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Cyclic Guanosine Monophosphate Signaling Cascade Mediates Pigment Aggregation in Freshwater Shrimp Chromatophores

Departamento de Biologia, FFCLRP, Universidade de São Paulo, Ribeirão Preto, 14040-901, São Paulo, Brazil

^* To whom correspondence should be addressed, at Departamento de Biologia, FFCLRP, Universidade de São Paulo, Av Bandeirantes, 3900 Ribeirão Preto 14040-901, SP, Brazil. E-mail: mcnamara{at}ffclrp.usp.br

The cell signaling cascades that mediate pigment movements in crustacean chromatophores are not yet well established, although Ca²⁺ and cyclic nucleotide second messengers are involved. Here, we examine the participation of cyclic guanosine monophosphate (cGMP) in pigment aggregation triggered by red pigment concentrating hormone (RPCH) in the red ovarian chromatophores of freshwater shrimp. In Ca²⁺-containing (5.5 mmol l^–1) saline, 10 µmol l^–1 dibutyryl cGMP alone produced complete pigment aggregation with the same time course (20 min) and peak velocity (17 µm/min) as 10^–8 mol l^–1 RPCH; however, in Ca²⁺-free saline (9 x 10^–11 mol l^–1 Ca²⁺), db-cGMP was without effect. The soluble guanylyl cyclase (GC-S) activators sodium nitroprusside (SNP, 0.5 µmol l^–1) and 3-morpholinosydnonimine (SIN-1, 100 µmol l^–1) induced moderate aggregation by themselves (35%–40%) but did not affect RPCH-triggered aggregation. The GC-S inhibitors zinc protoporphyrin IX (ZnPP-XI, 30 µmol l^–1) and 6-anilino-5,8-quinolinedione (LY83583, 10 µmol l^–1) partially inhibited RPCH-triggered aggregation by 35%. Escherichia coli heat-stable enterotoxin (STa, 1 µmol l^–1), a membrane-receptor guanylyl cyclase stimulator, did not induce or affect RPCH-triggered aggregation. We propose that the binding of RPCH to an unknown membrane-receptor type activates a Ca²⁺-dependent signaling cascade coupled via cytosolic guanylyl cyclase and cGMP to protein kinase G-phosphorylated proteins that regulate aggregation-associated, cytoskeletal molecular motor activity. This is a further example of a cGMP signaling cascade mediating the effect of a crustacean X-organ neurosecretory peptide.

Abbreviations: cAMP, cyclic adenosine monophosphate • cGMP, cyclic guanosine monophosphate • db-cGMP, dibutyryl 3':5'-cyclic guanosine monophosphate • GC-S, soluble guanylyl cyclase • LCS, low-calcium saline • LY83583, 6-anilino-5,8-quinolinedione • NCS, normal calcium saline • NO, nitric oxide • RPCH, red pigment concentrating hormone • SIN-1, 3-morpholinosydnonimine • SNP, sodium nitroprusside • STa, Escherichia coli heat-stable enterotoxin • ZnPP-XI, zinc protoporphyrin IX