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Arsenic-induced neurotoxicity: a mechanistic appraisal

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Abstract

Arsenic is a metalloid found in groundwater as a byproduct of soil/rock erosion and industrial and agricultural processes. This xenobiotic elicits its toxicity through different mechanisms, and it has been identified as a toxicant that affects virtually every organ or tissue in the body. In the central nervous system, exposure to arsenic can induce cognitive dysfunction. Furthermore, iAs has been linked to several neurological disorders, including neurodevelopmental alterations, and is considered a risk factor for neurodegenerative disorders. However, the exact mechanisms involved are still unclear. In this review, we aim to appraise the neurotoxic effects of arsenic and the molecular mechanisms involved. First, we discuss the epidemiological studies reporting on the effects of arsenic in intellectual and cognitive function during development as well as studies showing the correlation between arsenic exposure and altered cognition and mental health in adults. The neurotoxic effects of arsenic and the potential mechanisms associated with neurodegeneration are also reviewed including data from experimental models supporting epidemiological evidence of arsenic as a neurotoxicant. Next, we focused on recent literature regarding arsenic metabolism and the molecular mechanisms that begin to explain how arsenic damages the central nervous system including, oxidative stress, energy failure and mitochondrial dysfunction, epigenetics, alterations in neurotransmitter homeostasis and synaptic transmission, cell death pathways, and inflammation. Outlining the specific mechanisms by which arsenic alters the cell function is key to understand the neurotoxic effects that convey cognitive dysfunction, neurodevelopmental alterations, and neurodegenerative disorders.

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Abbreviations

Aβ:

Amyloid-beta peptide

AD:

Alzheimer’s disease

Akt:

Protein Kinase B

AMPA:

α-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid

AMPAR:

α-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor

AMPK:

AMP-dependent protein kinase

APP:

Amyloid precursor protein

AQP:

Aqua(glycerol)porins

As:

Arsenic

As(GS)3 :

Arsenic triglutathione

As2O3 :

Arsenic trioxide

AS3MT:

Arsenite methyltransferase

AsIII:

Arsenite

AsV:

Arsenate

BACE-1:

β-Secretase

BBB:

Blood–brain barrier

BHMT:

Betaine hydroxy methyltransferase

Ca:

Calcium

CBS:

Cystathionine beta synthase

Cd:

Cadmium

CNS:

Central nervous system

CoA:

Coenzyme A

COX:

Cyclooxygenase

CTH:

Cystathionine-γ-lyase or γ-cystathionase

Cys:

Cysteine

DMAIII(GS):

Dimethylarsinic GSH

DMAIII:

Dimethylarsinous acid

DMAV:

Dimethylarsinic acid

DMAH:

Dimethylarsine

DMA·:

Dimethylarsine radical

DMAOO·:

Dimethylarsine peroxyl radical

DMAOOH:

Dimethylated arsenic peroxide

EAAT:

Excitatory amino acid transporter

ER:

Endoplasmic reticulum

ERK:

Extracellular-signal-regulated kinase

γ-GCL:

Gamma-glutamylcysteine ligase (or synthase γ-GCS)

G3P:

Glyceraldehyde 3-phosphate

GAPDH:

Glyceraldehyde 3-phosphate dehydrogenase

GLUT:

Glucose transporters

GS:

Glutamine synthetase

GSH:

Glutathione

GSTs:

Glutathione-S transferases

HAT:

Histone acetyltransferases

iAs:

Inorganic As

iAsV-3-P-glycerate:

1-Arsenato-3-phospho-d-glycerate

IFNγ:

Interferon-gamma

IQ:

Intelligence quotient

IL-1β:

Interleukin 1-beta

iNOS:

Inducible NOS

JNK:

C-Jun N-terminal kinase

Keap1:

Kelch-like ECH-associated protein 1

LTP:

Long-term potentiation

MAPK:

Mitogen-activated protein kinase

MAT:

Methionine adenosyltransferase

5,10-MeTHF:

5,10-Methylene tetrahydrofolate

MeTs:

Methyltransferases

2-MG:

2-Methyl glycine

MMA(GS)2 :

Monomethylarsinic diglutathione

MMAIII:

Momomethylarsonous acid

MMAV:

Monomethylarsonic acid

MRP:

Multidrug resistance protein

MS:

Methionine synthase

MT:

Metallothionenin

MTF1:

Metal-responsive transcription factor-1

5-MTHF:

5-Methyl tetrahydrofolate

MTHFR:

Methyl tetrahydrofolate reductase

mTOR:

Mechanistic (or mammalian) target of rapamycin

NaAsO2 :

Sodium arsenite

NADPH:

Nicotinamide adenine dinucleotide phosphate

NF-κB:

Nuclear factor kappa-light-chain-enhancer of activated B cells

NMDA:

Glutamate/N-methyl-d-aspartate

NMDAR:

Glutamate/N-methyl-d-aspartate receptor

NO:

Nitric oxide

NOS:

Nitric oxide synthase

NOX:

NADPH oxidase

NQO1:

NADPH dehydrogenase quinone 1

Nrf2:

Nuclear factor (erythroid-derived 2)-like 2

p62:

Autophagic receptor sequestosome-1, p62/SQSTM1

Pb:

Lead

PD:

Parkinson’s disease

PDH:

Pyruvate dehydrogenase

PGC-1α:

Peroxisome proliferator-activated receptor gamma coactivator 1-alpha

PI3K:

Class III phosphatidylinositol 3-kinase

PNS:

Peripheral nervous system

Pi:

Phosphate

PPi:

Diphosphate

PTGEs:

Prostaglandin E synthase

RAGE:

Advanced glycation-end products

RNS:

Reactive nitrogen species

ROS:

Reactive oxygen species

SAH:

s-Adenosylhomocysteine

SAHH:

SAH hydrolase

SAM:

s-Adenosylmethionine

SOD:

Superoxide dismutase

TCA:

Tricarboxylic acid

TFAM:

Mitochondrial transcription factor A

TNF-α:

Tumor necrosis factor alpha

TR:

Trx reductase

Trx:

Thioredoxin

xCT:

Cystine/glutamate exchanger system

References

  1. Garza-Lombo C, Posadas Y, Quintanar L, Gonsebatt ME, Franco R (2018) Antioxid Redox Signal 28:1669–1703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Chou S, Harper C, Ingerman L, Llados F, Colman J, Chappell L, Osier M, Odin M, Sage G (2007) Toxicological profile for arsenic. The Agency Altanta, Altanta

    Google Scholar 

  3. Carlin DJ, Naujokas MF, Bradham KD, Cowden J, Heacock M, Henry HF, Lee JS, Thomas DJ, Thompson C, Tokar EJ, Waalkes MP, Birnbaum LS, Suk WA (2016) Environ Health Perspect 124:890–899

    Article  CAS  PubMed  Google Scholar 

  4. Mandal BK, Suzuki KT (2002) Talanta 58:201–235

    Article  CAS  PubMed  Google Scholar 

  5. Gundert-Remy U, Damm G, Foth H, Freyberger A, Gebel T, Golka K, Rohl C, Schupp T, Wollin KM, Hengstler JG (2015) Arch Toxicol 89:2219–2227

    Article  CAS  PubMed  Google Scholar 

  6. Tolins M, Ruchirawat M, Landrigan P (2014) Ann Glob Health 80:303–314

    Article  PubMed  Google Scholar 

  7. Farzan SF, Karagas MR, Chen Y (2013) Toxicol Appl Pharmacol 272:384–390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Calderon J, Navarro ME, Jimenez-Capdeville ME, Santos-Diaz MA, Golden A, Rodriguez-Leyva I, Borja-Aburto V, Diaz-Barriga F (2001) Environ Res 85:69–76

    Article  CAS  PubMed  Google Scholar 

  9. Rosado JL, Ronquillo D, Kordas K, Rojas O, Alatorre J, Lopez P, Garcia-Vargas G, Del Carmen Caamano M, Cebrian ME, Stoltzfus RJ (2007) Environ Health Perspect 115:1371–1375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Wasserman GA, Liu X, Loiacono NJ, Kline J, Factor-Litvak P, van Geen A, Mey JL, Levy D, Abramson R, Schwartz A, Graziano JH (2014) Environ Health 13:23

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Parvez F, Wasserman GA, Factor-Litvak P, Liu X, Slavkovich V, Siddique AB, Sultana R, Sultana R, Islam T, Levy D, Mey JL, van Geen A, Khan K, Kline J, Ahsan H, Graziano JH (2011) Environ Health Perspect 119:1665–1670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ramos-Chavez LA, Rendon-Lopez CR, Zepeda A, Silva-Adaya D, Del Razo LM, Gonsebatt ME (2015) Front Cell Neurosci 9:21

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Nelson-Mora J, Escobar ML, Rodriguez-Duran L, Massieu L, Montiel T, Rodriguez VM, Hernandez-Mercado K, Gonsebatt ME (2018) Arch Toxicol 92:1037–1048

    Article  CAS  PubMed  Google Scholar 

  14. Aung KH, Kyi-Tha-Thu C, Sano K, Nakamura K, Tanoue A, Nohara K, Kakeyama M, Tohyama C, Tsukahara S, Maekawa F (2016) Front Neurosci 10:137

    Article  PubMed  PubMed Central  Google Scholar 

  15. Hong YS, Song KH, Chung JY (2014) J Prev Med Public Health 47:245–252

    Article  PubMed  PubMed Central  Google Scholar 

  16. Tyler CR, Allan AM (2014) Curr Environ Health Rep 1:132–147

    Article  PubMed  PubMed Central  Google Scholar 

  17. Paul S, Das N, Bhattacharjee P, Banerjee M, Das JK, Sarma N, Sarkar A, Bandyopadhyay AK, Sau TJ, Basu S, Banerjee S, Majumder P, Giri AK (2013) J Expo Sci Environ Epidemiol 23:156–162

    Article  CAS  PubMed  Google Scholar 

  18. Mochizuki H, Phyu KP, Aung MN, Zin PW, Yano Y, Myint MZ, Thit WM, Yamamoto Y, Hishikawa Y, Thant KZ, Maruyama M, Kuroda Y (2019) Environ Health Prev Med 24:23

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Hafeman DM, Ahsan H, Louis ED, Siddique AB, Slavkovich V, Cheng Z, van Geen A, Graziano JH (2005) J Occup Environ Med 47:778–784

    Article  CAS  PubMed  Google Scholar 

  20. Le Quesne PM, McLeod JG (1977) J Neurol Sci 32:437–451

    Article  PubMed  Google Scholar 

  21. Vahidnia A, Romijn F, Tiller M, van der Voet GB, de Wolff FA (2006) Hum Exp Toxicol 25:667–674

    Article  CAS  PubMed  Google Scholar 

  22. Vahidnia A, Romijn F, van der Voet GB, de Wolff FA (2008) Chem Biol Interact 176:188–195

    Article  CAS  PubMed  Google Scholar 

  23. Garcia-Chavez E, Segura B, Merchant H, Jimenez I, Del Razo LM (2007) J Neurol Sci 258:104–110

    Article  CAS  PubMed  Google Scholar 

  24. Yang YW, Liou SH, Hsueh YM, Lyu WS, Liu CS, Liu HJ, Chung MC, Hung PH, Chung CJ (2018) Toxicol Appl Pharmacol 356:8–14

    Article  CAS  PubMed  Google Scholar 

  25. Sharma B, Sharma PM (2013) Toxicol Appl Pharmacol 273:180–188

    Article  CAS  PubMed  Google Scholar 

  26. Nino SA, Martel-Gallegos G, Castro-Zavala A, Ortega-Berlanga B, Delgado JM, Hernandez-Mendoza H, Romero-Guzman E, Rios-Lugo J, Rosales-Mendoza S, Jimenez-Capdeville ME, Zarazua S (2018) Chem Res Toxicol 31:13–21

    Article  CAS  PubMed  Google Scholar 

  27. Nino SA, Morales-Martinez A, Chi-Ahumada E, Carrizales L, Salgado-Delgado R, Perez-Severiano F, Diaz-Cintra S, Jimenez-Capdeville ME, Zarazua S (2019) ACS Chem Neurosci 10:323–336

    Article  CAS  PubMed  Google Scholar 

  28. Ashok A, Rai NK, Tripathi S, Bandyopadhyay S (2015) Toxicol Sci 143:64–80

    Article  CAS  PubMed  Google Scholar 

  29. Escudero-Lourdes C, Uresti-Rivera EE, Oliva-Gonzalez C, Torres-Ramos MA, Aguirre-Banuelos P, Gandolfi AJ (2016) Neurochem Res 41:2559–2572

    Article  CAS  PubMed  Google Scholar 

  30. Shavali S, Sens DA (2008) Toxicol Sci 102:254–261

    Article  CAS  PubMed  Google Scholar 

  31. Cholanians AB, Phan AV, Ditzel EJ, Camenisch TD, Lau SS, Monks TJ (2016) Toxicol Sci 153:271–281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Torres-Avila M, Leal-Galicia P, Sanchez-Pena LC, Del Razo LM, Gonsebatt ME (2010) Environ Res 110:443–447

    Article  CAS  PubMed  Google Scholar 

  33. Liu Z, Shen J, Carbrey JM, Mukhopadhyay R, Agre P, Rosen BP (2002) Proc Natl Acad Sci USA 99:6053–6058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Calatayud M, Barrios JA, Velez D, Devesa V (2012) Chem Res Toxicol 25:446–453

    Article  CAS  PubMed  Google Scholar 

  35. Sanchez-Pena LC, Petrosyan P, Morales M, Gonzalez NB, Gutierrez-Ospina G, Del Razo LM, Gonsebatt ME (2010) Environ Res 110:428–434

    Article  CAS  PubMed  Google Scholar 

  36. Leslie EM, Haimeur A, Waalkes MP (2004) J Biol Chem 279:32700–32708

    Article  CAS  PubMed  Google Scholar 

  37. Yoshino Y, Yuan B, Kaise T, Takeichi M, Tanaka S, Hirano T, Kroetz DL, Toyoda H (2011) Toxicol Appl Pharmacol 257:198–208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Shukalek CB, Swanlund DP, Rousseau RK, Weigl KE, Marensi V, Cole SP, Leslie EM (2016) Mol Pharmacol 90:127–139

    Article  CAS  PubMed  Google Scholar 

  39. Tadepalle N, Koehler Y, Brandmann M, Meyer N, Dringen R (2014) Neurochem Int 76:1–11

    Article  CAS  PubMed  Google Scholar 

  40. Liu J, Liu Y, Powell DA, Waalkes MP, Klaassen CD (2002) Toxicology 170:55–62

    Article  CAS  PubMed  Google Scholar 

  41. Watanabe T, Hirano S (2013) Arch Toxicol 87:969–979

    Article  CAS  PubMed  Google Scholar 

  42. Ding L, Saunders RJ, Drobna Z, Walton FS, Xun P, Thomas DJ, Styblo M (2012) Toxicol Appl Pharmacol 264:121–130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Thomas DJ (2010) Toxicol Sci 117:249–252

    Article  CAS  PubMed  Google Scholar 

  44. Hughes MF (2002) Toxicol Lett 133:1–16

    Article  CAS  PubMed  Google Scholar 

  45. Nemeti B, Regonesi ME, Tortora P, Gregus Z (2010) Toxicol Sci 117:270–281

    Article  CAS  PubMed  Google Scholar 

  46. Rodriguez VM, Del Razo LM, Limon-Pacheco JH, Giordano M, Sanchez-Pena LC, Uribe-Querol E, Gutierrez-Ospina G, Gonsebatt ME (2005) Toxicol Sci 84:157–166

    Article  CAS  PubMed  Google Scholar 

  47. Golmohammadi J, Jahanian-Najafabadi A, Aliomrani M (2019) Biol Trace Elem Res 189:172–179

    Article  CAS  PubMed  Google Scholar 

  48. Manthari RK, Tikka C, Ommati MM, Niu R, Sun Z, Wang J, Zhang J, Wang J (2018) Arch Toxicol 92:3255–3275

    Article  CAS  PubMed  Google Scholar 

  49. Rehman K, Naranmandura H (2012) Metallomics 4:881–892

    Article  CAS  PubMed  Google Scholar 

  50. Mizumura A, Watanabe T, Kobayashi Y, Hirano S (2010) Toxicol Appl Pharmacol 242:119–125

    Article  CAS  PubMed  Google Scholar 

  51. Zhang HN, Yang L, Ling JY, Czajkowsky DM, Wang JF, Zhang XW, Zhou YM, Ge F, Yang MK, Xiong Q, Guo SJ, Le HY, Wu SF, Yan W, Liu B, Zhu H, Chen Z, Tao SC (2015) Proc Natl Acad Sci USA 112:15084–15089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Shen S, Li XF, Cullen WR, Weinfeld M, Le XC (2013) Chem Rev 113:7769–7792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Zhou X, Sun X, Mobarak C, Gandolfi AJ, Burchiel SW, Hudson LG, Liu KJ (2014) Chem Res Toxicol 27:690–698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Qu W, Waalkes MP (2015) Toxicol Appl Pharmacol 282:267–274

    Article  CAS  PubMed  Google Scholar 

  55. Chang YY, Kuo TC, Hsu CH, Hou DR, Kao YH, Huang RN (2012) Arch Toxicol 86:911–922

    Article  CAS  PubMed  Google Scholar 

  56. Halliwell B, Cross CE (1994) Environ Health Perspect 102(Suppl 10):5–12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Olsen LF, Issinger OG, Guerra B (2013) Redox Rep 18:245–252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Forman HJ (2016) Free Radic Biol Med 97:398–407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Culotta VC, Yang M, O’Halloran TV (2006) Biochim Biophys Acta 1763:747–758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Schrader M, Fahimi HD (2006) Biochim Biophys Acta 1763:1755–1766

    Article  CAS  PubMed  Google Scholar 

  61. Finkel T (2011) J Cell Biol 194:7–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Reczek CR, Chandel NS (2015) Curr Opin Cell Biol 33:8–13

    Article  CAS  PubMed  Google Scholar 

  63. Patel M (2016) Trends Pharmacol Sci 37:768–778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Salim S (2017) J Pharmacol Exp Ther 360:201–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Garcia-Chavez E, Jimenez I, Segura B, Del Razo LM (2006) Neurotoxicology 27:1024–1031

    Article  CAS  PubMed  Google Scholar 

  66. Castro-Coronel Y, Del Razo LM, Huerta M, Hernandez-Lopez A, Ortega A, Lopez-Bayghen E (2011) Toxicol Sci 122:539–550

    Article  CAS  PubMed  Google Scholar 

  67. Negishi T, Takahashi M, Matsunaga Y, Hirano S, Tashiro T (2012) J Neuropathol Exp Neurol 71:468–479

    Article  CAS  PubMed  Google Scholar 

  68. Zhang Y, Duan X, Li J, Zhao S, Li W, Zhao L, Li W, Nie H, Sun G, Li B (2016) Neurochem Res 41:2119–2128

    Article  CAS  PubMed  Google Scholar 

  69. Garcia-Chavez E, Santamaria A, Diaz-Barriga F, Mandeville P, Juarez BI, Jimenez-Capdeville ME (2003) Brain Res 976:82–89

    Article  CAS  PubMed  Google Scholar 

  70. Jomova K, Jenisova Z, Feszterova M, Baros S, Liska J, Hudecova D, Rhodes CJ, Valko M (2011) J Appl Toxicol 31:95–107

    CAS  PubMed  Google Scholar 

  71. Flora SJ (2011) Free Radic Biol Med 51:257–281

    Article  CAS  PubMed  Google Scholar 

  72. Prakash C, Soni M, Kumar V (2015) Biol Trace Elem Res 167:121–129

    Article  CAS  PubMed  Google Scholar 

  73. Prakash C, Kumar V (2016) Chem Biol Interact 256:228–235

    Article  CAS  PubMed  Google Scholar 

  74. Zamora PL, Rockenbauer A, Villamena FA (2014) Chem Res Toxicol 27:765–774

    Article  CAS  PubMed  Google Scholar 

  75. Lau A, Zheng Y, Tao S, Wang H, Whitman SA, White E, Zhang DD (2013) Mol Cell Biol 33:2436–2446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. He X, Ma Q (2009) J Biol Chem 284:12609–12621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Rojas D, Rager JE, Smeester L, Bailey KA, Drobna Z, Rubio-Andrade M, Styblo M, Garcia-Vargas G, Fry RC (2015) Toxicol Sci 143:97–106

    Article  CAS  PubMed  Google Scholar 

  78. Martinez L, Jimenez V, Garcia-Sepulveda C, Ceballos F, Delgado JM, Nino-Moreno P, Doniz L, Saavedra-Alanis V, Castillo CG, Santoyo ME, Gonzalez-Amaro R, Jimenez-Capdeville ME (2011) Neurochem Int 58:574–581

    Article  CAS  PubMed  Google Scholar 

  79. Du X, Tian M, Wang X, Zhang J, Huang Q, Liu L, Shen H (2018) Environ Pollut 234:590–600

    Article  CAS  PubMed  Google Scholar 

  80. Samikkannu T, Chen CH, Yih LH, Wang AS, Lin SY, Chen TC, Jan KY (2003) Chem Res Toxicol 16:409–414

    Article  CAS  PubMed  Google Scholar 

  81. Schiller CM, Fowler BA, Woods JS (1977) Environ Health Perspect 19:205–207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Cronican AA, Fitz NF, Carter A, Saleem M, Shiva S, Barchowsky A, Koldamova R, Schug J, Lefterov I (2013) PLoS One 8:e53478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Tyler CR, Hafez AK, Solomon ER, Allan AM (2015) Toxicol Appl Pharmacol 288:40–51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Huo TG, Li WK, Zhang YH, Yuan J, Gao LY, Yuan Y, Yang HL, Jiang H, Sun GF (2015) Mol Neurobiol 51:980–994

    Article  CAS  PubMed  Google Scholar 

  85. Maekawa F, Tsuboi T, Oya M, Aung KH, Tsukahara S, Pellerin L, Nohara K (2013) Neurotoxicology 37:197–206

    Article  CAS  PubMed  Google Scholar 

  86. Monaco NM, Bartos M, Dominguez S, Gallegos C, Bras C, Esandi MDC, Bouzat C, Giannuzzi L, Minetti A, Gumilar F (2018) Neurotoxicology 67:37–45

    Article  CAS  PubMed  Google Scholar 

  87. Chandravanshi LP, Gupta R, Shukla RK (2019) Biol Trace Elem Res 189:118–133

    Article  CAS  PubMed  Google Scholar 

  88. Singh V, Gera R, Kushwaha R, Sharma AK, Patnaik S, Ghosh D (2016) Sci Rep 6:30601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Zhao F, Liao Y, Jin Y, Li G, Lv X, Sun G (2012) Toxicol In Vitro 26:24–31

    Article  CAS  PubMed  Google Scholar 

  90. Namgung U, Xia Z (2001) Toxicol Appl Pharmacol 174:130–138

    Article  CAS  PubMed  Google Scholar 

  91. Lu TH, Tseng TJ, Su CC, Tang FC, Yen CC, Liu YY, Yang CY, Wu CC, Chen KL, Hung DZ, Chen YW (2014) Toxicol Lett 224:130–140

    Article  CAS  PubMed  Google Scholar 

  92. Florea AM, Splettstoesser F, Busselberg D (2007) Toxicol Appl Pharmacol 220:292–301

    Article  CAS  PubMed  Google Scholar 

  93. Yen CC, Ho TJ, Wu CC, Chang CF, Su CC, Chen YW, Jinn TR, Lu TH, Cheng PW, Su YC, Liu SH, Huang CF (2011) Arch Toxicol 85:565–575

    Article  CAS  PubMed  Google Scholar 

  94. Pandey R, Rai V, Mishra J, Mandrah K, Kumar Roy S, Bandyopadhyay S (2017) Toxicol Sci 159:137–158

    Article  CAS  PubMed  Google Scholar 

  95. Doherty J, Baehrecke EH (2018) Nat Cell Biol 20:1110–1117

    Article  CAS  PubMed  Google Scholar 

  96. Li C, Liu Y, Liu H, Zhang W, Shen C, Cho K, Chen X, Peng F, Bi Y, Hou X, Yang Z, Zheng Z, Wang K, Wang X, Zhang J, Zhong C, Zou H, Zhang X, Zhao S (2015) Cell Physiol Biochem 35:1303–1316

    Article  CAS  PubMed  Google Scholar 

  97. BonakdarYazdi B, Khodagholi F, Shaerzadeh F, Sharifzadeh A, Ahmadi R, Sanati M, Mehdizadeh H, Payandehmehr B, Vali L, Jahromi MM, Taghizadeh G, Sharifzadeh M (2017) Eur J Pharmacol 796:54–61

    Article  CAS  PubMed  Google Scholar 

  98. Firdaus F, Zafeer MF, Waseem M, Ullah R, Ahmad M, Afzal M (2018) Biomed Pharmacother 102:1152–1160

    Article  CAS  PubMed  Google Scholar 

  99. Mao J, Yang J, Zhang Y, Li T, Wang C, Xu L, Hu Q, Wang X, Jiang S, Nie X, Chen G (2016) Toxicol Appl Pharmacol 303:79–89

    Article  CAS  PubMed  Google Scholar 

  100. Saha S, Sadhukhan P, Mahalanobish S, Dutta S, Sil PC (2018) J Nutr Biochem 55:26–40

    Article  CAS  PubMed  Google Scholar 

  101. Ali N, Hoque MA, Haque A, Salam KA, Karim MR, Rahman A, Islam K, Saud ZA, Khalek MA, Akhand AA, Hossain M, Mandal A, Karim MR, Miyataka H, Himeno S, Hossain K (2010) Environ Health 9:36

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  102. Chatterjee D, Bandyopadhyay A, Sarma N, Basu S, Roychowdhury T, Roy SS, Giri AK (2018) Environ Pollut 233:596–603

    Article  CAS  PubMed  Google Scholar 

  103. Sung K, Kim M, Kim H, Hwang GW, Kim K (2019) Biol Trace Elem Res 187:224–229

    Article  CAS  PubMed  Google Scholar 

  104. Nino SA, Morales-Martinez A, Chi-Ahumada E, Carrizales L, Salgado-Delgado R, Perez-Severiano F, Diaz-Cintra S, Jimenez-Capdeville ME, Zarazua S (2018) ACS Chem Neurosci. https://doi.org/10.1021/acschemneuro.8b00278

    Article  PubMed  Google Scholar 

  105. Baldissarelli LA, Capiotti KM, Bogo MR, Ghisleni G, Bonan CD (2012) Comp Biochem Physiol C Toxicol Pharmacol 155:566–572

    Article  CAS  PubMed  Google Scholar 

  106. Sarkar S, Mukherjee S, Chattopadhyay A, Bhattacharya S (2014) Ecotoxicol Environ Saf 107:1–8

    Article  CAS  PubMed  Google Scholar 

  107. de Castro MR, Lima JV, de Freitas DP, Valente Rde S, Dummer NS, de Aguiar RB, dos Santos LC, Marins LF, Geracitano LA, Monserrat JM, Barros DM (2009) Comp Biochem Physiol C Toxicol Pharmacol 150:337–342

    Article  PubMed  CAS  Google Scholar 

  108. Dipp VR, Valles S, Ortiz-Kerbertt H, Suarez JV, Bardullas U (2018) Zebrafish 15:575–585

    Article  CAS  PubMed  Google Scholar 

  109. Yu CW, Liao VH (2014) Metallomics 6:1824–1831

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the National Institutes of Health Grant P20RR17675 Centers of Biomedical Research Excellence (COBRE), the Research Council, and the Office of Research at the University of Nebraska-Lincoln.

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Authors and Affiliations

  1. Redox Biology Center, University of Nebraska-Lincoln, Lincoln, NE, 68588, USA

    Carla Garza-Lombó & Rodrigo Franco

  2. School of Veterinary Medicine and Biomedical Sciences, University of Nebraska-Lincoln, Lincoln, NE, 68583, USA

    Carla Garza-Lombó & Rodrigo Franco

  3. Departamento de Medicina Genómica y Toxicología Ambiental, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, 04510, Mexico City, Mexico

    Carla Garza-Lombó & María E. Gonsebatt

  4. Department of Molecular Biology and Genetics, Democritus University of Thrace, Alexandroupolis, Greece

    Aglaia Pappa

  5. Department of Applied Sciences, Northumbria University, Newcastle upon Tyne, UK

    Mihalis I. Panayiotidis

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  1. Carla Garza-Lombó
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  2. Aglaia Pappa
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  3. Mihalis I. Panayiotidis
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  4. María E. Gonsebatt
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  5. Rodrigo Franco
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Correspondence to Rodrigo Franco.

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Garza-Lombó, C., Pappa, A., Panayiotidis, M.I. et al. Arsenic-induced neurotoxicity: a mechanistic appraisal. J Biol Inorg Chem 24, 1305–1316 (2019). https://doi.org/10.1007/s00775-019-01740-8

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  • DOI: https://doi.org/10.1007/s00775-019-01740-8

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