Evolution of the regulatory control of vertebrate striated muscle: the roles of troponin I and myosin binding protein-C.
Troponin I (TnI) and myosin binding protein-C (MyBP-C) are key regulatory proteins of contractile function in vertebrate muscle. TnI modulates the Ca(2+) activation signal, while MyBP-C regulates cross-bridge cycling kinetics. In vertebrates, each protein is distributed as tissue-specific paralogs in fast skeletal (fs), slow skeletal (ss), and cardiac (c) muscles. The purpose of this study is to characterize how TnI and MyBP-C have changed during the evolution of vertebrate striated muscle and how tissue-specific paralogs have adapted to different physiological conditions. To accomplish this we have completed phylogenetic analyses using the amino acid sequences of all known TnI and MyBP-C isoforms. This includes 99 TnI sequences (fs, ss, and c) from 51 different species and 62 MyBP-C sequences from 26 species, with representatives from each vertebrate group. Results indicate that the role of protein kinase A (PKA) and protein kinase C (PKC) in regulating contractile function has changed during the evolution of vertebrate striated muscle. This is reflected in an increased number of phosphorylatable sites in cTnI and cMyBP-C in endothermic vertebrates and the loss of two PKC sites in fsTnI in a common ancestor of mammals, birds, and reptiles. In addition, we find that His(132), Val(134), and Asn(141) in human ssTnI, previously identified as enabling contractile function during cellular acidosis, are present in all vertebrate cTnI isoforms except those from monotremes, marsupials, and eutherian mammals. This suggests that the replacement of these residues with alternative residues coincides with the evolution of endothermy in the mammalian lineage.
Shaffer
Justin F
JF
Department of Bioengineering, University of Washington, Seattle, Washington, USA.
Gillis
Todd E
TE
D000595:Amino Acid Sequence; D000818:Animals; D001717:Birds; D002352:Carrier Proteins / Q000235:genetics / Q000378:metabolism / Q000502:physiology*; D019143:Evolution, Molecular; D006801:Humans; D008322:Mammals; D008394:Marsupialia; D008969:Molecular Sequence Data; D009007:Monotremata; D009119:Muscle Contraction / Q000235:genetics / Q000502:physiology; D054792:Muscle, Striated / Q000378:metabolism*; D010802:Phylogeny; D012045:Regulatory Sequences, Nucleic Acid / Q000235:genetics*; D012104:Reptiles; D017386:Sequence Homology, Amino Acid; D019210:Troponin I / Q000235:genetics / Q000378:metabolism / Q000502:physiology*; D014714:Vertebrates / Q000235:genetics*; D000099163:Myosin Binding Protein C
D002352:Carrier Proteins; D019210:Troponin I; D000099163:Myosin Binding Protein C