Role of the L-type lectin VIPL/Lman2la in the escape locomotion in zebrafish

Kazuhide Asakawa1,2,Koichi Kawakami1,2


An important feature of reactive behaviors is the ability to spatially localize a sensory stimulus and act accordingly. Such sensory-motor transformations must be precisely coordinated in escape locomotion, which determine whether an animal can survive a predatory attack. While the neural circuits for escape locomotion have been studied in various model animals, their molecular architectures have remained largely elusive. We studied the escape locomotion in the zebrafish, Danio rerio, and found that an evolutionary conserved sugar-binding protein VIPLa/lman2la has a critical role in determining the escape direction. The escape locomotion of zebraifsh embryo is initiated with a lateral body turn away from the tactile stimulus source. In order to identify genes that are required for the lateral turn, we performed a genetic screen for transposon insertion mutants that displayed an altered turn direction, and identified a recessive mutant that showed the lateral turn toward the tactile stimulus at a high frequency. The responsible gene for the mutation turned out to be the VIPLa/lman2la gene encoding a sugar-binding lectin that is implicated in glycoprotein trafficking. To understand in which tissue VIPLa functions, we performed phenotypic rescue experiments by using the targeted expression of VIPLa with the Gal4-UAS system. When the wild-type VIPLa gene was expressed in the brainstem, the abnormality of the turn direction was suppressed in VIPLa mutants, indicating that the VIPLa functions in the brainstem. Interestingly, in the VIPLa mutants, the axon of the Mauthner cell (M-cell), a brainstem reticulospinal neuron that initiates the lateral turn and whose axon guidance defect could result in an altered escape direction, normally descended to the contralateral side of the spinal cord. Altogether, the present study suggests that VIPLa is involved in the lateral turn some other mechanism than M-cell axon guidance and implies an unexpected link between VIPLa-mediated glycoprotein trafficking and brainstem control of locomotion.