Energy transport and cell polarity: Relationship of phosphagen kinase activity to sperm function

Abstract

The energy required for motility of sea urchin sperm is transported from the mitochondrion to the flagellum by a phosphocreatine shuttle involving diffusion of phosphocreatine (PCr) between isozymes of creatine kinase (CrK) localized at the two sites (Tombes and Shapiro, Cell, 41:325, '85; Tombes et al., Biophys. J., 52:75, '87). The present studies demonstrate that high sperm CrK (various echinoderms; sea squirt, bristle worm, salmon) or arginine kinase (molusc, barnacle, moth) activity is seen in several species with sperm of a primitive morphology (mitochondrion at the base of the head, relatively long flagellum). In contrast, CrK activity is 10-100-fold less abundant in sperm of other species (frog, mouse, rooster, rabbit, bull, and human) that either possess a modified morphology (mitochondria that extend along the flagellum) and/or utilize glycolytic metabolism. We interpret these findings as support for the use of phosphagen kinase-dependent energy transport in cells in which the production of adenosine triphosphate (ATP) by the mitochondrion is distant from its utilization, leading to a form of metabolic polarization. Two other cell types, frog photoreceptors and rabbit oviduct cells, whose morphology and function also suggest that they exhibit metabolic polarization, contain relatively high CrK activity. The presence of high phosphagen kinase activity in metabolically polarized gametes and somatic cells further substantiates the role of such enzymes in facilitating energy transport.

Arginine kinase in the demosponge Suberites domuncula:regulation of its expression and catalytic activity by silicic acid

“…The phosphagen kinases are localized at the sites of ATP hydrolysis and/or synthesis, allowing a temporal and spatial ATP buffer system as well as a tuned regulation of the intracellular phosphate concentration (reviewed in Ellington, 2001). In the present study the arginine kinase activity in S. domuncula was determined to be approximately 2.5·nmol·ATP·generated min -1 ·10·µg -1 ·protein, a value that is within the range of arginine and creatine kinase activities measured in the primitive-type sperm of certain marine invertebrates (Tombes and Shapiro, 1989).…”

ATP distribution and localization of mitochondria in Suberites domuncula (Olivi 1792) tissue

“…The AK reaction (and likely CK reaction) functions as a spatial ATP buffering system and is present in other polarized cells such as spermatozoa (Tombes et al, 1985). The presence of MtCK and FlgCK in primitive type sperm was described by Tombes and Shapiro (Tombes and Shapiro, 1989) whereas the potential roles of MtCK and protoflgCK in mediation of the spatial ATP buffering energy transport pathway were proposed by Suzuki and Ellington (Suzuki and Ellington, 2008). The spatial ATP buffering by the CK/PCr system in spermatozoa and sponge choanocytes confirms that the sponge spermatozoa develop from choanocytes during gametogenesis (Kaye and Reiswig, 1991).…”

The phosphocreatine shuttle of sea urchin sperm: flagellar creatine kinase resulted from a gene triplication.

“…1 (24,25). This situation may have arisen from an early duplication of a primordial phosphagen kinase, which then diverged into creatine and arginine kinases.…”

“…The high molecular weight form of CK is found in sperm from all echinoderms (24,25) ison, the percent identity to the human isozymes ofCK is also presented (32)(33)(34). It is noteworthy that while even the human brain and muscle isoforms are 80%6 identical, no two domains of TCK share more than 72% identity.…”