Amphiphysin (BIN1) negatively regulates dynamin 2 for normal muscle maturation

Cowling, Belinda S.; Prokić, Ivana; Tasfaout, Hichem; Rabai, Aymen; Humbert, F; Rinaldi, Bruno; Nicot, Anne-Sophie; Kretz, Christine; Friant, Sylvie; Roux, Aurélien; Laporte, Jocelyn

doi:10.1172/jci90542

Cited by 78 publications

(132 citation statements)

References 51 publications

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“…The muscle-specific exon 11 is upregulated during muscle differentiation both in vitro and in vivo, and is present in most muscle isoforms in mature murine and human muscle (Butler et al 1997;Wechsler-Reya et al 1997;Nicot et al 2007;Fugier et al 2011;Cowling et al 2017). Our Bin1x11-/model did not have significant defects in T-tubule structure at each of the time points tested (2 weeks, 12 weeks and 12 months of age).…”

Section: Bin1 Muscle-specific Isoforms and Muscle Regenerationmentioning

confidence: 57%

“…Skeletal muscle expresses several isoforms including ubiquitous isoforms that contain both the BAR and C-terminal SH3 domains and muscle-specific isoforms that in addition contain the inframe exon 11 (named exon 10 in previous studies on the cDNA) encoding a polybasic motif binding phosphoinositides (PIs) (Lee et al 2002;Fugier et al 2011). The PI+ muscle-specific isoforms appear during muscle development and are the prevalent isoforms in adult ( (Cowling et al 2017) and this study). Overexpression of the muscle-specific BIN1 iso8 (a PI+ isoform) but not ubiquitous (PI-) isoforms in C2C12 myoblasts and other cells results in the formation of numerous tubules connected to the plasma membrane, suggesting the PI domain promotes membrane remodeling (Lee et al 2002;Nicot et al 2007;Bohm et al 2013).…”

Section: Introductionmentioning

confidence: 74%

“…To address the physiological importance of BIN1 and generate a BIN1-CNM model, we created and analyzed Bin1x20-/-mice, deleted in the last exon 20 ( Figure 1C) and thus causing disruption of the SH3 domain similarly to some CNM patients (Figure S1B-C) (Cowling et al 2017). The complete homozygous deletion of Bin1 is lethal in the first hours after birth and cardiomyopathy was proposed to be the fatal cause (Muller et al 2003).…”

Section: Constitutive and Muscle-specific Homozygous Deletion Of Bin1mentioning

confidence: 99%

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Differential physiological role of BIN1 isoforms in skeletal muscle development, function and regeneration

Prokić

Cowling

Kutchukian

et al. 2018

Preprint

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Skeletal muscle development and regeneration are tightly regulated processes. How the intracellular organization of muscle fibers is achieved during these steps is unclear. Here we focus on the cellular and physiological roles of amphiphysin 2 (BIN1), a membrane remodeling protein mutated in both congenital and adult centronuclear myopathies, that is ubiquitously expressed and has skeletal muscle-specific isoforms. We created and characterized constitutive, muscle-specific and inducible Bin1 homozygous and heterozygous knockout mice targeting either ubiquitous or muscle-specific isoforms. Constitutive Bin1-deficient mice died at birth from lack of feeding due to a skeletal muscle defect. T-tubules and other organelles were misplaced and altered, supporting a general early role of BIN1 on intracellular organization in addition to membrane remodeling. Whereas restricted deletion of Bin1 in unchallenged adult muscles had no impact, the forced switch from the muscle-specific isoforms to the ubiquitous isoforms through deletion of the in-frame muscle-specific exon delayed muscle regeneration. Thus, BIN1 ubiquitous function is necessary for muscle development and function while its muscle-specific isoforms fine-tune muscle regeneration in adulthood, supporting that BIN1 centronuclear myopathy with congenital onset are due to developmental defects while later onset may be due to regeneration defects.

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Section: Bin1 Muscle-specific Isoforms and Muscle Regenerationmentioning

confidence: 57%

Section: Introductionmentioning

confidence: 74%

Section: Constitutive and Muscle-specific Homozygous Deletion Of Bin1mentioning

confidence: 99%

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Differential physiological role of BIN1 isoforms in skeletal muscle development, function and regeneration

Prokić

Cowling

Kutchukian

et al. 2018

Preprint

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“…A C‐terminal Src‐homology‐3 (SH‐3) domain, which is encoded by exons 19 and 20, is expressed in all isoforms. The SH‐3 domain mediates interactions with numerous proteins, such as dynamin 2 . In addition, there are intramolecular interactions with other domains; the reduced mobility of the BIN1‐SH3 domain in the context of BIN1 isoform 1 is caused by the involvement of intramolecular interactions with clathrin and AP‐2 binding (CLAP) domain (334‐376), whereas this domain has significant mobility in the context of BIN1 isoform 9 …”

Section: Bridging Integratormentioning

confidence: 99%

“…The SH-3 domain mediates interactions with numerous proteins, such as dynamin 2. 23 In addition, there are intramolecular interactions with other domains; the reduced mobility of the BIN1-SH3 domain in the context of BIN1 isoform 1 is caused by the involvement of intramolecular interactions with clathrin and AP-2 binding (CLAP) domain (334-376), whereas this domain has significant mobility in the context of BIN1 isoform 9. 22 The myc-binding domain is encoded by exons 17 and 18 and binds to the c-Myc transcription factor and regulates its function.…”

Section: The Structure Of Bin1mentioning

confidence: 99%

Effect of BIN1 on cardiac dysfunction and malignant arrhythmias

et al. 2019

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Heart failure (HF) is the end‐stage syndrome for most cardiac diseases, and the 5‐year morbidity and mortality of HF remain high. Malignant arrhythmia is the main cause of sudden death in the progression of HF. Recently, bridging integrator 1 (BIN1) was discovered as a regulator of transverse tubule function and calcium signalling in cardiomyocytes. BIN1 downregulation is linked to abnormal cardiac contraction, and it increases the possibility of malignant arrhythmias preceding HF. Because of the detectability of cardiac BIN1 in peripheral blood, BIN1 may serve as a predictor of HF and may be useful in therapy development. However, the mechanism of BIN1 downregulation in HF and how BIN1 regulates normal cardiac function under physiological conditions remain unclear. In this review, recent progress in the biological studies of BIN1‐related cardiomyocytes and the effect of cardiac dysfunction and malignant arrhythmia will be discussed.

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Imaging‐based evaluation of pathogenicity by novel DNM2 variants associated with centronuclear myopathy

et al. 2021

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A centronuclear myopathy (CNM) is a group of inherited congenital diseases showing clinically progressive muscle weakness associated with the presence of centralized myonuclei, diagnosed by genetic testing and muscle biopsy. The gene encoding dynamin 2, DNM2, has been identified as a causative gene for an autosomal dominant form of CNM. However, the information of a DNM2 variant alone is not always sufficient to gain a definitive diagnosis as the pathogenicity of many gene variants is currently unknown. In this study, we identified five novel DNM2 variants in our cohort. To establish the pathogenicity of these variants without using clinicopathological information, we used a simple in cellulo imaging‐based assay for T‐tubule‐like structures to provide quantitative data that enable objective determination of pathogenicity by novel DNM2 variants. With this assay, we demonstrated that the phenotypes induced by mutant dynamin 2 in cellulo are well correlated with biochemical gain‐of‐function features of mutant dynamin 2 as well as the clinicopathological phenotypes of each patient. Our approach of combining an in cellulo assay with clinical information of the patients also explains the course of a disease progression by the pathogenesis of each variant in DNM2‐associated CNM.

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Amphiphysin (BIN1) negatively regulates dynamin 2 for normal muscle maturation

Cited by 78 publications

References 51 publications

Differential physiological role of BIN1 isoforms in skeletal muscle development, function and regeneration

Differential physiological role of BIN1 isoforms in skeletal muscle development, function and regeneration

Effect of BIN1 on cardiac dysfunction and malignant arrhythmias

Imaging‐based evaluation of pathogenicity by novel DNM2 variants associated with centronuclear myopathy

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