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Characterization of early pathogenesis in the SOD1 G93A mouse model of ALS : part I, background and methods

Vinsant, Sharon, Mansfield, Carol, Jimenez‐Moreno, Ramon, Moore, Victoria Del Gaizo, Yoshikawa, Masaaki, Hampton, Thomas G., Prevette, David, Caress, James, Oppenheim, Ronald W., Milligan, Carol·2013·Brain and Behavior

Abstract

Charcot first described amyotrophic lateral sclerosis ( ALS ) in 1869; however, its causes remain largely unknown and effective, long‐term treatment strategies are not available. The first mouse model of ALS was developed after the identification of mutations in the superoxide dismutase 1 ( SOD1 ) gene in 1993, and accordingly most of our knowledge of the etiology and pathogenesis of the disease comes from studies carried out using this animal model. Although numerous preclinical trials have been conducted in the mutant SOD1 mouse models, the results have been disappointing because they did not positively translate to clinical trials. One explanation may be that current understanding of when and where pathogenesis begins is insufficient to accurately guide preclinical trials. Further characterization of these early events may provide insight into disease onset, help in the discovery of presymptomatic diagnostic disease markers, and identify novel therapeutic targets. Here, we describe the rationale, approach, and methods for our extensive analysis of early changes that included an ultrastructural examination of central and peripheral components of the neuromuscular system in the SOD1 G93A mouse and correlated these alterations with early muscle denervation, motor dysfunction, and motoneuron death. We also provide a discussion of published work to review what is known regarding early pathology in the SOD1 mouse model of ALS . The significance of this work is that we have examined early pathology simultaneously in both the spinal cord and peripheral neuromuscular system, and the results are presented in the companion paper (Part II, Results and Discussion). Our results provide evidence as to why a thorough characterization of animal models throughout the life span is critical for a strong foundation to design preclinical trials that may produce meaningful results.

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Figure 1 Illustration of approaches used to identify MNs. (A and B) The TA and soleus motor pools exhibit rostral caudal overlap when identified via retrograde labeling after muscle injections of fluorescently labeled Cholera toxin B subunit (CTB; A), but can be distinctly identified when soleus is injected with Alexa-Fluor 488 CTB (green in B) and TA is injected with Alexa-Fluor 555 CTB (red in B). (C) Immunohistochemistry was used to confirm CTB in MNs of mice where the TA was injected with CTB, confirming motor pool location. (D) Arrows in 1 mm toluidine blue stained sections (areas similar to those shown in A–C) from animals prepared for EM indicate αMNs typically used in the evaluation of synaptic type on MNs. Dotted line outlines the VH boundary, and the box indicates location of thin section. X-Y coordinates on the electron microscope were used to map the adjacent sections and located specific MNs. MNs, motoneurons; TA, tibialis anterior; VH, ventral horn.
Figure 1 Illustration of approaches used to identify MNs. (A and B) The TA and soleus motor pools exhibit rostral caudal overlap when identified via retrograde labeling after muscle injections of fluorescently labeled Cholera toxin B subunit (CTB; A), but can be distinctly identified when soleus is injected with Alexa-Fluor 488 CTB (green in B) and TA is injected with Alexa-Fluor 555 CTB (red in B). (C) Immunohistochemistry was used to confirm CTB in MNs of mice where the TA was injected with CTB, confirming motor pool location. (D) Arrows in 1 mm toluidine blue stained sections (areas similar to those shown in A–C) from animals prepared for EM indicate αMNs typically used in the evaluation of synaptic type on MNs. Dotted line outlines the VH boundary, and the box indicates location of thin section. X-Y coordinates on the electron microscope were used to map the adjacent sections and located specific MNs. MNs, motoneurons; TA, tibialis anterior; VH, ventral horn.CC BY · PubMed Central
Figure 2 (A) Lateral view of a right hind paw during one stride depicting instances of time in swing and stance. Stance is comprised of braking and propulsion. (B) Paw Placement Angle is measured between the long axis through the hind paw and a line drawn through the center of the animal in its direction of motion. (C) Illustration of additional measurements for motor behavior. As described in the companion paper, the SOD1 mice exhibit a more closed hind paw placement angle, and less consistent step-to-step paw placement (increased paw placement angle variability) compared to WT mice. SOD1, superoxide dismutase; WT, wild type.
Figure 2 (A) Lateral view of a right hind paw during one stride depicting instances of time in swing and stance. Stance is comprised of braking and propulsion. (B) Paw Placement Angle is measured between the long axis through the hind paw and a line drawn through the center of the animal in its direction of motion. (C) Illustration of additional measurements for motor behavior. As described in the companion paper, the SOD1 mice exhibit a more closed hind paw placement angle, and less consistent step-to-step paw placement (increased paw placement angle variability) compared to WT mice. SOD1, superoxide dismutase; WT, wild type.CC BY · PubMed Central
Figure 3 A wild-type (WT) mouse performing the loaded grid test is shown.
Figure 3 A wild-type (WT) mouse performing the loaded grid test is shown.CC BY · PubMed Central
Figure 4 Chronology of pathophysiology in the SOD1G93A mouse model of ALS. SOD1, superoxide dismutase; ALS, amyotrophic lateral sclerosis.
Figure 4 Chronology of pathophysiology in the SOD1G93A mouse model of ALS. SOD1, superoxide dismutase; ALS, amyotrophic lateral sclerosis.CC BY · PubMed Central
Figure 5 A summary diagram illustrating some of the pathological changes associated with mutant superoxide dismutase (SOD1) mouse models and putative patient disease progression. Research directed toward understanding how these events (puzzle pieces) are related and lead to clinical symptoms is critical to solving the puzzle for developing effective therapies.
Figure 5 A summary diagram illustrating some of the pathological changes associated with mutant superoxide dismutase (SOD1) mouse models and putative patient disease progression. Research directed toward understanding how these events (puzzle pieces) are related and lead to clinical symptoms is critical to solving the puzzle for developing effective therapies.CC BY · PubMed Central

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Cites

Research works printed but not linked: 106

  1. 10.1136/jnnp.73.2.199 · DOI
  2. 10.1111/j.1460-9568.2004.03745.x · DOI
  3. Appel S. H., 2011, The microglial‐motoneuron dialogue in ALS, Acta Myol., 30, 4
  4. 10.1097/00001756-199709080-00012 · DOI
  5. 10.1007/s10863‐011‐9392‐1 · DOI
  6. 10.1016/j.nbd.2006.12.015 · DOI
  7. 10.1016/S0022-510X(01)00627-X · DOI
  8. 10.1186/1471-2202-8-79 · DOI
  9. 10.1016/S0940-9602(98)80020-4 · DOI
  10. Bodian D., 1964, AN electron‐microscopic study of the monkey spinal cord. I. Fine structure of normal motor column. II. Effects of retrograde chromatolysis. III. Cytologic effects of mild and virulent poliovirus infection, Bull. Johns Hopkins Hosp., 114, 13
  11. 10.1126/science.151.3714.1093 · DOI
  12. 10.1083/jcb.44.1.115 · DOI
  13. Bodian D., 1972, Structure and function of synapses, 45
  14. 10.1172/JCI34613 · DOI
  15. 10.1016/j.neuron.2006.09.018 · DOI
  16. 10.1002/ana.410140304 · DOI
  17. 10.1007/BF01463929 · DOI
  18. 10.1586/14737175.6.3.417 · DOI
  19. 10.1146/annurev.neuro.27.070203.144244 · DOI · Paper page
  20. 10.1016/S0960-8966(97)00115-6 · DOI
  21. 10.1093/hmg/ddn319 · DOI
  22. 10.1073/pnas.0406173102 · DOI
  23. 10.1002/cne.901770106 · DOI
  24. 10.1016/S0091-679X(08)61933-0 · DOI
  25. 10.1126/science.1086071 · DOI
  26. 10.1016/S0166-2236(02)02255-5 · DOI
  27. 10.1038/375061a0 · DOI
  28. 10.1016/j.tins.2007.02.004 · DOI
  29. 10.1016/j.mcn.2012.06.001 · DOI
  30. 10.1093/hmg/ddm226 · DOI
  31. 10.1016/j.ymgme.2003.08.017 · DOI
  32. 10.1179/174313208X281235 · DOI
  33. 10.1152/ajpregu.00264.2003 · DOI
  34. 10.1016/S0960-9822(03)00206-9 · DOI · Paper page
  35. 10.1159/000107704 · DOI
  36. 10.1016/j.expneurol.2003.10.004 · DOI
  37. 10.1523/JNEUROSCI.20-07-02534.2000 · DOI
  38. 10.1073/pnas.0906809106 · DOI · Paper page
  39. 10.1371/journal.pone.0036000 · DOI
  40. 10.1523/JNEUROSCI.4057-07.2007 · DOI
  41. 10.1016/j.jns.2006.01.019 · DOI
  42. Gould T., 2012, Textbook of neural repair & rehabilitation
  43. 10.1016/j.neubiorev.2007.04.015 · DOI
  44. 10.1523/JNEUROSCI.2315-06.2006 · DOI
  45. 10.1172/JCI200317610 · DOI
  46. 10.1126/science.8209258 · DOI · Paper page
  47. 10.1126/science.1083129 · DOI
  48. 10.1080/00222890903272025 · DOI
  49. 10.1016/j.physbeh.2004.04.006 · DOI
  50. 10.1016/j.nbd.2007.07.003 · DOI
  51. 10.1002/cne.10648 · DOI
  52. 10.1097/01.ALC.0000148103.09378.81 · DOI
  53. 10.1083/jcb.23.2.217 · DOI
  54. 10.1083/jcb.200501085 · DOI
  55. 10.1126/science.277.5325.559 · DOI
  56. 10.1016/S0896-6273(02)00696-7 · DOI
  57. 10.1371/journal.pgen.0010004 · DOI
  58. 10.1097/00001756-200504250-00002 · DOI
  59. 10.1016/j.neures.2003.11.008 · DOI
  60. 10.1016/j.brainres.2011.06.033 · DOI
  61. 10.1073/pnas.1200658109 · DOI
  62. 10.1002/neu.480220707 · DOI
  63. 10.1371/journal.pone.0023244 · DOI
  64. 10.1093/brain/awg061 · DOI
  65. 10.1073/pnas.0609411103 · DOI
  66. 10.1073/pnas.93.11.5472 · DOI · Paper page
  67. 10.1016/B978-0-12-385870-2.00018-4 · DOI
  68. 10.1038/nature05289 · DOI
  69. 10.1093/hmg/ddq202 · DOI
  70. 10.1126/science.204007 · DOI
  71. Peters A., 1991, Fine structure of the nervous system: neurons and their supporting cells, 273
  72. 10.1038/ng1123 · DOI
  73. 10.1038/nn1653 · DOI
  74. 10.1038/nrneurol.2012.276 · DOI
  75. 10.1126/science.1068613 · DOI
  76. 10.1126/science.1094682 · DOI
  77. Robinson M. B., 2011, Neurodegeneration: theory, disorders and treatments, 45
  78. 10.1002/ana.21543 · DOI · Paper page
  79. 10.1523/JNEUROSCI.15-11-07727.1995 · DOI
  80. 10.1038/sj.cdd.4401560 · DOI
  81. 10.1007/s00401-004-0838-y · DOI
  82. 10.1016/S1474-4422(05)70142-3 · DOI
  83. 10.1016/j.pneurobio.2007.07.007 · DOI
  84. 10.1016/j.neuron.2011.06.031 · DOI
  85. 10.1038/nn.2297 · DOI · Paper page
  86. 10.1523/JNEUROSCI.17-15-05858.1997 · DOI · Paper page
  87. 10.1038/86042 · DOI · Paper page
  88. 10.1016/j.neuron.2011.06.003 · DOI · Paper page
  89. 10.1186/1749‐8104‐4‐42 · DOI
  90. 10.1002/ana.410390210 · DOI
  91. 10.1007/s004010050794 · DOI
  92. Suzuki M., 2007, GDNF secreting human neural progenitor cells protect dying motor neurons, but not their projection to muscle, in a rat model of familial ALS, PLoS One, 8, 1
  93. 10.1159/000046187 · DOI
  94. Truett G. E., 2000, Preparation of PCR‐quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT), Biotechniques, 29, 52, 54, 10.2144/00291bm09 · DOI
  95. 10.1002/mus.880070310 · DOI
  96. 10.1016/j.pneurobio.2008.01.001 · DOI
  97. 10.1523/JNEUROSCI.21-12-04249.2001 · DOI
  98. 10.2170/jjphysiol.16.570 · DOI
  99. 10.1371/journal.pone.0034640 · DOI
  100. 10.1016/j.nurt.2010.05.012 · DOI
  101. 10.1016/S0006-8993(98)01351-1 · DOI
  102. 10.1016/j.nmd.2006.07.024 · DOI
  103. 10.1038/4553 · DOI
  104. 10.1073/pnas.0802556105 · DOI · Paper page
  105. 10.1083/jcb.139.5.1307 · DOI
  106. 10.1161/CIRCULATIONAHA.105.565598 · DOI

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Metadata

Authors
Vinsant, S., Mansfield, C., Jimenez‐Moreno, R., Moore, V. D. G., Yoshikawa, M., Hampton, T. G., Prevette, D., Caress, J., Oppenheim, R. W., & Milligan, C.
Affiliations
  • Department of Neurobiology and Anatomy The Neuroscience Program and The ALS Center Winston‐Salem North Carolina
  • Department of Chemistry Elon University Elon North Carolina
  • Mouse Specifics Boston Massachusetts
  • Department of Neurology and the ALS Center Wake Forest University School of Medicine Winston‐Salem North Carolina
Venue
Brain and Behavior
Publisher
Wiley
Published
2013-06-11
Volume
3
Issue
4
Pages
335-350
ISSN
2162-3279
Cited by
105
References
7
Language
en

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