Alternative relay regulates the adenosine triphosphatase activity of Locusta migratoria striated muscle myosin.
ATPase
Locusta migratoria
alternative splicing
molecular motor
muscle
myosin
Journal
Insect science
ISSN: 1744-7917
Titre abrégé: Insect Sci
Pays: Australia
ID NLM: 101266965
Informations de publication
Date de publication:
24 Jul 2023
24 Jul 2023
Historique:
revised:
20
06
2023
received:
23
12
2022
accepted:
24
06
2023
pubmed:
25
7
2023
medline:
25
7
2023
entrez:
25
7
2023
Statut:
aheadofprint
Résumé
Locust (Locusta migratoria) has a single striated muscle myosin heavy chain (Mhc) gene, which contains 5 clusters of alternative exclusive exons and 1 differently included penultimate exon. The alternative exons of Mhc gene encode 4 distinct regions in the myosin motor domain, that is, the N-terminal SH3-like domain, one lip of the nucleotide-binding pocket, the relay, and the converter. Here, we investigated the role of the alternative regions on the motor function of locust muscle myosin. Using Sf9-baculovirus protein expression system, we expressed and purified 5 isoforms of the locust muscle myosin heavy meromyosin (HMM), including the major isoform in the thorax dorsal longitudinal flight muscle (FL1) and 4 isoforms expressed in the abdominal intersegmental muscle (AB1 to AB4). Among these 5 HMMs, FL1-HMM displayed the highest level of actin-activated adenosine triphosphatase (ATPase) activity (hereafter referred as ATPase activity). To identify the alternative region(s) responsible for the elevated ATPase activity of FL1-HMM, we produced a number of chimeras of FL1-HMM and AB4-HMM. Substitution with the relay of AB4-HMM (encoded by exon-14c) substantially decreased the ATPase activity of FL1-HMM, and conversely, the relay of FL1-HMM (encoded by exon-14a) enhanced the ATPase activity of AB4-HMM. Mutagenesis showed that the exon-14a-encoded residues Gly
Identifiants
pubmed: 37489033
doi: 10.1111/1744-7917.13257
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : National Natural Science Foundation of China
ID : 31672359
Organisme : National Natural Science Foundation of China
ID : 31970657
Organisme : State Key Laboratory of Integrated Management of Pest Insects and Rodents
ID : IPM1601
Informations de copyright
© 2023 Institute of Zoology, Chinese Academy of Sciences.
Références
Bernstein, S.I. and Milligan, R.A. (1997) Fine tuning a molecular motor: the location of alternative domains in the Drosophila myosin head. Journal of Molecular Biology, 271, 1-6.
Bloemink, M.J., Dambacher, C.M., Knowles, A.F., Melkani, G.C., Geeves, M.A. and Bernstein, S.I. (2009) Alternative exon 9-encoded relay domains affect more than one communication pathway in the Drosophila myosin head. Journal of Molecular Biology, 389, 707-721.
Bloemink, M.J., Melkani, G.C., Bernstein, S.I. and Geeves, M.A. (2016) The relay/converter interface influences hydrolysis of ATP by skeletal muscle myosin II. Journal of Biological Chemistry, 291, 1763-1773.
Caldwell, J.T., Mermelstein, D.J., Walker, R.C., Bernstein, S.I. and Huxford, T. (2020) X-ray crystallographic and molecular dynamic analyses of Drosophila melanogaster embryonic muscle myosin define domains responsible for isoform-specific properties. Journal of Molecular Biology, 432, 427-447.
Fischer, S., Windshugel, B., Horak, D., Holmes, K.C. and Smith, J.C. (2005) Structural mechanism of the recovery stroke in the myosin molecular motor. Proceedings of the National Academy of Sciences USA, 102, 6873-6878.
Foth, B.J., Goedecke, M.C. and Soldati, D. (2006) New insights into myosin evolution and classification. Proceedings of the National Academy of Sciences USA, 103, 3681-3686.
George, E.L., Ober, M.B. and Emerson, Jr., C.P. (1989) Functional domains of the Drosophila melanogaster muscle myosin heavy-chain gene are encoded by alternatively spliced exons. Molecular and Cellular Biology, 9, 2957-2974.
Himmel, D.M., Gourinath, S., Reshetnikova, L., Shen, Y., Szent-Gyorgyi, A.G. and Cohen, C. (2002) Crystallographic findings on the internally uncoupled and near-rigor states of myosin: further insights into the mechanics of the motor. Proceedings of the National Academy of Sciences USA, 99, 12645-12650.
Hooper, S.L. and Thuma, J.B. (2005) Invertebrate muscles: muscle specific genes and proteins. Physiological Reviews, 85, 1001-1060.
Kodama, T., Fukui, K. and Kometani, K. (1986) The initial phosphate burst in ATP hydrolysis by myosin and subfragment-1 as studied by a modified malachite green method for determination of inorganic phosphate. Journal of Biochemistry, 99, 1465-1472.
Kovacs, M., Toth, J., Hetenyi, C., Malnasi-Csizmadia, A. and Sellers, J.R. (2004) Mechanism of blebbistatin inhibition of myosin II. Journal of Biological Chemistry, 279, 35557-35563.
Kronert, W.A., Dambacher, C.M., Knowles, A.F., Swank, D.M. and Bernstein, S.I. (2008) Alternative relay domains of Drosophila melanogaster myosin differentially affect ATPase activity, in vitro motility, myofibril structure and muscle function. Journal of Molecular Biology, 379, 443-456.
Kronert, W.A., Melkani, G.C., Melkani, A. and Bernstein, S.I. (2010) Mutating the converter-relay interface of Drosophila myosin perturbs ATPase activity, actin motility, myofibril stability and flight ability. Journal of Molecular Biology, 398, 625-632.
Kronert, W.A., Melkani, G.C., Melkani, A. and Bernstein, S.I. (2012) Alternative relay and converter domains tune native muscle myosin isoform function in Drosophila. Journal of Molecular Biology, 416, 543-557.
Kronert, W.A., Melkani, G.C., Melkani, A. and Bernstein, S.I. (2014) Mapping interactions between myosin relay and converter domains that power muscle function. Journal of Biological Chemistry, 289, 12779-12790.
Li, J., Lu, Z., He, J., Chen, Q., Wang, X., Kang, L. et al. (2016) Alternative exon-encoding regions of Locusta migratoria muscle myosin modulate the pH dependence of ATPase activity. Insect Molecular Biology, 25, 689-700.
Li, X.D., Rhodes, T.E., Ikebe, R., Kambara, T., White, H.D. and Ikebe, M. (1998) Effects of mutations in the gamma-phosphate binding site of myosin on its motor function. Journal of Biological Chemistry, 273, 27404-27411.
Liu, C., Hao, J., Yao, L.L., Wei, M., Chen, W., Yang, Q. et al. (2022) Insect Sf9 cells are suitable for functional expression of insect, but not vertebrate, striated muscle myosin. Biochemical and Biophysical Research Communications, 635, 259-266.
Miller, B.M., Bloemink, M.J., Nyitrai, M., Bernstein, S.I. and Geeves, M.A. (2007) A variable domain near the ATP-binding site in Drosophila muscle myosin is part of the communication pathway between the nucleotide and actin-binding sites. Journal of Molecular Biology, 368, 1051-1066.
Mooseker, M.S. and Foth, B.J. (2008) The structural and functional diversity of the myosin family of actin-based molecular motors. In: Myosins: A Superfamily of Molecular Motors (ed. L.M. Coluccios), pp. 35-54. Springer, The Netherlands.
Odronitz, F. and Kollmar, M. (2008) Comparative genomic analysis of the arthropod muscle myosin heavy chain genes allows ancestral gene reconstruction and reveals a new type of ‘partially’ processed pseudogene. BMC Molecular Biology, 9, 21.
Pfluger, H.J. and Duch, C. (2011) Dynamic neural control of insect muscle metabolism related to motor behavior. Physiology (Bethesda), 26, 293-303.
Ramanath, S., Wang, Q., Bernstein, S.I. and Swank, D.M. (2011) Disrupting the myosin converter-relay interface impairs Drosophila indirect flight muscle performance. Biophysical Journal, 101, 1114-1122.
Snelling, E.P., Matthews, P.G. and Seymour, R.S. (2012a) Allometric scaling of discontinuous gas exchange patterns in the locust Locusta migratoria throughout ontogeny. Journal of Experimental Biology, 215, 3388-3393.
Snelling, E.P., Seymour, R.S., Matthews, P.G. and White, C.R. (2012b) Maximum metabolic rate, relative lift, wingbeat frequency and stroke amplitude during tethered flight in the adult locust Locusta migratoria. Journal of Experimental Biology, 215, 3317-3323.
Snelling, E.P., Seymour, R.S., Runciman, S., Matthews, P.G. and White, C.R. (2012c) Symmorphosis and the insect respiratory system: a comparison between flight and hopping muscle. Journal of Experimental Biology, 215, 3324-3333.
Swank, D.M., Bartoo, M.L., Knowles, A.F., Iliffe, C., Bernstein, S.I., Molloy, J.E. et al. (2001) Alternative exon-encoded regions of Drosophila myosin heavy chain modulate ATPase rates and actin sliding velocity. Journal of Biological Chemistry, 276, 15117-15124.
Swank, D.M., Knowles, A.F., Kronert, W.A., Suggs, J.A., Morrill, G.E., Nikkhoy, M. et al. (2003) Variable N-terminal regions of muscle myosin heavy chain modulate ATPase rate and actin sliding velocity. Journal of Biological Chemistry, 278, 17475-17482.
Tyska, M.J. and Warshaw, D.M. (2002) The myosin power stroke. Cell Motility and the Cytoskeleton, 51, 1-15.
Wang, F., Harvey, E.V., Conti, M.A., Wei, D. and Sellers, J.R. (2000) A conserved negatively charged amino acid modulates function in human nonmuscle myosin IIA. Biochemistry, 39, 5555-5560.
Yang, C., Ramanath, S., Kronert, W.A., Bernstein, S.I., Maughan, D.W. and Swank, D.M. (2008) Alternative versions of the myosin relay domain differentially respond to load to influence Drosophila muscle kinetics. Biophysical Journal, 95, 5228-5237.
Zhang, S. and Bernstein, S.I. (2001) Spatially and temporally regulated expression of myosin heavy chain alternative exons during Drosophila embryogenesis. Mechanisms of Development, 101, 35-45.