Reactive Oxygen Species and the Regulation of Hyperproliferation in a Colonial Hydroid

Abstract

Colonies of Podocoryna carnea circulate gastrovascular fluid among polyps via tubelike stolons. At polyp-stolon junctions, mitochondrion-rich cells in part regulate this gastrovascular flow. During competition, colonies hyperproliferate nematocytes and stolons; nematocysts are discharged until one colony is killed. Hyperproliferation then ceases, and normal growth resumes. Here, competing colonies were treated with azide, which inhibits respiration and upregulates reactive oxygen species (ROS). After the cessation of competition, azide-treated colonies continued to hyperproliferate. In azide-treated competing colonies, however, mitochondrion-rich cells were found to produce similar amounts of ROS as those in untreated competing colonies. Subsequent experiments showed that both azide treatment and competition diminished the lumen widths at polyp-stolon junctions, where mitochondrion-rich cells are found. In competing colonies, these diminished widths may also diminish the metabolic demand on these cells, causing mitochondria to enter the resting state and emit more ROS. Indeed, results with two fluorescent probes show that mitochondrion-rich cells in competing colonies produce more ROS than those in noncompeting colonies. In sum, these results suggest that competition perturbs the usual activity of mitochondrion-rich cells, altering their redox state and increasing ROS formation. Via uncharacterized pathways, these ROS may contribute to hyperproliferation.

Structure and signaling at hydroid polyp-stolon junctions, revisited

“…Given the intense metabolic demand, these myoepithelial cells become mitochondrion rich. The high levels of ROS emissions from the mitochondrion-rich cells and the sensitivity of these emissions to the food supply of the colony results in these cells becoming the locus of colony-wide redox signaling ( Blackstone, 1998b , 2001 , 2003 , 2009 ; Blackstone et al, 2004a ,b , 2005 ; Harmata and Blackstone, 2011 ).…”

Control of Hydroid Colony Form by Surface Heterogeneity

“…Podocoryna carnea was been the model organism for the study of colonial animal morphology [ 4 , 5 , 8 , 10 , 11 , 13 , 20 , 25 – 41 ]. We do not seek to replicate this considerable literature and will presume it understood that colonies do not naturally adopt a hydrorhizal network in the form of the Yale Y logo.…”