Formaldehyde initiates memory and motor impairments under weightlessness condition.
Journal
NPJ microgravity
ISSN: 2373-8065
Titre abrégé: NPJ Microgravity
Pays: United States
ID NLM: 101703605
Informations de publication
Date de publication:
28 Oct 2024
28 Oct 2024
Historique:
received:
27
10
2023
accepted:
21
10
2024
medline:
29
10
2024
pubmed:
29
10
2024
entrez:
29
10
2024
Statut:
epublish
Résumé
During space flight, prolonged weightlessness stress exerts a range of detrimental impacts on the physiology and psychology of astronauts. These manifestations encompass depressive symptoms, anxiety, and impairments in both short-term memory and motor functions, albeit the precise underlying mechanisms remain elusive. Recent studies have revealed that hindlimb unloading (HU) animal models, which simulate space weightlessness, exhibited a disorder in memory and motor function associated with endogenous formaldehyde (FA) accumulation in the hippocampus and cerebellum, disruption of brain extracellular space (ECS), and blockage of interstitial fluid (ISF) drainage. Notably, the impairment of the blood-brain barrier (BBB) caused by space weightlessness elicits the infiltration of albumin and hemoglobin from the blood vessels into the brain ECS. However, excessive FA has the potential to form cross-links between these two proteins and amyloid-beta (Aβ), thereby obstructing ECS and inducing neuron death. Moreover, FA can inhibit N-methyl-D-aspartate (NMDA) currents by crosslinking NR1 and NR2B subunits, thus impairing memory. Additionally, FA has the ability to modulate the levels of certain microRNAs (miRNAs) such as miRNA-29b, which can affect the expression of aquaporin-4 (AQP4) so as to regulate ECS structure and ISF drainage. Especially, the accumulation of FA may inactivate the ataxia telangiectasia-mutated (ATM) protein kinase by forming cross-linking, a process that is associated with ataxia. Hence, this review presents that weightlessness stress-derived FA may potentially serve as a crucial catalyst in the deterioration of memory and motor abilities in the context of microgravity.
Identifiants
pubmed: 39468074
doi: 10.1038/s41526-024-00441-0
pii: 10.1038/s41526-024-00441-0
doi:
Types de publication
Journal Article
Review
Langues
eng
Pagination
100Subventions
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 82071214
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 82071214
Informations de copyright
© 2024. The Author(s).
Références
Prasad, B. et al. Influence of microgravity on apoptosis in cells, tissues, and other systems in vivo and in vitro. Int. J. Mol. Sci. 21, https://doi.org/10.3390/ijms21249373 (2020).
Oluwafemi, F. A., Abdelbaki, R., Lai, J. C., Mora-Almanza, J. G. & Afolayan, E. M. A review of astronaut mental health in manned missions: potential interventions for cognitive and mental health challenges. Life Sci. Space Res. 28, 26–31 (2021).
doi: 10.1016/j.lssr.2020.12.002
Roy-O’Reilly, M., Mulavara, A. & Williams, T. A review of alterations to the brain during spaceflight and the potential relevance to crew in long-duration space exploration. NPJ Microgravity 7, 5 (2021).
pubmed: 33594073
pmcid: 7887220
doi: 10.1038/s41526-021-00133-z
Ai, L. et al. Endogenous formaldehyde is a memory-related molecule in mice and humans. Commun. Biol. 2, 446 (2019).
pubmed: 31815201
pmcid: 6884489
doi: 10.1038/s42003-019-0694-x
Palasz, A., Menezes, I. C. & Worthington, J. J. The role of brain gaseous neurotransmitters in anxiety. Pharm. Rep. 73, 357–371 (2021).
doi: 10.1007/s43440-021-00242-2
Kou, Y., Zhao, H., Cui, D., Han, H. & Tong, Z. Formaldehyde toxicity in age-related neurological dementia. Ageing Res. Rev. 73, 101512 (2022).
pubmed: 34798299
doi: 10.1016/j.arr.2021.101512
Yao, D. et al. Accumulation of formaldehyde causes motor deficits in an in vivo model of hindlimb unloading. Commun. Biol. 4, 933 (2021).
pubmed: 34413463
pmcid: 8376875
doi: 10.1038/s42003-021-02448-9
Yu, P. H. Deamination of methylamine and angiopathy; toxicity of formaldehyde, oxidative stress and relevance to protein glycoxidation in diabetes. J. Neural Transm. Suppl. 52, 201–216 (1998).
pubmed: 9564620
doi: 10.1007/978-3-7091-6499-0_19
Yu, P. H., Lai, C. T. & Zuo, D. M. Formation of formaldehyde from adrenaline in vivo; a potential risk factor for stress-related angiopathy. Neurochem Res. 22, 615–620 (1997).
pubmed: 9131641
doi: 10.1023/A:1022478221421
Zhang, J. et al. Illumination with 630 nm red light reduces oxidative stress and restores memory by photo-activating catalase and formaldehyde dehydrogenase in SAMP8 mice. Antioxid. Redox Signal. 30, 1432–1449 (2019).
pubmed: 29869529
doi: 10.1089/ars.2018.7520
Jelski, W., Sani, T. A. & Szmitkowski, M. [Class III alcohol dehydrogenase and its role in the human body]. Postepy Hig. Med. Dosw. 60, 406–409 (2006).
Han, H. et al. A novel MRI tracer-based method for measuring water diffusion in the extracellular space of the rat brain. IEEE J. Biomed. Health Inf. 18, 978–983 (2014).
doi: 10.1109/JBHI.2014.2308279
Jia, Y. et al. Transmembrane water-efflux rate measured by magnetic resonance imaging as a biomarker of the expression of aquaporin-4 in gliomas. Nat. Biomed. Eng. 7, 236–252 (2023).
pubmed: 36376487
doi: 10.1038/s41551-022-00960-9
Peng, S., Liu, J., Liang, C., Yang, L. & Wang, G. Aquaporin-4 in glymphatic system, and its implication for central nervous system disorders. Neurobiol. Dis. 179, 106035 (2023).
pubmed: 36796590
doi: 10.1016/j.nbd.2023.106035
Rager, J. E., Smeester, L., Jaspers, I., Sexton, K. G. & Fry, R. C. Epigenetic changes induced by air toxics: formaldehyde exposure alters miRNA expression profiles in human lung cells. Environ. Health Perspect. 119, 494–500 (2011).
pubmed: 21147603
doi: 10.1289/ehp.1002614
Li, G., Yang, J. & Ling, S. Formaldehyde exposure alters miRNA expression profiles in the olfactory bulb. Inhal. Toxicol. 27, 387–393 (2015).
pubmed: 26161908
doi: 10.3109/08958378.2015.1062580
Rager, J. E. et al. Formaldehyde and epigenetic alterations: microRNA changes in the nasal epithelium of nonhuman primates. Environ. Health Perspect. 121, 339–344 (2013).
pubmed: 23322811
pmcid: 3621188
doi: 10.1289/ehp.1205582
Teng, Z. et al. The effect of aquaporin-4 knockout on interstitial fluid flow and the structure of the extracellular space in the deep brain. Aging Dis. 9, 808–816, (2018).
pubmed: 30271658
pmcid: 6147590
doi: 10.14336/AD.2017.1115
Odackal, J. et al. Real-time Iontophoresis with tetramethylammonium to quantify volume fraction and tortuosity of brain extracellular space. J. Vis. Exp. https://doi.org/10.3791/55755 (2017).
Lei, Y., Han, H., Yuan, F., Javeed, A. & Zhao, Y. The brain interstitial system: anatomy, modeling, in vivo measurement, and applications. Prog. Neurobiol. 157, 230–246 (2017).
pubmed: 26837044
doi: 10.1016/j.pneurobio.2015.12.007
Aukland, K. & Reed, R. K. Interstitial-lymphatic mechanisms in the control of extracellular fluid volume. Physiol. Rev. 73, 1–78 (1993).
pubmed: 8419962
doi: 10.1152/physrev.1993.73.1.1
Khasawneh, A. H., Garling, R. J. & Harris, C. A. Cerebrospinal fluid circulation: what do we know and how do we know it? Brain Circ. 4, 14–18, (2018).
pubmed: 30276331
pmcid: 6057699
doi: 10.4103/bc.BC_3_18
Iliff, J. J. et al. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci. Transl. Med. 4, 147ra111 (2012).
pubmed: 22896675
pmcid: 3551275
doi: 10.1126/scitranslmed.3003748
Tarasoff-Conway, J. M. et al. Clearance systems in the brain-implications for Alzheimer’s disease. Nat. Rev. Neurol. 11, 457–470 (2015).
pubmed: 26195256
pmcid: 4694579
doi: 10.1038/nrneurol.2015.119
Ma, Q., Ineichen, B. V., Detmar, M. & Proulx, S. T. Outflow of cerebrospinal fluid is predominantly through lymphatic vessels and is reduced in aged mice. Nat. Commun. 8, 1434 (2017).
pubmed: 29127332
pmcid: 5681558
doi: 10.1038/s41467-017-01484-6
Jullienne, A. et al. Chronic cerebrovascular dysfunction after traumatic brain injury. J. Neurosci. Res. 94, 609–622 (2016).
pubmed: 27117494
pmcid: 5415378
doi: 10.1002/jnr.23732
Harrison, I. F. et al. Impaired glymphatic function and clearance of tau in an Alzheimer’s disease model. Brain 143, 2576–2593 (2020).
pubmed: 32705145
pmcid: 7447521
doi: 10.1093/brain/awaa179
Sundaram, S. et al. Establishing a framework for neuropathological correlates and glymphatic system functioning in Parkinson’s disease. Neurosci. Biobehav Rev. 103, 305–315 (2019).
pubmed: 31132378
pmcid: 6692229
doi: 10.1016/j.neubiorev.2019.05.016
Xia, M., Yang, L., Sun, G., Qi, S. & Li, B. Mechanism of depression as a risk factor in the development of Alzheimer’s disease: the function of AQP4 and the glymphatic system. Psychopharmacology 234, 365–379 (2017).
pubmed: 27837334
doi: 10.1007/s00213-016-4473-9
Munk, A. S. et al. PDGF-B is required for development of the glymphatic system. Cell Rep. 26, 2955–2969.e2953 (2019).
pubmed: 30865886
pmcid: 6447074
doi: 10.1016/j.celrep.2019.02.050
Pollay, M. The function and structure of the cerebrospinal fluid outflow system. Cerebrospinal Fluid Res. 7, 9 (2010).
pubmed: 20565964
pmcid: 2904716
doi: 10.1186/1743-8454-7-9
Louveau, A. et al. CNS lymphatic drainage and neuroinflammation are regulated by meningeal lymphatic vasculature. Nat. Neurosci. 21, 1380–1391 (2018).
pubmed: 30224810
pmcid: 6214619
doi: 10.1038/s41593-018-0227-9
Iliff, J. J. et al. Cerebral arterial pulsation drives paravascular CSF-interstitial fluid exchange in the murine brain. J. Neurosci. 33, 18190–18199 (2013).
pubmed: 24227727
pmcid: 3866416
doi: 10.1523/JNEUROSCI.1592-13.2013
Musiał, A., Gryglewski, R. W., Kielczewski, S., Loukas, M. & Wajda, J. Formalin use in anatomical and histological science in the 19th and 20th centuries. Folia Med. Cracov. 56, 31–40 (2016).
pubmed: 28275269
Pinto, J. P., Gladstone, G. R. & Yung, Y. L. Photochemical production of formaldehyde in Earth’s primitive atmosphere. Science 210, 183–185 (1980).
pubmed: 17741284
doi: 10.1126/science.210.4466.183
Robertson, M. P., & Miller, S. L. An efficient prebiotic synthesis is of cytosine and uracil. Nature 375, 772–774 (1995).
pubmed: 7596408
doi: 10.1038/375772a0
Lu, Z., Li, C. M., Qiao, Y., Yan, Y. & Yang, X. Effect of inhaled formaldehyde on learning and memory of mice. Indoor Air 18, 77–83 (2008).
pubmed: 18333987
doi: 10.1111/j.1600-0668.2008.00524.x
Kilburn, K. H., Warshaw, R. & Thornton, J. C. Formaldehyde impairs memory, equilibrium, and dexterity in histology technicians: effects which persist for days after exposure. Arch. Environ. Health 42, 117–120 (1987).
pubmed: 3579365
doi: 10.1080/00039896.1987.9935806
Kalász, H. Biological role of formaldehyde, and cycles related to methylation, demethylation, and formaldehyde production. Mini Rev. Med. Chem. 3, 175–192 (2003).
pubmed: 12570834
doi: 10.2174/1389557033488187
Zhuo, M., Small, S. A., Kandel, E. R. & Hawkins, R. D. Nitric oxide and carbon monoxide produce activity-dependent long-term synaptic enhancement in hippocampus. Science 260, 1946–1950 (1993).
pubmed: 8100368
doi: 10.1126/science.8100368
Bour, S. et al. Adipogenesis-related increase of semicarbazide-sensitive amine oxidase and monoamine oxidase in human adipocytes. Biochimie 89, 916–925 (2007).
pubmed: 17400359
doi: 10.1016/j.biochi.2007.02.013
Ozen, O. A. et al. Effect of formaldehyde inhalation on Hsp70 in seminiferous tubules of rat testes: an immunohistochemical study. Toxicol. Ind. Health 21, 249–254 (2005).
pubmed: 16463957
doi: 10.1191/0748233705th235oa
Frankenhaeuser, M. Behavior and circulating catecholamines. Brain Res. 31, 241–262 (1971).
pubmed: 5569149
doi: 10.1016/0006-8993(71)90180-6
Edmondson, D. E. & Binda, C. Monoamine oxidases. Subcell. Biochem. 87, 117–139 (2018).
pubmed: 29464559
doi: 10.1007/978-981-10-7757-9_5
Boor, P. J., Trent, M. B., Lyles, G. A., Tao, M. & Ansari, G. A. Methylamine metabolism to formaldehyde by vascular semicarbazide-sensitive amine oxidase. Toxicology 73, 251–258 (1992).
pubmed: 1631902
doi: 10.1016/0300-483X(92)90067-O
Yu, P. H., Davis, B. A. & Boulton, A. A. Aliphatic propargylamines: potent, selective, irreversible monoamine oxidase B inhibitors. J. Med. Chem. 35, 3705–3713 (1992).
pubmed: 1433183
doi: 10.1021/jm00098a017
Lu, J., Miao, J., Su, T., Liu, Y. & He, R. Formaldehyde induces hyperphosphorylation and polymerization of Tau protein both in vitro and in vivo. Biochim. Biophys. Acta 1830, 4102–4116 (2013).
pubmed: 23628704
doi: 10.1016/j.bbagen.2013.04.028
Tong, Z. et al. Accumulated hippocampal formaldehyde induces age-dependent memory decline. Age 35, 583–596 (2013).
pubmed: 22382760
doi: 10.1007/s11357-012-9388-8
Li, X. et al. Hydrogen sulfide ameliorates cognitive dysfunction in formaldehyde-exposed rats: involvement in the upregulation of brain-derived neurotrophic factor. Neuropsychobiology 79, 119–130 (2020).
pubmed: 31550727
doi: 10.1159/000501294
Li, Y. et al. Effects of formaldehyde exposure on anxiety-like and depression-like behavior, cognition, central levels of glucocorticoid receptor and tyrosine hydroxylase in mice. Chemosphere 144, 2004–2012 (2016).
pubmed: 26551198
doi: 10.1016/j.chemosphere.2015.10.102
Yue, X. et al. New insight into Alzheimer’s disease: light reverses Aβ-obstructed interstitial fluid flow and ameliorates memory decline in APP/PS1 mice.Alzheimers Dement. 5, 671–684 (2019).
Malek, F. A., Möritz, K. U. & Fanghänel, J. Formaldehyde inhalation & open field behaviour in rats. Indian J. Med. Res. 118, 90–96 (2003).
pubmed: 14680205
Sekeres, M. J., Winocur, G. & Moscovitch, M. The hippocampus and related neocortical structures in memory transformation. Neurosci. Lett. 680, 39–53 (2018).
pubmed: 29733974
doi: 10.1016/j.neulet.2018.05.006
Sarkar, P. et al. Proteomic analysis of mice hippocampus in simulated microgravity environment. J. Proteome Res. 5, 548–553 (2006).
pubmed: 16512669
pmcid: 2748658
doi: 10.1021/pr050274r
Santucci, D. et al. Evaluation of gene, protein and neurotrophin expression in the brain of mice exposed to space environment for 91 days. PLoS ONE 7, e40112 (2012).
pubmed: 22808101
pmcid: 3392276
doi: 10.1371/journal.pone.0040112
Leal, G., Comprido, D. & Duarte, C. B. BDNF-induced local protein synthesis and synaptic plasticity. Neuropharmacology 76, 639–656 (2014). Pt C.
pubmed: 23602987
doi: 10.1016/j.neuropharm.2013.04.005
Alonso, M. et al. BDNF-triggered events in the rat hippocampus are required for both short- and long-term memory formation. Hippocampus 12, 551–560 (2002).
pubmed: 12201640
doi: 10.1002/hipo.10035
Radecki, D. T., Brown, L. M., Martinez, J. & Teyler, T. J. BDNF protects against stress-induced impairments in spatial learning and memory and LTP. Hippocampus 15, 246–253 (2005).
pubmed: 15476265
doi: 10.1002/hipo.20048
Gao, Y. et al. Early changes to the extracellular space in the hippocampus under simulated microgravity conditions. Sci. China Life Sci. 65, 604–617 (2022).
pubmed: 34185240
doi: 10.1007/s11427-021-1932-3
Sun, X. Q., Xu, Z. P., Zhang, S., Cao, X. S. & Liu, T. S. Simulated weightlessness aggravates hypergravity-induced impairment of learning and memory and neuronal apoptosis in rats. Behav. Brain Res. 199, 197–202 (2009).
pubmed: 19100783
doi: 10.1016/j.bbr.2008.11.035
Ranjan, A., Behari, J. & Mallick, B. N. Cytomorphometric changes in hippocampal CA1 neurons exposed to simulated microgravity using rats as model. Front. Neurol. 5, 77 (2014).
pubmed: 24904521
pmcid: 4032998
doi: 10.3389/fneur.2014.00077
Wang, Y. et al. Effects of simulated microgravity on the expression of presynaptic proteins distorting the GABA/glutamate equilibrium–A proteomics approach. Proteomics 15, 3883–3891 (2015).
pubmed: 26359799
doi: 10.1002/pmic.201500302
Takamatsu, Y. et al. Protection against neurodegenerative disease on Earth and in space. NPJ Microgravity 2, 16013 (2016).
pubmed: 28725728
pmcid: 5515513
doi: 10.1038/npjmgrav.2016.13
Heck, H. D., White, E. L. & Casanova-Schmitz, M. Determination of formaldehyde in biological tissues by gas chromatography/mass spectrometry. Biomed. Mass Spectrom. 9, 347–353 (1982).
pubmed: 7126766
doi: 10.1002/bms.1200090808
Tong, Z. Q. et al. Urine formaldehyde level is inversely correlated to mini mental state examination scores in senile dementia. Neurobiol. Aging 32, 31–42, (2011).
pubmed: 19879019
doi: 10.1016/j.neurobiolaging.2009.07.013
Lee, C. H. & Gouaux, E. Amino terminal domains of the NMDA receptor are organized as local heterodimers. PLoS ONE 6, e19180 (2011).
pubmed: 21544205
pmcid: 3081335
doi: 10.1371/journal.pone.0019180
Karakas, E. & Furukawa, H. Crystal structure of a heterotetrameric NMDA receptor ion channel. Science 344, 992–997 (2014).
pubmed: 24876489
pmcid: 4113085
doi: 10.1126/science.1251915
Metz, B. et al. Identification of formaldehyde-induced modifications in proteins: reactions with insulin. Bioconjug. Chem. 17, 815–822 (2006).
pubmed: 16704222
doi: 10.1021/bc050340f
Toews, J., Rogalski, J. C., Clark, T. J. & Kast, J. Mass spectrometric identification of formaldehyde-induced peptide modifications under in vivo protein cross-linking conditions. Anal. Chim. Acta 618, 168–183 (2008).
pubmed: 18513538
doi: 10.1016/j.aca.2008.04.049
Ly, V., Velichala, S. R. & Hargens, A. R. Cardiovascular, lymphatic, and ocular health in space. Life 12, https://doi.org/10.3390/life12020268 (2022).
Carriot, J., Mackrous, I. & Cullen, K. E. Challenges to the vestibular system in space: how the brain responds and adapts to microgravity. Front. Neural Circuits 15, 760313 (2021).
pubmed: 34803615
pmcid: 8595211
doi: 10.3389/fncir.2021.760313
Koppelmans, V. et al. Brain plasticity and sensorimotor deterioration as a function of 70 days head down tilt bed rest. PLoS ONE 12, e0182236 (2017).
pubmed: 28767698
pmcid: 5540603
doi: 10.1371/journal.pone.0182236
Koppelmans, V., Bloomberg, J. J., Mulavara, A. P. & Seidler, R. D. Brain structural plasticity with spaceflight. NPJ Microgravity 2, 2 (2016).
pubmed: 28649622
pmcid: 5460234
doi: 10.1038/s41526-016-0001-9
Juhl, O. J. T. et al. Update on the effects of microgravity on the musculoskeletal system. NPJ Microgravity 7, 28 (2021).
pubmed: 34301942
pmcid: 8302614
doi: 10.1038/s41526-021-00158-4
Ishihara, A. et al. Comparison of the response of motoneurons innervating perineal and hind limb muscles to spaceflight and recovery. Muscle Nerve 23, 753–762 (2000).
pubmed: 10797399
doi: 10.1002/(SICI)1097-4598(200005)23:5<753::AID-MUS13>3.0.CO;2-J
Tajino, J. et al. Discordance in recovery between altered locomotion and muscle atrophy induced by simulated microgravity in rats. J. Mot. Behav. 47, 397–406 (2015).
pubmed: 25789843
doi: 10.1080/00222895.2014.1003779
Holstein, G. R., Kukielka, E. & Martinelli, G. P. Anatomical observations of the rat cerebellar nodulus after 24 h of spaceflight. J. Gravit. Physiol. 6, P47–P50 (1999).
pubmed: 11543023
Reschke, M. F. & Clément, G. Vestibular and sensorimotor dysfunction during space flight. Curr. Pathobiol. Rep. 6, 177–183 (2018).
doi: 10.1007/s40139-018-0173-y
Macaulay, T. R. et al. Developing proprioceptive countermeasures to mitigate postural and locomotor control deficits after long-duration spaceflight. Front. Syst. Neurosci. 15, 658985 (2021).
pubmed: 33986648
pmcid: 8111171
doi: 10.3389/fnsys.2021.658985
Salazar, A. P. et al. Neural working memory changes during a spaceflight analog with elevated carbon dioxide: a pilot study. Front. Syst. Neurosci. 14, 48 (2020).
pubmed: 32848641
pmcid: 7399639
doi: 10.3389/fnsys.2020.00048
Roberts, D. R. et al. Structural brain changes following long-term 6° head-down tilt bed rest as an analog for spaceflight. Am. J. Neuroradiol. 36, 2048–2054 (2015).
pubmed: 26185326
pmcid: 7964872
doi: 10.3174/ajnr.A4406
Lemberskiy, G. et al. Characterization of prostate microstructure using water diffusion and NMR relaxation. Front. Phys. 6, https://doi.org/10.3389/fphy.2018.00091 (2018).
Thach, W. T., Goodkin, H. P. & Keating, J. G. The cerebellum and the adaptive coordination of movement. Annu. Rev. Neurosci. 15, 403–442 (1992).
pubmed: 1575449
doi: 10.1146/annurev.ne.15.030192.002155
Marsden, J. F. Cerebellar ataxia. Handb. Clin. Neurol. 159, 261–281 (2018).
pubmed: 30482319
doi: 10.1016/B978-0-444-63916-5.00017-3
Glasauer, S. et al. Spatial orientation during locomotion [correction of locomation] following space flight. Acta Astronaut. 36, 423–431 (1995).
pubmed: 11540973
doi: 10.1016/0094-5765(95)00127-1
Layne, C. S., McDonald, P. V. & Bloomberg, J. J. Neuromuscular activation patterns during treadmill walking after space flight. Exp. Brain Res. 113, 104–116 (1997).
pubmed: 9028779
doi: 10.1007/BF02454146
Layne, C. S. et al. Adaptation of neuromuscular activation patterns during treadmill walking after long-duration space flight. Acta Astronaut. 43, 107–119 (1998).
pubmed: 11541918
doi: 10.1016/S0094-5765(98)00148-9
Kozlovskaya, I. B., Grigoriev, A. I. & Stepantzov, V. I. Countermeasure of the negative effects of weightlessness on physical systems in long-term space flights. Acta Astronaut. 36, 661–668 (1995).
pubmed: 11541002
doi: 10.1016/0094-5765(95)00156-5
Van Ombergen, A. et al. The effect of spaceflight and microgravity on the human brain. J. Neurol. 264, 18–22 (2017).
pubmed: 28271409
pmcid: 5610662
doi: 10.1007/s00415-017-8427-x
Cebolla, A. M. et al. Cerebellar contribution to visuo-attentional alpha rhythm: insights from weightlessness. Sci. Rep. 6, 37824 (2016).
pubmed: 27883068
pmcid: 5121637
doi: 10.1038/srep37824
Lee, J. K. et al. Spaceflight-associated brain white matter microstructural changes and intracranial fluid redistribution. JAMA Neurol. 76, 412–419, (2019).
pubmed: 30673793
pmcid: 6459132
doi: 10.1001/jamaneurol.2018.4882
Demertzi, A. et al. Cortical reorganization in an astronaut’s brain after long-duration spaceflight. Brain Struct. Funct. 221, 2873–2876 (2016).
pubmed: 25963710
doi: 10.1007/s00429-015-1054-3
Van Ombergen, A. et al. Brain tissue-volume changes in cosmonauts. N. Engl. J. Med. 379, 1678–1680 (2018).
pubmed: 30354959
doi: 10.1056/NEJMc1809011
Nguyen, H. P., Tran, P. H., Kim, K. S. & Yang, S. G. The effects of real and simulated microgravity on cellular mitochondrial function. NPJ Microgravity 7, 44 (2021).
pubmed: 34750383
pmcid: 8575887
doi: 10.1038/s41526-021-00171-7
Chen, H. L. et al. Simulated microgravity-induced oxidative stress in different areas of rat brain. Sheng Li Xue Bao 61, 108–114 (2009).
pubmed: 19377820
Krasnov, I. B. & Krasnikov, G. V. Purkinje’s cells in the vestibular and proprioceptive segments of rat’s cerebellum following 14-day space flight. Aviakosm Ekol. Med. 43, 43–47 (2009).
Qu, L., Yang, T., Yuan, Y., Zhong, P. & Li, Y. Protein nitration increased by simulated weightlessness and decreased by melatonin and quercetin in PC12 cells. Nitric Oxide 15, 58–63 (2006).
pubmed: 16881142
doi: 10.1016/j.niox.2005.12.006
Carpo, N., Tran, V., Biancotti, J. C., Cepeda, C. & Espinosa-Jeffrey, A. Space flight enhances stress pathways in human neural stem cells. Biomolecules 14, https://doi.org/10.3390/biom14010065 (2024).
Tao, R. et al. In situ imaging of formaldehyde in live mice with high spatiotemporal resolution reveals aldehyde dehydrogenase-2 as a potential target for Alzheimer’s disease treatment. Anal. Chem. 94, 1308–1317 (2022).
pubmed: 34962779
doi: 10.1021/acs.analchem.1c04520
Bi, L. et al. Ultrastructural changes in cerebral cortex and cerebellar cortex of rats under simulated weightlessness. Space Med. Med. Eng. 17, 180–183 (2004).
Sutherland, B. W., Toews, J. & Kast, J. Utility of formaldehyde cross-linking and mass spectrometry in the study of protein-protein interactions. J. Mass Spectrom. 43, 699–715 (2008).
pubmed: 18438963
doi: 10.1002/jms.1415
Bolt, H. M. Experimental toxicology of formaldehyde. J. Cancer Res. Clin. Oncol. 113, 305–309 (1987).
pubmed: 3298280
doi: 10.1007/BF00397713
Häder, D. P., Braun, M., Grimm, D. & Hemmersbach, R. Gravireceptors in eukaryotes-a comparison of case studies on the cellular level. NPJ Microgravity 3, 13 (2017).
pubmed: 28649635
pmcid: 5460273
doi: 10.1038/s41526-017-0018-8
Grimm, D. et al. The fight against cancer by microgravity: the multicellular spheroid as a metastasis model. Int. J. Mol. Sci. 23, https://doi.org/10.3390/ijms23063073 (2022).
Infanger, M. et al. Simulated weightlessness changes the cytoskeleton and extracellular matrix proteins in papillary thyroid carcinoma cells. Cell Tissue Res. 324, 267–277 (2006).
pubmed: 16432709
doi: 10.1007/s00441-005-0142-8
Abe, M., Takahashi, M., Horiuchi, K. & Nagano, A. The changes in crosslink contents in tissues after formalin fixation. Anal. Biochem. 318, 118–123 (2003).
pubmed: 12782039
doi: 10.1016/S0003-2697(03)00194-5
Andreeva, N. V. & Belyavsky, A. V. Formaldehyde fixation of extracellular matrix protein layers for enhanced primary cell growth. Bio Protoc. 7, e2374 (2017).
pubmed: 34541115
pmcid: 8413507
doi: 10.21769/BioProtoc.2374
Zhang, Y. et al. The cellular function and molecular mechanism of formaldehyde in cardiovascular disease and heart development. J. Cell Mol. Med. 25, 5358–5371 (2021).
pubmed: 33973354
pmcid: 8184665
doi: 10.1111/jcmm.16602
Metz, B. et al. Identification of formaldehyde-induced modifications in proteins: reactions with model peptides. J. Biol. Chem. 279, 6235–6243 (2004).
pubmed: 14638685
doi: 10.1074/jbc.M310752200
Gubisne-Haberle, D., Hill, W., Kazachkov, M., Richardson, J. S. & Yu, P. H. Protein cross-linkage induced by formaldehyde derived from semicarbazide-sensitive amine oxidase-mediated deamination of methylamine. J. Pharm. Exp. Ther. 310, 1125–1132 (2004).
doi: 10.1124/jpet.104.068601
Fei, X. et al. Degradation of FA reduces Aβ neurotoxicity and Alzheimer-related phenotypes. Mol. Psychiatry 26, 5578–5591 (2021).
pubmed: 33328587
doi: 10.1038/s41380-020-00929-7
Kang, J. E. et al. Amyloid-beta dynamics are regulated by orexin and the sleep-wake cycle. Science 326, 1005–1007 (2009).
pubmed: 19779148
pmcid: 2789838
doi: 10.1126/science.1180962
Taguchi, K., Okamoto, Y., Matsumoto, K., Otagiri, M. & Chuang, V. T. G. When albumin meets liposomes: a feasible drug carrier for biomedical applications. Pharmaceuticals 14, https://doi.org/10.3390/ph14040296 (2021).
Malka, R., Delgado, F. F., Manalis, S. R. & Higgins, J. M. In vivo volume and hemoglobin dynamics of human red blood cells. PLoS Comput. Biol. 10, e1003839 (2014).
pubmed: 25299941
pmcid: 4191880
doi: 10.1371/journal.pcbi.1003839
Bellone, J. A., Gifford, P. S., Nishiyama, N. C., Hartman, R. E. & Mao, X. W. Long-term effects of simulated microgravity and/or chronic exposure to low-dose gamma radiation on behavior and blood-brain barrier integrity. NPJ Microgravity 2, 16019 (2016).
pubmed: 28725731
pmcid: 5516431
doi: 10.1038/npjmgrav.2016.19
Soeters, P. B., Wolfe, R. R. & Shenkin, A. Hypoalbuminemia: pathogenesis and clinical significance. J. Parenter. Enter. Nutr. 43, 181–193 (2019).
doi: 10.1002/jpen.1451
Rifkind, J. M., Mohanty, J. G. & Nagababu, E. The pathophysiology of extracellular hemoglobin associated with enhanced oxidative reactions. Front. Physiol. 5, 500 (2014).
pubmed: 25642190
Liu, Y., Liu, R., Mou, Y. & Zhou, G. Spectroscopic identification of interactions of formaldehyde with bovine serum albumin. J. Biochem. Mol. Toxicol. 25, 95–100 (2011).
pubmed: 20957681
doi: 10.1002/jbt.20364
Hoberman, H. D. & George, San R. C. Reaction of tobacco smoke aldehydes with human hemoglobin. J. Biochem. Toxicol. 3, 105–119 (1988).
pubmed: 3236330
doi: 10.1002/jbt.2570030205
Stolzing, A. & Grune, T. Neuronal apoptotic bodies: phagocytosis and degradation by primary microglial cells. FASEB J. 18, 743–745 (2004).
pubmed: 14766802
doi: 10.1096/fj.03-0374fje
Stolzing, A., Widmer, R., Jung, T., Voss, P. & Grune, T. Degradation of glycated bovine serum albumin in microglial cells. Free Radic. Biol. Med. 40, 1017–1027 (2006).
pubmed: 16540397
doi: 10.1016/j.freeradbiomed.2005.10.061
Lee, R. C., Feinbaum, R. L. & Ambros, V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75, 843–854 (1993).
pubmed: 8252621
doi: 10.1016/0092-8674(93)90529-Y
Saliminejad, K., Khorram Khorshid, H. R., Soleymani Fard, S. & Ghaffari, S. H. An overview of microRNAs: biology, functions, therapeutics, and analysis methods. J. Cell Physiol. 234, 5451–5465 (2019).
pubmed: 30471116
doi: 10.1002/jcp.27486
Lu, T. X. & Rothenberg, M. E. MicroRNA. J. Allergy Clin. Immunol. 141, 1202–1207 (2018).
pubmed: 29074454
doi: 10.1016/j.jaci.2017.08.034
Anfossi, S., Babayan, A., Pantel, K. & Calin, G. A. Clinical utility of circulating non-coding RNAs—an update. Nat. Rev. Clin. Oncol. 15, 541–563 (2018).
pubmed: 29784926
doi: 10.1038/s41571-018-0035-x
Chen, L. et al. Trends in the development of miRNA bioinformatics tools. Brief. Bioinform. 20, 1836–1852 (2019).
pubmed: 29982332
pmcid: 7414524
doi: 10.1093/bib/bby054
Lewis, B. P., Burge, C. B. & Bartel, D. P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15–20 (2005).
pubmed: 15652477
doi: 10.1016/j.cell.2004.12.035
Tétreault, N. & De Guire, V. miRNAs: their discovery, biogenesis and mechanism of action. Clin. Biochem. 46, 842–845 (2013).
pubmed: 23454500
doi: 10.1016/j.clinbiochem.2013.02.009
Basak, I., Patil, K. S., Alves, G., Larsen, J. P. & Møller, S. G. microRNAs as neuroregulators, biomarkers and therapeutic agents in neurodegenerative diseases. Cell Mol. Life Sci. 73, 811–827 (2016).
pubmed: 26608596
doi: 10.1007/s00018-015-2093-x
Danborg, P. B., Simonsen, A. H., Waldemar, G. & Heegaard, N. H. The potential of microRNAs as biofluid markers of neurodegenerative diseases–a systematic review. Biomarkers 19, 259–268 (2014).
pubmed: 24678935
doi: 10.3109/1354750X.2014.904001
Cho, H. J. et al. MicroRNA-205 regulates the expression of Parkinson’s disease-related leucine-rich repeat kinase 2 protein. Hum. Mol. Genet. 22, 608–620 (2013).
pubmed: 23125283
doi: 10.1093/hmg/dds470
Lu, S. Y. et al. miR-218-2 regulates cognitive functions in the hippocampus through complement component 3-dependent modulation of synaptic vesicle release. Proc. Natl. Acad. Sci. USA 118, https://doi.org/10.1073/pnas.2021770118 (2021).
Li, Y. et al. MicroRNA-26a-3p rescues depression-like behaviors in male rats via preventing hippocampal neuronal anomalies. J. Clin. Investig. 131, https://doi.org/10.1172/jci148853 (2021).
Salta, E., Sierksma, A., Vanden Eynden, E. & De Strooper, B. miR-132 loss de-represses ITPKB and aggravates amyloid and TAU pathology in Alzheimer’s brain. EMBO Mol. Med. 8, 1005–1018 (2016).
pubmed: 27485122
pmcid: 5009807
doi: 10.15252/emmm.201606520
Salman, M. M. et al. Transcriptome analysis suggests a role for the differential expression of cerebral aquaporins and the MAPK signalling pathway in human temporal lobe epilepsy. Eur. J. Neurosci. 46, 2121–2132 (2017).
pubmed: 28715131
doi: 10.1111/ejn.13652
Denker, B. M., Smith, B. L., Kuhajda, F. P. & Agre, P. Identification, purification, and partial characterization of a novel Mr 28,000 integral membrane protein from erythrocytes and renal tubules. J. Biol. Chem. 263, 15634–15642 (1988).
pubmed: 3049610
doi: 10.1016/S0021-9258(19)37635-5
Badaut, J., Fukuda, A. M., Jullienne, A. & Petry, K. G. Aquaporin and brain diseases. Biochim. Biophys. Acta 1840, 1554–1565 (2014).
pubmed: 24513456
doi: 10.1016/j.bbagen.2013.10.032
MacAulay, N. & Zeuthen, T. Water transport between CNS compartments: contributions of aquaporins and cotransporters. Neuroscience 168, 941–956 (2010).
pubmed: 19761815
doi: 10.1016/j.neuroscience.2009.09.016
Silva, I., Silva, J., Ferreira, R. & Trigo, D. Glymphatic system, AQP4, and their implications in Alzheimer’s disease. Neurol Res. Pract. 3, 5 (2021).
Pirici, I. et al. Inhibition of aquaporin-4 improves the outcome of ischaemic stroke and modulates brain paravascular drainage pathways. Int. J. Mol. Sci. 19, https://doi.org/10.3390/ijms19010046 (2017).
Takano, T., Oberheim, N., Cotrina, M. L. & Nedergaard, M. Astrocytes and ischemic injury. Stroke 40, S8–S12 (2009).
pubmed: 19064795
doi: 10.1161/STROKEAHA.108.533166
Yao, X., Hrabetová, S., Nicholson, C. & Manley, G. T. Aquaporin-4-deficient mice have increased extracellular space without tortuosity change. J. Neurosci. 28, 5460–5464 (2008).
pubmed: 18495879
pmcid: 2659334
doi: 10.1523/JNEUROSCI.0257-08.2008
Jullienne, A. et al. Modulating the water channel AQP4 alters miRNA expression, astrocyte connectivity and water diffusion in the rodent brain. Sci. Rep. 8, 4186 (2018).
pubmed: 29520011
pmcid: 5843607
doi: 10.1038/s41598-018-22268-y
Wang, Y. et al. MicroRNA-29b is a therapeutic target in cerebral ischemia associated with aquaporin 4. J. Cereb. Blood Flow. Metab. 35, 1977–1984 (2015).
pubmed: 26126866
pmcid: 4671118
doi: 10.1038/jcbfm.2015.156
Sepramaniam, S., Ying, L. K., Armugam, A., Wintour, E. M. & Jeyaseelan, K. MicroRNA-130a represses transcriptional activity of aquaporin 4 M1 promoter. J. Biol. Chem. 287, 12006–12015 (2012).
pubmed: 22334710
pmcid: 3320947
doi: 10.1074/jbc.M111.280701
Zheng, Y. et al. Upregulation of miR-130b protects against cerebral ischemic injury by targeting water channel protein aquaporin 4 (AQP4). Am. J. Transl. Res. 9, 3452–3461 (2017).
pubmed: 28804561
pmcid: 5527259
Sepramaniam, S. et al. MicroRNA 320a functions as a novel endogenous modulator of aquaporins 1 and 4 as well as a potential therapeutic target in cerebral ischemia. J. Biol. Chem. 285, 29223–29230 (2010).
pubmed: 20628061
pmcid: 2937953
doi: 10.1074/jbc.M110.144576
Vandebroek, A. & Yasui, M. Regulation of AQP4 in the central nervous system. Int. J. Mol. Sci. 21, https://doi.org/10.3390/ijms21051603 (2020).
Kobayashi, M. et al. AGO CLIP reveals an activated network for acute regulation of brain glutamate homeostasis in ischemic stroke. Cell Rep. 28, 979–991.e976 (2019).
pubmed: 31340158
pmcid: 6784548
doi: 10.1016/j.celrep.2019.06.075
Zhong, Y. et al. MicroRNA-29b-3p aggravates 1,2-dichloroethane-induced brain edema by targeting aquaporin 4 in Sprague-Dawley rats and CD-1 mice. Toxicol. Lett. 319, 160–167 (2020).
pubmed: 31734271
doi: 10.1016/j.toxlet.2019.11.011
Zheng, L. et al. Overexpression of MicroRNA-145 ameliorates astrocyte injury by targeting aquaporin 4 in cerebral ischemic stroke. Biomed. Res. Int. 2017, 9530951 (2017).
pubmed: 29057271
pmcid: 5615955
doi: 10.1155/2017/9530951
Chen, Z. et al. microRNA-320a prevent Müller cells from hypoxia injury by targeting aquaporin-4. J. Cell Biochem. 121, 4711–4723 (2020).
pubmed: 32830348
doi: 10.1002/jcb.29524
Mao, X. W. et al. Spaceflight induces oxidative damage to blood-brain barrier integrity in a mouse model. FASEB J. 34, 15516–15530 (2020).
pubmed: 32981077
doi: 10.1096/fj.202001754R
Lackner, J. R. & DiZio, P. Human orientation and movement control in weightless and artificial gravity environments. Exp. Brain Res. 130, 2–26 (2000).
pubmed: 10638437
doi: 10.1007/s002210050002
Savitsky, K. et al. A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science 268, 1749–1753 (1995).
pubmed: 7792600
doi: 10.1126/science.7792600
Gatti, R. A. et al. Localization of an ataxia-telangiectasia gene to chromosome 11q22-23. Nature 336, 577–580 (1988).
pubmed: 3200306
doi: 10.1038/336577a0
Phan, L. M. & Rezaeian, A. H. ATM: main features, signaling pathways, and its diverse roles in DNA damage response, tumor suppression, and cancer development. Genes 12, https://doi.org/10.3390/genes12060845 (2021).
Tan, S. L. W. et al. A class of environmental and endogenous toxins induces BRCA2 haploinsufficiency and genome instability. Cell 169, 1105–1118.e1115 (2017).
pubmed: 28575672
pmcid: 5457488
doi: 10.1016/j.cell.2017.05.010
Ortega-Atienza, S., Wong, V. C., DeLoughery, Z., Luczak, M. W. & Zhitkovich, A. ATM and KAT5 safeguard replicating chromatin against formaldehyde damage. Nucleic Acids Res. 44, 198–209 (2016).
pubmed: 26420831
doi: 10.1093/nar/gkv957
Ditch, S. & Paull, T. T. The ATM protein kinase and cellular redox signaling: beyond the DNA damage response. Trends Biochem. Sci. 37, 15–22 (2012).
pubmed: 22079189
doi: 10.1016/j.tibs.2011.10.002
Kuang, X. et al. Activation of AMP-activated protein kinase in cerebella of Atm-/- mice is attributable to accumulation of reactive oxygen species. Biochem. Biophys. Res. Commun. 418, 267–272 (2012).
pubmed: 22260947
pmcid: 4109361
doi: 10.1016/j.bbrc.2012.01.008
Kim, T. S. et al. The ZFHX3 (ATBF1) transcription factor induces PDGFRB, which activates ATM in the cytoplasm to protect cerebellar neurons from oxidative stress. Dis. Model. Mech. 3, 752–762 (2010).
pubmed: 20876357
doi: 10.1242/dmm.004689
Kamsler, A. et al. Increased oxidative stress in ataxia telangiectasia evidenced by alterations in redox state of brains from Atm-deficient mice. Cancer Res. 61, 1849–1854 (2001).
pubmed: 11280737
Barlow, C. et al. ATM is a cytoplasmic protein in mouse brain required to prevent lysosomal accumulation. Proc. Natl. Acad. Sci. USA 97, 871–876 (2000).
pubmed: 10639172
pmcid: 15423
doi: 10.1073/pnas.97.2.871
Dar, I., Biton, S., Shiloh, Y. & Barzilai, A. Analysis of the ataxia telangiectasia mutated-mediated DNA damage response in murine cerebellar neurons. J. Neurosci. 26, 7767–7774 (2006).
pubmed: 16855104
pmcid: 6674276
doi: 10.1523/JNEUROSCI.2055-06.2006
Chang, J. H. et al. MicroRNA-203 modulates the radiation sensitivity of human malignant glioma cells. Int. J. Radiat. Oncol. Biol. Phys. 94, 412–420 (2016).
pubmed: 26678661
doi: 10.1016/j.ijrobp.2015.10.001
Abbott, N. J., Patabendige, A. A., Dolman, D. E., Yusof, S. R. & Begley, D. J. Structure and function of the blood-brain barrier. Neurobiol. Dis. 37, 13–25 (2010).
pubmed: 19664713
doi: 10.1016/j.nbd.2009.07.030
Ho, P. T. B., Clark, I. M. & Le, L. T. T. MicroRNA-based diagnosis and therapy. Int. J. Mol. Sci. 23, https://doi.org/10.3390/ijms23137167 (2022).