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Chapter 22 : Rabbit Model of Guillain-Barré Syndrome

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Rabbit Model of Guillain-Barré Syndrome, Page 1 of 2

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Abstract:

In acute motor axonal neuropathy (AMAN), immunoglobulin (Ig) G is deposited on the axolemma of the spinal anterior roots. This indicates that IgG, which binds effectively with complement, is an important factor in the development of AMAN. Patients who developed AMAN subsequent to enteritis had IgG antibodies against GM1, and their autoantibody titers decreased with the clinical course. Various ganglioside immunization protocols were examined to refine the procedure for establishing an animal model of AMAN. The most effective was subcutaneous injection of an emulsion of 2.5 mg of bovine brain ganglioside (BBG) mixtures, keyhole lympet hemocyanin (KLH) and complete Freund’s adjuvant (CFA), to Japanese white rabbits, with repeated injections at 3-week intervals. Under that protocol, all the rabbits developed marked flaccid paralysis associated with increased plasma anti-GM1 IgG antibody levels. Secondary breakdown of axons under severe demyelination in Guillain-Barré syndrome (GBS) patients has been reported. Electrophysiological evaluations were made for three rabbits inoculated with BBG, seven with GM1, eight with galactocerebroside (GalC), and seven control animals. In the AMAN rabbit model, despite marked limb weakness in the acute phase of the illness, neither compound muscle action potential amplitudes nor motor conduction velocities showed obvious changes, indicating that distal motor nerve conduction was preserved. Intravenous immunoglobulin (IVIG) is effective for GBS in shortening recovery time, but the mechanism of action has yet to be clarified. Anti-idiotypic antibodies in IVIG may affect antibody production by sending negative signals to B cells.

Citation: Yuki N. 2008. Rabbit Model of Guillain-Barré Syndrome, p 381-399. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch22

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Figures

Image of Figure 1.
Figure 1.

Molecular mimicry of gangliosides and LOS. isolate (CF90-26) from a patient with acute motor axonal neuropathy carries GM1-like and GD1a-like LOSs.

Citation: Yuki N. 2008. Rabbit Model of Guillain-Barré Syndrome, p 381-399. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch22
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Image of Figure 2.
Figure 2.

(A) Rabbit with limb weakness induced by sensitization with BBG mixture 14 days after onset. It could not maintain a normal standing position or lift its head or body. The muscles of the extremities and trunk were weak and slack, offering less than usual resistance to passive movement. (B) Rabbit with limb weakness induced by sensitization with the BBG mixture 4 days after onset. It lay splayed out, all extremities extended, and its head on the floor instead of sitting in the usual compact, hunched posture. This rabbit attempted to stand but could not. (C) Transverse section of the sciatic nerve from a BBG-immunized rabbit. Many myelin ovoids produced by Wallerian-like degeneration of the myelinated fibers are present. Toluidine blue–safranine stain. (D) Transverse section of the anterior root from a BBG-immunized rabbit. Clusters of small myelinated fibers indicative of regenerating sprouted fibers are present (arrowhead). Toluidine blue–safranine stain. (E) Myelin ovoids indicative of Wallerian-like degeneration of myelinated fibers from a BBG-immunized rabbit are present in three sciatic nerve teased fiber preparations. (F) Transverse section of the spinal anterior nerve root from a BBG-immunized rabbit with high anti-GM1 IgG antibody titer. Some axons are deeply stained by peroxidase-conjugated Protein G (arrowhead). Scale bars = 10 μm. From .

Citation: Yuki N. 2008. Rabbit Model of Guillain-Barré Syndrome, p 381-399. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch22
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Image of Figure 3.
Figure 3.

(A) Anti-ganglioside antibody from rabbits who developed limb weakness after sensitization with a BBG mixture. (a) TLC stained with the orcinol reagent for hexose. (b) Immunostained chromatogram that had been overlaid first with plasma from the rabbits then with peroxidase-conjugated anti-rabbit γ-chain-specific antibodies. Lanes 1 to 10, plasma from 10 rabbits showing limb weakness. Orcinol reagent stains GM1, GD1a, GD1b, and GT1b. Plasma IgGs from the rabbits strongly bind to GM1, and some weakly react with GD1b. (B) Target molecule for IgG autoantibodies among peripheral nerve gangliosides. (a) TLC stained with the orcinol reagent. (b) Immunostained chromatogram incubated first with plasma from a rabbit inoculated with BBG and then with peroxidase-conjugated anti-rabbit γ-chain-specific antibodies. (c) Binding of the peroxidase-conjugated cholera toxin B subunit. (d) Immunostained chromatogram incubated first with plasma from a rabbit inoculated with GM1 and then with peroxidase-conjugated anti-rabbit γ-chain-specific antibodies. Lane 1, BBG mixture (Cronassial). Lane 2, authentic GM1 (Sygen) from bovine brain. Lanes 3 to 5, monosialosyl-, disialosyl-, and polysialosylganglioside fractions from rabbit peripheral nerves. The mobility of the monosialosylganglioside, with which the cholera toxin B subunit and IgGs from the rabbits react, is similar to that of authentic GM1. (C) Negative secondary ion mass spectrum of the monosialosylganglioside that reacted with IgG from a paralyzed rabbit. Cer, ceramide; Hex, hexose; HexNAc, acetylhexosamine; NeuAc, acetylneuraminic acid. The ion at 1,544 consisted of stearic acid (C18:0) and sphingenine (d18:1), and that at 1,572 of C18:0 and icosasphingenine (d20:1). The seven major fragment ions of the sugar sequence ions in the spectrum were representative ceramides ( 564, 592; out of spectrum), glucosylceramides (a; 726, 754), lactosylceramides (b; 888, 916), gangliotriaosylceramides (c; 1,091, 1,119), gangliotetraosylceramides (d; 1,253, 1,281), II acetylneuraminosyllactosylceramides (e; 1,179, 1,207), and II acetylneuraminosylgangliotriaosylceramides (f; 1,382, 1,410). The two fragment ions that corresponded to the nonreducing terminal side of the carbohydrate chain were 833 (g; [(Hex-HexNAc-(NeuAc)Hex-OH)-H-H]) and 995 (h; [(Hex-Hex-HexNAc-(NeuAc)Hex-OH)-H-H]). The 290 and 308 ions that corresponded to acetylneuraminic acid also were present. Its spectrum, together with its mobility on the TLC plate similar to that of authentic GM1 and its binding with the cholera toxin B subunit, suggest that the structure of this ganglioside is Gal β1–3 GalNAc β1–4 (NeuAc α2–3) Gal β1–4 Glc β1–1′ Cer. (D) Cross section of normal rabbit sciatic nerve stained with the peroxidase-conjugated cholera toxin B subunit. Axons are stained. (E, F) Cross sections (E) and longitudinal (F) of normal rabbit sciatic nerve immunostained with plasma IgG that has anti-GM1 activity from a BBG-immunized rabbit. Axon surfaces are positively stained. Scale bars = 10 μm. From .

Citation: Yuki N. 2008. Rabbit Model of Guillain-Barré Syndrome, p 381-399. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch22
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Image of Figure 4.
Figure 4.

(A to E) Macrophages in nerve fibers. Cross sections of the cauda equina from a GM1-immunized rabbit. (A to C) Toluidine blue–safranine stain. Macrophages are present in the nerve fibers. Demyelination and remyelination are rare, and there are no inflammatory cells in the endoneurium. (D) Electron micrograph of the nerve fiber with macrophage infiltration shown in (A). A macrophage (m) occupies the periaxonal space, and the axon has disappeared. (E) Another example of a nerve fiber with macrophage infiltration. Macrophage (m) processes surround the atrophic axon (a). The surrounding myelin sheath appears almost normal. Scale bars = 10 μm. (F to K) IgG deposits on axons. Specimens from a BBG-immunized rabbit stained with serially diluted peroxidase-conjugated protein G. (F, G) Adjacent cross sections (20 μm thick) of ventral roots. (F) Some axons are strongly stained (arrow, arrowhead). (G) Staining intensity gradually decreases (arrow). (H) High-power magnification of the nerve fiber in (B) (arrowhead). The axon is stained diffusely. (I) Cross section of the cauda equina. Selective staining is seen along the axonal membrane. (J, K) Longitudinal sections of the cauda equina. (J) The axon is selectively stained for about 50 μm, the intensity gradually decreasing on both sides. (K) Ranvier nodes are stained selectively. Scale bars = 10 μm. From .

Citation: Yuki N. 2008. Rabbit Model of Guillain-Barré Syndrome, p 381-399. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch22
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Image of Figure 5.
Figure 5.

(A to F) Distal nerve conduction study results. Stainless steel needles were inserted close to the left sciatic nerve and its tibial branch at the ankle, knee, and sciatic notch to stimulate the nerves. At each level, a needle placed close to the nerve served as the cathode, and a remote subcutaneous one as the anode. Recording from plantar muscles was through subcutaneous needles, one placed transversely over the muscle bellies in the sole of the foot, the other at a distance. Compound muscle action potentials (CMAPs) were recorded after supramaximal stimulation. The upper, middle, and lower traces are for stimulus to the left sciatic nerve and its tibial branch at the three levels ankle, knee, and sciatic notch. (A to C) Serial nerve conduction studies of a galactocerebroside-sensitized rabbit. (A) CMAPs recorded before sensitization. CMAP amplitude is 13.0 mV, distal latency (DL) 2.10 ms, and motor conduction velocity (MCV) 48.0 m/s. (B) CMAPs recorded 2 weeks after the onset of limb weakness (nadir of the symptoms). Note that the amplitude scale is 1 mV per division. CMAPs show remarkable temporal dispersion, and their amplitudes are markedly decreased. CMAP amplitude is 1.5 mV, DL is prolonged to 3.40 ms, and MCV is decreased to 37.5 m/s. (C) CMAPs recorded 14 weeks after the onset of limb weakness. Muscle power has recovered almost to normal. CMAP amplitude has increased with the resolution of temporal dispersion (7.0 mV). DL is still prolonged (3.50 ms). MCV has recovered to 51.0 m/s. (D to F) Serial nerve conduction studies of a GM1-immunized rabbit. (D) CMAPs recorded 14 days before the onset of limb weakness. CMAP amplitude is 6.8 mV, DL 2.10 ms, and MCV 51.1 m/s. (E) CMAPs recorded 4 days after the onset of limb weakness. CMAP amplitude (6.4 mV) and DL (2.10 ms) show no marked changes. MCV is 62.5 m/s. (F) CMAPs recorded 6 weeks after the onset of limb weakness. Muscle power has gradually returned, but limb weakness and muscle atrophy are still present. CMAP amplitude has decreased to 2.5 mV, DL 2.30 ms, and MCV 52.3 m/s. (G to I) Serial F-wave recordings from a GM1-immunized rabbit. F waves were recorded after ankle stimulation. Ten consecutive recordings (minimum) were obtained after supramaximal stimulation delivered at the frequency of 1 Hz. (G) F waves before sensitization. (H) F waves recorded 4 days after onset of limb weakness. No late F-wave components have been elicited, whereas minimal F-wave latencies are preserved. (I) F waves recorded 2 weeks after onset of limb weakness. Clinical symptoms have begun to be ameliorated. Late F wave components again are recorded, but their latencies are slightly delayed. From .

Citation: Yuki N. 2008. Rabbit Model of Guillain-Barré Syndrome, p 381-399. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch22
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Image of Figure 6.
Figure 6.

(A) Rabbit with flaccid limb weakness induced by sensitization with LOS. It lies splayed out, all extremities extended, head on the floor, instead of sitting upright in the usual compact, hunched posture. (B) Anti-ganglioside antibody from rabbits that developed limb weakness after sensitization with LOS. Of the BBGs, plasma IgG from a paralyzed rabbit binds to GM1 (lane 1), isolated GM1 from bovine brain (lane 2), and GM1 from rabbit peripheral nerve (lane 3). IgGs from other three paralyzed rabbits and the GM1 from rabbit peripheral nerve (lane 3). (C to F) Macrophages in nerve fibers. Cross sections of the cauda equina from a paralyzed rabbit. (C, D) Toluidine blue stain. Macrophages are present in the nerve fibers (arrowheads). The initial degenerated axon stage also is shown (D, arrow). Demyelination and remyelination are rare, and there are no inflammatory cells in the endoneurium. (E, F) Electron micrographs of nerve fibers with macrophage infiltration. The nerve fiber in (E) is the same as in (C). Macrophages (m) occupy the periaxonal space between the atrophic axons (a) and surrounding myelin sheaths which appear almost normal. (G) Wallerian-like degeneration of nerve fibers. Cross sections of the sciatic nerve from a rabbit killed 39 days after onset. Toluidine blue stain. Myelin ovoids produced by Wallerian-like degeneration of the myelinated fibers are present (arrowheads). Scale bars = 10 μm. From .

Citation: Yuki N. 2008. Rabbit Model of Guillain-Barré Syndrome, p 381-399. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch22
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Image of Figure 7.
Figure 7.

Schematic presentation of the nodal disruption in peripheral motor nerve fibers in AMAN model. (A) Structures and molecular organizations at and near normal nodes of Ranvier. Nodal voltage-gated Na (NAV) channels are located at nodes and make multiprotein complexes, including cytoskeletal proteins such as βIV spectrin. Nav channel clusters are further stabilized by interaction between the complexes and Schwann cell microvilli. Contactin-associated protein (Caspr) forms axoglial junction at paranodes, which act as diffusion barrier to restrict lateral mobility of nodal Nav channels. Voltage-gated K (Kv) channels are localized to juxtaparanodes. (B) Autoimmune-mediated disruption of Nav channel clusters and nodes of Ranvier. Anti-GM1 IgG antibodies cause complement-mediated attack with membrane attack complex (MAC) formation at the nodal and paranodal axolemma. Nav channel clusters are altered by destruction of structures mediating their stabilization, including axonal cytoskeleton at nodes, Schwann cell microvilli, and paranodal junctions. As the autoimmune-mediated destruction extends, Nav channels and other components at and near nodes disappear. Kv channel clusters are preserved unless the immune attack extends to juxtaparanodes. From .

Citation: Yuki N. 2008. Rabbit Model of Guillain-Barré Syndrome, p 381-399. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch22
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