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Research Paper

PM2.5 induced neurotoxicity through unbalancing vitamin B12 metabolism by gut microbiota disturbance

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Article: 2267186 | Received 25 Apr 2023, Accepted 02 Oct 2023, Published online: 16 Oct 2023

References

  • Craig L, Brook JR, Chiotti Q, Croes B, Gower S, Hedley A, Krewski D, Krupnick A, Krzyzanowski M, Moran MD, et al. Air pollution and public health: a guidance document for risk managers. J Toxicol Env Heal A. 2008;71(9–10):588–21. doi:10.1080/15287390801997732.
  • Yue H, Yun Y, Gao R, Li G, Sang N. Winter polycyclic aromatic hydrocarbon-bound particulate matter from peri-urban North China promotes lung cancer cell metastasis. Environ Sci Technol. 2015;49(24):14484–14493. doi:10.1021/es506280c.
  • Eze IC, Hemkens LG, Bucher HC, Hoffmann B, Schindler C, Künzli N, Schikowski T, Probst-Hensch NM. Association between ambient air pollution and diabetes mellitus in Europe and North America: systematic review and meta-analysis. Environ Health Perspect. 2015;123(5):381–389. doi:10.1289/ehp.1307823.
  • Hamra GB, Guha N, Cohen A, Laden F, Raaschou-Nielsen O, Samet JM, Vineis P, Forastiere F, Saldiva P, Yorifuji T, et al. Outdoor particulate matter exposure and lung cancer: a systematic review and meta-analysis. Environ Health Perspect. 2014;122(9):906–911. doi:10.1289/ehp/1408092.
  • Brook RD, Rajagopalan S, Pope CA, Brook JR, Bhatnagar A, Diez-Roux AV, Holguin F, Hong Y, Luepker RV, Mittleman MA, et al. Particulate matter air pollution and cardiovascular disease. Circulation. 2010;121(21):2331–2378. doi:10.1161/CIR.0b013e3181dbece1.
  • Villeneuve PJ, Chen L, Rowe BH, Coates F. Outdoor air pollution and emergency department visits for asthma among children and adults: a case-crossover study in northern Alberta, Canada. Environ Health. 2007;6(1):40. doi:10.1186/1476-069X-6-40.
  • Araujo JA. Are ultrafine particles a risk factor for cardiovascular diseases? Rev Esp Cardiol. 2011;64(8):642–645. doi:10.1016/j.recesp.2011.05.002.
  • Ailshire JA, Clarke P. Fine particulate matter air pollution and cognitive function among U.S. older adults. J Gerontol B. 2015;70(2):322–328. doi:10.1093/geronb/gbu064.
  • Gatto NM, Henderson VW, Hodis HN, St. John JA, Lurmann F, Chen J, Mack WJ. Components of air pollution and cognitive function in middle-aged and older adults in Los Angeles. Neurotoxicology. 2014;40:1–7. doi:10.1016/j.neuro.2013.09.004.
  • Thiankhaw K, Chattipakorn N, Chattipakorn SC. PM2.5 exposure in association with AD-related neuropathology and cognitive outcomes. Environ Pollut. 2022;292(Pt A):118320. doi:10.1016/j.envpol.2021.118320.
  • Liu F, Liu C, Liu Y, Wang J, Wang Y, Yan B. Neurotoxicity of the air-borne particles: from molecular events to human diseases. J Hazard Mater. 2023;457:131827. doi:10.1016/j.jhazmat.2023.131827.
  • Guo C, Lyu Y, Xia S, Ren X, Li Z, Tian F, Zheng J. Organic extracts in PM2.5 are the major triggers to induce ferroptosis in SH-SY5Y cells. Ecotoxicol Environ Saf. 2023;249:114350. doi:10.1016/j.ecoenv.2022.114350.
  • Wei M, Bao G, Li S, Yang Z, Cheng C, Le W. PM2.5 exposure triggers cell death through lysosomal membrane permeabilization and leads to ferroptosis insensitivity via the autophagy dysfunction/p62-KEAP1-NRF2 activation in neuronal cells. Ecotoxicol Environ Saf. 2022;248:114333. doi:10.1016/j.ecoenv.2022.114333.
  • Basic M, Dardevet D, Abuja PM, Bolsega S, Bornes S, Caesar R, Calabrese FM, Collino M, De Angelis M, Gérard P, et al. Approaches to discern if microbiome associations reflect causation in metabolic and immune disorders. Gut Microbes. 2022;14(1):2107386. doi:10.1080/19490976.2022.2107386.
  • Dai S, Wang Z, Yang Y, Du P, Li X. PM2.5 induced weight loss of mice through altering the intestinal microenvironment: mucus barrier, gut microbiota, and metabolic profiling. J Hazard Mater. 2022;431:128653. doi:10.1016/j.jhazmat.2022.128653.
  • Mutlu EA, Comba IY, Cho T, Engen PA, Yazıcı C, Soberanes S, Hamanaka RB, Niğdelioğlu R, Meliton AY, Ghio AJ, et al. Inhalational exposure to particulate matter air pollution alters the composition of the gut microbiome. Environ Pollut. 2018;240:817–830. doi:10.1016/j.envpol.2018.04.130.
  • Li S, Guo B, Dong K, Huang S, Wu J, Zhou H, Wu K, Han X, Liang X, Pei X, et al. Association of long-term exposure to ambient PM2.5 and its constituents with gut microbiota: evidence from a China cohort. Sci Total Environ. 2023;884:163577. doi:10.1016/j.scitotenv.2023.163577.
  • Qin J, Wang J. Research progress on the effects of gut microbiome on lung damage induced by particulate matter exposure. Environ Res. 2023;233:116162. doi:10.1016/j.envres.2023.116162.
  • Smith AD, Warren MJ, Refsum H. Chapter six - Vitamin B12. In: Eskin NAM, editor. Advances in food and nutrition research. Vol. 2018. Academic Press; 2018. p. 215–279. doi:10.1016/bs.afnr.2017.11.005.
  • Mccarter SJ, Coon EA, Savica R, St Louis EK, Bower JH, Benarroch EE, Sandroni P, Low P, Singer W. Lower Vitamin B12 level at multiple system atrophy diagnosis is associated with shorter survival. Mov Disord. 2020;35(8):1462–1466. doi:10.1002/mds.28070.
  • Mccarter SJ, Teigen LM, Mccarter AR, Benarroch EE, St LE, Savica R. Low Vitamin B12 and Parkinson disease: potential link to reduced cholinergic transmission and severity of disease. Mayo Clin Proc. 2019;94(5):757–762. doi:10.1016/j.mayocp.2019.01.039.
  • Ji X, Li C, Zhu X, Yu W, Cai Y, Zhu X, Lu L, Qian Q, Hu Y, Zhu X, et al. Methylcobalamin alleviates neuronal apoptosis and cognitive decline induced by PM2.5 exposure in mice. J Alzheimer Dis. 2022;86(4):1783–1796. doi:10.3233/JAD-215384.
  • Zhang J, Holdorf AD, Walhout AJ. C. elegans and its bacterial diet as a model for systems-level understanding of host–microbiota interactions. Curr Opin Biotechnol. 2017;46:74–80. doi:10.1016/j.copbio.2017.01.008.
  • Backes C, Martinez-Martinez D, Cabreiro F. C. elegans: a biosensor for host–microbe interactions. Lab Anim (NY). 2021;50(5):127–135. doi:10.1038/s41684-021-00724-z.
  • Xu T, Zhang M, Hu J, Li Z, Wu T, Bao J, Wu S, Lei L, He D. Behavioral deficits and neural damage of Caenorhabditis elegans induced by three rare earth elements. Chemosphere. 2017;181:55–62. doi:10.1016/j.chemosphere.2017.04.068.
  • Ishihara T, Iino Y, Mohri A, Mori I, Gengyo-Ando K, Mitani S, Katsura I. HEN-1, a secretory protein with an LDL receptor motif, regulates sensory integration and learning in Caenorhabditis elegans. Cell. 2002;109(5):639–649. doi:10.1016/S0092-8674(02)00748-1.
  • Soares MV, Charão MF, Jacques MT, Dos Santos ALA, Luchese C, Pinton S, Ávila DS. Airborne toluene exposure causes germline apoptosis and neuronal damage that promotes neurobehavioural changes in Caenorhabditis elegans. Environ Pollut. 2020;256:113406. doi:10.1016/j.envpol.2019.113406.
  • Wu T, He K, Zhan Q, Ang S, Ying J, Zhang S, Zhang T, Xue Y, Tang M. MPA-capped CdTe quantum dots exposure causes neurotoxic effects in nematode Caenorhabditis elegans by affecting the transporters and receptors of glutamate, serotonin and dopamine at the genetic level, or by increasing ROS, or both. Nanoscale. 2015;7(48):20460–20473. doi:10.1039/C5NR05914C.
  • Lam AB, Kervin K, Tanis JE. Vitamin B12 impacts amyloid beta-induced proteotoxicity by regulating the methionine/S-adenosylmethionine cycle. Cell Rep. 2021;36(13):109753. doi:10.1016/j.celrep.2021.109753.
  • Giese GE, Walker MD, Ponomarova O, Zhang H, Li X, Minevich G, Walhout AJ. Caenorhabditis elegans methionine/S-adenosylmethionine cycle activity is sensed and adjusted by a nuclear hormone receptor. Elife. 2020;9:e60259. doi:10.7554/eLife.60259.
  • Qin S, Wang Y, Li L, Liu J, Xiao C, Duan D, Hao W, Qin C, Chen J, Yao L, et al. Early-life vitamin B12 orchestrates lipid peroxidation to ensure reproductive success via SBP-1/SREBP1 in Caenorhabditis elegans. Cell Rep. 2022;40(12):111381. doi:10.1016/j.celrep.2022.111381.
  • Strandwitz P. Neurotransmitter modulation by the gut microbiota. Brain Res. 2018;1693:128–133. doi:10.1016/j.brainres.2018.03.015.
  • Landini L, Dadson P, Gallo F, Honka M, Cena H. Microbiota in anorexia nervosa – potential for treatment. Nutr Res Rev. 2022;1–51. doi:10.1017/S0954422422000130.
  • Dalile B, Van Oudenhove L, Vervliet B, Verbeke K. The role of short-chain fatty acids in microbiota–gut–brain communication. Nat Rev Gastroenterol Hepatol. 2019;16(8):461–478. doi:10.1038/s41575-019-0157-3.
  • Chen Y, Xu J, Chen Y. Regulation of neurotransmitters by the gut microbiota and effects on cognition in neurological disorders. Nutrients. 2021;13(6):2099. doi:10.3390/nu13062099.
  • Bernhardt C, Zhu X, Schütz D, Fischer M, Bisping B. Cobalamin is produced by Acetobacter pasteurianus DSM 3509. Appl Microbiol Biotechnol. 2019;103(9):3875–3885. doi:10.1007/s00253-019-09704-3.
  • Zhu X, Xiang S, Feng X, Wang H, Tian S, Xu Y, Shi L, Yang L, Li M, Shen Y, et al. Impact of cyanocobalamin and methylcobalamin on inflammatory bowel disease and the intestinal microbiota composition. J Agric Food Chem. 2019;67(3):916–926. doi:10.1021/acs.jafc.8b05730.
  • Guetterman HM, Huey SL, Knight R, Fox AM, Mehta S, Finkelstein JL. Vitamin B-12 and the gastrointestinal microbiome: a systematic review. Adv Nutr. 2022;13(2):530–558. doi:10.1093/advances/nmab123.
  • Mohammed Y, Lee B, Kang Z, Du G. Development of a two-step cultivation strategy for the production of vitamin B12 by Bacillus megaterium. Microb Cell Fact. 2014;13(1):102. doi:10.1186/s12934-014-0102-7.
  • Yao L, Wang Y, Qin S, Zhu S, Wu L. The antidiabetic drug metformin aids bacteria in hijacking vitamin B12 from the environment through RcdA. Commun Biol. 2023;6(1):96. doi:10.1038/s42003-023-04475-0.
  • Nilaweera TD, Nyenhuis DA, Cafiso DS. Structural intermediates observed only in intact Escherichia coli indicate a mechanism for TonB-dependent transport. Elife. 2021;10:e68548. doi:10.7554/eLife.68548.
  • Thiankhaw K, Chattipakorn N, Chattipakorn SC. PM2.5 exposure in association with AD-related neuropathology and cognitive outcomes. Environ Pollut. 2022;292:118320. doi:10.1016/j.envpol.2021.118320.
  • Bailey MJ, Holzhausen EA, Morgan ZEM, Naik N, Shaffer JP, Liang D, Chang HH, Sarnat J, Sun S, Berger PK, et al. Postnatal exposure to ambient air pollutants is associated with the composition of the infant gut microbiota at 6-months of age. Gut Microbes. 2022;14(1):2105096. doi:10.1080/19490976.2022.2105096.
  • Sun L, Wu Q, Liao K, Yu P, Cui Q, Rui Q, Wang D. Contribution of heavy metals to toxicity of coal combustion related fine particulate matter (PM2.5) in Caenorhabditis elegans with wild-type or susceptible genetic background. Chemosphere. 2016;144:2392–2400. doi:10.1016/j.chemosphere.2015.11.028.
  • Yilmaz LS, Walhout AJM. Worms, bacteria, and micronutrients: an elegant model of our diet. Trends Genet. 2014;30(11):496–503. doi:10.1016/j.tig.2014.07.010.
  • Du M, Wang D. The neurotoxic effects of heavy metal exposure on GABAergic nervous system in nematode Caenorhabditis elegans. Environ Toxicol Pharmacol. 2009;27(3):314–320. doi:10.1016/j.etap.2008.11.011.
  • Treinin M, Jin Y. Cholinergic transmission in C. elegans: functions, diversity, and maturation of ACh‐activated ion channels. J Neurochem. 2021;158(6):1274–1291. doi:10.1111/jnc.15164.
  • Roth W, Mohamadzadeh M. Vitamin B12 and gut-brain homeostasis in the pathophysiology of ischemic stroke. EBioMedicine. 2021;73:103676. doi:10.1016/j.ebiom.2021.103676.
  • Zhu X, Xiang S, Feng X, Wang H, Tian S, Xu Y, Shi L, Yang L, Li M, Shen Y, et al. Impact of cyanocobalamin and methylcobalamin on inflammatory bowel disease and the intestinal microbiota composition. J Agric Food Chem. 2019;67(3):916–926. doi:10.1021/acs.jafc.8b05730.
  • Xu Y, Xiang S, Ye K, Zheng Y, Feng X, Zhu X, Chen J, Chen Y. Cobalamin (vitamin B12) induced a shift in microbial composition and metabolic activity in an in vitro colon simulation. Front Microbiol. 2018;9:2780. doi:10.3389/fmicb.2018.02780.
  • Yan F, Xiang S, Shi L, Zhu X. Synthesis of queuine by colonic gut microbiome via cross-feeding. Food Front. 2023. doi:10.1002/fft2.307.
  • O’Riordan KJ, Collins MK, Moloney GM, Knox EG, Aburto MR, Fülling C, Morley SJ, Clarke G, Schellekens H, Cryan JF, et al. Short chain fatty acids: microbial metabolites for gut-brain axis signalling. Mol Cell Endocrinol. 2022;546:111572. doi:10.1016/j.mce.2022.111572.
  • Shou Y, Zhu X, Zhu D, Yin H, Shi Y, Chen M, Lu L, Qian Q, Zhao D, Hu Y, et al. Ambient PM2.5 chronic exposure leads to cognitive decline in mice: from pulmonary to neuronal inflammation. Toxicol Lett. 2020;331:208–217. doi:10.1016/j.toxlet.2020.06.014.
  • Zhang X, Ye Y, Sun J, Wang JS, Tang L, Xu Y, Ji J, Sun X. Abnormal neurotransmission of GABA and serotonin in Caenorhabditis elegans induced by Fumonisin B1. Environ Pollut. 2022;304:119141. doi:10.1016/j.envpol.2022.119141.