Sulfation modification of dopamine in brain regulates aggregative behavior of animals

Author:

Chen Bing12,Tong Xiwen23,Zhang Xia2,Gui Wanying2,Ai Guoming4,Huang Lihua3,Ding Ding2,Zhang Jiangxu2,Kang Le12

Affiliation:

1. School of Life Science, Institutes of Life Science and Green Development, Hebei University, Baoding 071002, China

2. State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China

3. School of Life Sciences, South China Normal University, Guangzhou, 510631 China

4. State Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China

Abstract

Abstract Behavioral plasticity and the underlying neuronal plasticity represent a fundamental capacity of animals to cope with environmental stimuli. Behavioral plasticity is controlled by complex molecular networks that act under different layers of regulation. While various molecules have been found to be involved in the regulation of plastic behaviors across species, less is known about how organisms orchestrate the activity of these molecules as part of a coherent behavioral response to varying environments. Here we discover a mechanism for the regulation of animal behavioral plasticity involving molecular sulfation in brain, a modification of substrate molecules by sulfotransferase (ST)-catalyzed addition of a sulfonate group (SO3) from an obligate donor, 3’-phosphoadenosine 5’-phosphosulfate (PAPS) to the substrates. We investigated aggregation behaviors of the migratory locusts, which are well-known for extreme phase change plasticity triggered by population density. The processes of PAPS biosynthesis acted efficiently on induction of locust behavioral transition: Inhibition of PAPS synthesis solicited a behavioral shift from gregarious to solitarious states; external PAPS dosage, by contrast, promoted aggregation in solitarious locusts. Genetic or pharmacological intervention in the sulfation catalyzation resulted into pronounced solitarizing effects. Analysis of substrate-specific STs suggests a widespread involvement of sulfated neurotransmitters in the behavioral response. Dopamine in brain was finally identified to be actively sulfate conjugated, and the sulfate conjugation enhanced the free DA-mediated behavioral aggregation. Similar results in Caenorhabditis elegans and mouse indicate that sulfation may be involved more broadly in the modulation of animal aggregation. These findings revealed a general mechanism that effectively regulates animal social-like behavioral plasticity possibly through sulfation-mediated modification of neural networks.

Publisher

Oxford University Press (OUP)

Subject

Multidisciplinary

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