Differential autophagy power in the spinal cord and muscle of transgenic ALS mice
Open accessAbstract
Amyotrophic lateral sclerosis (ALS) is a motoneuron disease characterized by misfolded proteins aggregation in affected motoneurons. In mutant SOD1 (mutSOD1) ALS models, aggregation correlates to impaired functions of proteasome and/or autophagy, both essential for the intracellular chaperone-mediated protein quality control (PQC), and to a reduced mutSOD1 clearance from motoneurons. Skeletal muscle cells are also sensitive to mutSOD1 toxicity, but no mutSOD1 aggregates are formed in these cells, that might better manage mutSOD1 than motoneurons. Thus, we analyzed in spinal cord and in muscle of transgenic (tg) G93A-SOD1 mice at presymptomatic (PS, 8 weeks) and symptomatic (S, 16 weeks) stages, and in age-matched control mice, whether mutSOD1 differentially modulates relevant PQC players, such as HSPB8, BAG3, and BAG1. Possible sex differences were also considered. No changes of HSPB8, BAG3, and BAG1 at PS stage (8 weeks) were seen in all tissues examined in tg G93A-SOD1 and control mice. At S stage (16 weeks), HSPB8 dramatically increased in skeletal muscle of tg G93A-SOD1 mice, while a minor increase occurred in spinal cord of male, but not female tg G93A-SOD1 mice. BAG3 expression increased both in muscle and spinal cord of tg G93A-SOD1 mice at S stage, BAG1 expression increased only in muscle of the same mice. Since, HSPB8-BAG3 complex assists mutSOD1 autophagic removal, we analyzed two well-known autophagic markers, LC3 and p62. Both LC3 and p62 mRNAs were significantly up-regulated in skeletal muscle of tg G93A-SOD1 mice at S stage (16 weeks). This suggests that mutSOD1 expression induces a robust autophagic response specifically in muscle. Together these results demonstrate that, in muscle mutSOD1-induced autophagic response is much higher than in spinal cord. In addition, if mutSOD1 exerts toxicity in muscle, this may not be mediated by misfolded proteins accumulation. It remains unclear whether in muscle mutSOD1 toxicity is related to aberrant autophagy activation.
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Protein misfolding and its aggregation, axonal damage, and neuronal demyelination are among the main mechanisms leading to neurodegenerative lesions.
“they also suggest that protein misfolding and its aggregation, axonal damage, and neuronal demyelination are among the main mechanisms leading to neurodegenerative lesions.”
From Modulation of the gut–brain axis via the gut microbiota: a new era in treatment of amyotrophic lateral sclerosis (2023) · cites this paper as [86]
Dysregulated autophagy impairs clearance of polyubiquitinated protein aggregates in neurons and impairs endoplasmic reticulum (ER) homeostasis during stress, in aging, and in neurodegenerative diseases such as ALS.
“Dysregulated autophagy leads to impaired clearance of polyubiquitinated protein aggregates in neurons and impairs endoplasmic reticulum (ER) homeostasis during stress, in aging, and in neurodegenerative diseases such as ALS.”
From Modulation of the gut–brain axis via the gut microbiota: a new era in treatment of amyotrophic lateral sclerosis (2023) · cites this paper as [86]
The neuroinflammatory response causes the development and progression of neurological disorders.
“The resulting neuroinflammatory response causes the development and progression of neurological disorders.”
From Modulation of the gut–brain axis via the gut microbiota: a new era in treatment of amyotrophic lateral sclerosis (2023) · cites this paper as [86]
Dysregulated autophagy mediated by dysbiosis affects the integrity of the intestinal barrier, increases intestinal permeability, and translocates intestinal microbes, their metabolites, and microbial-associated molecular patterns to mesenteric lymphoid tissue.
“Dysregulated autophagy mediated by dysbiosis affects the integrity of the intestinal barrier and increases intestinal permeability, thereby translocating intestinal microbes, their metabolites, and microbial-associated molecular patterns to mesenteric lymphoid tissue.”
From Modulation of the gut–brain axis via the gut microbiota: a new era in treatment of amyotrophic lateral sclerosis (2023) · cites this paper as [86]
In ALS, inflammation propagates from somatic circulation to the brain via the cerebro-intestinal axis.
“in which inflammation propagates from somatic circulation to the brain via the cerebro-intestinal axis”
From Modulation of the gut–brain axis via the gut microbiota: a new era in treatment of amyotrophic lateral sclerosis (2023) · cites this paper as [86]
Failure of the autophagic system to clear misfolded proteins is a major trigger of neuroinflammation and is closely associated with the development of ALS.
“These findings suggest that the failure of the autophagic system to clear misfolded proteins is a major trigger of neuroinflammation and is closely associated with the development of ALS (86)”
From Modulation of the gut–brain axis via the gut microbiota: a new era in treatment of amyotrophic lateral sclerosis (2023) · cites this paper as [86]
Reduced ability to promote intestinal dysfunction affects the functioning of the brain-gut axis and plays an important role in the pathophysiological function of the intestine, affecting the development of ALS.
“At the same time, the reduced ability to promote intestinal dysfunction affects the functioning of the brain–gut axis and plays an important role in the pathophysiological function of the intestine, affecting the development of ALS (86).”
From Modulation of the gut–brain axis via the gut microbiota: a new era in treatment of amyotrophic lateral sclerosis (2023) · cites this paper as [86]
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- Authors
- Crippa, V., Boncoraglio, A., Galbiati, M., Aggarwal, T., Rusmini, P., Giorgetti, E., Cristofani, R., Carra, S., Pennuto, M., & Poletti, A.
- Affiliations
- University of Milan (IT)
- University Medical Center Groningen (NL)
- Italian Institute of Technology (IT)
- University of Modena and Reggio Emilia (IT)
- University of Trento (IT)
- Corresponding author
- Poletti, Angelo
- ORCID
- Venue
- Frontiers in Cellular Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2013
- Volume
- 7
- Pages
- 234-234
- ISSN
- 1662-5102 (ISSN-L)
- PMC
- PMC3840302
- OpenAlex
- W2118760738
- Cited by
- 63
- References
- 80
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 5 · 2023: 4 · 2022: 5 · 2021: 1 · 2020: 5 · 2019: 5 · 2018: 10 · 2017: 7 · 2016: 5 · 2015: 8 · 2014: 3
- FWCI
- 3.39
- Type
- journal article
- Language
- de
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Cellular Neuroscience (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Archivio Istituzionale della Ricerca (Universita Degli Studi Di Milano) (submittedVersion, other-oa)
- IRIS UNIMORE (University of Modena and Reggio Emilia) (submittedVersion, cc-by)
- Iris (University of Trento) (submittedVersion, cc-by)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- CINECA IRIS Institutial Research Information System (University of Genoa) (submittedVersion)
- Padua Research Archive (University of Padova) (submittedVersion, cc-by)
- Funders
- Muscular Dystrophy Association (196646)
- Università degli Studi di Milano
- Fondazione Cariplo (2008-2307)
- Regione Lombardia
- Hsinchu Science Park Bureau, Ministry of Science and Technology, Taiwan
- Topics
- Health Sciences › Medicine › Neurology › Amyotrophic Lateral Sclerosis Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Genetic Neurodegenerative Diseases
- Keywords
- amyotrophic lateral sclerosis, autophagy, mutant SOD1, protein quality control, HSPB8, BAG3, BAG-1, LC3, p62, skeletal muscle, spinal cord, sex differences, proteasome, protein aggregation
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