Adrenocorticotropic Hormone and Cyclic Adenosine Monophosphate are Involved in the Control of Shark Bioluminescence

Abstract

Among Etmopteridae and Dalatiidae, luminous species use hormonal control to regulate bioluminescence. Melatonin (MT) triggers light emission and, conversely, alpha melanocyte‐stimulating hormone (α‐MSH) actively reduces ongoing luminescence. Prolactin (PRL) acts differentially, triggering light emission in Etmopteridae and inhibiting it in Dalatiidae. Interestingly, these hormones are also known as regulators of skin pigment movements in vertebrates. One other hormone, the adrenocorticotropic hormone (ACTH), also members of the skin pigmentation regulators, is here pharmacologically tested on the light emission. Results show that ACTH inhibits luminescence in both families. Moreover, as MT and α‐MSH/ACTH receptors are members of the G‐protein coupled receptor (GPCR) family, we investigated the effect of hormonal treatments on the cAMP level of photophores through specific cAMP assays. Our results highlight the involvement of ACTH and cAMP in the control of light emission in sharks and suggest a functional similarity between skin pigment migration and luminescence control, this latter being mediated by pigment movements in the light organ‐associated iris‐like structure cells.

From extraocular photoreception to pigment movement regulation: a new control mechanism of the lanternshark luminescence

“…After 30 and 45 min, cAMP concentrations of 0.18 ± 0.01 µM cm −2 and 0.17 ± 0.02 µM cm −2 were observed, respectively. Results are consistent with previous cAMP concentration measurements performed on Etmopteridae skin patches treated with various hormones 48 . Here, results demonstrated the non-involvement of cAMP in the phototransduction events.…”

“…Indeed, luminous reactions can involve either a luciferase/luciferin or a photoprotein in which a co-factor such as an ion is needed. Concerning the ILS pigment motion regulation, previous studies demonstrated the implication of various molecules in the α-MSH/ACTH and MCR pathway such as Gαs, adenylate cyclase and cAMP in the luminescence control of E. spinax 44,48,76 . Studies on metazoan melanophore granule dispersion highlighted the effector role of the cAMP-dependent protein kinase (PKA) in the MSH/MCR pathway in which the second messenger cAMP increases due to the adenylate cyclase up-regulation leading to the release of the catalytic subunit of PKA 7,88,[111][112][113] ).…”

“…Twenty-four adult specimens of E. spinax were caught alive during a field session in May 2018 by longlines lowered at 220 m depth in the Raunefjord, Norway (60°169′ N; 05°089′ E) 44,48,71,72,121 . Specimens were directly placed in a 1 m 3 tank filled with running fresh seawater (6 °C) and kept in a dark cold room at Espegrend Marine Station (Bergen University, Norway) 44,48,71,72,121 . Animal procedures were conducted in compliance with the Belgian national guidelines and in agreement with the European directive 2010/63/UE, under the approval of the Animal Ethics Committee of the Université catholique de Louvain in Louvain-la-Neuve.…”

“…Sharks were sexed, measured and weighed before experimentation took place. Following Duchatelet et al (2020), round shape piece of skin (6 mm diameter; ±100 mg of fresh tissue) were dissected from the ventral skin of sharks 44,48 . These skin patches, full of photophores, were rinsed in shark saline (292 mmol l −1 NaCl, 3.2 mmol l −1 KCl, 5 mmol l −1 CaCl 2 , 0.6 mmol l −1 MgSO 4 , 1.6 mmol l −1 Na 2 SO 4 , 300 mmol l −1 urea, 150 mmol l −1 trimethylamine N-oxide (TMAO), 10 mmol l −1 glucose, 6 mmol l −1 NaHCO 3 ; total osmolarity: 1.080 mosmol; pH 7.7 122 ) during half a day at 4 °c before pharmacological tests and light exposure tests happen.…”

“…They display thousands of tiny organs, photophores, that emit blue-green light ( Fig. 1a-d) [47][48][49] . Among Etmopteridae, the velvet belly lanternshark, Etmopterus spinax is the most studied lanternshark.…”