Sarcoglycans are enriched at the neuromuscular junction in a nerve-dependent manner

被引:0
作者
Gloriani, Michela [1 ]
Cheli, Bianca [1 ]
D'Ercole, Chiara [2 ]
Ruggieri, Veronica [1 ]
Cosentino, Marianna [1 ]
Serrat Pineda, Mireia [1 ]
Lozanoska-Ochser, Biliana [1 ,3 ]
Grassi, Francesca [4 ]
Bouche, Marina [1 ]
Madaro, Luca [1 ]
Riera, Carles Sanchez [1 ]
机构
[1] Sapienza Univ Rome, Dept Anat Histol Forens & Orthoped Sci, I-00161 Rome, Italy
[2] Sorbonne Univ, Assoc Inst Myol, Ctr Rech Myol, INSERM UMRS 974, F-75013 Paris, France
[3] LUM Univ, Dept Med & Surg, Casamassima, Italy
[4] Sapienza Univ Rome, Dept Physiol & Pharmacol Vittorio Erspamer, I-00185 Rome, Italy
来源
CELL DEATH & DISEASE | 2025年 / 16卷 / 01期
关键词
DYSTROPHIN-RELATED PROTEIN; MUSCULAR-DYSTROPHY; NITRIC-OXIDE; SYNAPSE; EXPRESSION; DEFICIENT; REVEALS; MUSCLES; ABSENCE; TARGET;
D O I
10.1038/s41419-025-07353-1
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
Sarcoglycanopathies are heterogeneous proximo-distal diseases presenting severe muscle alterations. Although there are 6 different sarcoglycan isoforms, sarcoglycanopathies are caused exclusively by mutations in genes coding for one of the four sarcoglycan transmembrane proteins (alpha, beta, gamma and delta) forming the sarcoglycan complex (SGC) in skeletal and cardiac muscle. Little is known about the different roles of the SGC beyond the dystrophin glycoprotein complex (DGC) structural role. Here, we show that SGC proteins are enriched at the post-synaptic membrane of neuromuscular junctions (NMJs). Using a mouse model lacking the beta-sarcoglycan subunit, we describe for the first time that the loss of the SGC in the NMJ area results in alterations of pre- and postsynaptic membrane, as well as a significant reduction of membrane potential. Moreover, using different denervated wild-type mouse models, we demonstrate that nerve presence precedes the sarcoglycan enrichment at NMJ, suggesting a nerve-dependent sarcoglycan expression. Altogether, our findings suggest that pathological decline should no longer be understood only in terms of sarcolemma damage but also in terms of sarcoglycans' participation in the NMJ. Henceforth, our work paves the way for the identification of new mechanisms involving sarcoglycans and new approaches for the treatment of sarcoglycanopathies.
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页数:11
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共 64 条
[1]   Absence of α-syntrophin leads to structurally aberrant neuromuscular synapses deficient in utrophin [J].
Adams, ME ;
Kramarcy, N ;
Krall, SP ;
Rossi, SG ;
Rotundo, RL ;
Sealock, R ;
Froehner, SC .
JOURNAL OF CELL BIOLOGY, 2000, 150 (06) :1385-1397
[2]   New genotype-phenotype correlations in a large European cohort of patients with sarcoglycanopathy [J].
Alonso-Perez, Jorge ;
Gonzalez-Quereda, Lidia ;
Bello, Luca ;
Guglieri, Michela ;
Straub, Volker ;
Gallano, Pia ;
Semplicini, Claudio ;
Pegoraro, Elena ;
Zangaro, Vittoria ;
Nascimento, Andres ;
Ortez, Carlos ;
Comi, Giacomo Pietro ;
ten Dam, Leroy ;
De Visser, Marianne ;
van der Kooi, A. J. ;
Garrido, Cristina ;
Santos, Manuela ;
Schara, Ulrike ;
Gangfuss, Andrea ;
Lokken, Nicoline ;
Storgaard, Glesper Helbo ;
Vissing, John ;
Schoser, Benedikt ;
Dekomien, Gabriele ;
Udd, Bjarne ;
Palmio, Johanna ;
D'Amico, Adele ;
Politano, Luisa ;
Nigro, Vincenzo ;
Bruno, Claudio ;
Panicucci, Chiara ;
Sarkozy, Anna ;
Abdel-Mannan, Omar ;
Alonsolimenez, Alicia ;
Claeys, Kristl G. ;
Gomez-Andres, David ;
Munell, Francina ;
Costa-Comellas, Laura ;
Haberlova, Jana ;
Rohlenova, Marie ;
Elke, De Vos ;
De Bleecker, Jan L. ;
Dominguez-Gonzalez, Cristina ;
Tasca, Giorgio ;
Weiss, Claudia ;
Deconinck, Nicolas ;
Fernandez-Torron, Roberto ;
de Munain, Adolfo Lopez ;
Camacho-Salas, Ana ;
Melegh, Bela .
BRAIN, 2020, 143 :2696-2708
[3]   Truncated dystrophins can influence neuromuscular synapse structure [J].
Banks, Glen B. ;
Chamberlain, Jeffrey S. ;
Froehner, Stanley C. .
MOLECULAR AND CELLULAR NEUROSCIENCE, 2009, 40 (04) :433-441
[4]   Clinical, genetic profile and disease progression of sarcoglycanopathies in a large cohort from India: high prevalence of SGCB c.544A > C [J].
Bardhan, Mainak ;
Anjanappa, Ram Murthy ;
Polavarapu, Kiran ;
Preethish-Kumar, Veeramani ;
Vengalil, Seena ;
Nashi, Saraswati ;
Sanga, Shamita ;
Padmanabh, Hansashree ;
Valasani, Ravi Kiran ;
Nishadham, Vikas ;
Keerthipriya, Muddasu ;
Geetha, Thenral S. ;
Ramprasad, Vedam ;
Arunachal, Gautham ;
Thomas, Priya Treesa ;
Acharya, Moulinath ;
Nalini, Atchayaram .
NEUROGENETICS, 2022, 23 (03) :187-202
[5]   The role of the dystrophin glycoprotein complex on the neuromuscular system [J].
Belhasan, Dina C. ;
Akaaboune, Mohammed .
NEUROSCIENCE LETTERS, 2020, 722
[6]   Ecto-ATPase activity of α-sarcoglycan (adhalin) [J].
Betto, R ;
Senter, L ;
Ceoldo, S ;
Tarricone, E ;
Biral, D ;
Salviati, G .
JOURNAL OF BIOLOGICAL CHEMISTRY, 1999, 274 (12) :7907-7912
[7]   Primary γ-sarcoglycanopathy (LGMD 2C):: broadening of the mutational spectrum guided by the immunohistochemical profile [J].
Bönnemann, CG ;
Wong, J ;
Jones, KJ ;
Lidov, HGW ;
Feener, CA ;
Shapiro, F ;
Darras, BT ;
Kunkel, LM ;
North, KN .
NEUROMUSCULAR DISORDERS, 2002, 12 (03) :273-280
[8]   BETA-SARCOGLYCAN (A3B) MUTATIONS CAUSE AUTOSOMAL RECESSIVE MUSCULAR-DYSTROPHY WITH LOSS OF THE SARCOGLYCAN COMPLEX [J].
BONNEMANN, CG ;
MODI, R ;
NOGUCHI, S ;
MIZUNO, Y ;
YOSHIDA, M ;
GUSSONI, E ;
MCNALLY, EM ;
DUGGAN, DJ ;
ANGELINI, C ;
HOFFMAN, EP ;
OZAWA, E ;
KUNKEL, LM .
NATURE GENETICS, 1995, 11 (03) :266-273
[9]   The Structure, Function, and Physiology of the Fetal and Adult Acetylcholine Receptor in Muscle [J].
Cetin, Hakan ;
Beeson, David ;
Vincent, Angela ;
Webster, Richard .
FRONTIERS IN MOLECULAR NEUROSCIENCE, 2020, 13
[10]   Glutamate at the Vertebrate Neuromuscular Junction: From Modulation to Neurotransmission [J].
Colombo, Maria Nicol ;
Francolini, Maura .
CELLS, 2019, 8 (09)