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NO/cGMP Signaling and HSP90 Activity Represses Metamorphosis in the Sea Urchin Lytechinus pictus

Department of Molecular Biology and Biochemistry, Simon Fraser University, Burnaby, British Columbia V5A 1S6, Canada

* To whom correspondence should be addressed. Email: brandhor{at}sfu.ca

Nitric oxide (NO) signaling repressively regulates metamorphosis in two solitary ascidians and a gastropod. We present evidence for a similar role in the sea urchin Lytechinus pictus. NO commonly signals via soluble guanylyl cyclase (sGC). Nitric oxide synthase (NOS) activity in some mammalian cells, including neurons, depends on the molecular chaperone heat shock protein 90 (HSP90); this may be so in echinoid larvae as well. Pluteus larvae containing juvenile rudiments were treated with either radicicol L- or D-nitroarginine-methyl-ester (L-NAME and D-NAME), or IH-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one (ODQ), inhibitors of HSP90, NOS, and sGC, respectively. In all instances, drug treatment significantly increased the frequency of metamorphosis. SNAP, a NO donor, suppressed the inductive properties of L-NAME and biofilm, a natural inducer of metamorphosis. NADPH diaphorase histochemistry indicated NOS activity in cells in the lower lip of the larval mouth, the preoral hood, the gut, and in the tube feet of the echinus rudiment. Histochemical staining coincided with NOS immunostaining. Microsurgical removal of the oral hood or the pre-oral hood did not induce metamorphosis, but larvae lacking these structures retained the capacity to metamorphose in response to ODQ. We propose that the production of NO repressively regulates the initiation of metamorphosis and that a sensory response to environmental cues reduces the production of NO, and consequently cGMP, to initiate metamorphosis.

Abbreviations: D-NAME, D-nitroarginine-methyl-ester • GA, geldanamycin • GBD, geldanamycin binding domain • HSP90, heat shock protein 90 • L-NAME, L-nitroarginine-methyl-ester • NO, nitric oxide • NOS, nitric oxide synthase • ODQ, 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one • RD, radicicol • sGC, soluble guanyl cyclase • SNAP, S-nitroso-N-acetylpenicillamine

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