Delayed functional recovery in presymptomatic mSOD1G93A mice following facial nerve crush axotomy
DOI:
https://doi.org/10.5055/jndr.2013.0009Abstract
Amyotrophic lateral sclerosis (ALS) is a fatal neurodegenerative disease involving progressive loss of motoneurons (MN). Axonal pathology and presynaptic deafferentation precede MN degeneration during disease progression in patients and the ALS mouse model (mSOD1). Previously, we determined that a functional adaptive immune response is required for complete functional recovery following a facial nerve crush axotomy in wild-type (WT) mice. In this study, we investigated the effects of facial nerve crush axotomy on functional recovery and facial MN survival in presymptomatic mSOD1 mice, relative to WT mice. The results indicate that functional recovery and facial MN survival levels are significantly reduced in presymptomatic mSOD1, relative to WT, and similar to what has previously been observed in immunodeficient mice. It is concluded that a potential immune system defect exists in the mSOD1 mouse that negatively impacts neuronal survival and regeneration following target disconnection associated with peripheral nerve axotomy.
Keywords: Motoneuron survival, Functional recovery, Axotomy, SOD1, ALS
DOI:10.5055/jndr.2013.0009
References
Rowland LP, Shneider NA: Amyotrophic lateral sclerosis. N Engl J Med. 2001; 344: 1688-1700.
Gurney ME, Pu H, Chiu AY, et al.: Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science. 1994; 264: 1772-1775.
Deng HX, Hentati A, Tainer JA, et al.: Amyotrophic lateral sclerosis and structural defects in Cu,Zn superoxide dismutase. Science. 1993; 261: 1047-1051.
Shibata N: Transgenic mouse model for familial amyotrophic lateral sclerosis with superoxide dismutase-1 mutation. Neuropathology. 2001; 21: 82-92.
Dadon-Nachum M, Melamed E, Offen D: The “dying-back” phenomenon of motor neurons in ALS. J Mol Neurosci. 2011; 43: 470-477.
Fischer LR, Culver DG, Tennant P, et al.: Amyotrophic lateral sclerosis is a distal axonopathy: Evidence in mice and man. Exp Neurol. 2004; 185: 232-240.
Hegedus J, Putman CT, Gordon T: Time course of preferential motor unit loss in the SOD1 G93A mouse model of amyotrophic lateral sclerosis. Neurobiol Dis. 2007; 28: 154-164.
Kennel PF, Finiels F, Revah F, et al.: Neuromuscular function impairment is not caused by motor neurone loss in FALS mice: An electromyographic study. Neuroreport. 1996; 7: 1427-1431.
Miyazaki K, Nagai M, Morimoto N, et al.: Spinal anterior horn has the capacity to self-regenerate in amyotrophic lateral sclerosis model mice. J Neurosci Res. 2009; 87: 3639-3648.
Ikemoto A, Nakamura S, Akiguchi I, et al.: Differential expression between synaptic vesicle proteins and presynaptic plasma membrane proteins in the anterior horn of amyotrophic lateral sclerosis. Acta Neuropathol. 2002; 103: 179-187.
Zang DW, Lopes EC, Cheema SS: Loss of synaptophysin-positive boutons on lumbar motor neurons innervating the medial gastrocnemius muscle of the SOD1G93A G1H transgenic mouse model of ALS. J Neurosci Res. 2005; 79: 694-699.
Chiu IM, Phatnani H, Kuligowski M, et al.: Activation of innate and humoral immunity in the peripheral nervous system of ALS transgenic mice. Proc Natl Acad Sci USA. 2009; 106: 20960-20965.
Engelhardt JI, Tajti J, Appel SH: Lymphocytic infiltrates in the spinal cord in amyotrophic lateral sclerosis. Arch Neurol. 1993; 50: 30-36.
Mantovani S, Garbelli S, Pasini A, et al.: Immune system alterations in sporadic amyotrophic lateral sclerosis patients suggest an ongoing neuroinflammatory process. J Neuroimmunol. 2009; 210: 73-79.
McGeer PL, McGeer EG: Inflammatory processes in amyotrophic lateral sclerosis. Muscle Nerve. 2002; 26: 459-470.
Jinno S, Yamada J: Using comparative anatomy in the axotomy model to identify distinct roles for microglia and astrocytes in synaptic stripping. Neuron Glia Biol. 2012: 1-12.
Jones KJ, Serpe CJ, Byram SC, et al.: Role of the immune system in the maintenance of mouse facial motoneuron viability after nerve injury. Brain Behav Immun. 2005; 19: 12-19.
Moran LB, Graeber MB: The facial nerve axotomy model. Brain Res Brain Res Rev. 2004; 44: 154-178.
Mesnard NA, Sanders VM, Jones KJ: Differential gene expression in the axotomized facial motor nucleus of presymptomatic SOD1 mice. J Comp Neurol. 2011; 519: 3488-3506.
Beahrs T, Tanzer L, Sanders VM, et al.: Functional recovery and facial motoneuron survival are influenced by immunodeficiency in crush-axotomized mice. Exp Neurol. 2010; 221: 225-230.
Serpe CJ, Tetzlaff JE, Coers S, et al.: Functional recovery after facial nerve crush is delayed in severe combined immunodeficient mice. Brain Behav Immun. 2002; 16: 808-812.
Serpe CJ, Sanders VM, Jones KJ: Kinetics of facial motoneuron loss following facial nerve transection in severe combined immunodeficient mice. J Neurosci Res. 2000; 62: 273-278.
Serpe CJ, Kohm AP, Huppenbauer CB, et al.: Exacerbation of facial motoneuron loss after facial nerve transection in severe combined immunodeficient (scid) mice. J Neurosci. 1999; 19: RC7.
Kujawa KA, Kinderman NB, Jones KJ: Testosterone-induced acceleration of recovery from facial paralysis following crush axotomy of the facial nerve in male hamsters. Exp Neurol. 1989; 105: 80-85.
Lal D, Hetzler LT, Sharma N, et al.: Electrical stimulation facilitates rat facial nerve recovery from a crush injury. Otolaryngol Head Neck Surg. 2008; 139: 68-73.
Mesnard NA, Alexander TD, Sanders VM, et al.: Use of laser microdissection in the investigation of facial motoneuron and neuropil molecular phenotypes after peripheral axotomy. Exp Neurol. 2010; 225: 94-103.
Faul F, Erdfelder E, Lang AG, et al.: G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007; 39: 175-191.
Brown TJ, Khan T, Jones KJ: Androgen induced acceleration of functional recovery after rat sciatic nerve injury. Restor Neurol Neurosci. 1999; 15: 289-295.
Avellino AM, Hart D, Dailey AT, et al.: Differential macrophage responses in the peripheral and central nervous system during wallerian degeneration of axons. Exp Neurol. 1995; 136: 183-198.
Camara-Lemarroy CR, Guzman-de la Garza FJ, Fernandez-Garza NE: Molecular inflammatory mediators in peripheral nerve degeneration and regeneration. Neuroimmunomodulation. 2010; 17: 314-324.
Taskinen HS, Olsson T, Bucht A, et al.: Peripheral nerve injury induces endoneurial expression of IFN-gamma, IL-10 and TNFalpha mRNA. J Neuroimmunol. 2000; 102: 17-25.
Mariotti R, Cristino L, Bressan C, et al.: Altered reaction of facial motoneurons to axonal damage in the presymptomatic phase of a murine model of familial amyotrophic lateral sclerosis. Neuroscience. 2002; 115: 331-335.
Sharp PS, Dick JR, Greensmith L: The effect of peripheral nerve injury on disease progression in the SOD1(G93A) mouse model of amyotrophic lateral sclerosis. Neuroscience. 2005; 130: 897-910.
Marcuzzo S, Zucca I, Mastropietro A, et al.: Hind limb muscle atrophy precedes cerebral neuronal degeneration in G93A-SOD1 mouse model of amyotrophic lateral sclerosis: a longitudinal MRI study. Exp Neurol. 2011; 231: 30-37.
Graber DJ, Hickey WF, Harris BT: Progressive changes in microglia and macrophages in spinal cord and peripheral nerve in the transgenic rat model of amyotrophic lateral sclerosis. J Neuroinflammation. 2010; 7: 8.
Banerjee R, Mosley RL, Reynolds AD, et al.: Adaptive immune neuroprotection in G93A-SOD1 amyotrophic lateral sclerosis mice. PLoS One. 2008; 3: e2740.
Dibaj P, Steffens H, Zschuntzsch J, et al.: In Vivo imaging reveals distinct inflammatory activity of CNS microglia versus PNS macrophages in a mouse model for ALS. PLoS One. 2011; 6: e17910.
Schaefer AM, Sanes JR, Lichtman JW: A compensatory subpopulation of motor neurons in a mouse model of amyotrophic lateral sclerosis. J Comp Neurol. 2005; 490: 209-219.
Kano O, Beers DR, Henkel JS, et al.: Peripheral nerve inflammation in ALS mice: Cause or consequence. Neurology. 2012; 78: 833-835.
