Insulin-like growth factor 1 in diabetic neuropathy and amyotrophic lateral sclerosis

Neurobiology of Disease

Volumn 97, Issue , 2017, Pages 103-113

  Rauskolb, Stefanie ^a   Dombert, Benjamin ^a   Sendtner, Michael ^a  

^a UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

Author keywords

Alzheimer; Amyotrophic lateral sclerosis; Axonal degeneration; Diabetic polyneuropathy; IGF 1; IGF 1R; IGFBP5; Motoneuron; Myelination; Neuropathy

Indexed keywords

SOMATOMEDIN BINDING PROTEIN 5; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; AXON; DIABETIC NEUROPATHY; DISEASE MODEL; DOWN REGULATION; GLIA; HUMAN; MOLECULAR PATHOLOGY; MOTONEURON; MOTOR SYSTEM; NERVE FIBER; NERVE FIBER DEGENERATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SENSORY NERVE; TRANSGENIC MOUSE; UPREGULATION; ANIMAL; METABOLISM;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; DIABETIC NEUROPATHIES; HUMANS; INSULIN-LIKE GROWTH FACTOR I;

EID: 84966708298     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2016.04.007     Document Type: Review

References (259)

1. Adem, A., Growth factor receptors in amyotrophic lateral sclerosis. Mol. Neurobiol. 9 (1994), 225–231.
2. Adem, A., Insulin-like growth factor-1 receptors in human spinal cord: changes in amyotrophic lateral sclerosis. J. Neural Transm. Gen. Sect. 97 (1994), 73–84.
3. Alami, N.H., Axonal transport of TDP-43 mRNA granules is impaired by ALS-causing mutations. Neuron 81 (2014), 536–543.
4. Alberti, K.G., Zimmet, P.Z., Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet. Med. 15 (1998), 539–553.
5. Aleman, A., Torres-Aleman, I., Circulating insulin-like growth factor I and cognitive function: neuromodulation throughout the lifespan. Prog. Neurobiol. 89 (2009), 256–265.
6. Almeida, S., Modeling key pathological features of frontotemporal dementia with C9ORF72 repeat expansion in iPSC-derived human neurons. Acta Neuropathol. 126 (2013), 385–399.
7. Andersen, H., Isokinetic muscle strength in long-term IDDM patients in relation to diabetic complications. Diabetes 45 (1996), 440–445.
8. Andersen, H., Muscular atrophy in diabetic neuropathy: a stereological magnetic resonance imaging study. Diabetologia 40 (1997), 1062–1069.
9. Andersen, H., Muscle strength in type 2 diabetes. Diabetes 53 (2004), 1543–1548.
10. Andreassen, C.S., Muscle weakness: a progressive late complication in diabetic distal symmetric polyneuropathy. Diabetes 55 (2006), 806–812.
11. Aperghis, M., Different levels of neuroprotection by two insulin-like growth factor-I splice variants. Brain Res. 1009 (2004), 213–218.
12. Apfel, S.C., Neurotrophic factor therapy–prospects and problems. Clin. Chem. Lab. Med. 39 (2001), 351–355.
13. Appel, S.H., The microglial-motoneuron dialogue in ALS. Acta Myol. 30 (2011), 4–8.
14. Arakawa, Y., Survival effect of ciliary neurotrophic factor (CNTF) on chick embryonic motoneurons in culture: comparison with other neurotrophic factors and cytokines. J. Neurosci. 10 (1990), 3507–3515.
15. Ates, K., The IGF-I splice variant MGF increases progenitor cells in ALS, dystrophic, and normal muscle. FEBS Lett. 581 (2007), 2727–2732.
16. Azari, M.F., Effects of intraperitoneal injection of Rofecoxib in a mouse model of ALS. Eur. J. Neurol. 12 (2005), 357–364.
17. Azzouz, M., VEGF delivery with retrogradely transported lentivector prolongs survival in a mouse ALS model. Nature 429 (2004), 413–417.
18. Bach, L.A., IGF-binding proteins–the pieces are falling into place. Trends Endocrinol. Metab. 16 (2005), 228–234.
19. Banerjee, R., Adaptive immune neuroprotection in G93A-SOD1 amyotrophic lateral sclerosis mice. PLoS One, 3, 2008, e2740.
20. Barbeito, A.G., Motor neuron-immune interactions: the vicious circle of ALS. J. Neural. Transm (Vienna) 117 (2010), 981–1000.
21. Barneoud, P., Curet, O., Beneficial effects of lysine acetylsalicylate, a soluble salt of aspirin, on motor performance in a transgenic model of amyotrophic lateral sclerosis. Exp. Neurol. 155 (1999), 243–251.
22. Beauverd, M., Recombinant human insulin-like growth factor I (rhIGF-I) for the treatment of amyotrophic lateral sclerosis/motor neuron disease. Cochrane Database Syst. Rev., 11, 2012, CD002064.
23. Beck, K.D., Igf1 gene disruption results in reduced brain size, CNS hypomyelination, and loss of hippocampal granule and striatal parvalbumin-containing neurons. Neuron 14 (1995), 717–730.
24. Beers, D.R., Wild-type microglia extend survival in PU.1 knockout mice with familial amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 16021–16026.
25. Beers, D.R., CD4 + T cells support glial neuroprotection, slow disease progression, and modify glial morphology in an animal model of inherited ALS. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 15558–15563.
26. Bilic, E., Comparison of the growth hormone, IGF-1 and insulin in cerebrospinal fluid and serum between patients with motor neuron disease and healthy controls. Eur. J. Neurol. 13 (2006), 1340–1345.
27. Bilican, B., Mutant induced pluripotent stem cell lines recapitulate aspects of TDP-43 proteinopathies and reveal cell-specific vulnerability. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 5803–5808.
28. Boillee, S., Onset and progression in inherited ALS determined by motor neurons and microglia. Science 312 (2006), 1389–1392.
29. Bondy, C.A., Transient IGF-I gene expression during the maturation of functionally related central projection neurons. J. Neurosci. 11 (1991), 3442–3455.
30. Bondy, C., Lee, W.H., Correlation between insulin-like growth factor (IGF)-binding protein 5 and IGF-I gene expression during brain development. J. Neurosci. 13 (1993), 5092–5104.
31. Bondy, C., Cellular pattern of type-I insulin-like growth factor receptor gene expression during maturation of the rat brain: comparison with insulin-like growth factors I and II. Neuroscience 46 (1992), 909–923.
32. Bonni, A., Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 286 (1999), 1358–1362.
33. Borasio, G.D., A placebo-controlled trial of insulin-like growth factor-I in amyotrophic lateral sclerosis. European ALS/IGF-I Study Group. Neurology 51 (1998), 583–586.
34. Boulton, A.J., Guidelines for diagnosis and outpatient management of diabetic peripheral neuropathy. European Association for the Study of Diabetes, Neurodiab. Diabetes Metab. 24:Suppl. 3 (1998), 55–65.
35. Braunstein, G.D., Reviczky, A.L., Serum insulin-like growth factor-I levels in amyotrophic lateral sclerosis. J. Neurol. Neurosurg. Psychiatry 50 (1987), 792–794.
36. Bruijn, L.I., ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron 18 (1997), 327–338.
37. Bruijn, L.I., Aggregation and motor neuron toxicity of an ALS-linked SOD1 mutant independent from wild-type SOD1. Science 281 (1998), 1851–1854.
38. Brunet, A., Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96 (1999), 857–868.
39. Burkhardt, M.F., A cellular model for sporadic ALS using patient-derived induced pluripotent stem cells. Mol. Cell. Neurosci. 56 (2013), 355–364.
40. Caroni, P., Grandes, P., Nerve sprouting in innervated adult skeletal muscle induced by exposure to elevated levels of insulin-like growth factors. J. Cell Biol. 110 (1990), 1307–1317.
41. Carro, E., Serum insulin-like growth factor I regulates brain amyloid-beta levels. Nat. Med. 8 (2002), 1390–1397.
42. Cecconi, F., Apaf1 (CED-4 homolog) regulates programmed cell death in mammalian development. Cell 94 (1998), 727–737.
43. Chen, H., Modeling ALS with iPSCs reveals that mutant SOD1 misregulates neurofilament balance in motor neurons. Cell Stem Cell 14 (2014), 796–809.
44. Cheng, H.L., Characterization of insulin-like growth factor-I and its receptor and binding proteins in transected nerves and cultured Schwann cells. J. Neurochem. 66 (1996), 525–536.
45. Cheng, H.L., IGF-I promotes peripheral nervous system myelination. Ann. N. Y. Acad. Sci. 883 (1999), 124–130.
46. Chew, J., Neurodegeneration. C9ORF72 repeat expansions in mice cause TDP-43 pathology, neuronal loss, and behavioral deficits. Science 348 (2015), 1151–1154.
47. Chiu, I.M., T lymphocytes potentiate endogenous neuroprotective inflammation in a mouse model of ALS. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 17913–17918.
48. Chu, Q., Systemic Insulin-like growth factor-1 reverses hypoalgesia and improves mobility in a mouse model of diabetic peripheral neuropathy. Mol. Ther. 16 (2008), 1400–1408.
49. Clements, R.S. Jr., Diabetic neuropathy–new concepts of its etiology. Diabetes 28 (1979), 604–611.
50. Cohen, E., Reduced IGF-1 signaling delays age-associated proteotoxicity in mice. Cell 139 (2009), 1157–1169.
51. Contreras, P.C., Systemic administration of rhIGF-I enhanced regeneration after sciatic nerve crush in mice. J. Pharmacol. Exp. Ther. 274 (1995), 1443–1449.
52. Cooper-Knock, J., The widening spectrum of C9ORF72-related disease; genotype/phenotype correlations and potential modifiers of clinical phenotype. Acta Neuropathol. 127 (2014), 333–345.
53. Corti, S., Systemic transplantation of c-kit + cells exerts a therapeutic effect in a model of amyotrophic lateral sclerosis. Hum. Mol. Genet. 19 (2010), 3782–3796.
54. Crow, J.P., Manganese porphyrin given at symptom onset markedly extends survival of ALS mice. Ann. Neurol. 58 (2005), 258–265.
55. Cui, Q.L., Inhibition of Src-like kinases reveals Akt-dependent and -independent pathways in insulin-like growth factor I-mediated oligodendrocyte progenitor survival. J. Biol. Chem. 280 (2005), 8918–8928.
56. Dal Canto, M.C., Gurney, M.E., Neuropathological changes in two lines of mice carrying a transgene for mutant human Cu,Zn SOD, and in mice overexpressing wild type human SOD: a model of familial amyotrophic lateral sclerosis (FALS). Brain Res. 676 (1995), 25–40.
57. Dal Canto, M.C., Gurney, M.E., A low expressor line of transgenic mice carrying a mutant human Cu,Zn superoxide dismutase (SOD1) gene develops pathological changes that most closely resemble those in human amyotrophic lateral sclerosis. Acta Neuropathol. 93 (1997), 537–550.
58. D'Costa, A.P., Mechanisms of insulin-like growth factor regulation of programmed cell death of developing avian motoneurons. J. Neurobiol. 36 (1998), 379–394.
59. de Boer, A.S., Eggan, K., A perspective on stem cell modeling of amyotrophic lateral sclerosis. Cell Cycle 14 (2015), 3679–3688.
60. De Meyts, P., Whittaker, J., Structural biology of insulin and IGF1 receptors: implications for drug design. Nat. Rev. Drug Discov. 1 (2002), 769–783.
61. DeJesus-Hernandez, M., Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 72 (2011), 245–256.
62. Desnuelle, C., A double-blind, placebo-controlled randomized clinical trial of alpha-tocopherol (vitamin E) in the treatment of amyotrophic lateral sclerosis. ALS riluzole-tocopherol Study Group. Amyotroph Lateral Scler Other Motor. Neuron. Disord. 2 (2001), 9–18.
63. Desport, J.C., Nutritional status is a prognostic factor for survival in ALS patients. Neurology 53 (1999), 1059–1063.
64. Devlin, A.C., Human iPSC-derived motoneurons harbouring TARDBP or C9ORF72 ALS mutations are dysfunctional despite maintaining viability. Nat. Commun., 6, 2015, 5999.
65. Dobrowolny, G., Muscle expression of a local Igf-1 isoform protects motor neurons in an ALS mouse model. J. Cell Biol. 168 (2005), 193–199.
66. Dobrowolny, G., Local expression of mIgf-1 modulates ubiquitin, caspase and CDK5 expression in skeletal muscle of an ALS mouse model. Neurol. Res. 30 (2008), 131–136.
67. Dodge, J.C., Delivery of AAV-IGF-1 to the CNS extends survival in ALS mice through modification of aberrant glial cell activity. Mol. Ther. 16 (2008), 1056–1064.
68. Donnelly, C.J., RNA toxicity from the ALS/FTD C9ORF72 expansion is mitigated by antisense intervention. Neuron 80 (2013), 415–428.
69. Dore, S., Distribution and levels of insulin-like growth factor (IGF-I and IGF-II) and insulin receptor binding sites in the spinal cords of amyotrophic lateral sclerosis (ALS) patients. Brain Res. Mol. Brain Res. 41 (1996), 128–133.
70. Duan, C., Specifying the cellular responses to IGF signals: roles of IGF-binding proteins. J. Endocrinol. 175 (2002), 41–54.
71. Egawa, N., Drug screening for ALS using patient-specific induced pluripotent stem cells. Sci. Transl. Med., 4, 2012 (145ra104).
72. Farg, M.A., Ataxin-2 interacts with FUS and intermediate-length polyglutamine expansions enhance FUS-related pathology in amyotrophic lateral sclerosis. Hum. Mol. Genet. 22 (2013), 717–728.
73. Feldman, E.L., Insulin-like growth factors regulate neuronal differentiation and survival. Neurobiol. Dis. 4 (1997), 201–214.
74. Feldman, E.L., Intraspinal neural stem cell transplantation in amyotrophic lateral sclerosis: phase 1 trial outcomes. Ann. Neurol. 75 (2014), 363–373.
75. Fernandez, A.M., Torres-Aleman, I., The many faces of insulin-like peptide signalling in the brain. Nat. Rev. Neurosci. 13 (2012), 225–239.
76. Ferraiuolo, L., Molecular pathways of motor neuron injury in amyotrophic lateral sclerosis. Nat. Rev. Neurol. 7 (2011), 616–630.
77. Finkelstein, A., Abnormal changes in NKT cells, the IGF-1 axis, and liver pathology in an animal model of ALS. PLoS One, 6, 2011, e22374.
78. Finsterer, J., Burgunder, J.M., Recent progress in the genetics of motor neuron disease. Eur. J. Med. Genet. 57 (2014), 103–112.
79. Firth, S.M., Baxter, R.C., Cellular actions of the insulin-like growth factor binding proteins. Endocr. Rev. 23 (2002), 824–854.
80. Frakes, A.E., Microglia induce motor neuron death via the classical NF-kappaB pathway in amyotrophic lateral sclerosis. Neuron 81 (2014), 1009–1023.
81. Gao, W.Q., IGF-I deficient mice show reduced peripheral nerve conduction velocities and decreased axonal diameters and respond to exogenous IGF-I treatment. J. Neurobiol. 39 (1999), 142–152.
82. Gerber, Y.N., Early functional deficit and microglial disturbances in a mouse model of amyotrophic lateral sclerosis. PLoS One, 7, 2012, e36000.
83. Gitcho, M.A., TDP-43 A315T mutation in familial motor neuron disease. Ann. Neurol. 63 (2008), 535–538.
84. Glass, J.D., Lumbar intraspinal injection of neural stem cells in patients with amyotrophic lateral sclerosis: results of a phase I trial in 12 patients. Stem Cells 30 (2012), 1144–1151.
85. Gontier, G., Blocking IGF Signaling in Adult Neurons Alleviates Alzheimer's Disease Pathology through Amyloid-beta Clearance. J. Neurosci. 35 (2015), 11500–11513.
86. Gorecki, D.C., Neuroprotective effects of short peptides derived from the Insulin-like growth factor 1. Neurochem. Int. 51 (2007), 451–458.
87. Gros-Louis, F., Intracerebroventricular infusion of monoclonal antibody or its derived Fab fragment against misfolded forms of SOD1 mutant delays mortality in a mouse model of ALS. J. Neurochem. 113 (2010), 1188–1199.
88. Guo, H., The change of insulin-like growth factor-1 in diabetic patients with neuropathy. Chin. Med. J. 112 (1999), 76–79.
89. Gurney, M.E., Transgenic-mouse model of amyotrophic lateral sclerosis. N. Engl. J. Med. 331 (1994), 1721–1722.
90. Gurney, M.E., Benefit of vitamin E, riluzole, and gabapentin in a transgenic model of familial amyotrophic lateral sclerosis. Ann. Neurol. 39 (1996), 147–157.
91. Gurney, M.E., Riluzole preserves motor function in a transgenic model of familial amyotrophic lateral sclerosis. Neurology 50 (1998), 62–66.
92. Haenggeli, C., Therapeutic immunization with a glatiramer acetate derivative does not alter survival in G93A and G37R SOD1 mouse models of familial ALS. Neurobiol. Dis. 26 (2007), 146–152.
93. Hao, W., Hyperglycemia Promotes Schwann Cell De-differentiation and De-myelination via Sorbitol Accumulation and Igf1 Protein Down-regulation. J. Biol. Chem. 290 (2015), 17106–17115.
94. Haverkamp, L.J., Natural history of amyotrophic lateral sclerosis in a database population. Validation of a scoring system and a model for survival prediction. Brain 118:Pt 3 (1995), 707–719.
95. Henkel, J.S., Microglia in ALS: the good, the bad, and the resting. J. NeuroImmune Pharmacol. 4 (2009), 389–398.
96. Hicks, G.G., Fus deficiency in mice results in defective B-lymphocyte development and activation, high levels of chromosomal instability and perinatal death. Nat. Genet. 24 (2000), 175–179.
97. Hodge, R.D., Insulin-like growth factor-I accelerates the cell cycle by decreasing G1 phase length and increases cell cycle reentry in the embryonic cerebral cortex. J. Neurosci. 24 (2004), 10201–10210.
98. Hodge, R.D., Insulin-like growth factor-I (IGF-I) inhibits neuronal apoptosis in the developing cerebral cortex in vivo. Int. J. Dev. Neurosci. 25 (2007), 233–241.
99. Hosback, S., Circulating insulin-like growth factors and related binding proteins are selectively altered in amyotrophic lateral sclerosis and multiple sclerosis. Growth Hormon. IGF Res. 17 (2007), 472–479.
100. Houenou, L.J., Naturally occurring and axotomy-induced motoneuron death and its prevention by neurotrophic agents: a comparison between chick and mouse. Prog. Brain Res. 102 (1994), 217–226.
101. Hughes, R.A., Members of several gene families influence survival of rat motoneurons in vitro and in vivo. J. Neurosci. Res. 36 (1993), 663–671.
102. Hwa, V., The insulin-like growth factor-binding protein (IGFBP) superfamily. Endocr. Rev. 20 (1999), 761–787.
103. Ishii, D.N., Role of insulin-like growth factors in peripheral nerve regeneration. Pharmacol. Ther. 62 (1994), 125–144.
104. Isobe, T., Amyotrophic lateral sclerosis models derived from human embryonic stem cells with different superoxide dismutase 1 mutations exhibit differential drug responses. Stem Cell Res. 15 (2015), 459–468.
105. Jaarsma, D., Neuron-specific expression of mutant superoxide dismutase is sufficient to induce amyotrophic lateral sclerosis in transgenic mice. J. Neurosci. 28 (2008), 2075–2088.
106. Jablonski, M.R., Inhibiting drug efflux transporters improves efficacy of ALS therapeutics. Ann. Clin. Transl. Neurol. 1 (2014), 996–1005.
107. Jiang, F., Beneficial effect of ginseng root in SOD-1 (G93A) transgenic mice. J. Neurol. Sci. 180 (2000), 52–54.
108. Jiang, H.Q., Guanabenz delays the onset of disease symptoms, extends lifespan, improves motor performance and attenuates motor neuron loss in the SOD1 G93A mouse model of amyotrophic lateral sclerosis. Neuroscience 277 (2014), 132–138.
109. Johnston, J.A., Formation of high molecular weight complexes of mutant Cu, Zn-superoxide dismutase in a mouse model for familial amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U. S. A. 97 (2000), 12571–12576.
110. Julien, J.P., Kriz, J., Transgenic mouse models of amyotrophic lateral sclerosis. Biochim. Biophys. Acta 1762 (2006), 1013–1024.
111. Kabashi, E., TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat. Genet. 40 (2008), 572–574.
112. Kalichman, M.W., Reactive, degenerative, and proliferative Schwann cell responses in experimental galactose and human diabetic neuropathy. Acta Neuropathol. 95 (1998), 47–56.
113. Kasarskis, E.J., Nutritional status of patients with amyotrophic lateral sclerosis: relation to the proximity of death. Am. J. Clin. Nutr. 63 (1996), 130–137.
114. Kaspar, B.K., Retrograde viral delivery of IGF-1 prolongs survival in a mouse ALS model. Science 301 (2003), 839–842.
115. Kerkhoff, H., Insulin-like and fibroblast growth factors in spinal cords, nerve roots and skeletal muscle of human controls and patients with amyotrophic lateral sclerosis. Acta Neuropathol. 87 (1994), 411–421.
116. Kiaei, M., Thalidomide and lenalidomide extend survival in a transgenic mouse model of amyotrophic lateral sclerosis. J. Neurosci. 26 (2006), 2467–2473.
117. Kim, B., Feldman, E.L., Differential regulation of focal adhesion kinase and mitogen-activated protein kinase tyrosine phosphorylation during insulin-like growth factor-I-mediated cytoskeletal reorganization. J. Neurochem. 71 (1998), 1333–1336.
118. Kiskinis, E., Pathways disrupted in human ALS motor neurons identified through genetic correction of mutant SOD1. Cell Stem Cell 14 (2014), 781–795.
119. Klivenyi, P., Neuroprotective effects of creatine in a transgenic animal model of amyotrophic lateral sclerosis. Nat. Med. 5 (1999), 347–350.
120. Koppers, M., C9orf72 ablation in mice does not cause motor neuron degeneration or motor deficits. Ann. Neurol. 78 (2015), 426–438.
121. Kriz, J., Minocycline slows disease progression in a mouse model of amyotrophic lateral sclerosis. Neurobiol. Dis. 10 (2002), 268–278.
122. Kriz, J., Efficient three-drug cocktail for disease induced by mutant superoxide dismutase. Ann. Neurol. 53 (2003), 429–436.
123. Kuhnlein, P., Diagnosis and treatment of bulbar symptoms in amyotrophic lateral sclerosis. Nat. Clin. Pract. Neurol. 4 (2008), 366–374.
124. Kuida, K., Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 384 (1996), 368–372.
125. Kuroda, M., Male sterility and enhanced radiation sensitivity in TLS(−/−) mice. EMBO J. 19 (2000), 453–462.
126. Kwiatkowski, T.J. Jr., Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 323 (2009), 1205–1208.
127. Lai, E.C., Effect of recombinant human insulin-like growth factor-I on progression of ALS. A placebo-controlled study. The North America ALS/IGF-I Study Group. Neurology 49 (1997), 1621–1630.
128. Lattante, S., TARDBP and FUS mutations associated with amyotrophic lateral sclerosis: summary and update. Hum. Mutat. 34 (2013), 812–826.
129. Lee, S., Huang, E.J., Modeling ALS and FTD with iPSC-derived Neurons. 2015 (Brain Res).
130. LeRoith, D., Molecular and cellular aspects of the insulin-like growth factor I receptor. Endocr. Rev. 16 (1995), 143–163.
131. Lewis, S., Neurodegenerative disease: expanding neurodegeneration modelling. Nat. Rev. Neurosci., 16, 2015, 376.
132. Lewis, M.E., Insulin-like growth factor-I: potential for treatment of motor neuronal disorders. Exp. Neurol. 124 (1993), 73–88.
133. Li, M., Functional role of caspase-1 and caspase-3 in an ALS transgenic mouse model. Science 288 (2000), 335–339.
134. Liao, B., Transformation from a neuroprotective to a neurotoxic microglial phenotype in a mouse model of ALS. Exp. Neurol. 237 (2012), 147–152.
135. Ling, S.C., Converging mechanisms in ALS and FTD: disrupted RNA and protein homeostasis. Neuron 79 (2013), 416–438.
136. Lino, M.M., Accumulation of SOD1 mutants in postnatal motoneurons does not cause motoneuron pathology or motoneuron disease. J. Neurosci. 22 (2002), 4825–4832.
137. Liu, J.P., Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell 75 (1993), 59–72.
138. Liu, X.J., Identification of a nonpeptide ligand that releases bioactive insulin-like growth factor-I from its binding protein complex. J. Biol. Chem. 276 (2001), 32419–32422.
139. Liu, J., Toxicity of familial ALS-linked SOD1 mutants from selective recruitment to spinal mitochondria. Neuron 43 (2004), 5–17.
140. Liu, Y., Ryk-mediated Wnt repulsion regulates posterior-directed growth of corticospinal tract. Nat. Neurosci. 8 (2005), 1151–1159.
141. Lobsiger, C.S., Cleveland, D.W., Glial cells as intrinsic components of non-cell-autonomous neurodegenerative disease. Nat. Neurosci. 10 (2007), 1355–1360.
142. Lunetta, C., Impaired expression of insulin-like growth factor-1 system in skeletal muscle of amyotrophic lateral sclerosis patients. Muscle Nerve 45 (2012), 200–208.
143. Lunn, J.S., Autocrine production of IGF-I increases stem cell-mediated neuroprotection. Stem Cells 33 (2015), 1480–1489.
144. Malatesta, P., Neuronal or glial progeny: regional differences in radial glia fate. Neuron 37 (2003), 751–764.
145. Mancuso, R., Sigma-1R agonist improves motor function and motoneuron survival in ALS mice. Neurotherapeutics 9 (2012), 814–826.
146. Martin, L.J., Motor neuron degeneration in amyotrophic lateral sclerosis mutant superoxide dismutase-1 transgenic mice: mechanisms of mitochondriopathy and cell death. J. Comp. Neurol. 500 (2007), 20–46.
147. Migdalis, I.N., Insulin-like growth factor-I and IGF-I receptors in diabetic patients with neuropathy. Diabet. Med. 12 (1995), 823–827.
148. Miller, T.M., Virus-delivered small RNA silencing sustains strength in amyotrophic lateral sclerosis. Ann. Neurol. 57 (2005), 773–776.
149. Miller, T.M., Gene transfer demonstrates that muscle is not a primary target for non-cell-autonomous toxicity in familial amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 19546–19551.
150. Mitchell, J.D., Recombinant human insulin-like growth factor I (rhIGF-I) for amyotrophic lateral sclerosis/motor neuron disease. Cochrane Database Syst. Rev., 2002, CD002064.
151. Mitchell, J.C., Overexpression of human wild-type FUS causes progressive motor neuron degeneration in an age- and dose-dependent fashion. Acta Neuropathol. 125 (2013), 273–288.
152. Morgado, C., Tavares, I., C-fos expression at the spinal dorsal horn of streptozotocin-induced diabetic rats. Diabetes Metab. Res. Rev. 23 (2007), 644–652.
153. Morgado, C., Neuronal hyperactivity at the spinal cord and periaqueductal grey during painful diabetic neuropathy: effects of gabapentin. Eur. J. Pain 14 (2010), 693–699.
154. Muller, A.P., Reduced brain insulin-like growth factor I function during aging. Mol. Cell. Neurosci. 49 (2012), 9–12.
155. Nagano, I., Beneficial effects of intrathecal IGF-1 administration in patients with amyotrophic lateral sclerosis. Neurol. Res. 27 (2005), 768–772.
156. Naruse, I., Keino, H., Apoptosis in the developing CNS. Prog. Neurobiol. 47 (1995), 135–155.
157. Neff, N.T., Insulin-like growth factors: putative muscle-derived trophic agents that promote motoneuron survival. J. Neurobiol. 24 (1993), 1578–1588.
158. Nikolic, M., Postnatal neuronal apoptosis in the cerebral cortex: physiological and pathophysiological mechanisms. Neuroscience 254 (2013), 369–378.
159. Nishimura, A.L., Allele-specific knockdown of ALS-associated mutant TDP-43 in neural stem cells derived from induced pluripotent stem cells. PLoS One, 9, 2014, e91269.
160. Nixon, R.A., The role of autophagy in neurodegenerative disease. Nat. Med. 19 (2013), 983–997.
161. Ohnishi, S., Intra-bone marrow-bone marrow transplantation slows disease progression and prolongs survival in G93A mutant SOD1 transgenic mice, an animal model mouse for amyotrophic lateral sclerosis. Brain Res. 1296 (2009), 216–224.
162. Oliver, D., The quality of care and symptom control—the effects on the terminal phase of ALS/MND. J. Neurol. Sci. 139:Suppl (1996), 134–136.
163. Ono, S., Increased expression of insulin-like growth factor I in skin in amyotrophic lateral sclerosis. J. Neurol. Neurosurg. Psychiatry 69 (2000), 199–203.
164. O'Rourke, J.G., C9orf72 BAC transgenic mice display typical pathologic features of ALS/FTD. Neuron 88 (2015), 892–901.
165. Ozdinler, P.H., Macklis, J.D., IGF-I specifically enhances axon outgrowth of corticospinal motor neurons. Nat. Neurosci. 9 (2006), 1371–1381.
166. Park, I.S., Preferential expression of insulin-like growth factor binding proteins-1, -3, and -5 during early diabetic renal hypertrophy in rats. Am. J. Kidney Dis. 32 (1998), 1000–1010.
167. Pasinelli, P., Brown, R.H., Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Nat. Rev. Neurosci. 7 (2006), 710–723.
168. Pasinelli, P., Amyotrophic lateral sclerosis-associated SOD1 mutant proteins bind and aggregate with Bcl-2 in spinal cord mitochondria. Neuron 43 (2004), 19–30.
169. Patel, P., Early-stage treatment with Withaferin A reduces levels of misfolded superoxide dismutase 1 and extends lifespan in a mouse model of amyotrophic lateral sclerosis. Neurotherapeutics 12 (2015), 217–233.
170. Peters, O.M., Human C9ORF72 hexanucleotide expansion reproduces RNA foci and dipeptide repeat proteins but not neurodegeneration in BAC transgenic mice. Neuron 88 (2015), 902–909.
171. Petrou, P., Safety and clinical effects of mesenchymal stem cells secreting neurotrophic factor transplantation in patients with amyotrophic lateral sclerosis: results of phase 1/2 and 2a clinical trials. JAMA Neurol., 2016, 1–8.
172. Philips, T., Robberecht, W., Neuroinflammation in amyotrophic lateral sclerosis: role of glial activation in motor neuron disease. Lancet Neurol. 10 (2011), 253–263.
173. Polydefkis, M., New insights into diabetic polyneuropathy. J. Am. Med. Assoc. 290 (2003), 1371–1376.
174. Popken, G.J., In vivo effects of insulin-like growth factor-I (IGF-I) on prenatal and early postnatal development of the central nervous system. Eur. J. Neurosci. 19 (2004), 2056–2068.
175. Pramatarova, A., Neuron-specific expression of mutant superoxide dismutase 1 in transgenic mice does not lead to motor impairment. J. Neurosci. 21 (2001), 3369–3374.
176. Pu, S.F., Differential spatio-temporal expression of the insulin-like growth factor genes in regenerating sciatic nerve. Brain Res. Mol. Brain Res. 34 (1995), 18–28.
177. Pu, S.F., Insulin-like growth factor-II increases and IGF is required for postnatal rat spinal motoneuron survival following sciatic nerve axotomy. J. Neurosci. Res. 55 (1999), 9–16.
178. Quattrini, C., Tesfaye, S., Understanding the impact of painful diabetic neuropathy. Diabetes Metab. Res. Rev. 19:Suppl. 1 (2003), S2–S8.
179. Rabinovsky, E.D., Targeted expression of IGF-1 transgene to skeletal muscle accelerates muscle and motor neuron regeneration. FASEB J. 17 (2003), 53–55.
180. Ralph, G.S., Silencing mutant SOD1 using RNAi protects against neurodegeneration and extends survival in an ALS model. Nat. Med. 11 (2005), 429–433.
181. Ramji, N., Does diabetes mellitus target motor neurons?. Neurobiol. Dis. 26 (2007), 301–311.
182. Raoul, C., Lentiviral-mediated silencing of SOD1 through RNA interference retards disease onset and progression in a mouse model of ALS. Nat. Med. 11 (2005), 423–428.
183. Recio-Pinto, E., Ishii, D.N., Insulin and related growth factors: effects on the nervous system and mechanism for neurite growth and regeneration. Neurochem. Int. 12 (1988), 397–414.
184. Renton, A.E., A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 72 (2011), 257–268.
185. Riley, J., Intraspinal stem cell transplantation in amyotrophic lateral sclerosis: a phase I safety trial, technical note, and lumbar safety outcomes. Neurosurgery 71 (2012), 405–416 (discussion 416).
186. Riley, J., Intraspinal stem cell transplantation in amyotrophic lateral sclerosis: a phase I trial, cervical microinjection, and final surgical safety outcomes. Neurosurgery 74 (2014), 77–87.
187. Ripps, M.E., Transgenic mice expressing an altered murine superoxide dismutase gene provide an animal model of amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U. S. A. 92 (1995), 689–693.
188. Robberecht, W., Philips, T., The changing scene of amyotrophic lateral sclerosis. Nat. Rev. Neurosci. 14 (2013), 248–264.
189. Rodrigues, M.C., Immunological aspects in amyotrophic lateral sclerosis. Transl. Stroke Res. 3 (2012), 331–340.
190. Rosen, D.R., Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature, 364, 1993, 362.
191. Rothstein, J.D., Beta-lactam antibiotics offer neuroprotection by increasing glutamate transporter expression. Nature 433 (2005), 73–77.
192. Rowland, L.P., Shneider, N.A., Amyotrophic lateral sclerosis. N. Engl. J. Med. 344 (2001), 1688–1700.
193. Russell, J.W., Feldman, E.L., Insulin-like growth factor-I prevents apoptosis in sympathetic neurons exposed to high glucose. Horm. Metab. Res. 31 (1999), 90–96.
194. Russell, J.W., Insulin-like growth factor-I promotes myelination of peripheral sensory axons. J. Neuropathol. Exp. Neurol. 59 (2000), 575–584.
195. Rutherford, N.J., Novel mutations in TARDBP (TDP-43) in patients with familial amyotrophic lateral sclerosis. PLoS Genet., 4, 2008, e1000193.
196. Saenger, S., Functional improvement in mouse models of familial amyotrophic lateral sclerosis by PEGylated insulin-like growth factor I treatment depends on disease severity. Amyotroph. Lateral Scler. 13 (2012), 418–429.
197. Said, G., Diabetic neuropathy—a review. Nat. Clin. Pract. Neurol. 3 (2007), 331–340.
198. Sareen, D., Targeting RNA foci in iPSC-derived motor neurons from ALS patients with a C9ORF72 repeat expansion. Sci. Transl. Med., 5, 2013 (208ra149).
199. Schiffer, D., Fiano, V., Astrogliosis in ALS: possible interpretations according to pathogenetic hypotheses. Amyotroph Lateral Scler Other Motor. Neuron. Disord. 5 (2004), 22–25.
200. Schiffer, D., Reactive astrogliosis of the spinal cord in amyotrophic lateral sclerosis. J. Neurol. Sci. 139:Suppl (1996), 27–33.
201. Schmidt, R.E., Insulin-like growth factor I reverses experimental diabetic autonomic neuropathy. Am. J. Pathol. 155 (1999), 1651–1660.
202. Scott, S., Design, power, and interpretation of studies in the standard murine model of ALS. Amyotroph. Lateral Scler. 9 (2008), 4–15.
203. Seksenyan, A., Thymic involution, a co-morbidity factor in amyotrophic lateral sclerosis. J. Cell. Mol. Med. 14 (2010), 2470–2482.
204. Selvarajah, D., Early involvement of the spinal cord in diabetic peripheral neuropathy. Diabetes Care 29 (2006), 2664–2669.
205. Selvarajah, D., Thalamic neuronal dysfunction and chronic sensorimotor distal symmetrical polyneuropathy in patients with type 1 diabetes mellitus. Diabetologia 51 (2008), 2088–2092.
206. Shefner, J.M., A clinical trial of creatine in ALS. Neurology 63 (2004), 1656–1661.
207. Shelkovnikova, T.A., Fused in sarcoma (FUS) protein lacking nuclear localization signal (NLS) and major RNA binding motifs triggers proteinopathy and severe motor phenotype in transgenic mice. J. Biol. Chem. 288 (2013), 25266–25274.
208. Sima, A.A., New insights into the metabolic and molecular basis for diabetic neuropathy. Cell. Mol. Life Sci. 60 (2003), 2445–2464.
209. Simon, C.M., Dysregulated IGFBP5 expression causes axon degeneration and motoneuron loss in diabetic neuropathy. Acta Neuropathol. 130 (2015), 373–387.
210. Slieker, L.J., Modifications in the B10 and B26-30 regions of the B chain of human insulin alter affinity for the human IGF-I receptor more than for the insulin receptor. Diabetologia 40:Suppl. 2 (1997), S54–S61.
211. Song, S.E., IGFBP5 mediates high glucose-induced cardiac fibroblast activation. J. Mol. Endocrinol. 50 (2013), 291–303.
212. Sorenson, E.J., Subcutaneous IGF-1 is not beneficial in 2-year ALS trial. Neurology 71 (2008), 1770–1775.
213. Sreedharan, J., TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 319 (2008), 1668–1672.
214. Srinivasan, S., Diabetic peripheral neuropathy: evidence for apoptosis and associated mitochondrial dysfunction. Diabetes 49 (2000), 1932–1938.
215. Stallings, N.R., Progressive motor weakness in transgenic mice expressing human TDP-43. Neurobiol. Dis. 40 (2010), 404–414.
216. Strotmeyer, E.S., Diabetes and bone health. Diabetes Self Manag., 25(11–2), 2008, 14.
217. Swarup, V., Deregulation of TDP-43 in amyotrophic lateral sclerosis triggers nuclear factor kappaB-mediated pathogenic pathways. J. Exp. Med. 208 (2011), 2429–2447.
218. Syroid, D.E., A role for insulin-like growth factor-I in the regulation of Schwann cell survival. J. Neurosci. 19 (1999), 2059–2068.
219. Takahashi, K., Yamanaka, S., Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126 (2006), 663–676.
220. Takahashi, K., Induction of pluripotent stem cells from fibroblast cultures. Nat. Protoc. 2 (2007), 3081–3089.
221. Tan, K., Baxter, R.C., Serum insulin-like growth factor I levels in adult diabetic patients: the effect of age. J. Clin. Endocrinol. Metab. 63 (1986), 651–655.
222. Tanno, B., Expression of insulin-like growth factor-binding protein 5 in neuroblastoma cells is regulated at the transcriptional level by c-Myb and B-Myb via direct and indirect mechanisms. J. Biol. Chem. 277 (2002), 23172–23180.
223. Tanno, B., Silencing of endogenous IGFBP-5 by micro RNA interference affects proliferation, apoptosis and differentiation of neuroblastoma cells. Cell Death Differ. 12 (2005), 213–223.
224. Tesfaye, S., Advances in the management of diabetic peripheral neuropathy. Curr. Opin. Support. Palliat. Care 3 (2009), 136–143.
225. Thoenen, H., Sendtner, M., Neurotrophins: from enthusiastic expectations through sobering experiences to rational therapeutic approaches. Nat. Neurosci. 5:Suppl (2002), 1046–1050.
226. Thoenen, H., Trophic support of motoneurons: physiological, pathophysiological, and therapeutic implications. Exp. Neurol. 124 (1993), 47–55.
227. Torres-Aleman, I., The peripheral insulin-like growth factor system in amyotrophic lateral sclerosis and in multiple sclerosis. Neurology 50 (1998), 772–776.
228. Trejo, J.L., Central actions of liver-derived insulin-like growth factor I underlying its pro-cognitive effects. Mol. Psychiatry 12 (2007), 1118–1128.
229. Tsao, W., Rodent models of TDP-43: recent advances. Brain Res. 1462 (2012), 26–39.
230. Van Den Bosch, L., Minocycline delays disease onset and mortality in a transgenic model of ALS. Neuroreport 13 (2002), 1067–1070.
231. Vance, C., Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 323 (2009), 1208–1211.
232. Vergani, L., Systemic administration of insulin-like growth factor decreases motor neuron cell death and promotes muscle reinnervation. J. Neurosci. Res. 54 (1998), 840–847.
233. Vinik, A.I., Diabetic neuropathies. Diabetes Care 15 (1992), 1926–1975.
234. Wada, T., Amyotrophic lateral sclerosis model derived from human embryonic stem cells overexpressing mutant superoxide dismutase 1. Stem Cells Transl. Med. 1 (2012), 396–402.
235. Waibel, S., Rasagiline alone and in combination with riluzole prolongs survival in an ALS mouse model. J. Neurol. 251 (2004), 1080–1084.
236. Wainger, et al. Intrinsic membrane hyperexcitability of amyotrophic lateral sclerosis patient-derived motor neurons. Cell Rep. 7:1 (2014), 1–11, 10.1016/j.celrep.2014.03.019 Epub 2014 Apr 3.
237. Wang, L.J., Neuroprotective effects of glial cell line-derived neurotrophic factor mediated by an adeno-associated virus vector in a transgenic animal model of amyotrophic lateral sclerosis. J. Neurosci. 22 (2002), 6920–6928.
238. Wang, J., Copper-binding-site-null SOD1 causes ALS in transgenic mice: aggregates of non-native SOD1 delineate a common feature. Hum. Mol. Genet. 12 (2003), 2753–2764.
239. Wang, J., Somatodendritic accumulation of misfolded SOD1-L126Z in motor neurons mediates degeneration: alphaB-crystallin modulates aggregation. Hum. Mol. Genet. 14 (2005), 2335–2347.
240. Watanabe, Y., Mouse motor neuron disease caused by truncated SOD1 with or without C-terminal modification. Brain Res. Mol. Brain Res. 135 (2005), 12–20.
241. Wegorzewska, I., TDP-43 mutant transgenic mice develop features of ALS and frontotemporal lobar degeneration. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 18809–18814.
242. Wilczak, N., de Keyser, J., Insulin-like growth factor system in amyotrophic lateral sclerosis. Endocr. Dev. 9 (2005), 160–169.
243. Wilczak, N., Free insulin-like growth factor (IGF)-I and IGF binding proteins 2, 5, and 6 in spinal motor neurons in amyotrophic lateral sclerosis. Lancet 361 (2003), 1007–1011.
244. Wils, H., TDP-43 transgenic mice develop spastic paralysis and neuronal inclusions characteristic of ALS and frontotemporal lobar degeneration. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 3858–3863.
245. Wong, P.C., An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron 14 (1995), 1105–1116.
246. Wuarin, L., Early reduction in insulin-like growth factor gene expression in diabetic nerve. Exp. Neurol. 130 (1994), 106–114.
247. Xu, Y.F., Wild-type human TDP-43 expression causes TDP-43 phosphorylation, mitochondrial aggregation, motor deficits, and early mortality in transgenic mice. J. Neurosci. 30 (2010), 10851–10859.
248. Yamanaka, S., A fresh look at iPS cells. Cell 137 (2009), 13–17.
249. Yamanaka, K., Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nat. Neurosci. 11 (2008), 251–253.
250. Yan, J., Frameshift and novel mutations in FUS in familial amyotrophic lateral sclerosis and ALS/dementia. Neurology 75 (2010), 807–814.
251. Yang, Y.M., A small molecule screen in stem-cell-derived motor neurons identifies a kinase inhibitor as a candidate therapeutic for ALS. Cell Stem Cell 12 (2013), 713–726.
252. Ye, P., Myelination is altered in insulin-like growth factor-I null mutant mice. J. Neurosci. 22 (2002), 6041–6051.
253. Yoo, Y.E., Ko, C.P., Dihydrotestosterone ameliorates degeneration in muscle, axons and motoneurons and improves motor function in amyotrophic lateral sclerosis model mice. PLoS One, 7, 2012, e37258.
254. Zackenfels, K., Evidence for an important role of IGF-I and IGF-II for the early development of chick sympathetic neurons. Neuron 14 (1995), 731–741.
255. Zeslawski, W., The interaction of insulin-like growth factor-I with the N-terminal domain of IGFBP-5. EMBO J. 20 (2001), 3638–3644.
256. Zhang, K., The C9orf72 repeat expansion disrupts nucleocytoplasmic transport. Nature 525 (2015), 56–61.
257. Zhao, W., Regulatory T lymphocytes from ALS mice suppress microglia and effector T lymphocytes through different cytokine-mediated mechanisms. Neurobiol. Dis. 48 (2012), 418–428.
258. Zhu, S., Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature 417 (2002), 74–78.
259. Zhuang, H.X., Insulin-like growth factors reverse or arrest diabetic neuropathy: effects on hyperalgesia and impaired nerve regeneration in rats. Exp. Neurol. 140 (1996), 198–205.