Human diseases associated with NTE gene

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Abstract

Evolutionary conserved NTE gene is important for survival and functioning of nervous system cells, its dysfunction leads to various pathologies. Here we describe characteristics of different disorders induced by NTE protein activity inhibition (OPIDN) or by NTE gene mutations: hereditary spastic paraplegia (SPG39), Boucher – Neuhaüser, Gordon Holmes, Laurence – Moon, Oliver – McFarlane syndromes, Leber congenital amaurosis, pure cerebellar ataxia. Current review summarises accumulated data about clinical features of NTE associated diseases, presenting them in a historical way of biomedical studies, and observes molecular and genetic causes of these disorders.

About the authors

Pavel A. Melentev

Petersburg Nuclear Physics Institute named by B.P. Konstantinov of NRC “Kurchatov Institute”

Email: melentev_pa@pnpi.nrcki.ru

PhD student. Laboratory of Experimental and Applied Genetics

Russian Federation, Gatchina

Olga E. Agranovich

Turner Scientific Research Institute for Children’s Orthopedics

Email: olga_agranovich@yahoo.com

Doctor of Medicine, Head of Artrogriposis Department, Orthopedic Trauma Surgeon

Russian Federation, Pushkin, Saint Petersburg

Svetlana V. Sarantseva

Petersburg Nuclear Physics Institute named by B.P. Konstantinov of NRC “Kurchatov Institute”

Author for correspondence.
Email: sarantseva_sv@pnpi.nrcki.ru

Doctor of Science, Head of Laboratory of Experimental and Applied Genetics, Deputy Director for Science. Petersburg Nuclear Physics Institute named by B.P. Konstantinov of NRC

Russian Federation, Gatchina

References

  1. Kienesberger P, Oberer M, Lass A, Zechner R. Mammalian patatin domain containing proteins: a family with diverse lipolytic activities involved in multiple biological functions. J Lipid Res. 2008;50(Suppl):S63-S68. https://doi.org/ 10.1194/jlr.r800082-jlr200.
  2. Glynn P. Neural development and neurodegeneration: two faces of Neuropathy Target Esterase. Prog Neurobiol. 2000;61(1):61-74. https://doi.org/10.1016/s0301-0082(99)00043-x.
  3. Moser M, Stempfl T, Li Y, et al. Cloning and expression of the murine sws/NTE gene. Mech Dev. 2000;90(2):279-282. https://doi.org/10.1016/s0925-4773(99)00239-7.
  4. Moser M, Li Y, Vaupel K, et al. Placental failure and impaired vasculogenesis result in embryonic lethality for neuropathy target esterase-deficient mice. Mol Cell Biol. 2004;24(4):1667-1679. https://doi.org/10.1128/mcb.24.4.1667-1679.2004.
  5. Akassoglou K, Malester B, Xu J, et al. Brain-specific deletion of neuropathy target esterase/swiss cheese results in neurodegeneration. Proc Natl Acad Sci U S A. 2004;101(14):5075-5080. https://doi.org/10.1073/pnas.0401030101.
  6. Smith M, Elvove E. Pharmacological and chemical studies of the cause of so-called ginger paralysis: a preliminary report. Public Health Reports (1896-1970). 1930;45(30):1703. https://doi.org/10.2307/4579730.
  7. Aring C. The systemic nervous affinity of triorthocresyl phosphate (Jamaica ginger palsy). Brain. 1942;65(1):34-47. https://doi.org/10.1093/brain/65.1.34.
  8. Johnson M. Organophosphates and delayed neuropathy – is NTE alive and well? Toxicol Appl Pharmacol. 1990;102(3):385-399. https://doi.org/10.1016/0041-008x(90)90036-t.
  9. Hou W, Long D, Wang H, et al. The homeostasis of phosphatidylcholine and lysophosphatidylcholine was not disrupted during tri-o-cresyl phosphate-induced delayed neurotoxicity in hens. Toxicology. 2008;252(1-3):56-63. https://doi.org/10.1016/j.tox.2008.07.061.
  10. Johnson M, Jacobsen D, Meredith T, et al. Evaluation of antidotes for poisoning by organophosphorus pesticides. Emerg Med Australas. 2000;12(1):22-37. https://doi.org/10.1046/j.1442-2026.2000.00087.x.
  11. Salvi R. Neuropsychiatric Evaluation in subjects chronically exposed to organophosphate pesticides. Toxicol Sci. 2003;72(2):267-271. https://doi.org/10.1093/toxsci/kfg034.
  12. Johnson M. The delayed neurotoxic effect of some organophosphorus compounds. Identification of the phosphorylation site as an esterase. Biochem J. 1969;114(4):711-717. https://doi.org/10.1042/bj1140711.
  13. Johnson M. A phosphorylation site in brain and the delayed neurotoxic effect of some organophosphorus compounds. Biochem J. 1969;111(4): 487-495. https://doi.org/10.1042/bj1110487.
  14. Craig P, Barth M. Evaluation of the hazards of industrial exposure to tricresyl phosphate: a review and interpretation of the literature. J Toxicol Environ Health B Crit Rev. 1999;2(4):281-300. https://doi.org/10.1080/109374099281142.
  15. Emerick GL, Deoliveira GH, Santos ACD, Ehrich M. Mechanisms for consideration for intervention in the development of organophosphorus-induced delayed neuropathy. Chem Biol Interact. 2012;199(3):177-184. https://doi.org/10.1016/j.cbi.2012.07.002.
  16. Johnson MK. Improved assay of neurotoxic esterase for screening organophosphates for delayed neurotoxicity potential. Arch Toxicol. 1977;37(2): 113-115. https://doi.org/10.1007/bf00293860.
  17. Cavanagh JB. The toxic effects of tri-ortho-cresyl phosphate on the nervous system: an experimental study in hens. J Neurol Neurosurg Psychiatry. 1954;17(3):163-172. https://doi.org/10.1136/jnnp.17.3.163.
  18. Dudek BR, Richardson RJ. Evidence for the existence of neurotoxic esterase in neural and lymphatic tissue of the adult hen. Biochem Pharmacol. 1982;31(6):1117-1121. https://doi.org/ 10.1016/0006-2952(82)90351-3.
  19. Bertoncin D, Russolo A, Caroldi S, Lotti M. Neuropathy target esterase in human lymphocytes. Archives of Environmental Health: An International Journal. 1985;40(3):139-144. https://doi.org/10.1080/00039896.1985.10545905.
  20. Makhaeva GF, Rudakova EV, Sigolaeva LV, et al. Neuropathy target esterase in mouse whole blood as a biomarker of exposure to neuropathic organophosphorus compounds. J Appl Toxicol. 2016;36(11):1468-1475. https://doi.org/10.1002/jat.3305.
  21. Emerick GL, Peccinini RG, Oliveira GHD. Organophosphorus-induced delayed neuropathy: A simple and efficient therapeutic strategy. Toxicol Lett. 2010;192(2):238-244. https://doi.org/10.1016/j.toxlet.2009.10.032.
  22. Jortner BS. Preparation and analysis of the peripheral nervous system. Toxicol Pathol. 2010;39(1): 66-72. https://doi.org/10.1177/0192623310387618.
  23. Gupta RP, Abou-Donia MB. Tau proteins-enhanced Ca2/calmodulin (CaM)-dependent phosphorylation by the brain supernatant of diisopropyl phosphorofluoridate (DFP)-treated hen: tau mutants indicate phosphorylation of more amino acids in tau by CaM kinase II. Brain Res. 1998;813(1):32-43. https://doi.org/10.1016/s0006-8993(98)00988-3.
  24. Faber I, Pereira ER, Martinez AR, et al. Hereditary spastic paraplegia from 1880 to 2017: an historical review. Arq Neuropsiquiatr. 2017;75(11):813-818. https://doi.org/10.1590/0004-282X20170160.
  25. de Souza PV, de Rezende Pinto WB, de Rezende Batistella GN, et al. Hereditary spastic paraplegia: clinical and genetic hallmarks. The Cerebellum. 2017;16(2):525-551. https://doi.org/10.1007/s12311-016-0803-z.
  26. Seeligmüller A. Sklerose der seitenstrange des ruckenmards bei vier kindern derselben gamilie. Dtsch Med Wochenshnr. 1876;2:185-186.
  27. Strümpell A. Beiträge zur Pathologie des Rückenmarks. Eur Arch Psychiatry Clin Neurosci. 1880;10(3):676-717. https://doi.org/10.1007/bf02054821.
  28. Rhein JH. Family spastic paralysis. The Journal of Nervous and Mental Disease. 1916;44(2): 115-144. https://doi.org/10.1097/00005053-191609000-00004.
  29. Garland HG, Astley CE. Hereditary spastic paraplegia with amyotrophy and pes cavus. J Neurol Neurosurg Psychiatry Res. 1950;13(2):130-133. https://doi.org/10.1136/jnnp.13.2.130.
  30. Bickerstaff ER. Hereditary spastic paraplegia. J Neurol Neurosurg Psychiatry Res. 1950;13(2): 134-145. https://doi.org/10.1136/jnnp.13.2.134.
  31. Strümpell A. Die primäre Seitenstrangsklerose (spastische Spinalparalyse). Deutsche Zeitschrift für Nervenheilkunde. 1904;27(3-4):291-339. https://doi.org/10.1007/bf01667115.
  32. Deluca GC, Ebers GC, Esiri MM. The extent of axonal loss in the long tracts in hereditary spastic paraplegia. Neuropathol Appl Neurobiol. 2004;30(6):576-584. https://doi.org/10.1111/j.1365-2990.2004.00587.x.
  33. Schut JW, Haymaker W. Hereditary ataxia: a pathologic study of five cases of common ancestry. J Neuropathol Clin Neurol. 1951;1(3):183-213.
  34. Behan WM, Maia M. Strumpells familial spastic paraplegia: genetics and neuropathology. J Neurol Neurosurg Psychiatry Res. 1974;37(1):8-20. https://doi.org/10.1136/jnnp.37.1.8.
  35. Greenfield JG, Aring CD. The spino-cerebellar degenerations. Edited by Charles D. Aring. Blackwell Scientific Publications; 1954.
  36. Rainier S, Bui M, Mark E, et al. Neuropathy target esterase gene mutations cause motor neuron disease. Am J Hum Genet. 2008;82(3):780-785. https://doi.org/10.1016/j.ajhg.2007.12.018.
  37. Rainier S, Albers JW, Dyck PJ, et al. Motor neuron disease due to neuropathy target esterase gene mutation: clinical features of the index families. Muscle Nerve. 2010;43(1):19-25. https://doi.org/10.1002/mus.21777.
  38. Synofzik M, Gonzalez MA, Lourenco CM, et al. PNPLA6 mutations cause Boucher – Neuhäuser and Gordon Holmes syndromes as part of a broad neurodegenerative spectrum. Brain. 2013;137(1):69-77. https://doi.org/10.1093/brain/awt326.
  39. Tarnutzer AA, Gerth-Kahlert C, Timmann D, et al. Boucher – Neuhäuser syndrome: cerebellar degeneration, chorioretinal dystrophy and hypogonadotropic hypogonadism: two novel cases and a review of 40 cases from the literature. J Neurol. 2014;262(1):194-202. https://doi.org/10.1007/s00415-014-7555-9.
  40. Teive HA, Camargo CH, Sato MT, et al. Different cerebellar ataxia phenotypes associated with mutations of the PNPLA6 gene in Brazilian patients with recessive ataxias. The Cerebellum. 2017;17(3):380-385. https://doi.org/10.1007/s12311-017-0909-y.
  41. Boucher RJ, Gibberd FB. Familial ataxia, hypogonadism and retinal degeneration. Acta Neurol Scand. 2009;45(4):507-510. https://doi.org/10.1111/j.1600-0404.1969.tb01261.x.
  42. Neuhäuser G, Opitz JM. Autosomal recessive syndrome of cerebellar ataxia and hypogonadotropic hypogonadism. Clin Genet. 2008;7(5):426-434. https://doi.org/10.1111/j.1399-0004.1975.tb00353.x.
  43. Limber ER, Bresnick GH, Lebovitz RM, et al. Spinocerebellar ataxia, hypogonadotropic hypogonadism, and choroidal dystrophy (Boucher – Neuhäuser syndrome. Am J Med Genet. 1989;33(3):409-414. https://doi.org/10.1002/ajmg.1320330325.
  44. Rump R, Hamel BC, Pinckers AJ, Dop PAV. Two sibs with chorioretinal dystrophy, hypogonadotrophic hypogonadism, and cerebellar ataxia: Boucher – Neuhäuser syndrome. J Med Genet. 1997;34(9):767-771. https://doi.org/10.1136/jmg.34.9.767.
  45. Sak JJ, Grzybowski A, Baj J. Sir Gordon Morgan Holmes (1876–1965): one of the founders of modern neurology. Neurol Sci. 2017;39(1): 169-171. https://doi.org/10.1007/s10072-017-3180-6.
  46. Holmes G. A form of familial degeneration of the cerebellum. Brain. 1908;30(4):466-489. https://doi.org/10.1093/brain/30.4.466.
  47. Topaloglu AK, Lomniczi A, Kretzschmar D, et al. Loss-of-function mutations in PNPLA6 encoding neuropathy target esterase underlie pubertal failure and neurological deficits in Gordon Holmes syndrome. J Clin Endocrinol Metab. 2014;99(10). https://doi.org/10.1210/jc.2014-1836.
  48. Hufnagel RB, Arno G, Hein ND, et al. Neuropathy target esterase impairments cause Oliver – McFarlane and Laurence – Moon syndromes. J Med Genet. 2015;52(2):85-94. https://doi.org/10.1136/jmedgenet-2014-102856.
  49. Kmoch S, Majewski J, Ramamurthy V, et al. Mutations in PNPLA6 are linked to photoreceptor degeneration and various forms of childhood blindness. Nat Commun. 2015;6(1). https://doi.org/10.1038/ncomms6614.
  50. Oliver GL, McFarlane DC. Congenital trichomegaly: with associated pigmentary degeneration of the retina, dwarfism, and mental retardation. Arch Ophthalmol. 1965;74(2):169-171. https://doi.org/10.1001/archopht.1965.00970040171008.
  51. Patton M, Harding A, Baraitser M. Congenital trichomegaly, pigmentary retinal degeneration, and short stature. Am J Ophthalmol. 1986;101(4):490-491. https://doi.org/10.1016/0002-9394(86)90656-2.
  52. Laurence JZ. Four cases of retinitis pigmentosa occurring in the same family, and accompanied by general imperfections of development. Ophthalmol Rev. 1866;2:32-41.
  53. Laurence JZ, Moon RC. Four cases of «retinitis pigmentosa» occurring in the same family, and accompanied by general imperfections of development. Obes Res. 1995;3(4):400-403. https://doi.org/10.1002/j.1550-8528.1995.tb00166.x.
  54. Bowen P. The Laurence-Moon syndrome. Association with hypogonadotrophic hypogonadism and sex-chromosome aneuploidy. Arch Intern Med. 1965;116(4):598-604. https://doi.org/10.1001/archinte.116.4.598.
  55. Kumaran N, Moore AT, Weleber RG, Michaelides M. Leber congenital amaurosis/early-onset severe retinal dystrophy: clinical features, molecular genetics and therapeutic interventions. Br J Ophthalmol. 2017;101(9):1147-1154. https://doi.org/10.1136/bjophthalmol-2016-309975.
  56. Wiethoff S, Bettencourt C, Paudel R, et al. Pure Cerebellar Ataxia with Homozygous Mutations in the PNPLA6 Gene. The Cerebellum. 2016;16(1):262-267. https://doi.org/10.1007/s12311-016-0769-x.
  57. Synofzik M, Schüle R. Overcoming the divide between ataxias and spastic paraplegias: Shared phenotypes, genes, and pathways. Mov Disord. 2017;32(3):332-345. https://doi.org/10.1002/mds.26944.

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Copyright (c) 2020 Melentev P.A., Agranovich O.E., Sarantseva S.V.

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