Manganese transporter Slc39a14 deficiency revealed its key role in maintaining manganese homeostasis in mice

Cell Discovery

Volumn 3, Issue 1, 2017, Pages

  Xin, Yongjuan ^a   Gao, Hong ^b   Wang, Jia ^a   Qiang, Yuzhen ^a   Imam, Mustapha Umar ^a   Li, Yang ^a   Wang, Jianyao ^a   Zhang, Ruochen ^a   Zhang, Huizhen ^a   Yu, Yingying ^b   Wang, Hao ^b   Luo, Haiyang ^c   Shi, Changhe ^c   Xu, Yuming ^c   Hojyo, Shintaro ^d   Fukada, Toshiyuki ^e,f,g   Min, Junxia ^b   Wang, Fudi ^a,b  

^a ZHENGZHOU UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c THE FIRST AFFILIATED HOSPITAL OF ZHENGZHOU UNIVERSITY   (China)

^d DEUTSCHES RHEUMA FORSCHUNGSZENTRUM   (Germany)

^e TOKUSHIMA BUNRI UNIVERSITY   (Japan)

^f SHOWA UNIVERSITY   (Japan)

^g Institute of Physical and Chemical Research   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER; FPN1 PROTEIN; GLUCOSE TRANSPORTER 4; IRON; MANGANESE; MEMBRANE PROTEIN; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; SLC13A5 PROTEIN; SLC30A10 PROTEIN; SLC39A14 MANGANESETRANSPORTER; SLC39A8 PROTEIN; UNCLASSIFIED DRUG; ZINC;

ANIMAL TISSUE; ARTICLE; BODY WEIGHT LOSS; COMPARATIVE STUDY; CONTROLLED STUDY; DYSTONIA; GAIT; HOMEOSTASIS; INDUCTIVELY COUPLED PLASMA MASS SPECTROMETRY; LIVER CELL; LOCOMOTION; MOTOR DYSFUNCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ROTAROD TEST; RUNNING; TORTICOLLIS; UPREGULATION; WALKING;

EID: 85030755425     PISSN: 20565968     EISSN: 20565968     Source Type: Journal    
DOI: 10.1038/celldisc.2017.25     Document Type: Article

References (55)

1. Ward RJ, Zucca FA, Duyn JH, Crichton RR, Zecca L. The role of iron in brain ageing and neurodegenerative disorders. Lancet Neurol 2014; 13: 1045–1060.
2. Stys PK, Zamponi GW, van Minnen J, Geurts JJ. Will the real multiple sclerosis please stand up? Nat Rev Neurosci 2012; 13: 507–514.
3. Weekley CM, He C. Developing drugs targeting transition metal homeostasis. Curr Opin Chem Biol 2016; 37: 26–32.
4. Tuschl K, Meyer E, Valdivia LE et al. Mutations in SLC39A14 disrupt manganese homeostasis and cause childhood-onset parkinsonism-dystonia. Nat Commun 2016; 7: 11601.
5. Aschner JL, Aschner M. Nutritional aspects of manganese homeostasis. Mol Aspects Med 2005; 26: 353–362.
6. Roth JA. Correlation between the biochemical pathways altered by mutated parkinson-related genes and chronic exposure to manganese. Neurotoxicology 2014; 44: 314–325.
7. Keen CL, Baly DL, Lonnerdal B. Metabolic effects of high doses of manganese in rats. Biol Trace Elem Res 1984; 6: 309–315.
8. Salazar J, Mena N, Hunot S et al. Divalent metal transporter 1 (DMT1) contributes to neurodegeneration in animal models of Parkinson's disease. Proc Natl Acad Sci USA 2008; 105: 18578–18583.
9. Garrick MD, Singleton ST, Vargas F et al. DMT1: which metals does it transport? Biol Res 2006; 39: 79–85.
10. Crossgrove JS, Yokel RA. Manganese distribution across the blood-brain barrier. IV. Evidence for brain influx through store-operated calcium channels. Neurotoxicology 2005; 26: 297–307.
11. Chua AC, Morgan EH. Manganese metabolism is impaired in the Belgrade laboratory rat. J Comp Physiol B 1997; 167: 361–369.
12. Mitchell CJ, Shawki A, Ganz T, Nemeth E, Mackenzie B. Functional properties of human ferroportin, a cellular iron exporter reactive also with cobalt and zinc. Am J Physiol Cell Physiol 2014; 306: C450–C459.
13. Lin W, Vann DR, Doulias PT et al. Hepatic metal ion transporter ZIP8 regulates manganese homeostasis and manganese-dependent enzyme activity. J Clin Invest 2017; 127: 2407–2417.
14. Park JH, Hogrebe M, Gruneberg M et al. SLC39A8 deficiency: a disorder of manganese transport and glycosylation. Am J Hum Genet 2015; 97: 894–903.
15. Tuschl K, Clayton PT, Gospe SM Jr. et al. Syndrome of hepatic cirrhosis, dystonia, polycythemia, and hypermanganesemia caused by mutations in SLC30A10, a manganese transporter in man. Am J Hum Genet 2016; 99: 521.
16. Hutchens S, Liu C, Jursa T et al. Deficiency in the manganese efflux transporter SLC30A10 induces severe hypothyroidism in mice. J Biol Chem 2017; 292: 9760–9773.
17. Xia Z, Wei J, Li Y et al. Zebrafish slc30a10 deficiency revealed a novel compensatory mechanism of atp2c1 in maintaining manganese homeostasis. PLoS Genet 13(7): e1006892. 10.1371/journal.pgen.1006892.
18. Roth JA. Homeostatic and toxic mechanisms regulating manganese uptake, retention, and elimination. Biol Res 2006; 39: 45–57.
19. Chen P, Bowman AB, Mukhopadhyay S, Aschner M. SLC30A10: a novel manganese transporter. Worm 2015; 4: e1042648.
20. Zogzas CE, Aschner M, Mukhopadhyay S. Structural elements in the transmembrane and cytoplasmic domains of the metal transporter SLC30A10 are required for its manganese efflux activity. J Biol Chem 2016; 291: 15940–15957.
21. Gunter TE, Gerstner B, Gunter KK et al. Manganese transport via the transferrin mechanism. Neurotoxicology 2013; 34: 118–127.
22. Ponka P, Lok CN. The transferrin receptor: role in health and disease. Int J Biochem Cell Biol 1999; 31: 1111–1137.
23. Ding D, Salvi R, Roth JA. Cellular localization and developmental changes of Zip8, Zip14 and transferrin receptor 1 in the inner ear of rats. Biometals 2014; 27: 731–744.
24. Fujishiro H, Yoshida M, Nakano Y, Himeno S. Interleukin-6 enhances manganese accumulation in SH-SY5Y cells: implications of the up-regulation of ZIP14 and the down-regulation of ZnT10. Metallomics 2014; 6: 944–949.
25. Burnett WT Jr., Bigelow RR, Kimball AW, Sheppard CW. Radio-manganese studies on the mouse, rat and pancreatic fistula dog. Am J Physiol 1952; 168: 620–625.
26. Cotzias GC, Papavasiliou PS. Primordial Homeostasis in a mammal as shown by the control of manganese. Nature 1964; 201: 828–829.
27. Bertinchamps AJ, Miller ST, Cotzias GC. Interdependence of routes excreting manganese. Am J Physiol 1966; 211: 217–224.
28. Eide DJ. Zinc transporters and the cellular trafficking of zinc. Biochim Biophys Acta 2006; 1763: 711–722.
29. Boycott KM, Beaulieu CL, Kernohan KD et al. Autosomal-recessive intellectual disability with cerebellar atrophy syndrome caused by mutation of the manganese and zinc transporter gene SLC39A8. Am J Hum Genet 2015; 97: 886–893.
30. Leyva-Illades D, Chen P, Zogzas CE et al. SLC30A10 is a cell surface-localized manganese efflux transporter, and parkinsonism-causing mutations block its intracellular trafficking and efflux activity. J Neurosci 2014; 34: 14079–14095.
31. Aydemir TB, Chang SM, Guthrie GJ et al. Zinc transporter ZIP14 functions in hepatic zinc, iron and glucose homeostasis during the innate immune response (endotoxemia). PLoS ONE 2012; 7: e48679.
32. Hojyo S, Fukada T, Shimoda S et al. The zinc transporter SLC39A14/ZIP14 controls G-protein coupled receptor-mediated signaling required for systemic growth. PLoS ONE 2011; 6: e18059.
33. De Munter S, Verheijden S, Vanderstuyft E et al. Early-onset Purkinje cell dysfunction underlies cerebellar ataxia in peroxisomal multifunctional protein-2 deficiency. Neurobiol Dis 2016; 94: 157–168.
34. Unichenko P, Kirischuk S, Yang JW et al. Plasticity-related gene 1 affects mouse barrel cortex function via strengthening of glutamatergic thalamocortical transmission. Cereb Cortex 2016; 26: 3260–3272.
35. Hermann DM, Zechariah A, Kaltwasser B et al. Sustained neurological recovery induced by resveratrol is associated with angioneurogenesis rather than neuroprotection after focal cerebral ischemia. Neurobiol Dis 2015; 83: 16–25.
36. Zhang X, Li Y, Liu C et al. Alteration of enteric monoamines with monoamine receptors and colonic dysmotility in 6-hydroxydopamine-induced Parkinson's disease rats. Transl Res 2015; 166: 152–162.
37. Song Q, Deng Y, Yang X et al. Manganese-disrupted interaction of dopamine D1 and NMDAR in the striatum to injury learning and memory ability of mice. Mol Neurobiol 2016; 53: 6745–6758.
38. Vandeputte C, Taymans JM, Casteels C et al. Automated quantitative gait analysis in animal models of movement disorders. BMC Neurosci 2010; 11: 92.
39. Westin JE, Janssen ML, Sager TN, Temel Y. Automated gait analysis in bilateral parkinsonian rats and the role of L-DOPA therapy. Behav Brain Res 2012; 226: 519–528.
40. Jenkitkasemwong S, Wang CY, Coffey R et al. SLC39A14 is required for the development of hepatocellular iron overload in murine models of hereditary hemochromatosis. Cell Metab 2015; 22: 138–150.
41. Nisse C, Tagne-Fotso R, Howsam M, Richeval C, Labat L, Leroyer A. Blood and urinary levels of metals and metalloids in the general adult population of Northern France: The IMEPOGE study, 2008-2010. Int J Hyg Environ Health 2016; 220: 341–363.
42. Yedomon B, Menudier A, Etangs FL et al. Biomonitoring of 29 trace elements in whole blood from inhabitants of Cotonou (Benin) by ICP-MS. J Trace Elem Med Biol 2016; 10.1016/j.jtemb.2016.11.004.
43. Sun L, Yu Y, Huang T et al. Associations between ionomic profile and metabolic abnormalities in human population. PLoS ONE 2012; 7: e38845.
44. Domingo JL, Llobet JM, Corbella J. Protection of mice against the lethal effects of sodium metavanadate: a quantitative comparison of a number of chelating agents. Toxicol Lett 1985; 26: 95–99.
45. Jones MM, Basinger MA, Gale GR, Atkins LM, Smith AB, Stone A. Effect of chelate treatments on kidney, bone and brain lead levels of lead-intoxicated mice. Toxicology 1994; 89: 91–100.
46. Tuschl K, Mills PB, Clayton PT. Manganese and the brain. Int Rev Neurobiol 2013; 110: 277–312.
47. Liuzzi JP, Aydemir F, Nam H, Knutson MD, Cousins RJ. Zip14 (Slc39a14) mediates non-transferrin-bound iron uptake into cells. Proc Natl Acad Sci USA 2006; 103: 13612–13617.
48. Sato I, Matsusaka N, Kobayashi H, Nishimura Y. Effects of dietary manganese contents on 54Mn metabolism in mice. J Radiat Res 1996; 37: 125–132.
49. Chen P, Chakraborty S, Mukhopadhyay S et al. Manganese homeostasis in the nervous system. J Neurochem 2015; 134: 601–610.
50. Martinez-Finley EJ, Gavin CE, Aschner M, Gunter TE. Manganese neurotoxicity and the role of reactive oxygen species. Free Radic Biol Med 2013; 62: 65–75.
51. Peres TV, Schettinger MR, Chen P et al. Manganese-induced neurotoxicity: a review of its behavioral consequences and neuroprotective strategies. BMC Pharmacol Toxicol 2016; 17: 57.
52. Davis CD, Zech L, Greger JL. Manganese metabolism in rats: an improved methodology for assessing gut endogenous losses. Proc Soc Exp Biol Med 1993; 202: 103–108.
53. Malecki EA, Radzanowski GM, Radzanowski TJ, Gallaher DD, Greger JL. Biliary manganese excretion in conscious rats is affected by acute and chronic manganese intake but not by dietary fat. J Nutr 1996; 126: 489–498.
54. Guthrie GJ, Aydemir TB, Troche C, Martin AB, Chang SM, Cousins RJ. Influence of ZIP14 (slc39A14) on intestinal zinc processing and barrier function. Am J Physiol Gastrointest Liver Physiol 2015; 308: G171–G178.
55. Taba P. Metals and movement disorders. Curr Opin Neurol 2013; 26: 435–441.