxisome proliferator-activated receptor γ activation. Life Sci. 120:39–47. doi: 10.1016/j.lfs.2014.10.014.
  • Chiang N, Dalli J, Colas RA, Serhan CN. 2015. Identification of resolvin D2 receptor mediating resolution of infections and organ protection. J Exp Med. 212(8):1203–1217. doi: 10.1084/jem.20150225.
  • Crampton SP, Morawski PA, Bolland S. 2014. Linking susceptibility genes and pathogenesis mechanisms using mouse models of systemic lupus erythematosus. Dis Model Mech. 7(9):1033–1046. doi: 10.1242/dmm.016451.
  • Djuricic I, Calder PC. 2021. Beneficial outcomes of omega-6 and omega-3 polyunsaturated fatty acids on human health: an update for 2021. Nutrients. 2021. 13:2421. doi:10.3390/nu13072421.
  • Dubois EL, Horowitz RE, Demopoulos HB, Teplitz R. 1966. NZB/NZW mice as a model of systemic lupus erythematosus. JAMA. 195(4):285–289. doi: 10.1001/jama.1966.03100040091025.
  • Favor OK, Rajasinghe LD, Wierenga KA, Maddipati KR, Lee KSS, Olive AJ, Pestka JJ. 2023. Crystalline silica-induced proinflammatory eicosanoid storm in novel alveolar macrophage model quelled by docosahexaenoic acid supplementation [Original Research. Front Immunol. 14:1274147. doi: 10.3389/fimmu.2023.1274147.
  • Finckh A, Cooper GS, Chibnik LB, Costenbader KH, Watts J, Pankey H, Fraser PA, Karlson EW. 2006. Occupational silica and solvent exposures and risk of systemic lupus erythematosus in urban women. Arthritis Rheum. 54(11):3648–3654. doi: 10.1002/art.22210.
  • Flammer JR, Rogatsky I. 2011. Minireview: glucocorticoids in autoimmunity: unexpected targets and mechanisms. Mol Endocrinol. 25(7):1075–1086. doi: 10.1210/me.2011-0068.
  • Flurkey KM, Currer J, Harrison DE, et al. 2007. Chapter 20 - Mouse models in aging research. In: Fox JG, Davisson MT, Quimby FW, editors. The mouse in biomedical research 2nd ed. Burlington: Academic Press; p. 637–672.
  • Fredman G, Hellmann J, Proto JD, Kuriakose G, Colas RA, Dorweiler B, Connolly ES, Solomon R, Jones DM, Heyer EJ, et al. 2016. An imbalance between specialized pro-resolving lipid mediators and pro-inflammatory leukotrienes promotes instability of atherosclerotic plaques. Nat Commun. 7(1):12859. doi: 10.1038/ncomms12859.
  • Gelfand MC, Steinberg AD, Nagle R, Knepshield JH. 1972. Therapeutic studies in NZB-W mice. I. Synergy of azathioprine, cyclophosphamide and methylprednisolone in combination. Arthritis Rheum. 15(3):239–246. doi: 10.1002/art.1780150304.
  • Gilley KN, Wierenga KA, Chauhuan PS, Wagner JG, Lewandowski RP, Ross EA, Lock AL, Harkema JR, Benninghoff AD, Pestka JJ, et al. 2020. Influence of total western diet on docosahexaenoic acid suppression of silica-triggered lupus flaring in NZBWF1 mice. PLoS One. 15(5):e0233183. doi: 10.1371/journal.pone.0233183.
  • Godfrey DG, Stimson WH, Watson J, Belch JF, Sturrock RD. 1986. Effects of dietary supplementation on autoimmunity in the MRL/lpr mouse: a preliminary investigation. Ann Rheum Dis. 45(12):1019–1024. doi: 10.1136/ard.45.12.1019.
  • Hagan C. 2017. When are mice considered old? [cited. https://www.jax.org/news-and-insights/jax-blog/2017/November/when-are-mice-considered-old.
  • Halade GV, Williams PJ, Veigas JM, Barnes JL, Fernandes G. 2013. Concentrated fish oil (Lovaza(R)) extends lifespan and attenuates kidney disease in lupus-prone short-lived (NZBxNZW)F1 mice. Exp Biol Med (Maywood). 238(6):610–622. doi: 10.1177/1535370213489485.
  • Heine LK, Benninghoff AD, Ross EA, Rajasinghe LD, Wagner JG, Lewandowski RP, Richardson AL, Li QZ, Buchweitz JP, Zyskowski J, et al. 2022. Comparative effects of human-equivalent low, moderate, and high dose oral prednisone intake on autoimmunity and glucocorticoid-related toxicity in a murine model of environmental-triggered lupus. Front Immunol. 13:972108. doi: 10.3389/fimmu.2022.972108.
  • Hicks JD, Burnet FM. 1966. Apr Renal lesions in the "auto-immune" mouse strains NZB and F1 NZBxNZW. J Pathol Bacteriol. 91(2):467–476. doi: 10.1002/path.1700910221.
  • Hoy RF, Chambers DC. 2020. Silica‐related diseases in the modern world. Allergy. 75(11):2805–2817. doi: 10.1111/all.14202.
  • Hwang DH, Kim JA, Lee JY. 2016. Mechanisms for the activation of Toll-like receptor 2/4 by saturated fatty acids and inhibition by docosahexaenoic acid. Eur J Pharmacol. 785:24–35. doi: 10.1016/j.ejphar.2016.04.024.
  • Jin F, Li Y, Wang X, Yang X, Li T, Xu H, Wei Z, Liu H et al. 2022. Effect of sex differences in silicotic mice. Int J Mol Sci. 23(22):14203. doi: 10.3390/ijms232214203.
  • Lamore R, Parmar S, Patel K, Hilas O. 2012. Belimumab (Benlysta): a breakthrough therapy for systemic lupus erythematosus. P and T. 37(4):212–226.
  • Lands B, Bibus D, Stark KD. 2018. Sep Dynamic interactions of n-3 and n-6 fatty acid nutrients. Prostaglandins Leukot Essent Fatty Acids. 136:15–21. doi: 10.1016/j.plefa.2017.01.012.
  • Li X, Bi X, Wang S, Zhang Z, Li F, Zhao AZ. 2019. Therapeutic potential of ω-3 polyunsaturated fatty acids in human autoimmune diseases. front Immunol. 10:2241. doi: 10.3389/fimmu.2019.02241.
  • Li X, Yu Y, Funk CD. 2013. Dec Cyclooxygenase-2 induction in macrophages is modulated by docosahexaenoic acid via interactions with free fatty acid receptor 4 (FFA4). Faseb J. 27(12):4987–4997. doi: 10.1096/fj.13-235333.
  • Ostermann AI, Schebb NH. 2017. Effects of omega-3 fatty acid supplementation on the pattern of oxylipins: a short review about the modulation of hydroxy-, dihydroxy-, and epoxy-fatty acids. Food Funct. 8(7):2355–2367. Jul 06. doi: 10.1039/c7fo00403f.
  • Parks CG, Conrad K, Cooper GS. 1999. Occupational exposure to crystalline silica and autoimmune disease. Environ Health Perspect. 107 (Suppl 5):793–802. doi: 10.1289/ehp.99107s5793.
  • Parks CG, Cooper GS, Nylander-French LA, Sanderson WT, Dement JM, Cohen PL, Dooley MA, Treadwell EL, St Clair EW, Gilkeson GS, et al. 2002. Occupational exposure to crystalline silica and risk of systemic lupus erythematosus: a population-based, case-control study in the southeastern United States. Arthritis Rheum. 46(7):1840–1850. doi: 10.1002/art.10368.
  • Parks CG, de Souza Espindola Santos A, Barbhaiya M, Costenbader KH. 2017. Understanding the role of environmental factors in the development of systemic lupus erythematosus. Best Pract Res Clin Rheumatol. 31(3):306–320. doi: 10.1016/j.berh.2017.09.005.
  • Pestka JJ, Akbari P, Wierenga KA, Bates MA, Gilley KN, Wagner JG, Lewandowski RP, Rajasinghe LD, Chauhan PS, Lock AL, et al. 2021. Omega-3 polyunsaturated fatty acid intervention against established autoimmunity in a murine model of toxicant-triggered lupus. Front Immunol. 12:653464. doi: 10.3389/fimmu.2021.653464.
  • Pestka JJ, Vines LL, Bates MA, He K, Langohr I. 2014. Comparative effects of n-3, n-6 and n-9 unsaturated fatty acid-rich diet consumption on lupus nephritis, autoantibody production and CD4+ T cell-related gene responses in the autoimmune NZBWF1 mouse [Comparative Study Research Support, N.I.H., Extramural]. PLoS One. 9(6):e100255. doi: 10.1371/journal.pone.0100255.
  • Pestka JJ. 2010. n-3 Polyunsaturated fatty acids and autoimmune-mediated glomerulonephritis. Prostaglandins Leukot Essent Fatty Acids. 82(4-6):251–258. doi: 10.1016/j.plefa.2010.02.013.
  • Poinen-Rughooputh S, Rughooputh MS, Guo Y, Lai H, Sun W, Chen W. 2021. Sex-related differences in the risk of silicosis among chinese pottery workers: a cohort study. J Occup Environ Med. 63(1):74–79. doi: 10.1097/JOM.0000000000002068.
  • Porta S, Danza A, Arias Saavedra M, Carlomagno A, Goizueta MC, Vivero F, Ruiz-Irastorza G. 2020. Glucocorticoids in systemic lupus erythematosus. ten questions and some issues. J Clin Med. 9(9):2709–2709. doi: 10.3390/jcm9092709.
  • Prickett JD, Robinson DR, Steinberg AD. 1982. A diet enriched with eicosapentaenoic acid suppresses autoimmune nephritis in female (NZB x NZW) F1 mice. Trans Assoc Am Physicians. 95:145–154.
  • Raanan R, Zack O, Ruben M, Perluk I, Moshe S. 2022. Occupational silica exposure and dose; response for related disorders; silicosis, pulmonary TB, AIDs and renal diseases: results of a 15-year Israeli surveillance. Int J Environ Res Public Health. 19(22):15010. doi: 10.3390/ijerph192215010.
  • Radulescu CI, Cerar V, Haslehurst P, Kopanitsa M, Barnes SJ. 2021. The aging mouse brain: cognition, connectivity and calcium. Cell Calcium. 94:102358. 2021/03/01/doi: 10.1016/j.ceca.2021.102358.
  • Rajasinghe LD, Li Q-Z, Zhu C, Yan M, Chauhan PS, Wierenga KA, Bates MA, Harkema JR, Benninghoff AD, Pestka JJ, et al. 2020. Omega-3 fatty acid intake suppresses induction of diverse autoantibody repertoire by crystalline silica in lupus-prone mice. Autoimmunity. 53(7):415–433. doi: 10.1080/08916934.2020.1801651.
  • Ramos PS, Brown EE, Kimberly RP, Langefeld CD. 2010. Genetic factors predisposing to systemic lupus erythematosus and lupus nephritis. Semin Nephrol. 30(2):164–176. doi: 10.1016/j.semnephrol.2010.01.007.
  • Ray JL, Holian A. 2019. Sex differences in the inflammatory immune response to multi-walled carbon nanotubes and crystalline silica. Inhal Toxicol. 31(7):285–297. doi: 10.1080/08958378.2019.1669743.
  • Reeves WH, Lee PY, Weinstein JS, Satoh M, Lu L. 2009. Induction of autoimmunity by pristane and other naturally occurring hydrocarbons. Trends Immunol. 30(9):455–464. doi: 10.1016/j.it.2009.06.003.
  • Richard ML, Gilkeson G. 2018. Mouse models of lupus: what they tell us and what they don’t. Lupus Sci Med. 5(1):e000199. doi: 10.1136/lupus-2016-000199.
  • Ricote M, Glass CK. 2007. PPARs and molecular mechanisms of transrepression. Biochim Biophys Acta. 1771(8):926–935. doi: 10.1016/j.bbalip.2007.02.013.
  • Robinson DR, Prickett JD, Polisson R, Steinberg AD, Levine L. 1985. The protective effect of dietary fish oil on murine lupus. Prostaglandins. 30(1):51–75. doi: 10.1016/s0090-6980(85)80010-1.
  • Rudofsky UH, Lawrence DA. 1999. New Zealand mixed mice: a genetic systemic lupus erythematosus model for assessing environmental effects. Environ Health Perspect. 107 (Suppl 5):713–721. doi: 10.1289/ehp.99107s5713.
  • Serhan CN, Chiang N, Dalli J. 2015. The resolution code of acute inflammation: novel pro-resolving lipid mediators in resolution. Semin Immunol. 27(3):200–215. doi: 10.1016/j.smim.2015.03.004.
  • Sham HP, Walker KH, Abdulnour R-EE, Krishnamoorthy N, Douda DN, Norris PC, Barkas I, Benito-Figueroa S, Colby JK, Serhan CN, et al. 2018. Apr 15 15-epi-lipoxin A(4), resolvin D2, and resolvin D3 induce NF-kappa B regulators in bacterial pneumonia. J Immunol. 200(8):2757–2766. doi: 10.4049/jimmunol.1602090.
  • Titos E, Rius B, López-Vicario C, Alcaraz-Quiles J, García-Alonso V, Lopategi A, Dalli J, Lozano JJ, Arroyo V, Delgado S, et al. 2016. Signaling and immunoresolving actions of resolvin D1 in inflamed human visceral adipose tissue. J Immunol. 197(8):3360–3370. doi: 10.4049/jimmunol.1502522.
  • Tschanz SA, Burri PH, Weibel ER. 2011. A simple tool for stereological assessment of digital images: the STEPanizer. J Microsc. 243(1):47–59. doi: 10.1111/j.1365-2818.2010.03481.x.
  • Tsokos GC. 2011. Systemic lupus erythematosus. N Engl J Med. 365(22):2110–2121. doi: 10.1056/NEJMra1100359.
  • Watson J, Godfrey D, Stimson WH, Belch JJ, Sturrock RD. 1988. The therapeutic effects of dietary fatty acid supplementation in the autoimmune disease of the MRL-mp-lpr/lpr mouse. Int J Immunopharmacol. 10(4):467–471. doi: 10.1016/0192-0561(88)90135-x.
  • Weatherill AR, Lee JY, Zhao L, Lemay DG, Youn HS, Hwang DH. 2005. Saturated and polyunsaturated fatty acids reciprocally modulate dendritic cell functions mediated through TLR4. J Immunol. 174(9):5390–5397. doi: 10.4049/jimmunol.174.9.5390.
  • Weening JJ, D'Agati VD, Schwartz MM, Seshan SV, Alpers CE, Appel GB, Balow JE, Bruijn JA, Cook T, Ferrario F, et al. 2004. The classification of glomerulonephritis in systemic lupus erythematosus revisited. J Am Soc Nephrol. 15(2):241–250. doi: 10.1097/01.asn.0000108969.21691.5d.
  • Westberg G, Tarkowski A, Svalander C. 1989. Effect of eicosapentaenoic acid rich menhaden oil and MaxEPA on the autoimmune disease of Mrl/l mice. Int Arch Allergy Appl Immunol. 88(4):454–461. doi: 10.1159/000234732.
  • Wierenga KA, Harkema JR, Pestka JJ. 2019. Lupus, silica, and dietary omega-3 fatty acid interventions. Toxicol Pathol. 47(8):1004–1011. doi: 10.1177/0192623319878398.
  • Wierenga KA, Strakovsky RS, Benninghoff AD, Rajasinghe LD, Lock AL, Harkema JR, Pestka JJ. 2020. Requisite omega-3 HUFA biomarker thresholds for preventing murine lupus flaring. Front Immunol. 11:1796. doi: 10.3389/fimmu.2020.01796.
  • Wong SW, Kwon M-J, Choi AMK, Kim HP, Nakahira K, Hwang DH. 2009. Fatty acids modulate toll-like receptor 4 activation through regulation of receptor dimerization and recruitment into lipid rafts in a reactive oxygen species-dependent manner. J Biol Chem. 284(40):27384–27392. doi: 10.1074/jbc.M109.044065.
  • Wu H, Chang C, Lu Q. 2020. The Epigenetics of Lupus Erythematosus. Springer Singapore; p. 185–207.
  • Yan Y, Jiang W, Spinetti T, Tardivel A, Castillo R, Bourquin C, Guarda G, Tian Z, Tschopp J, Zhou R, et al. 2013. Omega-3 fatty acids prevent inflammation and metabolic disorder through inhibition of NLRP3 inflammasome activation. Immunity. 38(6):1154–1163. doi: 10.1016/j.immuni.2013.05.015.
  • Yu F, Haas M, Glassock R, Zhao MH. 2017. Redefining lupus nephritis: clinical implications of pathophysiologic subtypes. Nat Rev Nephrol. 13(8):483–495. doi: 10.1038/nrneph.2017.85.
  • Yu H, Nagafuchi Y, Fujio K. 2021. Clinical and Immunological Biomarkers for Systemic Lupus Erythematosus. Biomolecules. 11(7):928. doi: 10.3390/biom11070928.
  • Zucchi D, Elefante E, Schilirò D, Signorini V, Trentin F, Bortoluzzi A, Tani C. 2022. One year in review 2022: systemic lupus erythematosus. Clin Exp Rheumatol. 40(1):4–14. doi: 10.55563/clinexprheumatol/nolysy.