Perinatal exposure to lead (Pb) promotes Tau phosphorylation in the rat brain in a GSK-3β and CDK5 dependent manner: Relevance to neurological disorders

Toxicology

Volumn 347-349, Issue , 2016, Pages 17-28

  Gassowska, Magdalena ^a   Baranowska Bosiacka, Irena ^b   Moczydłowska, Joanna ^a   Tarnowski, Maciej ^b   Pilutin, Anna ^b   Gutowska, Izabela ^b   Struzyńska, Lidia ^a   Chlubek, Dariusz ^b   Adamczyk, Agata ^a  

^a MOSSAKOWSKI MEDICAL RESEARCH CENTRE   (Poland)

^b POMERANIAN MEDICAL UNIVERSITY   (Poland)

Author keywords

CDK5; GSK 3 ; Hyperphosphorylation; Lead neurotoxicity; Rat brain; Tau protein

Indexed keywords

CALPAIN; CYCLIN DEPENDENT KINASE 5; GLYCOGEN SYNTHASE KINASE 3BETA; LEAD ACETATE; MESSENGER RNA; PROTEIN P25; TAU PROTEIN; TRYPTOPHAN DERIVATIVE; CDK5 PROTEIN, RAT; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; LEAD;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CEREBELLUM; CONTROLLED STUDY; DENTATE GYRUS; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FEMALE; FOREBRAIN; GESTATIONAL AGE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; LEAD BLOOD LEVEL; MALE; NEUROPATHOLOGY; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PYRAMIDAL NERVE CELL; RAT; TISSUE STRUCTURE; UPREGULATION; WEANING; ANIMAL; BRAIN; CHEMICALLY INDUCED; DRUG EFFECTS; METABOLISM; NEUROLOGIC DISEASE; NEWBORN; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; WISTAR RAT;

ANIMALS; ANIMALS, NEWBORN; BRAIN; CYCLIN-DEPENDENT KINASE 5; FEMALE; GLYCOGEN SYNTHASE KINASE 3; LEAD; MALE; NERVOUS SYSTEM DISEASES; PHOSPHORYLATION; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, WISTAR; TAU PROTEINS;

EID: 84961588822     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2016.03.002     Document Type: Article

References (60)

1. Alonso A.D., Mederlyova A., Novak M., Grundke-Iqbal I., Iqbal K. Promotion of hyperphosphorylation by frontotemporal dementia tau mutations. J. Biol. Chem. 2004, 279:34873-34881.
2. Baranowska-Bosiacka I., Chlubek D. Biochemical mechanisms of neurotoxic lead activity. Postepy Biochem. 2006, 52(3):320-329.
3. Baranowska-Bosiacka I., Gutowska I., Rybicka M., Nowacki P., Chlubek D. Neurotoxicity of lead. Hypothetical molecular mechanisms of synaptic function disorders. Neurol. Neurochir. Pol. 2012, 46(6):569-578.
4. Baranowska-Bosiacka I., Gutowska I., Marchlewicz M., Marchetti C., Kurzawski M., Dziedziejko V., Kolasa A., Olszewska M., Rybicka M., Safranow K., Nowacki P., Wiszniewska B., Chlubek D. Disrupted pro- and antioxidative balance as a mechanism of neurotoxicity induced by perinatal exposure to lead. Brain Res. 2012, 1435:56-71.
5. Baranowska-Bosiacka I., Struzyńska L., Gutowska I., Machalińska A., Kolasa A., Kłos P., Czapski G.A., Kurzawski M., Prokopowicz A., Marchlewicz M., Safranow K., Machaliński B., Wiszniewska B., Chlubek D. Perinatal exposure to lead induces morphological, ultrastructural and molecular alterations in the hippocampus. Toxicology 2013, 7(303):187-200.
6. Basha M.R., Wei W., Bakheet S.A., Benitez N., Siddiqi H.K., Ge Y.W., Lahiri D.K., Zawia N.H. The fetal basis of amyloidogenesis: exposure to lead and latent overexpression of amyloid precursor protein and beta-amyloid in the aging brain. J. Neurosci. 2005, 25(4):823-829.
7. Basha M.R., Murali M., Siddiqi H.K., Ghosal K., Siddiqi O.K., Lashuel H.A., Ge Y.W., Lahiri D.K., Zawia N.H. Lead (Pb) exposure and its effect on APP proteolysis and Abeta aggregation. FASEB J. 2005, 19(14):2083-2084.
8. Bellinger D.C. Very low lead exposures and children's neurodevelopment. Curr. Opin. Pediatr. 2008, 20:172-177.
9. Bihaqi S.W., Zawia N.H. Enhanced taupathy and AD-like pathology in aged primate brains decades after infantile exposure to lead (Pb). Neurotoxicology 2013, 39:95-101.
10. Bihaqi S.W., Bahmani A., Adem A., Zawia N.H. Infantile postnatal exposure to lead (Pb) enhances tau expression in the cerebral cortex of aged mice: relevance to AD. Neurotoxicology 2014, 44:114-120.
11. Bihaqi S.W., Bahmani A., Subaiea G.M., Zawia N.H. Infantile exposure to lead and late-age cognitive decline: relevance to AD. Alzheimers Dement. 2014, 10(2):187-195.
12. Bramblett G.T., Goedert M., Jakes R., Merrick S.E., Trojanowski J.Q., Lee V.M. Abnormal tau phosphorylation at Ser396 in Alzheimer's disease recapitulates development and contributes to reduce microtubule binding. Neuron 1993, 10(6):1089-1099.
13. CDC (Centers for Disease Control and Prevention) Interpreting and managing blood lead levels <10 μg/dL in children and reducing childhood exposures to lead: recommendations of CDC's advisory committee on childhood lead poisoning prevention. MMWR Recomm. Rep. 2007, 56:1-16. Available:. http://www.cdc.gov/mmwr/preview/mmwrhtml/rr5608a1.htm.
14. Canfield R.L., Henderson C.R., Cory-Slechta D., Cox C., Jusko T.A., Lanphear B.P. Intellectual impairment in children with blood lead concentrations below 10 microg per decilitre. N. Engl. J. Med. 2003, 348:1517-1526.
15. Chiodo L.M., Jacobson S.W., Jacobson J.L. Neurodevelopmental effects of postnatal lead exposure at very low levels. Neurotoxicol. Teratol. 2004, 3:359-371.
16. Collins M.F., Hrdina P.D., Whittle E. Lead in blood and brain regions of rats chronically exposed to low doses of the metal. Toxicol. Appl. Pharmacol. 1982, 65(2):314-322.
17. Coon S., Stark A., Peterson E., Gloi A., Kortsha G., Pounds J., Chettle D., Gorell J. Whole-body lifetime occupational lead exposure and risk of Parkinson's disease. Environ. Health Perspect. 2006, 114(12):1872-1876.
18. Counter S.A., Buchanan L.H., Ortega F. Neurocognitive impairment in lead-exposed children of Andean lead-glazing workers. J. Occup. Environ. Med. 2005, 47:306-312.
19. Duka T., Rusnak M., Drolet R.E., Duka V., Wersinger Ch., Goudreau J.L., Sidhu A. Alpha-Synuclein induces hyperphosphorylation of Tau in the MPTP model of Parkinsonism. FASEB J. 2006, 20(13):2302-2312.
20. Duka T., Duka V., Joyce J.N., Sidhu A. α-Synuclein contributes to GSK-3-catalyzed Tau phosphorylation in Parkinson's disease models. FASEB J. 2009, 23:2820-2830.
21. Engmann O., Giese K.P. Crosstalk between Cdk5 and GSK3beta: implications for Alzheimer's disease. Front. Mol. Neurosci. 2009, 2(2):1-5.
22. Frasier M., Walzer M., McCarthy L., Magnuson D., Lee J.M., Haas C., Kahle P., Wolozin B. Tau phosphorylation increases in symptomatic mice overexpressing A30P α-synuclein. Exp. Neurol. 2005, 192(2):274-287.
23. Fuentes-Albero M., Puig-Alcaraz C., Cauli O. Lead excretion in Spanish children with autism spectrum disorder. Brain Sci. 2015, 5:58-68.
24. Garcia M.L., Cleveland D.W. Going new places using an old MAP: tau, microtubules and human neurodegenerative disease. Curr. Opin. Cell Biol. 2001, 13:41-48.
25. Geddes J.W. α-Synuclein: a potent inducer of tau pathology. Exp. Neurol. 2005, 192(2):244-250.
26. Gendron T.F., Petrucelli L. The role of tau in neurodegeneration. Mol. Neurodegener. 2009, 4(13):1-19.
27. Gu H., Robison G., Hong L., Barrea R., Wei X., Farlow M.R., Pushkar Y.N., Du Y., Zheng W. Increased β-amyloid deposition in Tg-SWDI transgenic mouse brain following in vivo lead exposure. Toxicol. Lett. 2012, 213(2):211-219.
28. Haggerty Th., Credle J., Rodriguez O., Wills J., Oaks A.W., Masliah E., Sidhu A. Hyperphosphorylated Tau in an α-synuclein-overexpressing transgenic model of Parkinson's disease. Eur. J. Neurosci. 2011, 33(9):1598-1610.
29. Igbal K., Liu F., Gong C.X., Grundke-Iqbal I. Tau in Alzheimer disease and related tauopathies. Curr. Alzheimer Res. 2010, 7(8):656-664.
30. Johnson G.V., Stoothoff W.H. Tau phosphorylation in neuronal cell function and dysfunction. J. Cell Sci. 2004, 117(Pt. 24):5721-5729.
31. Jope R.S., Yuskaitis J., Ch Beurel E. Glycogen synthase kinase 3 (GSK3): inflammation, diseases, and therapeutics. Neurochem. Res. 2007, 32(4-5):577-595.
32. Jusko T.A., Henderson C.R., Lanphear B.P., Cory-Slechta D.A., Parsons P.J., Canfield R.L. Blood lead concentrations <10 microg/dl and child intelligence at 6 years of age. Environ. Health Perspect. 2008, 116:243-248.
33. Kadak M.T., Cetin I., Tarakçioğlu M.C., Özer Ö.F., Kaçar S., Çimen B. Low serum level α-synuclein and tau protein in autism spectrum disorder compared to controls. Neuropediatrics 2015, 46(6):410-415.
34. Kang H.G., Jeong S.H., Cho M.R., Cho J.H., Bischoff K. Time-dependent changes in lead and delta-aminolevulinic acid after subchronic lead exposure in rats. Hum. Exp. Toxicol. 2009, 28(10):647-654.
35. Kawakami F., Suzuki M., Shimada N., Kagiya G., Ohta E., Tamura K., Maruyama H., Ichikawa T. Stimulatory effect of α-synuclein on the tau-phosphorylation by GSK-3b. FEBS J. 2011, 278(24):4895-4904.
36. Khandelwal P.J., Dumanis S.B., Feng L.R., Maguire-Zeiss K., Rebeck G., Lashuel H.A., Moussa C.E. Parkinson-related parkin reduces α-synuclein phosphorylation in a gene transfer model. Mol. Neurodegener. 2010, 5(47):1-13.
37. Kim S.M., Han D.H., Lyoo H.S., Min K.J., Kim K.H., Renshaw P. Exposure to environmental toxins in mothers of children with autism spectrum disorder. Psychiatry Investig. 2010, 7(2):122-127.
38. Kusakawa G., Saito T., Onuki R., Ishiguro K., Kishimoto T., Hisanaga S. Calpain-dependent proteolytic cleavage of the p35 cyclin-dependent kinase 5 activator to p25. J. Biol. Chem. 2000, 275(22):17166-17172.
39. Lee G., Thangavel R., Sharma V.M., Litersky J.M., Bhaskar K., Fang S.M., Do L.H., Andreadis A., Van Hoesen G., Ksiezak-Reding H. Phosphorylation of tau by fyn: implications for Alzheimer's disease. J. Neurosci. 2004, 24(9):2304-2312.
40. Lei P., Ayton S., Finkelstein D.I., Adlard P.A., Masters C.L., Bush A.I. Tau protein: eelevance to Parkinson's disease. Int. J. Biochem. Cell Biol. 2010, 42(11):1775-1778.
41. Li T., Paudel H.K. Glycogen synthase kinase 3beta phosphorylates Alzheimer's disease-specific Ser396 of microtubule-associated protein tau by a sequential mechanism. Biochemistry 2006, 45(10):3125-3133.
42. Lindsky Th.I., Shneider J.S. Autism and autistic symptoms associated with childhood lead poisoning. J. Appl. Res. 2005, 5(1):80-87.
43. Liu F., Xue Z., Li N., Huang H., Ying Y., Li J., Wang L., Li W. Effects of lead exposure on the expression of amyloid β and phosphorylated tau proteins in the C57BL/6 mouse hippocampus at different life stages. J. Trace Elem. Med. Biol. 2014, 28(2):227-232.
44. Mietelska-Porowska A., Wasik U., Goras M., Filipek A., Niewiadomska G. Tau protein modifications and interactions: their role in function and dysfunction. Int. J. Mol. Sci. 2014, 15(3):4671-4713.
45. Modgil S., Lahiri D.K., Sharma V.L., Anand A. Role of early life exposure and environment on neurodegeneration: implications on brain disorders. Transl. Neurodegener. 2014, 3(9):1-14.
46. Muntane G., Dalfo E., Martinez A., Ferrer I. Phosphorylation of Tau and α-synuclein in synaptic-enriched fractions of the frontal cortex in Alzheimer's disease, and in Parkinson's disease and related α-synucleinopathies. Neuroscience 2008, 152(4):913-923.
47. Patrick G.N., Zukerberg L., Nikolic M., de la Monte S., Dikkes P., Tsai L.H. Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 1999, 402(6762):615-622.
48. Rahbar M.H., Samms-Vaughan M., Dickerson A.S., Loveland K.A., Ardjomand-Hessabi M., Bressler J., Shakespeare-Pellington S., Grove M.L., Pearson D.A., Boerwinkle E. Blood lead concentrations in Jamaican children with and without autism spectrum disorder. Int. J. Environ. Res. Public Health 2014, 12(1):83-105.
49. Rahman A., Brew B.J., Guillemin G.J. Lead dysregulates serine/threonine protein phosphatases in human neurons. Neurochem. Res. 2011, 36(2):195-204.
50. Rahman A., Khan K.M., Al-Khaledi G., Khan I., Attur S. Early postnatal lead exposure induces tau phosphorylation in the brain of young rats. Acta Biol. Hung. 2012, 63(4):411-425.
51. Stansfield K.H., Pilsner J.R., Lu Q., Wright R.O., Guilarte T.R. Dysregulation of BDNF-TrkB signaling in developing hippocampal neurons by Pb(2+): implications for an environmental basis of neurodevelopmental disorders. Toxicol. Sci. 2012, 127(1):277-295.
52. Struzyńska L., Dabrowska-Bouta B., Koza K., Sulkowski G. Inflammation-like glial response in lead-exposed immature rat brain. Toxicol. Sci. 2007, 95(1):156-162.
53. Wang Y., Mandelkow E. Tau in physiology and pathology. Nat. Rev. Neurosci. 2016, 17(1):22-35.
54. Weisskopf M.G., Weuve J., Nie H., Saint-Hilaire M.H., Sudarsky L., Simon D.K., Hersh B., Schwartz J., Wright R.O., Hu H. Association of cumulative lead exposure with Parkinson's disease. Environ. Health Perspect. 2010, 118(11):1609-1613.
55. Wu J., Basha M.R., Brock B., Cox D.P., Cardozo-Pelaez F., McPherson C.A., Harry J., Rice D.C., Maloney B., Chen D., Lahiri D.K., Zawia N.H. Alzheimer's disease (AD)-like pathology in aged monkeys after infantile exposure to environmental metal lead (Pb): evidence for a developmental origin and environmental link for AD. J. Neurosci. 2008, 28(1):3-9.
56. Xu S.Z., Bullock L., Shan C.J., Cornelius K., Rajanna B. PKC isoforms were reduced by lead in the developing rat brain. Int. J. Dev. Neurosci. 2005, 23(1):53-64.
57. Yamaguchi H., Ishiguro K., Uchida T., Takashima A., Lemere C.A., Imahori K. Preferential labeling of Alzheimer neurofibrillary tangles with antisera for tau protein kinase (TPK) I/glycogen synthase kinase-3 beta and cyclin-dependent kinase 5, a component of TPK II. Acta Neuropathol. 1996, 92(3):232-241.
58. Yassa H.A. Autism: a form of lead and mercury toxicity. Environ. Toxicol. Pharmacol. 2014, 38(3):1016-1024.
59. Zhang J., Cai T., Zhao F., Yao T., Chen Y., Liu X., Luo W., Chen J. The role of α-synuclein and tau hyperphosphorylation-mediated autophagy and apoptosis in lead-induced learning and memory injury. Int. J. Biol. Sci. 2012, 8(7):935-944.
60. Zhang X.L., Guariglia S.R., McGlothan J.L., Stansfield K.H., Stanton P.K., Guilarte T.R. Presynaptic mechanisms of lead neurotoxicity: effects on vesicular release, vesicle clustering and mitochondria number. PLoS One 2015, 10(5):1-21.