2-Amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) is selectively toxic to primary dopaminergic neurons In Vitro

Toxicological Sciences

Volumn 140, Issue 1, 2014, Pages 179-189

  Griggs, Amy M ^a,b,c   Agim, Zeynep S ^a   Mishra, Vartika R ^b   Tambe, Mitali A ^b   Director Myska, Alison E ^d   Turteltaub, Kenneth W ^e   McCabe, George P ^f   Rochet, Jean Christophe ^b   Cannon, Jason R ^a  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

^c Med Institute Inc Lafayette   (United States)

^d DEFENSE THREAT REDUCTION AGENCY   (United States)

^e LAWRENCE LIVERMORE NATIONAL LABORATORY   (United States)

^f PURDUE UNIVERSITY   (United States)

Author keywords

Heterocyclic amines; Neurotoxicity; Parkinson's disease; PhIP

Indexed keywords

2 AMINO 1 METHYL 6 PHENYLIMIDAZO[4,5 B]PYRIDINE; 3 NITROTYROSINE; 4 HYDROXYNONENAL; ACETYLCYSTEINE; BLUEBERRY EXTRACT; 2-AMINO-1-METHYL-6-PHENYLIMIDAZO(4,5-B)PYRIDINE; ANTIOXIDANT; DOPAMINE TRANSPORTER; IMIDAZOLE DERIVATIVE; PLANT EXTRACT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; IN VITRO STUDY; MEAT; METABOLITE; NEURITE; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIMARY CULTURE; RAT; ANIMAL; BINDING COMPETITION; BLUEBERRY; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; EMBRYOLOGY; ISOLATION AND PURIFICATION; MESENCEPHALON; METABOLISM; NEUROTOXICITY SYNDROMES; PATHOLOGY; PRIMARY CELL CULTURE; SPRAGUE DAWLEY RAT; TOXICITY;

ANIMALS; ANTIOXIDANTS; BINDING, COMPETITIVE; BLUEBERRY PLANT; CELL SURVIVAL; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; DOPAMINERGIC NEURONS; IMIDAZOLES; MESENCEPHALON; NEURITES; NEUROTOXICITY SYNDROMES; OXIDATIVE STRESS; PLANT EXTRACTS; PRIMARY CELL CULTURE; RATS, SPRAGUE-DAWLEY;

EID: 84903833597     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfu060     Document Type: Article

References (51)

1. Adams, L. S., Kanaya, N., Phung, S., Liu, Z., and Chen, S. (2011).Whole blueberry powder modulates the growth and metastasis of MDA-MB-231 triple negative breast tumors in nude mice. J. Nutr. 141, 1805-1812.
2. Barbaresko, J., Koch, M., Schulze, M. B., and Nothlings, U. (2013). Dietary pattern analysis and biomarkers of low-grade inflammation: A systematic literature review. Nutr. Rev. 71, 511-527.
3. Bickford, P. C., Shukitt-Hale, B., and Joseph, J. (1999). Effects of aging on cerebellar noradrenergic function and motor learning: nutritional interventions. Mech. Ageing Dev. 111, 141-154.
4. Braak, H., Ghebremedhin, E., Rub, U., Bratzke, H., and Del Tredici, K. (2004). Stages in the development of Parkinson's disease-related pathology. Cell Tissue Res. 318, 121-134.
5. Cannon, J. R., Geghman, K. D., Tapias, V., Sew, T., Dail, M. K., Li, C., and Greenamyre, J. T. (2013). Expression of human E46K-mutated alphasynuclein in BAC-transgenic rats replicates early-stage Parkinson's disease features and enhances vulnerability to mitochondrial impairment. Exp. Neurol. 240, 44-56.
6. Cannon, J. R., and Greenamyre, J. T. (2010). Neurotoxic in vivo models of Parkinson's disease recent advances. Prog. Brain Res. 184, 17-33.
7. Cannon, J. R., and Greenamyre, J. T. (2011). The role of environmental exposures in neurodegeneration and neurodegenerative diseases. Toxicol. Sci. 124, 225-250.
8. Cannon, J. R., and Greenamyre, J. T. (2013). Gene-environment interactions in Parkinson's disease: Specific evidence in humans and mammalian models. Neurobiol. Dis. 57, 38-46.
9. Cannon, J. R., Tapias, V., Na, H. M., Honick, A. S., Drolet, R. E., and Greenamyre, J. T. (2009). A highly reproducible rotenone model of Parkinson's disease. Neurobiol. Dis. 34, 279-290.
10. Chen, C., Ma, X., Malfatti, M. A., Krausz, K.W., Kimura, S., Felton, J. S., Idle, J. R., and Gonzalez, F. J. (2007). A comprehensive investigation of 2-amino- 1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) metabolism in the mouse using a multivariate data analysis approach. Chem. Res. Toxicol. 20, 531-542.
11. Chen, H., Zhang, S. M., Hernan, M. A., Willett, W. C., and Ascherio, A. (2003). Dietary intakes of fat and risk of Parkinson's disease. Am. J. Epidemiol. 157, 1007-1014.
12. Cooper, A. A., Gitler, A. D., Cashikar, A., Haynes, C. M., Hill, K. J., Bhullar, B., Liu, K., Xu, K., Strathearn, K. E., Liu, F., et al. (2006). Alpha-synuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson's models. Science 313, 324-328.
13. Dorsey, E. R., Constantinescu, R., Thompson, J. P., Biglan, K. M., Holloway, R. G., Kieburtz, K., Marshall, F. J., Ravina, B. M., Schifitto, G., Siderowf, A., et al. (2007). Projected number of people with Parkinson disease in the most populous nations, 2005 through 2030. Neurology 68, 384-386.
14. Felton, J. S., Knize, M. G., Shen, N. H., Andresen, B. D., Bjeldanes, L. F., and Hatch, F. T. (1986a). Identification of the mutagens in cooked beef. Environ. Health Perspect. 67, 17-24.
15. Felton, J. S., Knize, M. G., Shen, N. H., Lewis, P. R., Andresen, B. D., Happe, J., and Hatch, F. T. (1986b). The isolation and identification of a new mutagen from fried ground beef: 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP). Carcinogenesis 7, 1081-1086.
16. Felton, J. S., Knize, M. G., Wood, C., Wuebbles, B. J., Healy, S. K., Stuermer, D. H., Bjeldanes, L. F., Kimble, B. J., and Hatch, F. T. (1984). Isolation and characterization of new mutagens from fried ground beef. Carcinogenesis 5, 95-102.
17. Gao, X., Cassidy, A., Schwarzschild, M. A., Rimm, E. B., and Ascherio, A. (2012). Habitual intake of dietary flavonoids and risk of Parkinson disease. Neurology 78, 1138-1145.
18. Hakkinen, S. H., Karenlampi, S. O., Heinonen, I. M., Mykkanen, H. M., and Torronen, A. R. (1999). Content of the flavonols quercetin, myricetin, and kaempferol in 25 edible berries. J. Agric. Food Chem. 47, 2274-2279.
19. Hastings, T. G., and Zigmond, M. J. (1994). Identification of catechol-protein conjugates in neostriatal slices incubated with [3H]dopamine: Impact of ascorbic acid and glutathione. J. Neurochem. 63, 1126-1132.
20. Holme, J. A., Wallin, H., Brunborg, G., Soderlund, E. J., Hongslo, J. K., and Alexander, J. (1989). Genotoxicity of the food mutagen 2-amino-1-methyl- 6-phenylimidazo[4,5-b]pyridine (PhIP): Formation of 2-hydroxamino-PhIP, a directly acting genotoxic metabolite. Carcinogenesis 10, 1389-1396.
21. Horowitz, M. P., Milanese, C., Di Maio, R., Hu, X., Montero, L. M., Sanders, L. H., Tapias, V., Sepe, S., van Cappellen,W. A., Burton, E. A., et al. (2011). Single-cell redox imaging demonstrates a distinctive response of dopaminergic neurons to oxidative insults. Antioxid. Redox Signal. 15, 855-871.
22. Ichinose, H., Ozaki, N., Nakahara, D., Naoi, M., Wakabayashi, K., Sugimura, T., and Nagatsu, T. (1988). Effects of heterocyclic amines in food on dopamine metabolism in nigro-striatal dopaminergic neurons. Biochem. Pharmaco. 37, 3289-3295.
23. Inzelberg, R., Cohen, O. S., Aharon-Peretz, J., Schlesinger, I.,Gershoni-Baruch, R.,Djaldetti, R.,Nitsan, Z., Ephraty, L., Tunkel, O., Kozlova, E., et al. (2012). The LRRK2 G2019S mutation is associated with Parkinson disease and concomitant non-skin cancers. Neurology 78, 781-786.
24. Joseph, J. A., Denisova,N. A., Arendash, G., Gordon, M.,Diamond, D., Shukitt- Hale, B., and Morgan, D. (2003). Blueberry supplementation enhances signaling and prevents behavioral deficits in an Alzheimer disease model. Nutr. Neurosci. 6, 153-162.
25. Joseph, J. A., Shukitt-Hale, B., Denisova, N. A., Bielinski, D., Martin, A., McEwen, J. J., and Bickford, P. C. (1999). Reversals of age-related declines in neuronal signal transduction, cognitive, and motor behavioral deficits with blueberry, spinach, or strawberry dietary supplementation. J. Neurosci. 19, 8114-8121.
26. Kojima, T., Naoi, M., Wakabayashi, K., Sugimura, T., and Nagatsu, T. (1990). 3-Amino-1-methyl-5H-pyrido[4,3-b]indole (Trp-P-2) and other heterocyclic amines as inhibitors of mitochondrial monoamine oxidases separated from human brain synaptosomes. Neurochem. Int. 16, 51-57.
27. Liu, F., Nguyen, J. L., Hulleman, J. D., Li, L., and Rochet, J. C. (2008). Mechanisms of DJ-1 neuroprotection in a cellular model of Parkinson's disease. J. Neurochem. 105, 2435-2453.
28. Logroscino, G., Marder, K., Graziano, J., Freyer, G., Slavkovich, V., Lojacono, N., Cote, L., and Mayeux, R. (1998). Dietary iron, animal fats, and risk of Parkinson's disease. Mov. Disord. 13(Suppl. 1), 13-16.
29. Louis, E. D., Factor-Litvak, P., Gerbin, M., Slavkovich, V., Graziano, J. H., Jiang, W., and Zheng, W. (2011). Blood harmane, blood lead, and severity of hand tremor: Evidence of additive effects. Neurotoxicology 32, 227-232.
30. Louis, E. D., Jiang, W., Pellegrino, K. M., Rios, E., Factor-Litvak, P., Henchcliffe, C., and Zheng, W. (2008). Elevated blood harmane (1-methyl-9Hpyrido[ 3,4-b]indole) concentrations in essential tremor. Neurotoxicology 29, 294-300.
31. Louis, E. D., Michalec, M., Jiang, W., Factor-Litvak, P., and Zheng, W. (2014). Elevated blood harmane (1-methyl-9H-pyrido[3,4-b]indole) concentrations in Parkinson's disease. Neurotoxicology 40, 52-56.
32. Malfatti, M. A., Kulp, K. S., Knize, M. G., Davis, C., Massengill, J. P., Williams, S., Nowell, S., MacLeod, S., Dingley, K. H., Turteltaub, K. W., et al. (1999). The identification of [2-(14)C]2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine metabolites in humans. Carcinogenesis 20, 705-713.
33. Maruyama,W., Ota, A., Takahashi, A., Nagatsu, T., and Naoi,M. (1994). Foodderived heterocyclic amines, 3-amino-1,4-dimethyl-5H-pyrido[4,3-b]indole and related amines, as inhibitors of monoamine metabolism. J. Neural Transm. Suppl. 41, 327-333.
34. Nguyen, T. M., and Novak, M. (2007). Synthesis and decomposition of an ester derivative of the procarcinogen and promutagen, PhIP, 2-amino-1-methyl-6-phenyl-1H-imidazo[4,5-b]pyridine: Unusual nitrenium ion chemistry. J. Org. Chem. 72, 4698-4706.
35. Olive, M. F., Cleva, R. M., Kalivas, P. W., and Malcolm, R. J. (2012). Glutamatergic medications for the treatment of drug and behavioral addictions. Pharmacol. Biochem. Behav. 100, 801-810.
36. Ota, M., Naoi, M., Hamanaka, T., and Nagatsu, T. (1990). Inhibition of human brain aromatic L-amino acid decarboxylase by cooked food-derived 3-amino 1-methyl-5H-pyrido[4,3-b]indole (Trp-P-2) and other heterocyclic amines. Neurosci. Lett. 116, 372-378.
37. Peng, L., Dasari, S., Tabb, D. L., and Turesky, R. J. (2012). Mapping serum albumin adducts of the food-borne carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine by data-dependent tandemmass spectrometry. Chem. Res. Toxicol. 25, 2179-2193.
38. Rendeiro, C., Spencer, J. P., Vauzour, D., Butler, L. T., Ellis, J. A., and Williams, C. M. (2009). The impact of flavonoids on spatial memory in rodents: From behaviour to underlying hippocampal mechanisms. Genes Nutr. 4, 251-270.
39. Rub, U., Del Tredici, K., Schultz, C., Ghebremedhin, E., de Vos, R. A., Jansen Steur, E., and Braak, H. (2002). Parkinson's disease: The thalamic components of the limbic loop are severely impaired by alpha-synuclein immunopositive inclusion body pathology. Neurobiol. Aging 23, 245-254.
40. Rubi, B., and Maechler, P. (2010). Minireview: New roles for peripheral dopamine on metabolic control and tumor growth: let's seek the balance. Endocrinology 151, 5570-5581.
41. Samuni, Y., Goldstein, S., Dean, O. M., and Berk, M. (2013). The chemistry and biological activities of N-acetylcysteine. Biochim. Biophys. Acta 1830, 4117-4129.
42. Shulman, J. M., De Jager, P. L., and Feany, M. B. (2011). Parkinson's disease: genetics and pathogenesis. Annu. Rev. Pathol. 6, 193-222.
43. Strathearn, K. E., Yousef, G. G., Grace, M. H., Roy, S. L., Tambe, M. A., Ferruzzi, M. G., Wu, Q. L., Simon, J. E., Lila, M. A., and Rochet, J. C. (2014).Neuroprotective effects of anthocyanin- and proanthocyanidin-rich extracts in cellular models of Parkinsons disease. Brain Res. 1555, 60-77.
44. Surmeier, D. J., Guzman, J. N., Sanchez-Padilla, J., and Schumacker, P. T. (2011). The role of calcium and mitochondrial oxidant stress in the loss of substantia nigra pars compacta dopaminergic neurons in Parkinson's disease. Neuroscience 198, 221-231.
45. Tapias, V., Cannon, J. R., and Greenamyre, J. T. (2014). Pomegranate juice exacerbates oxidative stress and nigrostriatal degeneration in Parkinson's disease. Neurobiol. Aging 35, 1162-1176.
46. Tete, S., Nicoletti, M., Saggini, A., Maccauro, G., Rosati, M., Conti, F., Cianchetti, E., Tripodi, D., Toniato, E., Fulcheri, M., et al. (2012). Nutrition and cancer prevention. Int. J. Immunopathol. Pharmacol. 25, 573-581.
47. Teunissen, S. F., Vlaming, M. L., Rosing, H., Schellens, J. H., Schinkel, A. H., and Beijnen, J. H. (2010). Development and validation of a liquid chromatography-tandem mass spectrometry assay for the analysis of 2- amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) and its metabolite 2-hydroxyamino-1-methyl-6-phenylimidazo[4,5-b]pyridine (N-OH-PhIP) in plasma, urine, bile, intestinal contents, faeces and eight selected tissues from mice. J. Chromatogr. B. Analyt. Technol. Biomed. Life Sci. 878, 2353-2362.
48. Turteltaub, K. W., Dingley, K. H., Curtis, K. D., Malfatti, M. A., Turesky, R. J., Garner, R. C., Felton, J. S., and Lang, N. P. (1999). Macromolecular adduct formation and metabolism of heterocyclic amines in humans and rodents at low doses. Cancer Lett. 143, 149-155.
49. Wang, Y., Chang, C. F., Chou, J., Chen, H. L., Deng, X., Harvey, B. K., Cadet, J. L., and Bickford, P. C. (2005). Dietary supplementation with blueberries, spinach, or spirulina reduces ischemic brain damage. Exp. Neurol. 193, 75-84.
50. Weisburger, J. H. (2000). Eat to live, not live to eat. Nutrition 16, 767-773.
51. Willis, L. M., Shukitt-Hale, B., and Joseph, J. A. (2009). Modulation of cognition and behavior in aged animals: Role for antioxidant- and essential fatty acid-rich plant foods. Am. J. Clin. Nutr. 89, 1602S-1606S.