Amiloride causes changes in the mechanical properties of hair cell bundles in the fish lateral line similar to those induced by dihydrostreptomycin

Amiloride is a known blocker of the mechano–electrical transduction current in sensory hair cells. Measurements of cupular motion in the lateral line organ of fish now show that amiloride concurrently changes the micromechanical properties of the hair cell bundles. The effects of amiloride on the mechanics and receptor potentials of the hair cells resemble those previously observed for the aminoglycoside drug dihydrostreptomycin (DHSM) and are similarly antagonized by Ca2+. We hypothesize that amiloride and DHSM act on hair cells in two correlated ways which manifest themselves in both the electrical and mechanical properties of the transduction process. One action is the reduction of the transduction current with a concurrent increase of the hair bundle stiffness. The other action is a shift of the hair cell's operating point on a current–displacement curve, with a concomitant shift along the associated hair bundle stiffness–displacement curve. The latter action has the opposite effect to that of the first and thus may lead, at relatively low blocker concentrations, to both an increase of transduction current and a decrease in hair bundle stiffness.

[1]  P Tsang.  Laser interferometric flow measurements in the lateral line organ , 1997 .

[2]  D. Benos,et al.  Putative immunolocalization of the mechanoelectrical transduction channels in mammalian cochlear hair cells , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[3]  A. Hudspeth,et al.  Blockage of the transduction channels of hair cells in the bullfrog's sacculus by aminoglycoside antibiotics , 1989, Hearing Research.

[4]  M G Evans,et al.  The actions of calcium on the mechano‐electrical transducer current of turtle hair cells. , 1991, The Journal of physiology.

[5]  M Kössl,et al.  Nonlinear mechanical responses of mouse cochlear hair bundles , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[6]  A. J. Hudspeth,et al.  Compliance of the hair bundle associated with gating of mechanoelectrical transduction channels in the Bullfrog's saccular hair cell , 1988, Neuron.

[7]  J. Santos-Sacchi,et al.  Whole cell currents and mechanical responses of isolated outer hair cells , 1988, Hearing Research.

[8]  M. Lannoo.  Neuromast topography in urodele amphibians , 1987, Journal of morphology.

[9]  M J Mulroy,et al.  The organization of actin filaments in the stereocilia of cochlear hair cells , 1980, The Journal of cell biology.

[10]  D P Corey,et al.  Kinetics of the receptor current in bullfrog saccular hair cells , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  S. V. Netten,et al.  Hair Cell Mechanics Controls the Dynamic Behaviour of the Lateral Line Cupula , 1989 .

[12]  D. Benos,et al.  The binding site on cochlear stereocilia for antisera raised against renal Na+ channels is blocked by amiloride and dihydrostreptomycin , 1996, Hearing Research.

[13]  N. Hacohen,et al.  Regulation of tension on hair-cell transduction channels: displacement and calcium dependence , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  H. Ohmori,et al.  Dihydrostreptomycin modifies adaptation and blocks the mechano-electric transducer in chick cochlear hair cells , 1993, Brain Research.

[15]  Olav Sand,et al.  The Lateral Line and Sound Reception , 1981 .

[16]  H. Ohmori,et al.  Amiloride blocks the mechano‐electrical transduction channel of hair cells of the chick. , 1988, The Journal of physiology.

[17]  A. Flock,et al.  Stiffness of sensory-cell hair bundles in the isolated guinea pig cochlea , 1984, Hearing Research.

[18]  N A Schellart,et al.  Velocity- and acceleration-sensitive units in the trunk lateral line of the trout. , 1992, Journal of neurophysiology.

[19]  S Coombs,et al.  Physiological characterization of lateral line function in the Antarctic fish Trematomus bernacchii. , 1992, Brain, behavior and evolution.

[20]  A J Hudspeth,et al.  Mechanical relaxation of the hair bundle mediates adaptation in mechanoelectrical transduction by the bullfrog's saccular hair cell. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[21]  S Coombs,et al.  Form and function relationships in lateral line systems: comparative data from six species of Antarctic notothenioid fish. , 1994, Brain, behavior and evolution.

[22]  A J Hudspeth,et al.  Detection of Ca2+ entry through mechanosensitive channels localizes the site of mechanoelectrical transduction in hair cells. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Alfon B. A. Kroese,et al.  Sensory Transduction in Lateral Line Hair cells , 1989 .

[24]  A. Flock,et al.  Sensory Transduction in Hair Cells , 1971 .

[25]  Phosphate Analogs Block Adaptation in Hair Cells by Inhibiting Adaptation-Motor Force Production , 1996, Neuron.

[26]  D P Corey,et al.  Adaptation of mechanoelectrical transduction in hair cells of the bullfrog's sacculus , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  Application of incident light polarization microscopy. , 1990 .

[28]  Accepted September,et al.  Single unit activity in the peripheral lateral line system of the cichlid fish Sarotherodon niloticus L. , 1985 .

[29]  Madhu S. Sharma.  The Cephalic Lateral-Line System in Notopterus chitala (Ham.) , 1964 .

[30]  Shyam M. Khanna,et al.  Effects of quinine on the mechanical frequency response of the cupula in the fish lateral line , 1994, Hearing Research.

[31]  I. Russell,et al.  The Effect of Efferent Stimulation on the Phase and Amplitude of Extracellular Receptor Potentials in the Lateral Line System of the Perch (Perca Fluviatius) , 1983 .

[32]  S M Khanna,et al.  Basilar membrane tuning in the cat cochlea. , 1982, Science.

[33]  J. O. Pickles,et al.  Cross-links between stereocilia in the guinea pig organ of Corti, and their possible relation to sensory transduction , 1984, Hearing Research.

[34]  P. Sellick,et al.  Measurement of potassium and chloride ion concentrations in the cupulae of the lateral lines of Xenopus laevis. , 1976, Journal of Physiology.

[35]  P M Sellick,et al.  Intracellular studies of hair cells in the mammalian cochlea. , 1978, The Journal of physiology.

[36]  Sietse M. van Netten,et al.  Laser interferometer microscope for the measurement of nanometer vibrational displacements of a light‐scattering microscopic object , 1988 .

[37]  G. Richardson,et al.  Block by amiloride and its derivatives of mechano‐electrical transduction in outer hair cells of mouse cochlear cultures. , 1994, The Journal of physiology.

[38]  S M Khanna,et al.  Stiffness changes of the cupula associated with the mechanics of hair cells in the fish lateral line. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[39]  A. Kroese,et al.  Extracellular Receptor Potentials from the Lateral-Line Organ of Xenopus Laevis , 1980 .

[40]  E. Schwartz.  Lateral-Line Mechano-Receptors in Fishes and Amphibians , 1974 .

[41]  J. Assad,et al.  An active motor model for adaptation by vertebrate hair cells , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  W. Denk,et al.  Mechanical response of frog saccular hair bundles to the aminoglycoside block of mechanoelectrical transduction. , 1992, Journal of neurophysiology.

[43]  J. Wersäll,et al.  A Functional Interpretation of the Electron-Microscopic Structure of the Sensory Hairs in the Cristæ of the Elasmobranch Raja clavata in Terms of Directional Sensitivity , 1959, Nature.

[44]  Winfried Denk,et al.  Calcium imaging of single stereocilia in hair cells: Localization of transduction channels at both ends of tip links , 1995, Neuron.

[45]  F. McGlone,et al.  Measurement of calcium ion concentrations in the lateral line cupulae of Xenopus laevis. , 1979, The Journal of experimental biology.

[46]  M G Evans,et al.  Activation and adaptation of transducer currents in turtle hair cells. , 1989, The Journal of physiology.

[47]  Jan Willem Kuiper,et al.  The microphonic effect of the lateral line organ: A study on the biophysics and the function of the lateral line organ of Acernina cernua L. , 1956 .

[48]  C. Hackney,et al.  Kinematic analysis of shear displacement as a means for operating mechanotransduction channels in the contact region between adjacent stereocilia of mammalian cochlear hair cells , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[49]  I. J. Russell,et al.  Amphibian Lateral Line Receptors , 1976 .

[50]  S. M. van Netten.  Hydrodynamics of the excitation of the cupula in the fish canal , 1991 .

[51]  A J Hudspeth,et al.  Extracellular current flow and the site of transduction by vertebrate hair cells , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  S. V. Netten,et al.  Dynamic Behavior and Micromechanical Properties of the Cupula , 1989 .

[53]  Sietse M. van Netten,et al.  Mechanophysiological Properties of the Supraorbital Lateral Line Canal in Ruffe (Acerina cernua L.) , 1994 .

[54]  H. Münz,et al.  Functional Organization of the Lateral Line Periphery , 1989 .

[55]  J. Montgomery,et al.  Sensory Tuning of Lateral Line Receptors in Antarctic Fish to the Movements of Planktonic Prey , 1987, Science.

[56]  A. Kroese,et al.  Effects of ototoxic antibiotics on sensory hair cell functioning , 1982, Hearing Research.

[57]  D P Corey,et al.  Analysis of the microphonic potential of the bullfrog's sacculus , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  Sietse M. van Netten,et al.  Laser interferometric measurements on the dynamic behaviour of the cupula in the fish lateral line , 1987, Hearing Research.

[59]  A J Hudspeth,et al.  DIRECTIONAL SENSITIVITY OF INDIVIDUAL VERTEBRATE HAIR CELLS TO CONTROLLED DEFLECTION OF THEIR HAIR BUNDLES * , 1981, Annals of the New York Academy of Sciences.

[60]  J. Pickles,et al.  Paired development of hair cells in neuromasts of the teleost lateral line , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.