Watery and dark axons in Wallerian degeneration of the opossum's optic nerve: different patterns of cytoskeletal breakdown?

Anais da Academia Brasileira de Ciencias - Tập 73 Số 2 - Trang 231-243 - 2001
Marcelo Sampaio Narciso1, Jan Nora Hokoç2, Ana Maria Blanco Martinez1
1Universidade Federal do Rio de Janeiro
2Universidade Federal do Rio de Janeiro, Brasil

Tóm tắt

In this paper we report a qualitative morphological analysis of Wallerian degeneration in a marsupial. Right optic nerves of opossums Didelphis marsupialis were crushed with a fine forceps and after 24, 48, 72, 96 and 168 hours the animals were anaesthetized and perfused with fixative. The optic nerves were immersed in fixative and processed for routine transmission electron microscopy. Among the early alterations typical of axonal degeneration, we observed nerve fibers with focal degeneration of the axoplasmic cytoskeleton, watery degeneration and dark degeneration, the latter being prevalent at 168 hours after crush. Our results point to a gradual disintegration of the axoplasmic cytoskeleton, opposed to the previous view of an "all-or-nothing'' process (Griffin et al 1995). We also report that, due to an unknown mechanism, fibers show either a dark or watery pattern of axonal degeneration, as observed in axon profiles. We also observed fibers undergoing early myelin breakdown in the absence of axonal alterations.

Từ khóa


Tài liệu tham khảo

ALLODI S, 1990, Observations on the arrangement of axons according to diameter in the optic tract of the opossum Didelphis marsupialis, Braz J Med Biol Res, 23, 539

AVELLINO AM, 1995, Differential macrophage responses in the peripheral and central nervous system during Wallerian degeneration of axons, Exp Neurol, 136, 183, 10.1006/exnr.1995.1095

BARTUS RT, 1997, The calpain hypothesis of neurodegeneration: evidence for a common cytotoxic pathway, The Neuroscientist, 3, 314, 10.1177/107385849700300513

BIGNAMI A, 1981, The fate of axonal debris in Wallerian degeneration of rat optic and sciatic nerves, J Neuropathol and Exp Neurol, 40, 537, 10.1097/00005072-198109000-00005

BLAUGRUND E, 1992, Disappearance of astrocytes and invasion of macrophages following crush injury of adult rodent optic nerves: implications for regeneration, Exp Neurol, 118, 105, 10.1016/0014-4886(92)90027-N

BRUCK W, 1997, The role of macrophages in Wallerian degeneration, Brain Pathol, 7, 741, 10.1111/j.1750-3639.1997.tb01060.x

BUTT AM, 1996, Glial cells in transected optic nerves of immature rats: I. An analysis of individual cells by intracellular dye-injection, J Neurocytol, 25, 365, 10.1007/BF02284808

BUTT AM, 1996, Glial cells in transected optic nerves of immature rats: II. An immunohistochemical study, J Neurocytol, 25, 381, 10.1007/BF02284809

CADELLI DS, 1992, Oligodendrocyte- and myelin-associated inhibitors of neurite outgrowth: their involvement in the lack of CNS regeneration, Exp Neurol, 115, 189, 10.1016/0014-4886(92)90246-M

CARBONEL AL, 1991, Ultrastructural study of the neuroglial and macrophagic reaction in Wallerian degeneration of the adult rat optic nerve, Histol Histopathol, 6, 443

CARROL EW, 1992, Wallerian degeneration in the optic nerve of the Wabbler-Lethal (wl/wl) mouse, Brain Res Bul, 29, 411, 10.1016/0361-9230(92)90077-B

CAVALCANTE LA, 1992, Fiber order in the opossum's optic tract, Anat Embryol, 186, 589, 10.1007/BF00186982

CAVALCANTE LA, 1991, Patterns of myelination in the opossum superior colliculus with additional reference to the optic tract, Anat Embryol, 183, 273, 10.1007/BF00192215

COOK RD, 1978, Primary demyelination in cat optic nerves associated with surgically induced axonal degeneration, Neuropathol Applied Neurobiol, 4, 357, 10.1111/j.1365-2990.1978.tb01348.x

COOK RD, 1987, The spatio-temporal pattern of Wallerian degeneration in the Rhesus monkey optic nerve, Acta Neuropathol, 72, 261, 10.1007/BF00691099

COOK RD, 1974, The pattern of Wallerian degeneration in the optic nerve of newborn kittens: an ultrastructural study, Brain Res, 75, 261, 10.1016/0006-8993(74)90746-X

CREVEL H VAN, 1963, The rate of secondary degeneration in the central nervous system: II. The optic nerve of the cat, J Anat, 97, 451

DAVID S, 1990, Macrophages can modify the non-permissive nature of the adult mammalian CNS, Neuron, 5, 463, 10.1016/0896-6273(90)90085-T

DONAT JR, 1973, The spatio-temporal pattern of Wallerian degeneration in mammalian peripheral nerves, Brain Res, 53, 41, 10.1016/0006-8993(73)90765-8

FRANK M, 1996, Cellular reactions at the lesion site after crushing of the rat optic nerve, Glia, 16, 227, 10.1002/(SICI)1098-1136(199603)16:3<227::AID-GLIA5>3.0.CO;2-Z

GEORGE EB, 1995, Axotomy-induced axonal degeneration is mediated by calcium influx through ion-specific channels, J Neurosci, 15, 6445, 10.1523/JNEUROSCI.15-10-06445.1995

GLASS JD, 1991, Neurofilament redistribution in transected nerves: evidence for bidirectional transport of neurofilaments, J Neurosci, 11, 3146, 10.1523/JNEUROSCI.11-10-03146.1991

GLASS JD, 1994, Calcium-mediated degeneration of the axonal cytoskeleton in the Ola mouse, J Neurochem, 62, 2472, 10.1046/j.1471-4159.1994.62062472.x

GRIFFIN JW, 1993, Degeneration and Regeneration in the Peripheral Nervous System, 361

GRIFFIN JW, 1995, Axonal degeneration and disorders of the axonal cytoskeleton, 375, 10.1093/acprof:oso/9780195082937.003.0020

GUILLERY RW, 1995, A note on the relative rates of degeneration in the crossed and the uncrossed retinofugal fibers in the opossum Didelphis marsupialis, J Neurocytol, 24, 155, 10.1007/BF01181532

GUILLERY RW, 1993, Different rates of axonal degeneration in the crossed and uncrossed retinofugal pathways of Monodelphis domestica, J Neurocytol, 22, 707, 10.1007/BF01181316

HALL SM, 1993, Observations on the progress of Wallerian degeneration in transected peripheral nerves of C57BL/Wld mice in the presence of recruited macrophages, J Neurocytol, 22, 480, 10.1007/BF01181567

HASEGAWA M, 1988, Nodal and paranodal structural changes in mouse and rat optic nerve during Wallerian degeneration, Brain Res, 452, 345, 10.1016/0006-8993(88)90039-X

HOKOÇ JN, 1978, Quantitative analysis of the opossum's optic nerve: An electron microscope study, J Comp Neurol, 178, 773, 10.1002/cne.901780411

ISHISE J, 1986, Nodal and paranodal structural changes in frog optic nerve during early Wallerian degeneration, J Neurocytol, 15, 657, 10.1007/BF01611864

JOSEPH BS, 1973, Somatofugal events in Wallerian degeneration: A conceptual Overview, Brain Res, 59, 1, 10.1016/0006-8993(73)90250-3

KIRBY MA, 1982, Quantitative analysis of the optic nerve of the North American opossum (Didelphis virginiana): An electron microscopic study, J Comp Neurol, 211, 318, 10.1002/cne.902110310

KRUGER L, 1969, Wallerian degeneration in the optic nerve of a reptile: An electron microscopic study, Amer J Anat, 125, 247, 10.1002/aja.1001250302

LAWSON LJ, 1994, Quantification of the mononuclear phagocyte response to Wallerian degeneration of the optic nerve, J Neurocytol, 23, 729, 10.1007/BF01268086

LIN H, 1973, Axonal degeneration in the peripheral optic pathway of the cat, Exp Neurol, 39, 234, 10.1016/0014-4886(73)90226-4

LOPACHIN RM, 1997, Mechanism of calcium entry during axon injury and degeneration, Toxicol Appl Pharmacol., 143, 233, 10.1006/taap.1997.8106

LUBINSKA L, 1977, Early course of Wallerian degeneration in myelinated fibers of the rat phrenic nerve, Brain Res, 130, 47, 10.1016/0006-8993(77)90841-1

LUDWIN SK, 1995, Pathology of the myelin sheath, 412

LUNN ER, 1990, The pattern of axonal degeneration in the Peripheral Nervous System varies with different types of lesion, Neuroscience, 35, 157, 10.1016/0306-4522(90)90130-V

MALBOUISSON AMB, 1984, The non-directional pattern of axonal changes in Wallerian degeneration: A computer-aided morphometric analysis, J Anat, 139, 159

MALBOUISSON AMB, 1985, Axonal degeneration in large and small nerve fibers - An electron microscopic and morphometric study, J Neurol Sci, 67, 307, 10.1016/0022-510X(85)90155-8

MARTINEZ AMB, 2000, Early myelin breakdown following sural nerve crush: a freeze-fracture study, Braz J Med Biol Res, 33, 1477, 10.1590/S0100-879X2000001200012

MARTINEZ AMB, 1998, Ultrastructural localization of calcium in peripheral nerve fibers undergoing Wallerian degeneration: an oxalate-pyroantimonate and X-ray microanalysis study, J Submicrosc Cytol Pathol, 30, 451

PERRY VH, 1990, Evidence that very slow Wallerian degeneration in C57BL/Ola mice is an intrinsic property of the peripheral nerve, Eur J Neurosc, 2, 802, 10.1111/j.1460-9568.1990.tb00472.x

PETERS A, 1991, Third

REIER PJ, 1995, Degeneration and Regeneration in the Nervous System, 593

SAITO K, 1993, Widespread activation of calcium-activated neutral proteinase (calpain) in the brain in Alzheimer disease: A potential molecular basis for neuronal degeneration, Proc Nat Acad Sci USA, 90, 2628, 10.1073/pnas.90.7.2628

SCHLAEPFER WW, 1977, Structural alterations of peripheral nerve induced by the calcium ionophore A23187, Brain Res, 136, 1, 10.1016/0006-8993(77)90126-3

SCHLAEPFER WW, 1984, Persistence of immunoreactive neurofilament protein breakdown products in transected rat sciatic nerve, J Neurochem, 43, 857, 10.1111/j.1471-4159.1984.tb12809.x

WALLER AV, Experiments on the section of the glossopharyngeal and hypoglossal nerves of the frog, and observations of the alterations produced thereby in the structure of their primitive fibers, Phil Transac Royal Soc London, 140, 423, 10.1098/rstl.1850.0021

WAXMAN SG, 1992, Ultrastructural concomitants of anoxic injury and early post-anoxic recovery in rat optic nerve, Brain Res, 574, 105, 10.1016/0006-8993(92)90806-K

WAXMAN SG, 1993, Protection of the axonal cytoskeleton in anoxic optic nerve by decreased extracellular calcium, Brain Res, 614, 137, 10.1016/0006-8993(93)91027-P