Influences of thermal acclimation and acute temperature change on the motility of epithelial wound-healing cells (keratocytes) of tropical,temperate and Antarctic fish

Abstract

SUMMARYThe ability to heal superficial wounds is an important element in an organism's repertoire of adaptive responses to environmental stress. In fish,motile cells termed keratocytes are thought to play important roles in the wound-healing process. Keratocyte motility, like other physiological rate processes, is likely to be dependent on temperature and to show adaptive variation among differently thermally adapted species. We have quantified the effects of acute temperature change and thermal acclimation on actin-based keratocyte movement in primary cultures of keratocytes from four species of teleost fish adapted to widely different thermal conditions: two eurythermal species, the longjaw mudsucker Gillichthys mirabilis (environmental temperature range of approximately 10-37°C) and a desert pupfish, Cyprinodon salinus (10-40°C), and two species from stable thermal environments, an Antarctic notothenioid, Trematomus bernacchii(-1.86°C), and a tropical clownfish, Amphiprion percula(26-30°C). For all species, keratocyte speed increased with increasing temperature. G. mirabilis and C. salinus keratocytes reached maximal speeds at 25°C and 35°C, respectively, temperatures within the species' normal thermal ranges. Keratocytes of the stenothermal species continued to increase in speed as temperature increased above the species'normal temperature ranges. The thermal limits of keratocyte motility appear to exceed those of whole-organism thermal tolerance, notably in the case of T. bernacchii. Keratocytes of T. bernacchii survived supercooling to -6°C and retained motility at temperatures as high as 20°C. Mean keratocyte speed was conserved at physiological temperatures for the three temperate and tropical species, which suggests that a certain rate of motility is advantageous for wound healing. However, there was no temperature compensation in speed of movement for keratocytes of the Antarctic fish, which have extremely slow rates of movement at physiological temperatures. Keratocytes from all species moved in a persistent,unidirectional manner at low temperatures but at higher temperatures began to take more circular or less-persistent paths. Thermal acclimation affected the persistence and turning magnitude of keratocytes, with warmer acclimations generally yielding more persistent cells that followed straighter paths. However, acclimation did not alter the effect of experimental temperature on cellular speed. These findings suggest that more than one temperature-sensitive mechanism may govern cell motility: the rate-limiting process(es) responsible for speed is distinct from the mechanism(s) underlying directionality and persistence. Keratocytes represent a useful study system for evaluating the effects of temperature at the cellular level and for studying adaptive variation in actin-based cellular movement and capacity for wound healing.

Hypothermia-Associated Loss of Dendritic Spines

“…However, studies on cellular dynamics have shown that actin-dependent motility, resulting in significant changes in cell morphology, is strongly attenuated at reduced temperatures, with a Q 10 of ϳ4 ranging from 29 to 39°C (Hartmann-Petersen et al, 2000). Similar values have been recorded for epithelial cells from various teleosts (Ream et al, 2003).…”

“…A possible explanation for this striking difference in cold sensitivity lies in the contrast in cytoskeletal structure between the dendritic spine, which is based on filamentous actin, and the dendrite shaft where microtubules predominate (Matus et al, 1982;Halpain, 2000;Kaech et al, 2001). The high content of dynamic actin filaments in dendritic spines not only drives their high motility (Fischer et al, 1998) but also renders them sensitive to the low temperature, which inhibits actin filament dynamics resulting in reduced cell motility (Pollard, 1976;HartmannPetersen et al, 2000;Ream et al, 2003).…”

Polarization and Movement of Keratocytes: A Multiscale Modelling Approach

“…A paradigm system for actin based cell motility is the fish epidermal keratocyte Ream et al, 2003), a cell that moves smoothly, (with speed circa 0.25 µm/s (Laurent et al, 2005)) while retaining a typical crescent shape. This mode of cell motion is not restricted to keratocytes, as other cell lineages can present this behaviour as well (see Discussion).…”

Influence of Incision Location on Transmitter Loss, Healing, Incision Lengths, Suture Retention, and Growth of Juvenile Chinook Salmon

“…However, as temperature increases, the rate of responses accelerates (Roberts 1989). For example, Ream et al (2003) showed that as temperature increased, so did the motility of epithelial wound-healing cells (keratocytes), which migrate across wounded areas to inhibit infection (Radice 1980a(Radice , 1980bEuteneuer and Schliwa 1984). Anderson and Roberts (1975) found the White Cloud Mountain minnow (Tanichthyes albonubes) experimentally wounded (2-4 mm long, 0.6-1 mm deep) with a scalpel healed more quickly when held at elevated temperatures than the Atlantic salmon (Salmo salar) held at lower temperatures.…”