Erucin, a Natural Isothiocyanate, Prevents Polyglutamine-Induced Toxicity in Caenorhabditis elegans via aak-2/AMPK and daf-16/FOXO Signaling
Several neurodegenerative diseases (NDDs), such as Huntington’s disease, six of the spinocerebellar ataxias, dentatorubral-pallidoluysian atrophy, and spinobulbar muscular atrophy, are caused by abnormally long polyglutamine (polyQ) tracts. Natural compounds capable of alleviating polyQ-induced toxi...
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| Vydáno v: | International journal of molecular sciences Ročník 25; číslo 22; s. 12220 |
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14.11.2024
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| Abstract | Several neurodegenerative diseases (NDDs), such as Huntington’s disease, six of the spinocerebellar ataxias, dentatorubral-pallidoluysian atrophy, and spinobulbar muscular atrophy, are caused by abnormally long polyglutamine (polyQ) tracts. Natural compounds capable of alleviating polyQ-induced toxicity are currently of great interest. In this work, we investigated the modulatory effect against polyQ neurotoxic aggregates exerted by erucin (ERN), an isothiocyanate naturally present in its precursor glucoerucin in rocket salad leaves and in its oxidized form, sulforaphane (SFN), in broccoli. Using C. elegans models expressing polyQ in different tissues, we demonstrated that ERN protects against polyQ-induced toxicity and that its action depends on the catalytic subunit of AMP-activated protein kinase (aak-2/AMPKα2) and, downstream in this pathway, on the daf-16/FOXO transcription factor, since nematodes deficient in aak-2/AMPKα2 and daf-16 did not respond to the treatment, respectively. Although triggered by a different source of neurotoxicity than polyQ diseases, i.e., by α-synuclein (α-syn) aggregates, Parkinson’s disease (PD) was also considered in our study. Our results showed that ERN reduces α-syn aggregates and slightly improves the motility of worms. Therefore, further preclinical studies in mouse models of protein aggregation are justified and could provide insights into testing whether ERN could be a potential neuroprotective compound in humans. |
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| AbstractList | Several neurodegenerative diseases (NDDs), such as Huntington's disease, six of the spinocerebellar ataxias, dentatorubral-pallidoluysian atrophy, and spinobulbar muscular atrophy, are caused by abnormally long polyglutamine (polyQ) tracts. Natural compounds capable of alleviating polyQ-induced toxicity are currently of great interest. In this work, we investigated the modulatory effect against polyQ neurotoxic aggregates exerted by erucin (ERN), an isothiocyanate naturally present in its precursor glucoerucin in rocket salad leaves and in its oxidized form, sulforaphane (SFN), in broccoli. Using C. elegans models expressing polyQ in different tissues, we demonstrated that ERN protects against polyQ-induced toxicity and that its action depends on the catalytic subunit of AMP-activated protein kinase (aak-2/AMPKα2) and, downstream in this pathway, on the daf-16/FOXO transcription factor, since nematodes deficient in aak-2/AMPKα2 and daf-16 did not respond to the treatment, respectively. Although triggered by a different source of neurotoxicity than polyQ diseases, i.e., by α-synuclein (α-syn) aggregates, Parkinson's disease (PD) was also considered in our study. Our results showed that ERN reduces α-syn aggregates and slightly improves the motility of worms. Therefore, further preclinical studies in mouse models of protein aggregation are justified and could provide insights into testing whether ERN could be a potential neuroprotective compound in humans.Several neurodegenerative diseases (NDDs), such as Huntington's disease, six of the spinocerebellar ataxias, dentatorubral-pallidoluysian atrophy, and spinobulbar muscular atrophy, are caused by abnormally long polyglutamine (polyQ) tracts. Natural compounds capable of alleviating polyQ-induced toxicity are currently of great interest. In this work, we investigated the modulatory effect against polyQ neurotoxic aggregates exerted by erucin (ERN), an isothiocyanate naturally present in its precursor glucoerucin in rocket salad leaves and in its oxidized form, sulforaphane (SFN), in broccoli. Using C. elegans models expressing polyQ in different tissues, we demonstrated that ERN protects against polyQ-induced toxicity and that its action depends on the catalytic subunit of AMP-activated protein kinase (aak-2/AMPKα2) and, downstream in this pathway, on the daf-16/FOXO transcription factor, since nematodes deficient in aak-2/AMPKα2 and daf-16 did not respond to the treatment, respectively. Although triggered by a different source of neurotoxicity than polyQ diseases, i.e., by α-synuclein (α-syn) aggregates, Parkinson's disease (PD) was also considered in our study. Our results showed that ERN reduces α-syn aggregates and slightly improves the motility of worms. Therefore, further preclinical studies in mouse models of protein aggregation are justified and could provide insights into testing whether ERN could be a potential neuroprotective compound in humans. Several neurodegenerative diseases (NDDs), such as Huntington’s disease, six of the spinocerebellar ataxias, dentatorubral-pallidoluysian atrophy, and spinobulbar muscular atrophy, are caused by abnormally long polyglutamine (polyQ) tracts. Natural compounds capable of alleviating polyQ-induced toxicity are currently of great interest. In this work, we investigated the modulatory effect against polyQ neurotoxic aggregates exerted by erucin (ERN), an isothiocyanate naturally present in its precursor glucoerucin in rocket salad leaves and in its oxidized form, sulforaphane (SFN), in broccoli. Using C. elegans models expressing polyQ in different tissues, we demonstrated that ERN protects against polyQ-induced toxicity and that its action depends on the catalytic subunit of AMP-activated protein kinase (aak-2 /AMPKα2) and, downstream in this pathway, on the daf-16 /FOXO transcription factor, since nematodes deficient in aak-2 /AMPKα2 and daf-16 did not respond to the treatment, respectively. Although triggered by a different source of neurotoxicity than polyQ diseases, i.e., by α-synuclein (α-syn) aggregates, Parkinson’s disease (PD) was also considered in our study. Our results showed that ERN reduces α-syn aggregates and slightly improves the motility of worms. Therefore, further preclinical studies in mouse models of protein aggregation are justified and could provide insights into testing whether ERN could be a potential neuroprotective compound in humans. Several neurodegenerative diseases (NDDs), such as Huntington's disease, six of the spinocerebellar ataxias, dentatorubral-pallidoluysian atrophy, and spinobulbar muscular atrophy, are caused by abnormally long polyglutamine (polyQ) tracts. Natural compounds capable of alleviating polyQ-induced toxicity are currently of great interest. In this work, we investigated the modulatory effect against polyQ neurotoxic aggregates exerted by erucin (ERN), an isothiocyanate naturally present in its precursor glucoerucin in rocket salad leaves and in its oxidized form, sulforaphane (SFN), in broccoli. Using models expressing polyQ in different tissues, we demonstrated that ERN protects against polyQ-induced toxicity and that its action depends on the catalytic subunit of AMP-activated protein kinase ( /AMPKα2) and, downstream in this pathway, on the /FOXO transcription factor, since nematodes deficient in /AMPKα2 and did not respond to the treatment, respectively. Although triggered by a different source of neurotoxicity than polyQ diseases, i.e., by α-synuclein (α-syn) aggregates, Parkinson's disease (PD) was also considered in our study. Our results showed that ERN reduces α-syn aggregates and slightly improves the motility of worms. Therefore, further preclinical studies in mouse models of protein aggregation are justified and could provide insights into testing whether ERN could be a potential neuroprotective compound in humans. |
| Audience | Academic |
| Author | Balducci, Martina Pérez, Mar Collado Tarozzi, Andrea Pérez, Julia Tortajada del Río, Cristina Trujillo Carranza, Andrea del Valle Gomez Escribano, Ana Pilar Vázquez-Manrique, Rafael P. |
| AuthorAffiliation | 3 Joint Unit for Rare Diseases IIS La Fe-CIPF, 46012 Valencia, Spain 2 Laboratory of Molecular, Cellular and Genomic Biomedicine, Instituto de Investigación Sanitaria La Fe, 46012 Valencia, Spain; julia_tortajada@iislafe.es (J.T.P.); cristina_trujillo@iislafe.es (C.T.d.R.); mar_collado@iislafe.es (M.C.P.); andrea_carranza@iislafe.es (A.d.V.C.); ana_pilar_gomez@iislafe.es (A.P.G.E.); rafael_vazquez@iislafe.es (R.P.V.-M.) 4 Centro de Investigación Biomédica en Red (CIBER), 28029 Madrid, Spain 1 Department for Life Quality Studies, University of Bologna, 47921 Rimini, Italy 5 Biostructures and Biosystems National Institute (INBB), 00136 Rome, Italy |
| AuthorAffiliation_xml | – name: 3 Joint Unit for Rare Diseases IIS La Fe-CIPF, 46012 Valencia, Spain – name: 2 Laboratory of Molecular, Cellular and Genomic Biomedicine, Instituto de Investigación Sanitaria La Fe, 46012 Valencia, Spain; julia_tortajada@iislafe.es (J.T.P.); cristina_trujillo@iislafe.es (C.T.d.R.); mar_collado@iislafe.es (M.C.P.); andrea_carranza@iislafe.es (A.d.V.C.); ana_pilar_gomez@iislafe.es (A.P.G.E.); rafael_vazquez@iislafe.es (R.P.V.-M.) – name: 4 Centro de Investigación Biomédica en Red (CIBER), 28029 Madrid, Spain – name: 1 Department for Life Quality Studies, University of Bologna, 47921 Rimini, Italy – name: 5 Biostructures and Biosystems National Institute (INBB), 00136 Rome, Italy |
| Author_xml | – sequence: 1 givenname: Martina orcidid: 0000-0002-9657-6340 surname: Balducci fullname: Balducci, Martina – sequence: 2 givenname: Julia Tortajada surname: Pérez fullname: Pérez, Julia Tortajada – sequence: 3 givenname: Cristina Trujillo surname: del Río fullname: del Río, Cristina Trujillo – sequence: 4 givenname: Mar Collado surname: Pérez fullname: Pérez, Mar Collado – sequence: 5 givenname: Andrea del Valle orcidid: 0000-0003-2823-2869 surname: Carranza fullname: Carranza, Andrea del Valle – sequence: 6 givenname: Ana Pilar orcidid: 0000-0003-4391-5932 surname: Gomez Escribano fullname: Gomez Escribano, Ana Pilar – sequence: 7 givenname: Rafael P. orcidid: 0000-0002-1594-0033 surname: Vázquez-Manrique fullname: Vázquez-Manrique, Rafael P. – sequence: 8 givenname: Andrea orcidid: 0000-0001-7983-8575 surname: Tarozzi fullname: Tarozzi, Andrea |
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| Cites_doi | 10.1016/S0962-8924(00)01852-3 10.1016/j.ydbio.2021.01.015 10.1021/acschemneuro.4c00184 10.1016/bs.mcb.2024.03.004 10.1016/j.nbd.2021.105560 10.1038/s12276-019-0264-9 10.1016/j.jnutbio.2015.01.004 10.18632/aging.202512 10.3390/toxins2040593 10.1093/hmg/ddv513 10.1016/j.crfs.2022.05.001 10.1242/dmm.046110 10.3390/nu10050580 10.1895/wormbook.1.101.1 10.1136/jnnp-2016-314597.267 10.1093/hmg/ddw073 10.1073/pnas.231476398 10.1016/j.fitote.2015.08.001 10.1038/srep42717 10.1073/pnas.100107297 10.1007/s11095-011-0500-z 10.1016/j.phrs.2011.07.005 10.3390/ijms130910899 10.1016/j.jnutbio.2022.109017 10.1016/j.ejmech.2019.111745 10.1523/JNEUROSCI.0277-12.2012 10.3390/ijms232415593 10.1016/j.phrs.2020.105105 10.1101/gad.1255404 10.1002/mnfr.201400104 10.1111/jnc.12647 10.1371/journal.pgen.1000027 10.1007/s11064-006-9203-y 10.1016/B978-0-444-63233-3.00009-9 10.1016/j.ejogrb.2022.07.006 10.15252/embr.202255556 10.1007/s11011-022-01087-1 10.1007/s12035-024-04206-4 10.1002/mnfr.201200225 10.1146/annurev-pathmechdis-012418-012857 10.3390/biom13030478 10.1038/srep24399 10.1080/07924259.2014.940470 10.1021/acs.jafc.7b04641 |
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| Keywords | Caenorhabditis elegans AMPK erucin neuroprotection polyQ toxicity daf-16/FOXO |
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| SubjectTerms | Aggregates AMP-Activated Protein Kinases - metabolism Animals Caenorhabditis elegans - drug effects Caenorhabditis elegans - metabolism Caenorhabditis elegans Proteins - genetics Caenorhabditis elegans Proteins - metabolism Cyclic adenylic acid Degeneration Disease prevention Forkhead Transcription Factors - genetics Forkhead Transcription Factors - metabolism Genomes Glutamine Health aspects Human subjects Huntingtons disease Isothiocyanates - pharmacology Kinases Nematodes Nervous system Organosulfur compounds Peptides - metabolism Peptides - pharmacology Physiological aspects Protein kinases Proteins Signal transduction Signal Transduction - drug effects Sulfides Sulfoxides - pharmacology Thiocyanates Toxicity Transcription factors Worms Young adults |
| Title | Erucin, a Natural Isothiocyanate, Prevents Polyglutamine-Induced Toxicity in Caenorhabditis elegans via aak-2/AMPK and daf-16/FOXO Signaling |
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