Trk receptor signaling and sensory neuron fate are perturbed in human neuropathy caused by Gars mutations

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 16, 2017, Pages E3324-E3333

  Sleigha, James N ^a   Dawesb, John M ^b   Westb, Steven J ^b   Weic, Na ^c   Spauldingd, Emily L ^d,e   Gómez Martína, Adriana ^a   Zhangc, Qian ^c   Burgessd, Robert W ^d,e   Caderb, M Zameel ^b   Talbotb, Kevin ^b   Yangc, Xiang Lei ^c   Bennettb, David L ^b   Schiavoa, Giampietro ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d JACKSON LABORATORY   (United States)

^e UNIVERSITY OF MAINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN PROTEIN; TROPOMYOSIN; TROPOMYOSIN RECEPTOR KINASE A RECEPTOR; TROPOMYOSIN RECEPTOR KINASE B RECEPTOR; TROPOMYOSIN RECEPTOR KINASE C RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN FUNCTION; CELL FATE; FEMALE; GARS GENE; IN VITRO STUDY; MALE; MOUSE; MUTATOR GENE; NERVE CELL DIFFERENTIATION; NEUROPATHOLOGY; NEUROPATHY; NONHUMAN; PRIORITY JOURNAL; SENSORY DYSFUNCTION; SENSORY NERVE; SENSORY NERVE CELL; SPINAL GANGLION;

EID: 85017657631     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1614557114/-/DCSupplemental     Document Type: Article

References (74)

1. Reilly MM, Murphy SM, Laurá M (2011) Charcot-Marie-Tooth disease. J Peripher Nerv Syst 16:1-14.
2. El-Abassi R, England JD, Carter GT (2014) Charcot-Marie-Tooth disease: An overview of genotypes, phenotypes, and clinical management strategies. PM R 6:342-355.
3. Skre H (1974) Genetic and clinical aspects of Charcot-Marie-Tooth's disease. Clin Genet 6:98-118.
4. Antonellis A, et al. (2003) Glycyl tRNA synthetase mutations in Charcot-Marie-Tooth disease type 2D and distal spinal muscular atrophy type V. Am J Hum Genet 72:1293-1299.
5. Jordanova A, et al. (2006) Disrupted function and axonal distribution of mutant tyrosyl-TRNA synthetase in dominant intermediate Charcot-Marie-Tooth neuropathy. Nat Genet 38:197-202.
6. Latour P, et al. (2010) A major determinant for binding and aminoacylation of tRNA(Ala) in cytoplasmic Alanyl-TRNA synthetase is mutated in dominant axonal Charcot-Marie-Tooth disease. Am J Hum Genet 86:77-82.
7. McLaughlin HM, et al.; NISC Comparative Sequencing Program (2010) Compound heterozygosity for loss-of-function lysyl-TRNA synthetase mutations in a patient with peripheral neuropathy. Am J Hum Genet 87:560-566.
8. Vester A, et al.; NISC Comparative Sequencing Program (2013) A loss-of-function variant in the human histidyl-TRNA synthetase (HARS) gene is neurotoxic in vivo. Hum Mutat 34:191-199.
9. Motley WW, Talbot K, Fischbeck KH (2010) GARS axonopathy: Not every neuron's cup of tRNA. Trends Neurosci 33:59-66.
10. Storkebaum E (2016) Peripheral neuropathy via mutant tRNA synthetases: Inhibition of protein translation provides a possible explanation. BioEssays 38:818-829.
11. Seburn KL, Nangle LA, Cox GA, Schimmel P, Burgess RW (2006) An active dominant mutation of glycyl-TRNA synthetase causes neuropathy in a Charcot-Marie-Tooth 2D mouse model. Neuron 51:715-726.
12. Achilli F, et al. (2009) An ENU-induced mutation in mouse glycyl-TRNA synthetase (GARS) causes peripheral sensory and motor phenotypes creating a model of Charcot- Marie-Tooth type 2D peripheral neuropathy. Dis Model Mech 2:359-373.
13. Nangle LA, Zhang W, Xie W, Yang XL, Schimmel P (2007) Charcot-Marie-Tooth disease-Associated mutant tRNA synthetases linked to altered dimer interface and neurite distribution defect. Proc Natl Acad Sci USA 104:11239-11244.
14. Xie W, Nangle LA, Zhang W, Schimmel P, Yang XL (2007) Long-range structural effects of a Charcot-Marie-Tooth disease-causing mutation in human glycyl-TRNA synthetase. Proc Natl Acad Sci USA 104:9976-9981.
15. Motley WW, et al. (2011) Charcot-Marie-Tooth-linked mutant GARS is toxic to peripheral neurons independent of wild-Type GARS levels. PLoS Genet 7:e1002399.
16. He W, et al. (2011) Dispersed disease-causing neomorphic mutations on a single protein promote the same localized conformational opening. Proc Natl Acad Sci USA 108: 12307-12312.
17. Grice SJ, et al. (2015) Dominant, toxic gain-of-function mutations in gars lead to noncell autonomous neuropathology. Hum Mol Genet 24:4397-4406.
18. He W, et al. (2015) CMT2D neuropathy is linked to the neomorphic binding activity of glycyl-TRNA synthetase. Nature 526:710-714.
19. Park MC, et al. (2012) Secreted human glycyl-TRNA synthetase implicated in defense against ERK-Activated tumorigenesis. Proc Natl Acad Sci USA 109:E640-E647.
20. Sivakumar K, et al. (2005) Phenotypic spectrum of disorders associated with glycyltRNA synthetase mutations. Brain 128:2304-2314.
21. Del Bo R, et al. (2006) Coexistence of CMT-2D and distal SMA-V phenotypes in an Italian family with a GARS gene mutation. Neurology 66:752-754.
22. Hamaguchi A, Ishida C, Iwasa K, Abe A, Yamada M (2010) Charcot-Marie-Tooth disease type 2D with a novel glycyl-TRNA synthetase gene (GARS) mutation. J Neurol 257:1202-1204.
23. Sun A, et al. (2015) A novel mutation of the glycyl-TRNA synthetase (GARS) gene associated with Charcot-Marie-Tooth type 2D in a Chinese family. Neurol Res 37:782-787.
24. Lee HJ, et al. (2012) Two novel mutations of GARS in Korean families with distal hereditary motor neuropathy type V. J Peripher Nerv Syst 17:418-421.
25. VanLangenhove T, vanderZee J, VanBroeckhoven C (2012) The molecular basis of the frontotemporal lobar degeneration-Amyotrophic lateral sclerosis spectrum. Ann Med 44:817-828.
26. LePichon CE, Chesler AT (2014) The functional and anatomical dissection of somatosensory subpopulations using mouse genetics. Front Neuroanat 8:21.
27. Lallemend F, Ernfors P (2012) Molecular interactions underlying the specification of sensory neurons. Trends Neurosci 35:373-381.
28. Sleigh JN, Grice SJ, Burgess RW, Talbot K, Cader MZ (2014) Neuromuscular junction maturation defects precede impaired lower motor neuron connectivity in Charcot- Marie-Tooth type 2D mice. Hum Mol Genet 23:2639-2650.
29. Harper AA, Lawson SN (1985) Conduction velocity is related to morphological cell type in rat dorsal root ganglion neurones. J Physiol 359:31-46.
30. Chen XJ, et al. (2007) Proprioceptive sensory neuropathy in mice with a mutation in the cytoplasmic Dynein heavy chain 1 gene. J Neurosci 27:14515-14524.
31. G93A displays early pathology of sensory small fibers associated to accumulation of a neurotoxic splice variant of peripherin. Hum Mol Genet 25:1588-1599.
32. Sommer EW, Kazimierczak J, Droz B (1985) Neuronal subpopulations in the dorsal root ganglion of the mouse as characterized by combination of ultrastructural and cytochemical features. Brain Res 346:310-326.
33. Lawson SN, Harper AA, Harper EI, Garson JA, Anderton BH (1984) A monoclonal antibody against neurofilament protein specifically labels a subpopulation of rat sensory neurones. J Comp Neurol 228:263-272.
34. Parysek LM, Goldman RD (1988) Distribution of a novel 57 kDa intermediate filament (IF) protein in the nervous system. J Neurosci 8:555-563.
35. Ferri GL, et al. (1990) Neuronal intermediate filaments in rat dorsal root ganglia: differential distribution of peripherin and neurofilament protein immunoreactivity and effect of capsaicin. Brain Res 515:331-335.
36. Bae JY, KimJH, Cho YS, Mah W, Bae YC (2015) Quantitative analysis of afferents expressing substance P, calcitonin gene-related peptide, isolectin B4, neurofilament 200, and Peripherin in the sensory root of the rat trigeminal ganglion. J Comp Neurol 523:126-138.
37. Zhao J, et al. (2010) Small RNAs control sodium channel expression, nociceptor excitability, and pain thresholds. J Neurosci 30:10860-10871.
38. Lekan HA, Chung K, Yoon YW, Chung JM, Coggeshall RE (1997) Loss of dorsal root ganglion cells concomitant with dorsal root axon sprouting following segmental nerve lesions. Neuroscience 81:527-534.
39. Tandrup T, Woolf CJ, Coggeshall RE (2000) Delayed loss of small dorsal root ganglion cells after transection of the rat sciatic nerve. J Comp Neurol 422:172-180.
40. Stifani N (2014) Motor neurons and the generation of spinal motor neuron diversity. Front Cell Neurosci 8:293.
41. Friese A, et al. (2009) Gamma and alpha motor neurons distinguished by expression of transcription factor Err3. Proc Natl Acad Sci USA 106:13588-13593.
42. Spaulding EL, et al. (2016) Synaptic deficits at neuromuscular junctions in two mouse models of Charcot-Marie-Tooth type 2d. J Neurosci 36:3254-3267.
43. deNooij JC, Doobar S, Jessell TM (2013) Etv1 inactivation reveals proprioceptor subclasses that reflect the level of NT3 expression in muscle targets. Neuron 77:1055-1068.
44. Alvarez FJ, Morris HR, Priestley JV (1991) Sub-populations of smaller diameter trigeminal primary afferent neurons defined by expression of calcitonin gene-related peptide and the cell surface oligosaccharide recognized by monoclonal antibody LA4. J Neurocytol 20:716-731.
45. Scherrer G, et al. (2009) Dissociation of the opioid receptor mechanisms that control mechanical and heat pain. Cell 137:1148-1159.
46. Cavanaugh DJ, et al. (2009) Distinct subsets of unmyelinated primary sensory fibers mediate behavioral responses to noxious thermal and mechanical stimuli. Proc Natl Acad Sci USA 106:9075-9080.
47. McCoy ES, et al. (2013) Peptidergic CGRPα primary sensory neurons encode heat and itch and tonically suppress sensitivity to cold. Neuron 78:138-151.
48. Oliveira Fernandes M, Tourtellotte WG (2015) Egr3-dependent muscle spindle stretch receptor intrafusal muscle fiber differentiation and fusimotor innervation homeostasis. J Neurosci 35:5566-5578.
49. Wickramasinghe SR, et al. (2008) Serum response factor mediates NGF-dependent target innervation by embryonic DRG sensory neurons. Neuron 58:532-545.
50. Patel TD, Jackman A, Rice FL, Kucera J, Snider WD (2000) Development of sensory neurons in the absence of NGF/TrkA signaling in vivo. Neuron 25:345-357.
51. Lu J, Zhou XF, Rush RA (2001) Small primary sensory neurons innervating epidermis and viscera display differential phenotype in the adult rat. Neurosci Res 41:355-363.
52. 2+indicators with greatly improved fluorescence properties. J Biol Chem 260:3440-3450.
53. Caterina MJ, et al. (1997) The capsaicin receptor: A heat-Activated ion channel in the pain pathway. Nature 389:816-824.
54. Lindsay RM (1996) Role of neurotrophins and trk receptors in the development and maintenance of sensory neurons: An overview. Philos Trans R Soc Lond B Biol Sci 351:365-373.
55. Terenzio M, et al. (2014) Bicaudal-D1 regulates the intracellular sorting and signalling of neurotrophin receptors. EMBO J 33:1582-1598.
56. Huang EJ, Reichardt LF (2003) Trk receptors: Roles in neuronal signal transduction. Annu Rev Biochem 72:609-642.
57. Patapoutian A, Reichardt LF (2001) Trk receptors: Mediators of neurotrophin action. Curr Opin Neurobiol 11:272-280.
58. Kitao Y, Robertson B, Kudo M, Grant G (1996) Neurogenesis of subpopulations of rat lumbar dorsal root ganglion neurons including neurons projecting to the dorsal column nuclei. J Comp Neurol 371:249-257.
59. Maro GS, et al. (2004) Neural crest boundary cap cells constitute a source of neuronal and glial cells of the PNS. Nat Neurosci 7:930-938.
60. Stucky CL, DeChiara T, Lindsay RM, Yancopoulos GD, Koltzenburg M (1998) Neurotrophin 4 is required for the survival of a subclass of hair follicle receptors. J Neurosci 18:7040-7046.
61. Smeyne RJ, et al. (1994) Severe sensory and sympathetic neuropathies in mice carrying a disrupted Trk/NGF receptor gene. Nature 368:246-249.
62. Ernfors P, Lee KF, Kucera J, Jaenisch R (1994) Lack of neurotrophin-3 leads to deficiencies in the peripheral nervous system and loss of limb proprioceptive afferents. Cell 77:503-512.
63. Moqrich A, et al. (2004) Expressing TrkC from the TrkA locus causes a subset of dorsal root ganglia neurons to switch fate. Nat Neurosci 7:812-818.
64. Fitzgerald M (2005) The development of nociceptive circuits. Nat Rev Neurosci 6:507-520.
65. von Hehn CA, Baron R, Woolf CJ (2012) Deconstructing the neuropathic pain phenotype to reveal neural mechanisms. Neuron 73:638-652.
66. Sleigh JN, Schiavo G (2016) Older but not slower: Aging does not alter axonal transport dynamics of signalling endosomes in vivo. J Neurosci Methods 257:26-33.
67. Sleigh JN, et al. (2014) Chondrolectin affects cell survival and neuronal outgrowth in in vitro and in vivo models of spinal muscular atrophy. Hum Mol Genet 23:855-869.
68. Sleigh JN, Weir GA, Schiavo G (2016) A simple, step-by-step dissection protocol for the rapid isolation of mouse dorsal root ganglia. BMC Res Notes 9:82.
69. Malin SA, Davis BM, Molliver DC (2007) Production of dissociated sensory neuron cultures and considerations for their use in studying neuronal function and plasticity. Nat Protoc 2:152-160.
70. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53:55-63.
71. Carter RJ, Morton J, Dunnett SB (2001) Motor coordination and balance in rodents. Curr Protoc Neurosci Chapter 8:Unit 8.12.
72. Randall LO, Selitto JJ (1957) A method for measurement of analgesic activity on inflamed tissue. Arch Int Pharmacodyn Ther 111:409-419.
73. Hargreaves K, Dubner R, Brown F, Flores C, Joris J (1988) A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32:77-88.
74. Bogdanik LP, et al. (2013) Loss of the E3 ubiquitin ligase LRSAM1 sensitizes peripheral axons to degeneration in a mouse model of Charcot-Marie-Tooth disease. Dis Model Mech 6:780-792.