Signal transduction, plasma membrane calcium movements, and pigment translocation in freshwater shrimp chromatophores.
Crustacean color change results from the differential translocation of chromatophore pigments, regulated by neurosecretory peptides like red pigment concentrating hormone (RPCH) that, in the red ovarian chromatophores of the freshwater shrimp Macrobrachium olfersi, triggers pigment aggregation via increased cytosolic cGMP and Ca(2+) of both smooth endoplasmatic reticulum (SER) and extracellular origin. However, Ca(2+) movements during RPCH signaling and the mechanisms that regulate intracellular [Ca(2+)] are enigmatic. We investigate Ca(2+) transporters in the chromatophore plasma membrane and Ca(2+) movements that occur during RPCH signal transduction. Inhibition of the plasma membrane Ca(2+)-ATPase by La(3+) and indirect inhibition of the Na(+)/Ca(2+) exchanger by ouabain induce pigment aggregation, revealing a role for both in Ca(2+) extrusion. Ca(2+) channel blockade by La(3+) or Cd(2+) strongly inhibits slow-phase RPCH-triggered aggregation during which pigments disperse spontaneously. L-type Ca(2+) channel blockade by gabapentin markedly reduces rapid-phase translocation velocity; N- or P/Q-type blockade by ω-conotoxin MVIIC strongly inhibits RPCH-triggered aggregation and reduces velocity, effects revealing RPCH-signaled influx of extracellular Ca(2+). Plasma membrane depolarization, induced by increasing external K(+) from 5 to 50 mM, produces Ca(2+)-dependent pigment aggregation, whereas removal of K(+) from the perfusate causes pigment hyperdispersion, disclosing a clear correlation between membrane depolarization and pigment aggregation; K(+) channel blockade by Ba(2+) also partially inhibits RPCH action. We suggest that, during RPCH signal transduction, Ca(2+) released from the SER, together with K(+) channel closure, causes chromatophore membrane depolarization, leading to the opening of predominantly N- and/or P/Q-type voltage-gated Ca(2+) channels, and a Ca(2+)/cGMP cascade, resulting in pigment aggregation.
Milograna
Sarah Ribeiro
SR
Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, São Paulo, Brazil.
Bell
Fernanda Tinti
FT
McNamara
John Campbell
JC
D000588:Amines / Q000494:pharmacology; D000818:Animals; D019256:Cadmium Chloride / Q000494:pharmacology; D002118:Calcium / Q000037:antagonists & inhibitors / Q000502:physiology*; D015220:Calcium Channels / Q000502:physiology; D002462:Cell Membrane / Q000502:physiology*; D002856:Chromatophores / Q000502:physiology*; D003509:Cyclohexanecarboxylic Acids / Q000494:pharmacology; D004305:Dose-Response Relationship, Drug; D005260:Female; D000077206:Gabapentin; D007811:Lanthanum / Q000494:pharmacology; D008564:Membrane Potentials / Q000502:physiology; D009842:Oligopeptides / Q000502:physiology*; D010042:Ouabain / Q000494:pharmacology; D033541:Palaemonidae / Q000502:physiology*; D011761:Pyrrolidonecarboxylic Acid / Q000031:analogs & derivatives*; D015398:Signal Transduction / Q000502:physiology*; D005680:gamma-Aminobutyric Acid / Q000494:pharmacology; D020960:omega-Conotoxins / Q000494:pharmacology
D000588:Amines; D015220:Calcium Channels; D003509:Cyclohexanecarboxylic Acids; D009842:Oligopeptides; D020960:omega-Conotoxins; C028521:lanthanum chloride; C075851:omega-conotoxin-MVIIC; C022059:red pigment-concentrating hormone; D005680:gamma-Aminobutyric Acid; D010042:Ouabain; D000077206:Gabapentin; D007811:Lanthanum; D019256:Cadmium Chloride; D002118:Calcium; D011761:Pyrrolidonecarboxylic Acid