Invertebrate troponin: Insights into the evolution and regulation of striated muscle contraction

Abstract

The troponin complex plays a central role in regulating the contraction and relaxation of striated muscles. Among the three protein subunits of troponin, the calcium receptor subunit, TnC, belongs to the calmodulin family of calcium signaling proteins whereas the inhibitory subunit, TnI, and tropomyosin-binding/thin filament-anchoring subunit, TnT, are striated muscle-specific regulatory proteins. TnI and TnT emerged early in bilateral symmetric invertebrate animals and have coevolved during the 500-700 million years of muscle evolution. To understand the divergence as well as conservation of the structures of TnI and TnT in invertebrate and vertebrate organisms adds novel insights into the structure-function relationship of troponin and the muscle type isoforms of TnI and TnT. Based on the significant growth of genomic database of multiple species in the past decade, this focused review studied the primary structure features of invertebrate troponin subunits in comparisons with the vertebrate counterparts. The evolutionary data demonstrate valuable information for a better understanding of the thin filament regulation of striated muscle contractility in health and diseases.

The glutamic acid-rich–long C-terminal extension of troponin T has a critical role in insect muscle functions

“…TnT is encoded by a single gene in insects [6]. A significantly diverged structure of insect TnT is the Glu-rich long C-terminal extension [11].…”

“…Troponin emerged during early animal evolution approximately 700 million years ago. Genes encoding the subunits of troponin are found in all invertebrate animals higher than Cnidaria (jellyfish and sponges) [6]. This phylogenetic chronicle corresponds to the emergence of central nervous system [7], implying an essential role of troponin in the more coordinated muscle contractions of higher animal species.…”

“…By interaction with tropomyosin in the thin filament, TnT plays an organizer role in the center of the sarcomeric Ca 2+ regulatory system [8]. Vertebrates have evolved with three homologous genes encoding the cardiac, fast and slow skeletal muscle type isoforms of TnT, while most invertebrates such as insects have only a single TnT gene [6]. Gene structure and molecular evolution studies identified the fast skeletal muscle TnT as the ancestral form of the three vertebrate muscle type-specific isoforms [9].…”

“…The presence of the mutually exclusive alternative exon 10A or 10B produced different binding affinities for tropomyosin and TnC (Fig. 4), indicating functional impacts of this alternatively spliced segment of TnT, which are under investigation together with vertebrate counterparts, exon 16 and exon 17, in fast TnT [5,6].…”

Evolution of Flight Muscle Contractility and Energetic Efficiency

“…Many of their anatomic and physiologic similarities reflect the adaptation to common selective pressures such as high power output with energetic efficiency for sustainable flights. On the other hand, the unique properties of insect, avian, and bat flight muscles such as resting sarcomere length, passive stiffness, and the mode of Ca 2+ -activated or stretch-activated contractions indicate adaptations to specific selective pressures for a particular type of flight activity ( Cutts, 1986 ; Cao et al, 2019 ).…”