Pigment Translocation in Caridean Shrimp Chromatophores: Receptor Type, Signal Transduction, Second Messengers, and Cross Talk Among Multiple Signaling Cascades

Abstract

Pigment aggregation in shrimp chromatophores is triggered by red pigment concentrating hormone (RPCH), a neurosecretory peptide whose plasma membrane receptor may be a G-protein coupled receptor (GPCR). While RPCH binding activates the Ca /cGMP signaling cascades, a role for cyclic AMP (cAMP) in pigment aggregation is obscure, as are the steps governing Ca release from the smooth endoplasmic reticulum (SER). A role for the antagonistic neuropeptide, pigment dispersing homone (α-PDH) is also unclear. In red, ovarian chromatophores from the freshwater shrimp Macrobrachium olfersi, we show that a G-protein antagonist (AntPG) strongly inhibits RPCH-triggered pigment aggregation, suggesting that RPCH binds to a GPCR, activating an inhibitory G-protein. Decreasing cAMP levels may cue pigment aggregation, since cytosolic cAMP titers, when augmented by cholera toxin, forskolin or vinpocentine, completely or partially impair pigment aggregation. Triggering opposing Ca /cGMP and cAMP cascades by simultaneous perfusion with lipid-soluble cyclic nucleotide analogs induces a "tug-of-war" response, pigments aggregating in some chromatosomes with unpredictable, oscillatory movements in others. Inhibition of cAMP-dependent protein kinase accelerates aggregation and reduces dispersion velocities, suggesting a role in phosphorylation events, possibly regulating SER Ca release and pigment aggregation. The second messengers IP and cADPR do not stimulate SER Ca release. α-PDH does not sustain pigment dispersion, suggesting that pigment translocation in caridean chromatophores may be regulated solely by RPCH, since PDH is not required. We propose a working hypothesis to further unravel key steps in the mechanisms of pigment translocation within crustacean chromatophores that have remained obscure for nearly a century.

Characterisation and pharmacological analysis of a crustacean G protein-coupled receptor: the red pigment-concentrating hormone receptor of Daphnia pulex

“…Despite the paucity of information on crustacean RPCHR sequences, the RPCH signalling cascade has been investigated in several decapod crustacean species on a physiological and biochemical level 30 . From one such recent investigation with a G-protein antagonist, it was experimentally deduced that Panbo-RPCH lowers cAMP levels in ovarian chromatophores of the freshwater shrimp, Macrobrachium olfersi 31 . In insects on the other hand, the AKHs seem to increase intracellular Ca 2+ and cAMP levels 32 .…”

Rapid colour changes inEuglena sanguinea(Euglenophyceae) caused by internal lipid globule migration

“…There is reference to migration of pigmented globules in microalgae in old observations on Euglena sanguinea (Heidt, 1934). Analogous observations have been made in animal cells, such as in the chromatophores of crustaceans, where the mechanism of pigmented bodies transport has been better studied (Boyle & McNamara, 2005;Fuhrmann et al, 2011;Milograna et al, 2016). Moreover, Ast has been reported to be the pigment responsible for the colour in Antarctic krill (Auerswald et al, 2008).…”

“…This mechanism allows E. sanguinea neustonic colonies to deal with daily changes in irradiance but also with more rapid variations caused by cloudiness or shading by riparian vegetation. Although similar mechanisms of intracellular pigmented organelles migration have been studied in specialised colour changing cells (chromatophores or melanophores) in animals such as amphibians, reptiles or shrimps (Immerstrand et al, 2007;Milograna et al, 2016), to our knowledge in phototrophs, a similar process has been only described in H. lacustris,…”

A Crab Is Not a Fish: Unique Aspects of the Crustacean Endocrine System and Considerations for Endocrine Toxicology

“…In this model, RPCH activates cyclic guanosine monophosphate (cGMP) and Ca 2+ second messenger cascades, which in turn stimulate a protein kinase to phosphorylate a myosin II molecular motor. As a result, pigment aggregation is effectuated by the movement of pigment granules along actin filaments in the chromatophore [for details see ( 198 , 218 )]. More recently, highly specific RPCH receptors (RPCHR) have been cloned and functionally deorphanized in D. pulex and C. maenas ( 83 , 210 ).…”