TY - JOUR
T1 - Functional divergence of the sarcomeric myosin, MYH7b, supports species-specific biological roles
AU - Lee, Lindsey A.
AU - Barrick, Samantha K.
AU - Meller, Artur
AU - Walklate, Jonathan
AU - Lotthammer, Jeffrey M.
AU - Tay, Jian Wei
AU - Stump, W. Tom
AU - Bowman, Gregory
AU - Geeves, Michael A.
AU - Greenberg, Michael J.
AU - Leinwand, Leslie A.
N1 - Funding Information:
This work was supported by the National Institutes of Health (NIH grant R01GM029090; to L. A. Leinwand), NIH fellowship (grant no.: F31DC017927; to L. A. Lee), and the NIH grant (R01HL141086; to M. G.). M. A. G. was supported by the European Union Horizon 2020 grant (grant no.: 777204 SILICO; to F. C. M.). J. M. L. was supported by the National Science Foundation via grant number DGE-2139839. G. R. B. was funded by National Science Foundation CAREER Award (MCB-1552471) and NIH grants R01GM124007 and RF1AG067194. G. R. B. holds a Packard Fellowship for Science and Engineering from The David & Lucile Packard Foundation. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH, the National Science Foundation, or the European Commission.
Funding Information:
We thank Dr Angela Peter and Dr Anastasia Karabina for supplying python tissue and preparing the protein gel for mass spectrometry. We thank Dr Monika Dzieciatkowska and the University of Colorado School of Medicine Biological Mass Spectrometry Proteomics Core Facility for their mass spectrometry services. We thank the BioFrontiers Institute Advanced Light Microscopy Core for use of microscopy equipment and for imaging support. L. A. Lee, M. J. G. and L. A. Leinwand conceptualization; A. M. J. M. L. and M. A. G. methodology; J. W. T. software; L. A. Lee, S. K. B. A. M. J. M. L. and W. T. S. formal analysis; L. A. Lee, S. K. B. A. M. J. W. J. M. L. and W. T. S. investigation; W. T. S. and M. A. G. resources; A. M. and J. M. L. data curation; L. A. Lee and S. K. B. writing–original draft; L. A. Lee, S. K. B. A. M. J. W. J. M. L. J. W. T. W. T. S. M. A. G. M. J. G. and L. A. Leinwand writing–review and editing; L. A. Lee, S. K. B. A. M. and J. M. L. visualization; G. B. M. A. G. M. J. G. and L. A. Leinwand supervision; G. B. M. A. G. M. J. G. and L. A. Leinwand funding acquisition. This work was supported by the National Institutes of Health (NIH grant R01GM029090; to L. A. Leinwand), NIH fellowship (grant no.: F31DC017927; to L. A. Lee), and the NIH grant (R01HL141086; to M. G.). M. A. G. was supported by the European Union Horizon 2020 grant (grant no.: 777204 SILICO; to F. C. M.). J. M. L. was supported by the National Science Foundation via grant number DGE-2139839. G. R. B. was funded by National Science Foundation CAREER Award (MCB-1552471) and NIH grants R01GM124007 and RF1AG067194. G. R. B. holds a Packard Fellowship for Science and Engineering from The David & Lucile Packard Foundation. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH, the National Science Foundation, or the European Commission.
Publisher Copyright:
© 2022 The Authors
PY - 2023/1
Y1 - 2023/1
N2 - Myosin heavy chain 7b (MYH7b) is an evolutionarily ancient member of the sarcomeric myosin family, which typically supports striated muscle function. However, in mammals, alternative splicing prevents MYH7b protein production in cardiac and most skeletal muscles and limits expression to a subset of specialized muscles and certain nonmuscle environments. In contrast, MYH7b protein is abundant in python cardiac and skeletal muscles. Although the MYH7b expression pattern diverges in mammals versus reptiles, MYH7b shares high sequence identity across species. So, it remains unclear how mammalian MYH7b function may differ from that of other sarcomeric myosins and whether human and python MYH7b motor functions diverge as their expression patterns suggest. Thus, we generated recombinant human and python MYH7b protein and measured their motor properties to investigate any species-specific differences in activity. Our results reveal that despite having similar working strokes, the MYH7b isoforms have slower actin-activated ATPase cycles and actin sliding velocities than human cardiac β-MyHC. Furthermore, python MYH7b is tuned to have slower motor activity than human MYH7b because of slower kinetics of the chemomechanical cycle. We found that the MYH7b isoforms adopt a higher proportion of myosin heads in the ultraslow, super-relaxed state compared with human cardiac β-MyHC. These findings are supported by molecular dynamics simulations that predict MYH7b preferentially occupies myosin active site conformations similar to those observed in the structurally inactive state. Together, these results suggest that MYH7b is specialized for slow and energy-conserving motor activity and that differential tuning of MYH7b orthologs contributes to species-specific biological roles.
AB - Myosin heavy chain 7b (MYH7b) is an evolutionarily ancient member of the sarcomeric myosin family, which typically supports striated muscle function. However, in mammals, alternative splicing prevents MYH7b protein production in cardiac and most skeletal muscles and limits expression to a subset of specialized muscles and certain nonmuscle environments. In contrast, MYH7b protein is abundant in python cardiac and skeletal muscles. Although the MYH7b expression pattern diverges in mammals versus reptiles, MYH7b shares high sequence identity across species. So, it remains unclear how mammalian MYH7b function may differ from that of other sarcomeric myosins and whether human and python MYH7b motor functions diverge as their expression patterns suggest. Thus, we generated recombinant human and python MYH7b protein and measured their motor properties to investigate any species-specific differences in activity. Our results reveal that despite having similar working strokes, the MYH7b isoforms have slower actin-activated ATPase cycles and actin sliding velocities than human cardiac β-MyHC. Furthermore, python MYH7b is tuned to have slower motor activity than human MYH7b because of slower kinetics of the chemomechanical cycle. We found that the MYH7b isoforms adopt a higher proportion of myosin heads in the ultraslow, super-relaxed state compared with human cardiac β-MyHC. These findings are supported by molecular dynamics simulations that predict MYH7b preferentially occupies myosin active site conformations similar to those observed in the structurally inactive state. Together, these results suggest that MYH7b is specialized for slow and energy-conserving motor activity and that differential tuning of MYH7b orthologs contributes to species-specific biological roles.
KW - actin
KW - cardiac muscle
KW - interacting heads motif
KW - kinetics
KW - molecular motor
KW - myosin
KW - skeletal muscle
KW - structure–function
KW - super-relaxed state
UR - http://www.scopus.com/inward/record.url?scp=85144609242&partnerID=8YFLogxK
U2 - 10.1016/j.jbc.2022.102657
DO - 10.1016/j.jbc.2022.102657
M3 - Article
C2 - 36334627
AN - SCOPUS:85144609242
SN - 0021-9258
VL - 299
JO - Journal of Biological Chemistry
JF - Journal of Biological Chemistry
IS - 1
M1 - 102657
ER -