Mucin-like glycopolymer gels in electrosensory tissues generate cues which direct electrolocation in amphibians and neuronal activation in mammals

Abstract

Mucin-like glycoproteins have established roles in epithelial boundary protection and lubricative roles in some tissues. This mini-review illustrates alternative functional roles which rely on keratan sulphate and sialic acid modifications to mucin glycopolymers which convey charge properties suggestive of novel electroconductive properties not previously ascribed to these polymers. Many tumour cells express mucin-like glycopolymers modified with highly sulphated keratan sulphate and sialic which can be detected using diagnostic biosensors. The mucin-like keratan sulphate glycopolymer present in the ampullae of lorenzini is a remarkable sensory polymer which elasmobranch fish (sharks, rays, skate) use to detect weak electrical fields emitted through muscular activity of prey fish. Information on the proton gradients is conveyed to neuromast cells located at the base of the ampullae and mechanotransduced to neural networks. This ampullae keratan sulphate sensory gel is the most sensitive proton gradient detection polymer known in nature. This process is known as electrolocation, and allows the visualization of prey fish under conditions of low visibility. The bony fish have similar electroreceptors located along their lateral lines which consist of neuromast cells containing sensory hairs located within a cupula which contains a sensory gel polymer which detects distortions in fluid flow in channels within the lateral lines and signals are sent back to neural networks providing information on the environment around these fish. One species of dolphin, the Guiana dolphin, has electrosensory pits in its bill with similar roles to the ampullae but which have evolved from its vibrissal system. Only two terrestrial animals can undertake electrolocation, these are the Duck-billed platypus and long and short nosed Echidna. In this case the electrosensor is a highly evolved innervated mucous gland. The platypus has 40,000 electroreceptors around its bill through which it electrolocates food species. The platypus has poor eyesight, is a nocturnal feeder and closes its eyes, nostrils and ears when it hunts, so electrolocation is an essential sensory skill. Mammals also have sensory cells containing stereocilia which are important in audition in the organ of corti of the cochlea and in olfaction in the olfactory epithelium. The rods and cones of the retina also have an internal connecting cilium with roles in the transport of phototransduced chemical signals and activation of neurotransmitter release to the optic nerve. Mucin-like glycopolymer gels surround the stereocilia of these sensory hair cells but these are relatively poorly characterized however they deserve detailed characterization since they may have important functional attributes.

Keywords: electrolocation; glycosaminoglycan; keratan sulfate; monosulphated keratan sulfate; mucin glycopolymers; neuroregulation; neurosensory hair cells; neurosensory proteoglycan.