HSP90 regulates larval settlement of the bryozoan Bugula neritina through NO pathway

Abstract

The larvae of many sessile marine invertebrates go through a settlement process, during which planktonic larvae attach to a substrate and metamorphose into sessile juveniles. Larval attachment and metamorphosis (herein defined as 'settlement') are complex processes mediated by many signalling pathways. Nitric oxide (NO) signalling is one of the pathways that inhibits larval settlement in marine invertebrates across different phyla. NO is synthesized by NO synthase (NOS), which is a client of the molecular chaperone heat shock protein 90 (HSP90). In the present study, we provide evidence that NO, a gaseous messenger, regulates larval settlement of By using pharmacological bioassays and western blotting, we demonstrated that NO inhibits larval settlement of and that NO signals occur mainly in the sensory organ of swimming larvae. The settlement rate of larvae decreased after heat shock treatment. Inhibition of HSP90 induced larval settlement, and attenuated the inhibition of NO donors during larval settlement. In addition, the expression level of both HSP90 and NOS declined upon settlement. These results demonstrate that HSP90 regulates the larval settlement of by interacting with the NO pathway.

Behavioral and transcriptomic changes in butenolide treated larvae of the cosmopolitan fouling bryozoan Bugulina (Bugula) neritina

“…NO signal was previously detected in the equatorial nerve ring of B. neritina larvae and we have experimentally established that high endogenous or exogenous NO level inhibits larval settlement (Yang et al, 2018b). In addition, the gene expression level of NOS and sGC or GC were all up-regulated during the larval settlement process (Wang et al, 2016;Yang et al, 2018a).…”

Novel Insights on Nitric Oxide Synthase and NO Signaling in Ascidian Metamorphosis

“…Different NO molecular chaperone or downstream targets have been so far identified in different organisms. The NO signaling through the activation of downstream soluble guanylyl cyclase with consequent cGMP production was reported to be operative alone or in association with the heat shock protein 90 (HSP90) during settlement and metamorphosis in several invertebrates [ 34 , 35 , 36 , 37 , 38 , 41 , 43 , 47 , 48 , 71 ]. HSP90 is one of the upstream regulators for NOS, it acts as a molecular chaperone and its binding to NOS activates the enzyme and consequent NO production [ 72 , 73 , 74 ].…”

“…During development, NO is involved in metamorphosis, a biological process by which the animal’s body structure changes rapidly with possible consequences on nutrition and behavior. Pharmacological manipulation experiments on NO signaling have evidenced that the regulatory role of NO on larval settlement and metamorphosis is highly conserved throughout evolution from sponges to chordates [ 33 , 34 , 35 , 36 , 37 , 38 , 39 , 40 , 41 , 42 , 43 , 44 , 45 , 46 , 47 , 48 ]. As reported in other species, in ascidians NO has been shown to act both as a negative regulator, repressing metamorphosis ( Boltenia villosa and Cnemidocarpa.…”

Stage-Specific Transcriptomes of the Mussel Mytilus coruscus Reveals the Developmental Program for the Planktonic to Benthic Transition

“…Subsequent studies of the adrenergic receptor genes corroborated the importance of this system in the metamorphosis of the hard-shelled mussel (M. coruscus) and oyster (Crassostrea angulata) [10,11]. Furthermore, the metamorphosis of many marine invertebrates, such as the bryozoan (Bugula neritina), mussel (M. coruscus), and oyster (C. gigas), is negatively regulated by the nitric oxide (NO) signaling pathway [12][13][14].…”