Biomechanics of Stretch-induced Beading

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 1999 May 8

PMID 10233101

Citations 11

Authors

V S Markin

D L Tanelian

R A Jersild Jr

S Ochs

Affiliations

Soon will be listed here.

Abstract

To account for the beading of myelinated fibers, and axons of unmyelinated nerve fibers as well of neurites of cultured dorsal root ganglia caused by mild stretching, a model is presented. In this model, membrane tension and hydrostatic pressure are the basic factors responsible for axonal constriction, which causes the movement of axonal fluid from the constricted regions into the adjoining axon, there giving rise to the beading expansions. Beading ranges from a mild undulation, with the smallest degree of stretch, to more globular expansions and narrow intervening constrictions as stretch is increased: the degree of constriction is physically limited by the compaction of the cytoskeleton within the axons. The model is a general one, encompassing the possibility that the membrane skeleton, composed mainly of spectrin and actin associated with the inner face of the axolemma, could be involved in bringing about the constrictions and beading.

Citing Articles

The role of mechanics in axonal stability and development.

Ghose A, Pullarkat P Semin Cell Dev Biol. 2022; 140:22-34.

PMID: 35786351 PMC: 7615100. DOI: 10.1016/j.semcdb.2022.06.006.

CROP: a retromer-PROPPIN complex mediating membrane fission in the endo-lysosomal system.

Courtellemont T, De Leo M, Gopaldass N, Mayer A EMBO J. 2022; 41(10):e109646.

PMID: 35466426 PMC: 9108610. DOI: 10.15252/embj.2021109646.

WIPI1 promotes fission of endosomal transport carriers and formation of autophagosomes through distinct mechanisms.

De Leo M, Berger P, Mayer A Autophagy. 2021; 17(11):3644-3670.

PMID: 33685363 PMC: 8632285. DOI: 10.1080/15548627.2021.1886830.

The Roles of Microtubules and Membrane Tension in Axonal Beading, Retraction, and Atrophy.

Datar A, Ameeramja J, Bhat A, Srivastava R, Mishra A, Bernal R Biophys J. 2019; 117(5):880-891.

PMID: 31427070 PMC: 6731471. DOI: 10.1016/j.bpj.2019.07.046.

Characterization of neurite dystrophy after trauma by high speed structured illumination microscopy and lattice light sheet microscopy.

Phillips J, Sherman S, Cotton K, Heddleston J, Taylor A, Finan J J Neurosci Methods. 2018; 312:154-161.

PMID: 30529411 PMC: 6342006. DOI: 10.1016/j.jneumeth.2018.12.005.

References

Ochs S, Pourmand R, Jersild Jr R, Friedman R . The origin and nature of beading: a reversible transformation of the shape of nerve fibers. Prog Neurobiol. 1997; 52(5):391-426. DOI: 10.1016/s0301-0082(97)00022-1. View

Ochs S, Jersild Jr R, Pourmand R, Potter C . The beaded form of myelinated nerve fibers. Neuroscience. 1994; 61(2):361-72. DOI: 10.1016/0306-4522(94)90237-2. View

Ochs S . BEADING OF MYELINATED NERVE FIBERS. Exp Neurol. 1965; 12:84-95. DOI: 10.1016/0014-4886(65)90100-7. View

Allen B, Rogers S, Ghilardi J, Menning P, Kuskowski M, Basbaum A . Noxious cutaneous thermal stimuli induce a graded release of endogenous substance P in the spinal cord: imaging peptide action in vivo. J Neurosci. 1997; 17(15):5921-7. PMC: 6573203. View

Elgsaeter A, Stokke B, Mikkelsen A, Branton D . The molecular basis of erythrocyte shape. Science. 1986; 234(4781):1217-23. DOI: 10.1126/science.3775380. View

Pourmand R, Ochs S, Jersild Jr R . The relation of the beading of myelinated nerve fibers to the bands of Fontana. Neuroscience. 1994; 61(2):373-80. DOI: 10.1016/0306-4522(94)90238-0. View

Mantyh P, DeMaster E, Malhotra A, Ghilardi J, Rogers S, Mantyh C . Receptor endocytosis and dendrite reshaping in spinal neurons after somatosensory stimulation. Science. 1995; 268(5217):1629-32. DOI: 10.1126/science.7539937. View

Mantyh P, Allen C, Ghilardi J, Rogers S, Mantyh C, Liu H . Rapid endocytosis of a G protein-coupled receptor: substance P evoked internalization of its receptor in the rat striatum in vivo. Proc Natl Acad Sci U S A. 1995; 92(7):2622-6. PMC: 42270. DOI: 10.1073/pnas.92.7.2622. View

Moses . Instability and "pearling" states produced in tubular membranes by competition of curvature and tension. Phys Rev Lett. 1994; 73(10):1392-1395. DOI: 10.1103/PhysRevLett.73.1392. View

10.

Ochs S, Pourmand R, Jersild Jr R . Origin of beading constrictions at the axolemma: presence in unmyelinated axons and after beta,beta'-iminodipropionitrile degradation of the cytoskeleton. Neuroscience. 1996; 70(4):1081-96. DOI: 10.1016/0306-4522(95)00390-8. View

11.

Zhu H, Wu F, Schacher S . Site-specific and sensory neuron-dependent increases in postsynaptic glutamate sensitivity accompany serotonin-induced long-term facilitation at Aplysia sensorimotor synapses. J Neurosci. 1997; 17(13):4976-86. PMC: 6573320. View

12.

Ochs S, Jersild Jr R . Cytoskeletal organelles and myelin structure of beaded nerve fibers. Neuroscience. 1987; 22(3):1041-56. DOI: 10.1016/0306-4522(87)92979-4. View

13.

Wang Z, van den Berg R, Ypey D . Resting membrane potentials and excitability at different regions of rat dorsal root ganglion neurons in culture. Neuroscience. 1994; 60(1):245-54. DOI: 10.1016/0306-4522(94)90218-6. View

14.

Tanelian D, Markin V . Biophysical and functional consequences of receptor-mediated nerve fiber transformation. Biophys J. 1997; 72(3):1092-108. PMC: 1184495. DOI: 10.1016/S0006-3495(97)78759-9. View

15.

Ochs S, Jersild Jr R . Myelin intrusions in beaded nerve fibers. Neuroscience. 1990; 36(2):553-67. DOI: 10.1016/0306-4522(90)90445-a. View