Redox signaling in colonial hydroids: many pathways for peroxide

Abstract

Studies of mitochondrial redox signaling predict that the colonial hydroids Eirene viridula and Podocoryna carnea should respond to manipulations of reactive oxygen species (ROS). Both species encrust surfaces with feeding polyps connected by networks of stolons; P. carnea is more 'sheet-like' with closely spaced polyps and short stolons, while E. viridula is more 'runner-like' with widely spaced polyps and long stolons. Treatment with the chemical antioxidant vitamin C diminishes ROS in mitochondrion-rich epitheliomuscular cells (EMCs) and produces phenotypic effects (sheet-like growth) similar to uncouplers of oxidative phosphorylation. In peripheral stolon tips, treatment with vitamin C triggers a dramatic increase of ROS that is followed by tissue death and stolon regression. The enzymatic anti-oxidant catalase is probably not taken up by the colony but, rather, converts hydrogen peroxide in the medium to water and oxygen. Exogenous catalase does not affect ROS in mitochondrion-rich EMCs, but does increase the amounts of ROS emitted from peripheral stolons, resulting in rapid, runner-like growth. Treatment with exogenous hydrogen peroxide increases ROS levels in stolon tips and results in somewhat faster colony growth. Finally, untreated colonies of E. viridula exhibit higher levels of ROS in stolon tips than untreated colonies of P. carnea. ROS may participate in a number of putative signaling pathways: (1) high levels of ROS may trigger cell and tissue death in peripheral stolon tips; (2) more moderate levels of ROS in stolon tips may trigger outward growth, inhibit branching and, possibly, mediate the redox signaling of mitochondrion-rich EMCs; and (3) ROS may have an extra-colony function, perhaps in suppressing the growth of bacteria.

Type and cellular location of reactive oxygen species determine activation or suppression of programmed cell death in Arabidopsis suspension cultures

“…8 The fact that ascorbate and glutathione are not specific in the forms of ROS that they scavenge, but that catalase specifically scavenges hydrogen peroxide (H 2 O 2 ) only, 9 may explain their different effects on AL-PCD induction. Additionally, catalase is a large tetramer of 350 kDa that cannot diffuse across cell membranes 10 and so its effects must have been extracellular, while ascorbate and glutathione are small molecules that may have entered the cells themselves and affected the intracellular redox status. By reducing levels of toxic ROS, ascorbate and glutathione treatments may have reduced cellular stress levels, allowing the cells to initiate AL-PCD during the heat treatment, rather than experiencing uncontrolled necrotic death, which occurs during high stress exposure.…”

Causes and consequences of stolon regression in a colonial hydroid

“…Colonies treated with exogenous vitamin C exhibit stolon regression as well as elevated levels of ROS and RNS in stolon tips (Blackstone et al, 2004;Blackstone et al, 2005;Cherry Vogt et al, 2008). However, in colonies treated with the caspase inhibitor, z-DEVDfmk, ROS levels are suppressed (Fig.3A-F).…”

“…Treatment with exogenous peroxide at low concentrations (20-50moll -1 ) has no effect on colony morphology (Blackstone et al, 2005). At higher concentrations (5mmoll -1 ), treatment with peroxide has been shown to trigger high rates of stolon regression (Cherry Vogt et al, 2008).…”

“…When stolon regression was induced using vitamin C (Blackstone et al, 2005), the poly-caspase inhibitor z-DEVD-fmk [benzyloxycarbonyl-Asp(OMe)-Glu(OMe)-ValAsp(OMe)-fluoromethylketone; BioVision, Inc., Mountain View, CA, USA] was used. This inhibitor is thought to affect caspases 3 and 7 and possibly caspases 6, 8 and 9 as well (Duval et al, 2002;Fahy et al, 1999).…”

“…Colonies were treated with a 2moll -1 solution of z-DEVD-fmk and seawater. Vitamin C in seawater adjusted to pH8 was then added to a final concentration of 100moll -1 and the colonies were incubated for 1h (Blackstone et al, 2005). Following the addition of a fluorescent probe for detecting peroxide [2Ј,7Ј-dichlorodihydrofluorescein diacetate (H 2 DCFDA); Molecular Probes, Eugene, OR, USA], colonies were incubated for an additional hour before imaging three stolon tips per colony.…”