Skip to main content
Erschienen in: Neurological Sciences 7/2022

19.02.2022 | Original Article

Effects of low-intensity training on the brain and muscle in the congenital muscular dystrophy 1D model

verfasst von: Clarissa M. Comim, Jaime A. Soares, Adriano Alberti, Viviane Freiberger, Letícia Ventura, Paula Dias, Aryadnne L. Schactae, Leoberto R. Grigollo, Amanda V. Steckert, Daniel F. Martins, Rudy J. Nodari Junior, Mariz Vainzof, João Quevedo

Erschienen in: Neurological Sciences | Ausgabe 7/2022

Einloggen, um Zugang zu erhalten

Abstract

Introduction

Congenital Muscular Dystrophy type 1D (MDC1D) is characterized by a hypoglycosylation of α-dystroglycan protein (α-DG), and this may be strongly implicated in increased skeletal muscle tissue degeneration and abnormal brain development, leading to cognitive impairment. However, the pathophysiology of brain involvement is still unclear. Low-intensity exercise training (LIET) is known to contribute to decreased muscle degeneration in animal models of other forms of progressive muscular dystrophies.

Aim

The objective of this study was to analyze the effects of LIET on cognitive involvement and oxidative stress in brain tissue and gastrocnemius muscle.

Methods

Male homozygous (Largemyd−/−), heterozygous (Largemyd+/−), and wild-type mice were used. To complete 28 days of life, they were subjected to a low-intensity exercise training (LIET) for 8 weeks. After the last day of training, 24 h were expected when the animals were submitted to inhibitory avoidance and open-field test. The striatum, prefrontal cortex, hippocampus, cortex, and gastrocnemius were collected for evaluation of protein carbonylation, lipid peroxidation, and catalase and superoxide dismutase activity.

Results

LIET was observed to reverse the alteration in aversive and habituation memory. Increased protein carbonylation in the striatum, prefrontal cortex, and hippocampus and lipid peroxidation in the prefrontal cortex and hippocampus were also reversed by LIET. In the evaluation of the antioxidant activity, LIET increased catalase activity in the hippocampus and cortex. In the gastrocnemius, LIET decreased the protein carbonylation and lipid peroxidation and increased catalase and superoxide dismutase activity.

Conclusion

In conclusion, it can be inferred that LIET for 8 weeks was able to reverse the cognitive damage and oxidative stress in brain tissue and gastrocnemius muscle in MDC1D animals.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat Bulfield G, Siller WG, Wight PA, Moore KJ (1984) X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA 81:1189–1192PubMedPubMedCentralCrossRef Bulfield G, Siller WG, Wight PA, Moore KJ (1984) X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA 81:1189–1192PubMedPubMedCentralCrossRef
2.
Zurück zum Zitat Durbeej M, Campbell KP (2002) Muscular dystrophies involving the dystrophin- glycoprotein complex: an overview of current mouse models. Curr Opin Genet Dev 12:349–361PubMedCrossRef Durbeej M, Campbell KP (2002) Muscular dystrophies involving the dystrophin- glycoprotein complex: an overview of current mouse models. Curr Opin Genet Dev 12:349–361PubMedCrossRef
3.
Zurück zum Zitat Longman C, Brockington M, Torelli S, Jimenez-Mallebrera C, Kennedy C, Khalil N et al (2003) Mutations in the human LARGE gene cause MDC1D, a novel form of congenital muscular dystrophy with severe mental retardation and abnormal glycosylation of alpha-dystroglycan. Hum Mol Genet 12:285–361CrossRef Longman C, Brockington M, Torelli S, Jimenez-Mallebrera C, Kennedy C, Khalil N et al (2003) Mutations in the human LARGE gene cause MDC1D, a novel form of congenital muscular dystrophy with severe mental retardation and abnormal glycosylation of alpha-dystroglycan. Hum Mol Genet 12:285–361CrossRef
4.
Zurück zum Zitat Yoshida A, Kobayashi K, Manya H, Taniguchi K, Kano H, Mizuno M et al (2001) Muscular and neuronal migration disorder caused by mutations in a glycosyltransferase, POMGnT1. Dev Cell 1:717–724PubMedCrossRef Yoshida A, Kobayashi K, Manya H, Taniguchi K, Kano H, Mizuno M et al (2001) Muscular and neuronal migration disorder caused by mutations in a glycosyltransferase, POMGnT1. Dev Cell 1:717–724PubMedCrossRef
5.
Zurück zum Zitat Comim CM, Mendonça BP, Dominguini D, Cipriano AL, Steckert AV, Scaini G et al (2013) Central nervous system involvement in the animal model of myodystrophy. Mol Neurobiol 48:71–77PubMedCrossRef Comim CM, Mendonça BP, Dominguini D, Cipriano AL, Steckert AV, Scaini G et al (2013) Central nervous system involvement in the animal model of myodystrophy. Mol Neurobiol 48:71–77PubMedCrossRef
6.
Zurück zum Zitat Comim CM, Schactae AL, Soares JA, Ventura L, Freiberger V, Mina F et al (2016) Behavioral responses in animal model of congenital muscular dystrophy 1D. Mol Neurobiol 53:402–407PubMedCrossRef Comim CM, Schactae AL, Soares JA, Ventura L, Freiberger V, Mina F et al (2016) Behavioral responses in animal model of congenital muscular dystrophy 1D. Mol Neurobiol 53:402–407PubMedCrossRef
7.
Zurück zum Zitat Odom GL, Gregorevic P, Chamberlain JS (2007) Viral-mediated gene therapy for the muscular dystrophies: successes, limitations and recent advances. Biochim Biophys Acta 1772:243–262PubMedCrossRef Odom GL, Gregorevic P, Chamberlain JS (2007) Viral-mediated gene therapy for the muscular dystrophies: successes, limitations and recent advances. Biochim Biophys Acta 1772:243–262PubMedCrossRef
8.
Zurück zum Zitat Grange RW, Call JA (2007) Recommendations to define exercise prescription for Duchenne muscular dystrophy. Exerc Sport Sci Rev 35:12–17PubMedCrossRef Grange RW, Call JA (2007) Recommendations to define exercise prescription for Duchenne muscular dystrophy. Exerc Sport Sci Rev 35:12–17PubMedCrossRef
9.
Zurück zum Zitat Andrade LS, Marreiro DN (2011) Aspectos sobre a relação entre exercício físico, estresse oxidativo e zinco. Rev Nutr 24:629–640CrossRef Andrade LS, Marreiro DN (2011) Aspectos sobre a relação entre exercício físico, estresse oxidativo e zinco. Rev Nutr 24:629–640CrossRef
10.
11.
Zurück zum Zitat Ansved T (2003) Muscular dystrophies: influence of physical conditioning on the disease evolution. Curr Opin Clin Nutr Metab Care 6:435–439PubMed Ansved T (2003) Muscular dystrophies: influence of physical conditioning on the disease evolution. Curr Opin Clin Nutr Metab Care 6:435–439PubMed
12.
Zurück zum Zitat Kaczor JJ, Hall JE, Payne E, Tarnopolsky MA (2007) Low intensity training decreases markers of oxidative stress in skeletal muscle of mdx mice. Free Radic Biol Med 43:145–154PubMedCrossRef Kaczor JJ, Hall JE, Payne E, Tarnopolsky MA (2007) Low intensity training decreases markers of oxidative stress in skeletal muscle of mdx mice. Free Radic Biol Med 43:145–154PubMedCrossRef
13.
Zurück zum Zitat Schactae AL, Palmas D, Michels M, Generoso JS, Barichello T, Dal-Pizzol F et al (2017) Congenital muscular dystrophy 1D causes matrix metalloproteinase activation and blood-brain barrier impairment. Curr Neurovasc Res 14:60–64PubMedCrossRef Schactae AL, Palmas D, Michels M, Generoso JS, Barichello T, Dal-Pizzol F et al (2017) Congenital muscular dystrophy 1D causes matrix metalloproteinase activation and blood-brain barrier impairment. Curr Neurovasc Res 14:60–64PubMedCrossRef
14.
Zurück zum Zitat Draper HH, Hadley M (1990) Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol 186:421–431PubMedCrossRef Draper HH, Hadley M (1990) Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol 186:421–431PubMedCrossRef
15.
Zurück zum Zitat Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593PubMedCrossRef Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593PubMedCrossRef
17.
Zurück zum Zitat Bannister JV, Calabrese L (1987) Assays for superoxide dismutase. Methods Biochem Anal 32:279–312PubMed Bannister JV, Calabrese L (1987) Assays for superoxide dismutase. Methods Biochem Anal 32:279–312PubMed
18.
Zurück zum Zitat Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J BiolChem 193:265–275 Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J BiolChem 193:265–275
19.
Zurück zum Zitat Lawler JM (2011) Exacerbation of pathology by oxidative stress in respiratory and locomotor muscles with Duchenne muscular dystrophy. J Physiol 589:216–170CrossRef Lawler JM (2011) Exacerbation of pathology by oxidative stress in respiratory and locomotor muscles with Duchenne muscular dystrophy. J Physiol 589:216–170CrossRef
20.
Zurück zum Zitat Chelly J, Desguerre I (2013) Progressive muscular dystrophies. Handb Clin Neurol 113:1343–1366PubMedCrossRef Chelly J, Desguerre I (2013) Progressive muscular dystrophies. Handb Clin Neurol 113:1343–1366PubMedCrossRef
21.
Zurück zum Zitat Wicklund MP (2013) The muscular dystrophies. Continuum (Minneap Minn) 19:1535–1570 Wicklund MP (2013) The muscular dystrophies. Continuum (Minneap Minn) 19:1535–1570
22.
Zurück zum Zitat Lowe DA, Williams BO, Thomas DD, Grange RW (2006) Molecular and cellular contractile dysfunction of dystrophic muscle from young mice. Muscle Nerve 34:92–100PubMedCrossRef Lowe DA, Williams BO, Thomas DD, Grange RW (2006) Molecular and cellular contractile dysfunction of dystrophic muscle from young mice. Muscle Nerve 34:92–100PubMedCrossRef
23.
Zurück zum Zitat Cotman CW, Nicole CB (2002) Exercício: uma intervenção comportamental para melhorar a saúde do cérebro e plasticidade. Tendências em Neurociências 25:295–301 Cotman CW, Nicole CB (2002) Exercício: uma intervenção comportamental para melhorar a saúde do cérebro e plasticidade. Tendências em Neurociências 25:295–301
24.
Zurück zum Zitat Hammock EAD, Larry JY (2005) Microsatellite instability generates diversity in brain and sociobehavioral traits. Science 308:1630–1634PubMedCrossRef Hammock EAD, Larry JY (2005) Microsatellite instability generates diversity in brain and sociobehavioral traits. Science 308:1630–1634PubMedCrossRef
25.
Zurück zum Zitat Molteni R, Ying Z, Gomez-Pinilla F (2002) Differential effects of acute and chronic exercise on plasticity – related genes in the rat hippocampus revealed by microarray. Eur J Neurosci 16:1107–1116PubMedCrossRef Molteni R, Ying Z, Gomez-Pinilla F (2002) Differential effects of acute and chronic exercise on plasticity – related genes in the rat hippocampus revealed by microarray. Eur J Neurosci 16:1107–1116PubMedCrossRef
26.
Zurück zum Zitat Van Praag, H (1999) Running improves neurogenesis, learning, and long-term potentiation in mice. Pro Nat Acad Sci 96:427–31 Van Praag, H (1999) Running improves neurogenesis, learning, and long-term potentiation in mice. Pro Nat Acad Sci 96:427–31
27.
Zurück zum Zitat Kempermann G, van Praag H, Gage FH (1999) Regulação dependente de atividade da plasticidade neuronal e auto reparo. Prog Brain Res 127:35–48CrossRef Kempermann G, van Praag H, Gage FH (1999) Regulação dependente de atividade da plasticidade neuronal e auto reparo. Prog Brain Res 127:35–48CrossRef
28.
Zurück zum Zitat Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A et al (1993) Mutations in Cu/Zn-superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362:59–62PubMedCrossRef Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A et al (1993) Mutations in Cu/Zn-superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362:59–62PubMedCrossRef
29.
Zurück zum Zitat Spangenburg EE, Booth FW (2003) Molecular regulation of individual skeletal muscle fibre types. Acta Physiol Scand 178:413–424PubMedCrossRef Spangenburg EE, Booth FW (2003) Molecular regulation of individual skeletal muscle fibre types. Acta Physiol Scand 178:413–424PubMedCrossRef
30.
Zurück zum Zitat Rada ́k Z, Asano K, Inoue M, Kizaki T, Oh-ishi S, Suzuki K. et al (1995) Superoxide dismutase derivative reduces oxidative damage in skeletal muscle of rats during exhaustive exercise. J Appl Physiol 79:129–35 Rada ́k Z, Asano K, Inoue M, Kizaki T, Oh-ishi S, Suzuki K. et al (1995) Superoxide dismutase derivative reduces oxidative damage in skeletal muscle of rats during exhaustive exercise. J Appl Physiol 79:129–35
31.
Zurück zum Zitat Somani SM, Ravi R, Rybak LP (1995) Effect of exercise training on antioxidant system in brain regions of rat. Pharmacol Biochem Behav 50:635–639PubMedCrossRef Somani SM, Ravi R, Rybak LP (1995) Effect of exercise training on antioxidant system in brain regions of rat. Pharmacol Biochem Behav 50:635–639PubMedCrossRef
32.
Zurück zum Zitat Emery J, Kumar S, Smith H (1998) Patient understanding of genetic principles and their expectations of genetic services within the NHS: a qualitative study. CommunityGenet 1:78–83 Emery J, Kumar S, Smith H (1998) Patient understanding of genetic principles and their expectations of genetic services within the NHS: a qualitative study. CommunityGenet 1:78–83
33.
Zurück zum Zitat Pinho RA, Silveira PC, Piazza M, Tuon T, Silva GA, Dal-Pizzol F et al (2006) Exercício físico regular diminui o estresse oxidativo pulmonar em ratos após exposição aguda ao carvão mineral. Revista Brasileira de Medicina do Esporte 12:81–84CrossRef Pinho RA, Silveira PC, Piazza M, Tuon T, Silva GA, Dal-Pizzol F et al (2006) Exercício físico regular diminui o estresse oxidativo pulmonar em ratos após exposição aguda ao carvão mineral. Revista Brasileira de Medicina do Esporte 12:81–84CrossRef
34.
Zurück zum Zitat Ding Q, Vaynman S, Akhavan M, Ying Z, Gomez-Pinilla F (2006) Insulin-like growth factor I interfaces with brain-derived neurotrophic factor-mediated synaptic plasticity to modulate aspects of exercise-induced cognitive function. Neurosci 140:823–833CrossRef Ding Q, Vaynman S, Akhavan M, Ying Z, Gomez-Pinilla F (2006) Insulin-like growth factor I interfaces with brain-derived neurotrophic factor-mediated synaptic plasticity to modulate aspects of exercise-induced cognitive function. Neurosci 140:823–833CrossRef
35.
Zurück zum Zitat Cui L, Hofer T, Rani A, Leeuwenburgh C, Foster TC (2009) Comparison of lifelong and late life exercise on oxidative stress in the cerebellum. Neurobiol Aging 30:903–909PubMedCrossRef Cui L, Hofer T, Rani A, Leeuwenburgh C, Foster TC (2009) Comparison of lifelong and late life exercise on oxidative stress in the cerebellum. Neurobiol Aging 30:903–909PubMedCrossRef
36.
Zurück zum Zitat Kirchner L, Chen WQ, Afjehi-Sadat L, Viidik A, Skalicky M, Höger H et al (2008) Hippocampal metabolic proteins are modulated in voluntary and treadmill exercise rats. Exp Neurol 212:145–151PubMedCrossRef Kirchner L, Chen WQ, Afjehi-Sadat L, Viidik A, Skalicky M, Höger H et al (2008) Hippocampal metabolic proteins are modulated in voluntary and treadmill exercise rats. Exp Neurol 212:145–151PubMedCrossRef
37.
Zurück zum Zitat Opii WO, Joshi G, Head E, Milgram NW, Muggenburg BA, Klein JB et al (2008) Proteomic identification of brain proteins in the canine model of human aging following a long-term treatment with antioxidants and a program of behavioral enrichment: relevance to Alzheimer’s disease. Neurobiol Aging 29:51–70PubMedCrossRef Opii WO, Joshi G, Head E, Milgram NW, Muggenburg BA, Klein JB et al (2008) Proteomic identification of brain proteins in the canine model of human aging following a long-term treatment with antioxidants and a program of behavioral enrichment: relevance to Alzheimer’s disease. Neurobiol Aging 29:51–70PubMedCrossRef
38.
Zurück zum Zitat Selcher JC, Nekrasova T, Paylor R, Landreth GE, Sweatt J (2001) Mice lacking the ERK1 isoform of MAP kinase are unimpaired in emotional learning. Learn Mem 8:11–19PubMedPubMedCentralCrossRef Selcher JC, Nekrasova T, Paylor R, Landreth GE, Sweatt J (2001) Mice lacking the ERK1 isoform of MAP kinase are unimpaired in emotional learning. Learn Mem 8:11–19PubMedPubMedCentralCrossRef
39.
Zurück zum Zitat Aksu I, Topcu A, Camsari UM, Acikgoz O (2009) Effect of acute and chronic exercise on oxidant-antioxidant equilibrium in rat hippocampus, prefrontal cortex and striatum. Neurosci Lett 452:281–285PubMedCrossRef Aksu I, Topcu A, Camsari UM, Acikgoz O (2009) Effect of acute and chronic exercise on oxidant-antioxidant equilibrium in rat hippocampus, prefrontal cortex and striatum. Neurosci Lett 452:281–285PubMedCrossRef
40.
Zurück zum Zitat Dishman RK, Berthoud HR, Booth FW, Cotman CW, Edgerton VR, Fleshner MR et al (2006) Neurobiology of exercise. Obesity (Silver Spring) 14:345–356CrossRef Dishman RK, Berthoud HR, Booth FW, Cotman CW, Edgerton VR, Fleshner MR et al (2006) Neurobiology of exercise. Obesity (Silver Spring) 14:345–356CrossRef
41.
Zurück zum Zitat Dupont-Versteegden EE1, McCarter RJ, Katz MS (1994) Voluntary exercise decreases progression of muscular dystrophy in diaphragm of mdx mice. J Appl Physiol 77:1736–41 Dupont-Versteegden EE1, McCarter RJ, Katz MS (1994) Voluntary exercise decreases progression of muscular dystrophy in diaphragm of mdx mice. J Appl Physiol 77:1736–41
42.
Zurück zum Zitat Carter GT, Wineinger MA, Walsh SA, Horasek SJ, Abresch RT, Fowler WM Jr (1995) Effect of voluntary wheel-running exercise on muscles of the mdx mouse. Neuromuscul Disord 5:323–332PubMedCrossRef Carter GT, Wineinger MA, Walsh SA, Horasek SJ, Abresch RT, Fowler WM Jr (1995) Effect of voluntary wheel-running exercise on muscles of the mdx mouse. Neuromuscul Disord 5:323–332PubMedCrossRef
43.
Zurück zum Zitat Granchelli JA, Pollina C, Hudecki MS (2000) Pre-clinical screening of drugs using the mdx mouse. Neuromuscul Disord 10:235–239PubMedCrossRef Granchelli JA, Pollina C, Hudecki MS (2000) Pre-clinical screening of drugs using the mdx mouse. Neuromuscul Disord 10:235–239PubMedCrossRef
44.
Zurück zum Zitat Eagle M (2002) Report on the muscular dystrophy campaign workshop: exercise in neuromuscular diseases, Newcastle, January 2002. Neuromuscul Disord 12:975–983PubMedCrossRef Eagle M (2002) Report on the muscular dystrophy campaign workshop: exercise in neuromuscular diseases, Newcastle, January 2002. Neuromuscul Disord 12:975–983PubMedCrossRef
45.
Zurück zum Zitat Akimoto T, Sorg BS, Yan Z (2004) Real-time imaging of peroxisome proliferator- activated receptor gamma-coactivator-1alpha promoter activity in skeletal muscles of living mice. Am J Physiol Cell Physiol 287:790–796CrossRef Akimoto T, Sorg BS, Yan Z (2004) Real-time imaging of peroxisome proliferator- activated receptor gamma-coactivator-1alpha promoter activity in skeletal muscles of living mice. Am J Physiol Cell Physiol 287:790–796CrossRef
46.
Metadaten
Titel
Effects of low-intensity training on the brain and muscle in the congenital muscular dystrophy 1D model
verfasst von
Clarissa M. Comim
Jaime A. Soares
Adriano Alberti
Viviane Freiberger
Letícia Ventura
Paula Dias
Aryadnne L. Schactae
Leoberto R. Grigollo
Amanda V. Steckert
Daniel F. Martins
Rudy J. Nodari Junior
Mariz Vainzof
João Quevedo
Publikationsdatum
19.02.2022
Verlag
Springer International Publishing
Erschienen in
Neurological Sciences / Ausgabe 7/2022
Print ISSN: 1590-1874
Elektronische ISSN: 1590-3478
DOI
https://doi.org/10.1007/s10072-022-05928-w

Weitere Artikel der Ausgabe 7/2022

Neurological Sciences 7/2022 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Niedriger diastolischer Blutdruck erhöht Risiko für schwere kardiovaskuläre Komplikationen

25.04.2024 Hypotonie Nachrichten

Wenn unter einer medikamentösen Hochdrucktherapie der diastolische Blutdruck in den Keller geht, steigt das Risiko für schwere kardiovaskuläre Ereignisse: Darauf deutet eine Sekundäranalyse der SPRINT-Studie hin.

Frühe Alzheimertherapie lohnt sich

25.04.2024 AAN-Jahrestagung 2024 Nachrichten

Ist die Tau-Last noch gering, scheint der Vorteil von Lecanemab besonders groß zu sein. Und beginnen Erkrankte verzögert mit der Behandlung, erreichen sie nicht mehr die kognitive Leistung wie bei einem früheren Start. Darauf deuten neue Analysen der Phase-3-Studie Clarity AD.

Viel Bewegung in der Parkinsonforschung

25.04.2024 Parkinson-Krankheit Nachrichten

Neue arznei- und zellbasierte Ansätze, Frühdiagnose mit Bewegungssensoren, Rückenmarkstimulation gegen Gehblockaden – in der Parkinsonforschung tut sich einiges. Auf dem Deutschen Parkinsonkongress ging es auch viel um technische Innovationen.

Demenzkranke durch Antipsychotika vielfach gefährdet

23.04.2024 Demenz Nachrichten

Wenn Demenzkranke aufgrund von Symptomen wie Agitation oder Aggressivität mit Antipsychotika behandelt werden, sind damit offenbar noch mehr Risiken verbunden als bislang angenommen.

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.