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Overexpression of miniparamyosin causes muscle dysfunction and age-dependant myo®bril degeneration in the indirect ¯ight muscles of Drosophila melanogaster JUAN J. ARREDONDO 1 , MICHELLE MARDAHL-DUMESNIL 2,3 , RICHARD M. CRIPPS 2,4 , MARGARITA CERVERA 1 and SANFORD I. BERNSTEIN 2, * 1 Departamento de BioquõÂmica and Instituto Investigaciones BiomeÂdicas, CSIC, Facultad de Medicina, Universidad Auto Ânoma de Madrid, Arzobispo Morcillo 4, 28029 Madrid, Spain; 2 Department of Biology and Molecular Biology Institute, San Diego State University, San Diego, CA 92182-4614, USA Received 1 February 2001; accepted in revised form 29 June 2001 Abstract Miniparamyosin (mPM) is a protein of invertebrate muscle thick ®laments. Its similarity to paramyosin (PM) suggests that it regulates thick ®lament and myo®bril assembly. To determine its role in muscle structure and function we overexpressed mPM in muscles of Drosophila melanogaster. Surprisingly, myo®brils accumulating excess mPM assemble nearly normally, with thick ®lament electron density and sarcomere length unaected. Myo®brils in some indirect ¯ight muscle groups are misaligned and young ¯ies exhibit a moderate level of ¯ight impairment. This phenotype is exacerbated with age. Transgenic ¯ies undergo progressive myo®bril deterioration that increases ¯ight muscle dysfunction. Our observations indicate that the correct stoichiometry of mPM is important for maintenance of myo®bril integrity and for the proper function of the ¯ight musculature. Introduction Isoforms of many myo®brillar proteins are dierentially expressed during muscle development (Bernstein et al., 1993; Epstein and Fischman, 1991). At least some of these changes in isoform expression are critical to de®ning the structural and functional properties of the contractile apparatus. To investigate the function of the muscle protein miniparamyosin (mPM), a unique isoform of the invertebrate contractile protein paramyosin (PM), we produced transgenic organisms that express excess levels of mPM. We then determined the consequences upon the structure and function of the indirect ¯ight muscles, a muscle group that can be manipulated without aecting the viability of the transgenic organisms. mPM is a recently-discovered muscle protein of unknown function (Becker et al., 1992) that is associated with thick ®laments of the myo®bril (Maroto et al., 1996). It was ®rst found in Drosophila melanogaster, where its transcripts arise from alternative promoter choice in the PM gene (Maroto et al., 1995). Drosophila PM and mPM (see Figure 1) have an identical C- terminal domain. This domain contains 363 amino acid residues that form an a-helix. However, mPM has a unique 114 amino acid residue N-terminus that lacks homology to other known proteins (Becker et al., 1992). Although mPM is present in many invertebrates includ- ing arthropods, annelids, mollusks, and echinoderms, it is absent from the nematode Canenorhabditis elegans and from vertebrates (Maroto et al., 1995). Since mPM and PM share a C-terminal domain, the two proteins may perform similar functions. PM is thought to facilitate thick ®lament assembly and is located in the ®lament core (Deitiker and Epstein, 1993). It forms an a-helical coiled-coil dimer that is proposed to interface with its homologous counterpart, the myosin rod dimer (Szent-Gyorgyi et al., 1971; Epstein et al., 1976; Harris and Epstein, 1977; Bennett and Elliott, 1984; Hoppe and Waterston, 1996). Mutant analysis in C. elegans shows that thick ®lament length and diameter are aected by PM content (Mackenzie and Epstein, 1980). PM may also regulate the electron density of thick ®laments since there is a direct corre- lation between this property and the level of PM in muscles of various invertebrates (Bullard et al., 1973a). Expression of PM isoforms is dierentially regulated in Drosophila, both temporally and spatially (Arredondo et al., 2001). While mPM and PM are found in all types of adult muscles (for review of these muscles see Bernstein et al., 1993), expression levels vary (Maroto et al., 1996). Both isoforms accumulate in tubular muscles and in the ®brillar indirect ¯ight muscles (IFM)(Vino s et al., 1991; Becker et al., 1992). However, mPM levels are lower than PM levels in the IFM, leg and abdominal muscles (Becker et al., 1992; Maroto et al., 1996). Endogenous mPM thoracic expression is highest Current addresses: 3 Department of Cell Biology MB24, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037-1092, USA; 4 Department of Biology, University of New Mexico, Albuquerque, NM 87131-1091, USA * To whom correspondence should be addressed: Tel.: 1-619-594- 5629; Fax: 1-619-594-5676; E-mail: [email protected] Journal of Muscle Research and Cell Motility 22: 287±299, 2001. 287 Ó 2001 Kluwer Academic Publishers. Printed in the Netherlands.
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Overexpression of miniparamyosin causes muscle dysfunction and age-dependant myofibril degeneration in the indirect flight muscles of Drosophila melanogaster

Jan 28, 2023

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Page 1: Overexpression of miniparamyosin causes muscle dysfunction and age-dependant myofibril degeneration in the indirect flight muscles of Drosophila melanogaster

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https://www.researchgate.net/publication/14503127_Drosophila_paramyosinminiparamyosin_gene_products_show_a_large_diversity_in_quantity_localization_and_isoform_pattern_a_possible_role_in_muscle_maturation_and_function?el=1_x_8&enrichId=rgreq-0b79905af78a70b7df5f3a855c4d2ed4-XXX&enrichSource=Y292ZXJQYWdlOzIyNjkxNzU4MTtBUzoxMDIyNjUzMjI5OTk4MDhAMTQwMTM5MzM2MTE3NA==
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Page 2: Overexpression of miniparamyosin causes muscle dysfunction and age-dependant myofibril degeneration in the indirect flight muscles of Drosophila melanogaster

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Page 3: Overexpression of miniparamyosin causes muscle dysfunction and age-dependant myofibril degeneration in the indirect flight muscles of Drosophila melanogaster

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Page 4: Overexpression of miniparamyosin causes muscle dysfunction and age-dependant myofibril degeneration in the indirect flight muscles of Drosophila melanogaster

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https://www.researchgate.net/publication/14503127_Drosophila_paramyosinminiparamyosin_gene_products_show_a_large_diversity_in_quantity_localization_and_isoform_pattern_a_possible_role_in_muscle_maturation_and_function?el=1_x_8&enrichId=rgreq-0b79905af78a70b7df5f3a855c4d2ed4-XXX&enrichSource=Y292ZXJQYWdlOzIyNjkxNzU4MTtBUzoxMDIyNjUzMjI5OTk4MDhAMTQwMTM5MzM2MTE3NA==
Page 5: Overexpression of miniparamyosin causes muscle dysfunction and age-dependant myofibril degeneration in the indirect flight muscles of Drosophila melanogaster

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https://www.researchgate.net/publication/21390800_Development_of_indirect_flight_muscles_of_Drosophila?el=1_x_8&enrichId=rgreq-0b79905af78a70b7df5f3a855c4d2ed4-XXX&enrichSource=Y292ZXJQYWdlOzIyNjkxNzU4MTtBUzoxMDIyNjUzMjI5OTk4MDhAMTQwMTM5MzM2MTE3NA==
https://www.researchgate.net/publication/21390800_Development_of_indirect_flight_muscles_of_Drosophila?el=1_x_8&enrichId=rgreq-0b79905af78a70b7df5f3a855c4d2ed4-XXX&enrichSource=Y292ZXJQYWdlOzIyNjkxNzU4MTtBUzoxMDIyNjUzMjI5OTk4MDhAMTQwMTM5MzM2MTE3NA==
Page 6: Overexpression of miniparamyosin causes muscle dysfunction and age-dependant myofibril degeneration in the indirect flight muscles of Drosophila melanogaster

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Page 9: Overexpression of miniparamyosin causes muscle dysfunction and age-dependant myofibril degeneration in the indirect flight muscles of Drosophila melanogaster

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Page 10: Overexpression of miniparamyosin causes muscle dysfunction and age-dependant myofibril degeneration in the indirect flight muscles of Drosophila melanogaster

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Page 11: Overexpression of miniparamyosin causes muscle dysfunction and age-dependant myofibril degeneration in the indirect flight muscles of Drosophila melanogaster

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https://www.researchgate.net/publication/12216937_Control_of_Drosophila_paramyosinminiparamyosin_gene_expression_-_Differential_regulatory_mechanisms_for_muscle-specific_transcription?el=1_x_8&enrichId=rgreq-0b79905af78a70b7df5f3a855c4d2ed4-XXX&enrichSource=Y292ZXJQYWdlOzIyNjkxNzU4MTtBUzoxMDIyNjUzMjI5OTk4MDhAMTQwMTM5MzM2MTE3NA==
https://www.researchgate.net/publication/12216937_Control_of_Drosophila_paramyosinminiparamyosin_gene_expression_-_Differential_regulatory_mechanisms_for_muscle-specific_transcription?el=1_x_8&enrichId=rgreq-0b79905af78a70b7df5f3a855c4d2ed4-XXX&enrichSource=Y292ZXJQYWdlOzIyNjkxNzU4MTtBUzoxMDIyNjUzMjI5OTk4MDhAMTQwMTM5MzM2MTE3NA==
https://www.researchgate.net/publication/12216937_Control_of_Drosophila_paramyosinminiparamyosin_gene_expression_-_Differential_regulatory_mechanisms_for_muscle-specific_transcription?el=1_x_8&enrichId=rgreq-0b79905af78a70b7df5f3a855c4d2ed4-XXX&enrichSource=Y292ZXJQYWdlOzIyNjkxNzU4MTtBUzoxMDIyNjUzMjI5OTk4MDhAMTQwMTM5MzM2MTE3NA==
https://www.researchgate.net/publication/21515921_Biochemical_comparison_of_fast-_and_slow-contracting_squid_muscle?el=1_x_8&enrichId=rgreq-0b79905af78a70b7df5f3a855c4d2ed4-XXX&enrichSource=Y292ZXJQYWdlOzIyNjkxNzU4MTtBUzoxMDIyNjUzMjI5OTk4MDhAMTQwMTM5MzM2MTE3NA==
Page 12: Overexpression of miniparamyosin causes muscle dysfunction and age-dependant myofibril degeneration in the indirect flight muscles of Drosophila melanogaster

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Page 13: Overexpression of miniparamyosin causes muscle dysfunction and age-dependant myofibril degeneration in the indirect flight muscles of Drosophila melanogaster

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