Increased APLP1 expression and neurodegeneration in the frontal cortex of manganese-exposed non-human primates

Journal of Neurochemistry

Volumn 105, Issue 5, 2008, Pages 1948-1959

  Guilarte, Tomás R ^a   Burton, Neal C ^a   Verina, Tatyana ^a   Prabhu, Vinaykumar V ^b   Becker, Kevin G ^b   Syversen, Tore ^c   Schneider, Jay S ^d  

^a The Johns Hopkins University   (United States)

^b NATIONAL INSTITUTE ON AGING   (United States)

^c NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^d THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Alzheimer's disease; Amyloid ; Amyloid precursor like protein 1; Manganese; Neurodegeneration; Non human primates; P53

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; MANGANESE; PROTEIN P53;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CYCLE REGULATION; CONTROLLED STUDY; FRONTAL CORTEX; GENE EXPRESSION; GENE IDENTIFICATION; IMMUNOHISTOCHEMISTRY; MALE; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CEREBRAL CORTEX; GENE EXPRESSION REGULATION; HUMANS; MACACA FASCICULARIS; MALE; MANGANESE; NERVE DEGENERATION; UP-REGULATION;

ANIMALIA; MACACA; PARKINSONIA; PRIMATES;

EID: 43549118615     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05295.x     Document Type: Article

References (72)

1. Alafuzoff I., Pikkarainen M., Al Sarraj S. et al. (2006) Interlaboratory comparison of assessments of Alzheimer disease-related lesions: a study of the Brain Net Europe Consortium. J. Neuropathol. Exp. Neurol. 65, 740 757.
2. Aschner M., Guilarte T. R., Schneider J. S. Zheng W. (2007) Manganese: recent advances in understanding its transport and neurotoxicity. Toxicol. Appl. Pharmacol. 221, 131 147.
3. Bast-Pettersen R., Ellingsen D. G., Hetland S. M. Thomassen Y. (2004) Neuropsychological function in manganese alloy plant workers. Int. Arch. Occup. Environ. Health 77, 277 287.
4. Bayer T. A., Paliga K., Weggen S., Wiestler O. D., Beyreuther K. Multhaup G. (1997) Amyloid precursor-like protein 1 accumulates in neuritic plaques in Alzheimer's disease. Acta Neuropathol. (Berl.) 94, 519 524.
5. Bouchard M., Mergler D., Baldwin M., Panisset M., Bowler R. Roels H. A. (2007) Neurobehavioral functioning after cessation of manganese exposure: a follow-up after 14 years. Am. J. Ind. Med. 50, 831 840.
6. Bowler R. M., Gysens S., Diamond E., Nakagawa S., Drezgic M. Roels H. A. (2006) Manganese exposure: neuropsychological and neurological symptoms and effects in welders. Neurotoxicology 27, 315 326.
7. Bowler R. M., Roels H. A., Nakagawa S. et al. (2007) Dose-effect relationships between manganese exposure and neurological, neuropsychological and pulmonary function in confined space bridge welders. Occup. Environ. Med. 64, 167 177.
8. Bush A. I. (2003) The metallobiology of Alzheimer's disease. Trends Neurosci. 26, 207 214.
9. Cervoni L., Egistelli L., Eufemi M., d'Abusco A. S., Altieri F., Lascu I., Turano C. Giartosio A. (2006) DNA sequences acting as binding sites for NM23/NDPK proteins in melanoma M14 cells. J. Cell. Biochem. 98, 421 428.
10. Cheadle C., Vawter M. P., Freed W. J. Becker K. G. (2003) Analysis of microarray data using Z score transformation. J. Mol. Diagn. 5, 73 81.
11. Culmsee C. Mattson M. P. (2005) p53 in neuronal apoptosis. Biochem. Biophys. Res. Commun. 331, 761 777.
12. Czasch S., Paul S. Baumgartner W. (2006) A comparison of immunohistochemical and silver staining methods for the detection of diffuse plaques in the aged canine brain. Neurobiol. Aging 27, 293 305.
13. Dumanchin-Njock C., Alves da Costa C. A., Mercken L., Pradier L. Checler F. (2001) The caspase-derived C-terminal fragment of betaAPP induces caspase-independent toxicity and triggers selective increase of Abeta42 in mammalian cells. J. Neurochem. 78, 1153 1161.
14. Galvan V., Chen S., Lu D., Logvinova A., Goldsmith P., Koo E. H. Bredesen D. E. (2002) Caspase cleavage of members of the amyloid precursor family of proteins. J. Neurochem. 82, 283 294.
15. Guilarte T. R., Chen M. K., McGlothan J. L. et al. (2006a) Nigrostriatal dopamine system dysfunction and subtle motor deficits in manganese-exposed non-human primates. Exp. Neurol. 202, 381 390.
16. Guilarte T. R., McGlothan J. L., Degaonkar M., Chen M. K., Barker P. B., Syversen T. Schneider J. S. (2006b) Evidence for cortical dysfunction and widespread manganese accumulation in the nonhuman primate brain following chronic manganese exposure: a 1H-MRS and MRI study. Toxicol. Sci. 94, 351 358.
17. HaMai D. Bondy S. C. (2004) Oxidative basis of manganese neurotoxicity. Ann. NY Acad. Sci. 1012, 129 141.
18. Hazell A. S., Normandin L., Norenberg M. D., Kennedy G. Yi J. H. (2006) Alzheimer type II astrocytic changes following sub-acute exposure to manganese and its prevention by antioxidant treatment. Neurosci. Lett. 396, 167 171.
19. Hirata Y. (2002) Manganese-induced apoptosis in PC12 cells. Neurotoxicol. Teratol. 24, 639 653.
20. Iinuma Y., Kubota M., Uchiyama M., Yagi M., Kanada S., Yamazaki S., Murata H., Okamoto K., Suzuki M. Nitta K. (2003) Whole-blood manganese levels and brain manganese accumulation in children receiving long-term home parenteral nutrition. Pediatr. Surg. Int. 19, 268 272.
21. Jin Y. J., Wang J., Qiao C., Hei T. K., Brandt-Rauf P. W. Yin Y. (2006) A novel mechanism for p53 to regulate its target gene ECK in signaling apoptosis. Mol. Cancer Res. 4, 769 778.
22. Josephs K. A., Ahlskog J. E., Klos K. J., Kumar N., Fealey R. D., Trenerry M. R. Cowl C. T. (2005) Neurologic manifestations in welders with pallidal MRI T1 hyperintensity. Neurology 64, 2033 2039.
23. Kaiser J. (2003) Manganese: a high-octane dispute. Science 300, 926 928.
24. Kim T. W., Wu K., Xu J. L., McAuliffe G., Tanzi R. E., Wasco W. Black I. B. (1995) Selective localization of amyloid precursor-like protein 1 in the cerebral cortex postsynaptic density. Brain Res. Mol. Brain Res. 32, 36 44.
25. Kim E. A., Cheong H. K., Choi D. S., Sakong J., Ryoo J. W., Park I. Kang D. M. (2007) Effect of occupational manganese exposure on the central nervous system of welders: (1)H magnetic resonance spectroscopy and MRI findings. Neurotoxicology 28, 276 283.
26. Kimura N., Yanagisawa K., Terao K., Ono F., Sakakibara I., Ishii Y., Kyuwa S. Yoshikawa Y. (2005) Age-related changes of intracellular Abeta in Cynomolgus monkey brains. Neuropathol. Appl. Neurobiol. 31, 170 180.
27. Klos K. J., Ahlskog J. E., Kumar N., Cambern S., Butz J., Burritt M., Fealey R. D., Cowl C. T., Parisi J. E. Josephs K. A. (2006a) Brain metal concentrations in chronic liver failure patients with pallidal T1 MRI hyperintensity. Neurology 67, 1984 1989.
28. Klos K. J., Chandler M., Kumar N., Ahlskog J. E. Josephs K. A. (2006b) Neuropsychological profiles of manganese neurotoxicity. Eur. J. Neurol. 13, 1139 1141.
29. Ko L. J., Shieh S. Y., Chen X., Jayaraman L., Tamai K., Taya Y., Prives C. Pan Z. Q. (1997) p53 is phosphorylated by CDK7-cyclin H in a p36MAT1-dependent manner. Mol. Cell. Biol. 17, 7220 7229.
30. Komaki H., Maisawa S., Sugai K., Kobayashi Y. Hashimoto T. (1999) Tremor and seizures associated with chronic manganese intoxication. Brain Dev. 21, 122 124.
31. Kowall N. W. Beal M. F. (1988) Cortical somatostatin, neuropeptide Y, and NADPH diaphorase neurons: normal anatomy and alterations in Alzheimer's disease. Ann. Neurol. 23, 105 114.
32. LaFerla F. M., Hall C. K., Ngo L. Jay G. (1996) Extracellular deposition of beta-amyloid upon p53-dependent neuronal cell death in transgenic mice. J. Clin. Invest. 98, 1626 1632.
33. Laine A., Topisirovic I., Zhai D., Reed J. C., Borden K. L. Ronai Z. (2006) Regulation of p53 localization and activity by Ubc13. Mol. Cell. Biol. 26, 8901 8913.
34. Latchoumycandane C., Anantharam V., Kitazawa M., Yang Y., Kanthasamy A. Kanthasamy A. G. (2005) Protein kinase Cdelta is a key downstream mediator of manganese-induced apoptosis in dopaminergic neuronal cells. J. Pharmacol. Exp. Ther. 313, 46 55.
35. Levy B. S. Nassetta W. J. (2003) Neurologic effects of manganese in humans: a review. Int. J. Occup. Environ. Health 9, 153 163.
36. Li Q. Sudhof T. C. (2004) Cleavage of amyloid-beta precursor protein and amyloid-beta precursor-like protein by BACE 1. J. Biol. Chem. 279, 10542 10550.
37. Liu G., Huang W., Moir R. D., Vanderburg C. R., Lai B., Peng Z., Tanzi R. E., Rogers J. T. Huang X. (2006) Metal exposure and Alzheimer's pathogenesis. J. Struct. Biol. 155, 45 51.
38. Lu H., Fisher R. P., Bailey P. Levine A. J. (1997) The CDK7-cycH-p36 complex of transcription factor IIH phosphorylates p53, enhancing its sequence-specific DNA binding activity in vitro. Mol. Cell. Biol. 17, 5923 5934.
39. Lu D. C., Rabizadeh S., Chandra S., Shayya R. F., Ellerby L. M., Ye X., Salvesen G. S., Koo E. H. Bredesen D. E. (2000) A second cytotoxic proteolytic peptide derived from amyloid beta-protein precursor. Nat. Med. 6, 397 404.
40. Lucchini R. G., Albini E., Benedetti L., Borghesi S., Coccaglio R., Malara E. C., Parrinello G., Garattini S., Resola S. Alessio L. (2007) High prevalence of Parkinsonian disorders associated to manganese exposure in the vicinities of ferroalloy industries. Am. J. Ind. Med. 50, 788 800.
41. Marx J. (2003) Neuroscience. Possible role for environmental copper in Alzheimer's disease. Science 301, 905.
42. Matsui T., Katsuno Y., Inoue T., Fujita F., Joh T., Niida H., Murakami H., Itoh M. Nakanishi M. (2004) Negative regulation of Chk2 expression by p53 is dependent on the CCAAT-binding transcription factor NF-Y. J. Biol. Chem. 279, 25093 25100.
43. McNamara M. J., Ruff C. T., Wasco W., Tanzi R. E., Thinakaran G. Hyman B. T. (1998) Immunohistochemical and in situ analysis of amyloid precursor-like protein-1 and amyloid precursor-like protein-2 expression in Alzheimer disease and aged control brains. Brain Res. 804, 45 51.
44. Meral H., Kutukcu Y., Atmaca B., Ozer F. Hamamcioglu K. (2007) Parkinsonism caused by chronic usage of intravenous potassium permanganate. Neurologist 13, 92 94.
45. Miller F. D., Pozniak C. D. Walsh G. S. (2000) Neuronal life and death: an essential role for the p53 family. Cell Death Differ. 7, 880 888.
46. Moll U. M., Wolff S., Speidel D. Deppert W. (2005) Transcription- independent pro-apoptotic functions of p53. Curr. Opin. Cell Biol. 17, 631 636.
47. de la Monte S. M., Sohn Y. K. Wands J. R. (1997) Correlates of p53- and Fas (CD95)-mediated apoptosis in Alzheimer's disease. J. Neurol. Sci. 152, 73 83.
48. Morimoto I., Sasaki Y., Ishida S., Imai K. Tokino T. (2002) Identification of the osteopontin gene as a direct target of TP53. Genes Chromosomes Cancer 33, 270 278.
49. Morrison R. S. Kinoshita Y. (2000) The role of p53 in neuronal cell death. Cell Death Differ. 7, 868 879.
50. Nadon N. L., Mohr D. Becker K. G. (2005) National Institute on Aging microarray facility - resources for gerontology research. J. Gerontol. A Biol. Sci. Med. Sci. 60, 413 415.
51. Neumann S., Schobel S., Jager S., Trautwein A., Haass C., Pietrzik C. U. Lichtenthaler S. F. (2006) Amyloid precursor-like protein 1 influences endocytosis and proteolytic processing of the amyloid precursor protein. J. Biol. Chem. 281, 7583 7594.
52. Perl D. P. Olanow C. W. (2007) The neuropathology of manganese-induced Parkinsonism. J. Neuropathol. Exp. Neurol. 66, 675 682.
53. Raina A. K., Zhu X., Rottkamp C. A., Monteiro M., Takeda A. Smith M. A. (2000) Cyclin' toward dementia: cell cycle abnormalities and abortive oncogenesis in Alzheimer disease. J. Neurosci. Res. 61, 128 133.
54. Riudavets M. A., Iacono D., Resnick S. M., O'brien R., Zonderman A. B., Martin L. J., Rudow G., Pletnikova O. Troncoso J. C. (2007) Resistance to Alzheimer's pathology is associated with nuclear hypertrophy in neurons. Neurobiol. Aging 28, 1484 1492.
55. Rodriguez-Agudelo Y., Riojas-Rodriguez H., Rios C., Rosas I., Sabido P. E., Miranda J., Siebe C., Texcalac J. L. Santos-Burgoa C. (2006) Motor alterations associated with exposure to manganese in the environment in Mexico. Sci. Total Environ. 368, 542 556.
56. Rollin H., Mathee A., Levin J., Theodorou P. Wewers F. (2005) Blood manganese concentrations among first-grade schoolchildren in two South African cities. Environ. Res. 97, 93 99.
57. Romier C., Cocchiarella F., Mantovani R. Moras D. (2003) The NF-YB/NF-YC structure gives insight into DNA binding and transcription regulation by CCAAT factor NF-Y. J. Biol. Chem. 278, 1336 1345.
58. Schneider J. S., Decamp E., Koser A. J., Fritz S., Gonczi H., Syversen T. Guilarte T. R. (2006) Effects of chronic manganese exposure on cognitive and motor functioning in non-human primates. Brain Res. 1118, 222 231.
59. Shin T. H., Paterson A. J. Kudlow J. E. (1995) p53 stimulates transcription from the human transforming growth factor alpha promoter: a potential growth-stimulatory role for p53. Mol. Cell. Biol. 15, 4694 4701.
60. Sikk K., Taba P., Haldre S., Bergquist J., Nyholm D., Zjablov G., Asser T. Aquilonius S. M. (2007) Irreversible motor impairment in young addicts - ephedrone, manganism or both? Acta Neurol. Scand. 115, 385 389.
61. Smiley J. F., Levey A. I. Mesulam M. M. (1998) Infracortical interstitial cells concurrently expressing m2-muscarinic receptors, acetylcholinesterase and nicotinamide adenine dinucleotide phosphate-diaphorase in the human and monkey cerebral cortex. Neuroscience 84, 755 769.
62. Squitti R., Gorgone G., Binetti G., Ghidoni R., Pasqualetti P., Draicchio F., Albini E., Benedetti L., Lucchini R. Rossigni P. M. (2007) Metals and oxidative stress in Parkinson's Disease from industrial areas with exposure to environmental toxins or metal pollution. G. Ital. Med. Lav. Ergon. 29, 294 296 In Italian).
63. Takser L., Mergler D., Hellier G., Sahuquillo J. Huel G. (2003) Manganese, monoamine metabolite levels at birth, and child psychomotor development. Neurotoxicology 24, 667 674.
64. Tang X., Milyavsky M., Goldfinger N. Rotter V. (2007) Amyloid-beta precursor-like protein APLP1 is a novel p53 transcriptional target gene that augments neuroblastoma cell death upon genotoxic stress. Oncogene 26, 7302 7312.
65. Waggoner D. J., Bartnikas T. B. Gitlin J. D. (1999) The role of copper in neurodegenerative disease. Neurobiol. Dis. 6, 221 230.
66. Walsh M. P. (2007) The global experience with lead in gasoline and the lessons we should apply to the use of MMT. Am. J. Ind. Med. 50, 853 860.
67. Wang X. W., Yeh H., Schaeffer L., Roy R., Moncollin V., Egly J. M., Wang Z., Freidberg E. C., Evans M. K. Taffe B. G. (1995) p53 modulation of TFIIH-associated nucleotide excision repair activity. Nat. Genet. 10, 188 195.
68. Wang L., Wu Q., Qiu P., Mirza A., McGuirk M., Kirschmeier P., Greene J. R., Wang Y., Pickett C. B. Liu S. (2001) Analyses of p53 target genes in the human genome by bioinformatic and microarray approaches. J. Biol. Chem. 276, 43604 43610.
69. Wang D., Du X. Zheng W. (2008) Alteration of saliva and serum concentrations of manganese, copper, zinc, cadmium and lead among career welders. Toxicol. Lett. 176, 40 47.
70. Wasserman G. A., Liu X., Parvez F. et al. (2006) Water manganese exposure and children's intellectual function in Araihazar, Bangladesh. Environ. Health Perspect. 114, 124 129.
71. Yang Y., Mufson E. J. Herrup K. (2003) Neuronal cell death is preceded by cell cycle events at all stages of Alzheimer's disease. J. Neurosci. 23, 2557 2563.
72. Zhong S., Wu K., Black I. B. Schaar D. G. (1996) Characterization of the genomic structure of the mouse APLP1 gene. Genomics 32, 159 162.