Skeletal muscle transformation into electric organ in s. macrurus depends on innervation

Abstract

The cells of the electric organ, called electrocytes, of the weakly electric fish Sternopygus macrurus derive from the fusion of mature fast muscle fibers that subsequently disassemble and downregulate their sarcomeric components. Previously, we showed a reversal of the differentiated state of electrocytes to that of their muscle fiber precursors when neural input is eliminated. The dependence of the mature electrocyte phenotype on neural input led us to test the hypothesis that innervation is also critical during formation of electrocytes. We used immunohistochemical analyses to examine the regeneration of skeletal muscle and electric organ in the presence or absence of innervation. We found that blastema formation is a nerve-dependent process because regeneration was minimal when tail amputation and denervation were performed at the same time. Denervation at the onset of myogenesis resulted in the differentiation of both fast and slow muscle fibers. These were fewer in number, but in a spatial distribution similar to controls. However, in the absence of innervation, fast muscle fibers did not progress beyond the formation of closely apposed clusters, suggesting that innervation is required for their fusion and subsequent transdifferentiation into electrocytes. This study contributes further to our knowledge of the influence of innervation on cell differentiation in the myogenic lineage.

Mechanisms of muscle gene regulation in the electric organ ofSternopygus macrurus

“…Determining whether these processes are conserved in S. macrurus electrocytes and how electrocytes have exploited them to differentially suppress specific features of the muscle program provide exciting opportunities to further our understanding of the evolution of striated muscle into specialized electrogenic cells. The fact that the suppression of select muscle gene expression in mature electrocytes is reversible and depends on a continuous, high-frequency electrical activation pattern -a process that is also implicated during the transformation of skeletal muscle fibers into electrocytes during tail regeneration (Unguez and Zakon, 2002) -also emphasizes the conserved regulation of vertebrate muscle properties by the nervous system. Such progress in our understanding of how electrocytes maintain a partial muscle phenotype has invigorated a more thorough dissection of the molecular and cellular mechanisms that can independently activate or suppress specific features of the skeletal muscle program.…”

“…As the nervous system plays a major role in the maintenance and plasticity of muscle fibers in adult vertebrates, it is important to note that the EO of S. macrurus is innervated by a population of spinal motoneurons that exerts activation patterns (continuous rate of 50-200Hz) (Bennett, 1971;Mills et al, 1992) that are markedly different from those that activate muscle fibers (Bellemare et al, 1983;Coughlin and Rome, 1999). Characterization of skeletal muscle and EO properties in S. macrurus has helped establish this gymnotiform as an ideal experimental system to study the cellular mechanisms responsible for the phenotypic transformation of muscle fibers into electrocytes (Unguez and Zakon, 1998a;Unguez and Zakon, 2002) and the regulatory processes that allow electrocytes to downregulate some, but not all, components of the muscle program (Cuellar et al, 2006;Kim et al, 2004;Kim et al, 2008;Unguez and Zakon, 1998a;Unguez and Zakon, 1998b). The wide phylogenetic distribution of the MyoD family across animal taxa (Atchley et al, 1994;Zhang et al, 1999) and…”

The case for sequencing the genome of the electric eel Electrophorus electricus

“…This involved changes in the development of noncontractile electrocytes from skeletal muscle tissues (Unguez & Zakon, 1996;1998a, b;Unguez et al, 2001Unguez & Zakon, 2002). The origin of the electric organ from muscle remains poorly understood, but such understanding is a reachable goal in the near future (Zakon, 2005).…”

“…Electrocytes are not contractile, although they do retain some muscle proteins, including cytoskeletal (Mermelstein et al, 1997(Mermelstein et al, , 2000Cartaud et al, 2000), sarcomeric (Unguez & Zakon, 2002;, neuromuscular junction proteins (Asher et al, 1994) and even myogenic transcription factor proteins (Kim et al, 2004;Neville & Schmidt, 1992;Ellisman & Levinson, 1982). Electrocytes are also known to differ from myocytes in an FIG.…”

Ontogeny of the Electric Organs in the Electric Eel, Electrophorus electricus: Physiological, Histological, and Fine Structural Investigations

“…Recent experimental work on the regenerating blastema after tail amputation in Sternopygus macrurus , utilizing immunochemical antibody analysis, as reported by Zakon and Unguez [1999], Unguez and Zakon [2002], for example, seems to indicate great flexibility in myocyte or electrocyte determination in that particular species. The last mentioned authors also report a determining role of nervous innervation for electrocyte formation.…”