BDE-47 and 6-OH-BDE-47 modulate calcium homeostasis in primary fetal human neural progenitor cells via ryanodine receptor-independent mechanisms

Archives of Toxicology

Volumn 88, Issue 8, 2014, Pages 1537-1548

  Gassmann, Kathrin ^a   Schreiber, Timm ^a   Dingemans, Milou M L ^b   Krause, Guido ^c   Roderigo, Claudia ^c   Giersiefer, Susanne ^a   Schuwald, Janette ^a   Moors, Michaela ^a   Unfried, Klaus ^a   Bergman, Åke ^d   Westerink, Remco H S ^b   Rose, Christine R ^c   Fritsche, Ellen ^a,c  

^a IUF LEIBNIZ RESEARCH INSTITUTE FOR ENVIRONMENTAL MEDICINE   (Germany)

^b UTRECHT UNIVERSITY   (Netherlands)

^c HEINRICH HEINE UNIVERSITY   (Germany)

^d STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

Brominated flame retardant; Calcium; Human neural progenitor cell; Neurotoxicity; Polybrominated diphenyl ether; Ryanodine receptor

Indexed keywords

CALCIUM; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; PHOSPHOLIPASE C; POLYBROMINATED DIPHENYL ETHER; RYANODINE RECEPTOR; 2,2',4,4'-TETRABROMODIPHENYL ETHER; 6-OH-BDE-47; DIPHENYL ETHER DERIVATIVE; POLYBROMINATED BIPHENYL;

ARTICLE; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL DIFFERENTIATION; CELL MEMBRANE; CELL VIABILITY; CYTOPLASM; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; MEMBRANE POTENTIAL; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; CELL CULTURE; DRUG EFFECTS; FETAL STEM CELL; GESTATIONAL AGE; HOMEOSTASIS; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; PRIMARY CELL CULTURE;

ANIMALIA;

CALCIUM; CELLS, CULTURED; FETAL STEM CELLS; GESTATIONAL AGE; HALOGENATED DIPHENYL ETHERS; HOMEOSTASIS; HUMANS; MEMBRANE POTENTIALS; NEURAL STEM CELLS; NEUROGENESIS; PATCH-CLAMP TECHNIQUES; POLYBROMINATED BIPHENYLS; PRIMARY CELL CULTURE; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL;

EID: 84904975494     PISSN: 03405761     EISSN: 14320738     Source Type: Journal    
DOI: 10.1007/s00204-014-1217-7     Document Type: Article

References (60)

1. Athanasiadou M, Cuadra SN, Marsh G, Bergman A, Jakobsson K (2008) Polybrominated diphenyl ethers (PBDEs) and bioaccumulative hydroxylated PBDE metabolites in young humans from Managua, Nicaragua. Environ Health Perspect 116:400-408 (Pubitemid 351395611)
2. Baumann N, Pham-Dinh D (2001) Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol Rev 81:871-927 (Pubitemid 32267079)
3. Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1:11-21
4. Brown AD (1978) Compatible solutes and extreme water stress in eukaryotic micro-organisms. Adv Microb Physiol 17:181-242
5. Butt AM (2011) ATP: a ubiquitous gliotransmitter integrating neuronglial networks. Semin Cell Dev Biol 22(2):205-213
6. Ciccolini F, Collins TJ, Sudhoelter J, Lipp P, Berridge MJ, Bootman MD (2003) Local and global spontaneous calcium events regulate neurite outgrowth and onset of GABAergic phenotype during neural precursor differentiation. J Neurosci 23:103-111 (Pubitemid 36050409)
7. Costa LG, Giordano G (2007) Developmental neurotoxicity of polybrominated diphenyl ether (PBDE) flame retardants. Neurotoxicology 28:1047-1067 (Pubitemid 350026603)
8. Delmas P, Brown DA (2002) Junctional signaling microdomains: bridging the gap between the neuronal cell surface and Ca2+ stores. Neuron 36:787-790 (Pubitemid 35447851)
9. Dingemans MM, Ramakers GM, Gardoni F, van Kleef RG, Bergman A, Di Luca M, van den Berg M, Westerink RH, Vijverberg HP (2007) Neonatal exposure to brominated flame retardant BDE-47 reduces long-term potentiation and postsynaptic protein levels in mouse hippocampus. Environ Health Perspect 115:865-870 (Pubitemid 46902240)
10. Dingemans MM, de Groot A, van Kleef RG, Bergman A, van den Berg M, Vijverberg HP, Westerink RH (2008) Hydroxylation increases the neurotoxic potential of BDE-47 to affect exocytosis and calcium homeostasis in PC12 cells. Environ Health Perspect 116:637-643 (Pubitemid 351864280)
11. Dingemans MM, Heusinkveld HJ, Bergman A, van den Berg M, Westerink RH (2010) Bromination pattern of hydroxylated metabolites of BDE-47 affects their potency to release calcium from intracellular stores in PC12 cells. Environ Health Perspect 118:519-525
12. Dingemans MM, van den Berg M, Westerink RH (2011) Neurotoxicity of brominated flame retardants: (in)direct effects of parent and hydroxylated polybrominated diphenyl ethers on the (developing) nervous system. Environ Health Perspect 119:900-907
13. Ebert AD, McMillan EL, Svendsen CN (2008) Isolating, expanding, and infecting human and rodent fetal neural progenitor cells. Curr Protoc Stem Cell Biol Chap 2, Unit 2D.2
14. Eskenazi B, Chevrier J, Rauch SA, Kogut K, Harley KG, Johnson C, Trujillo C, Sjödin A, Bradman A (2013) In utero and childhood polybrominated diphenyl ether (PBDE) exposures and neurodevelopment in the CHAMACOS study. Environ Health Perspect 121:257-262
15. Faure AV, Grunwald D, Moutin MJ, Hilly M, Mauger JP, Marty I, De Waard M, Villaz M, Albrieux M (2001) Developmental expression of the calcium release channels during early neurogenesis of the mouse cerebral cortex. Eur J Neurosci 14(10):1613-1622 (Pubitemid 35478030)
16. Fessenden JD, Wang Y, Moore RA, Chen SR, Allen PD, Pessah IN (2000) Divergent functional properties of ryanodine receptor types 1 and 3 expressed in a myogenic cell line. Biophys J 79:2509-2525
17. Fonnum F, Mariussen E (2009) Mechanisms involved in the neurotoxic effects of environmental toxicants such as polychlorinated biphenyls and brominated flame retardants. J Neurochem 111:1327-1347
18. Frederiksen M, Vorkamp K, Thomsen M, Knudsen LE (2009) Human internal and external exposure to PBDEs - a review of levels and sources. Int J Hyg Environ Health 212:109-134
19. Fritsche E, Cline JE, Nguyen NH, Scanlan TS, Abel J (2005) Polychlorinated biphenyls disturb differentiation of normal human neural progenitor cells: clue for involvement of thyroid hormone receptors. Environ Health Perspect 113:871-876 (Pubitemid 40984187)
20. Fritsche E, Gassmann K, Schreiber T (2011) Neurospheres as a model for developmental neurotoxicity testing. Methods Mol Biol 758:99-114
21. Gafni J, Wong PW, Pessah IN (2004) Non-coplanar 2,2′,3,5′,6- pentachlorobiphenyl (PCB 95) amplifies ionotropic glutamate receptor signaling in embryonic cerebellar granule neurons by a mechanism involving ryanodine receptors. Toxicol Sci 77:72-82 (Pubitemid 38128647)
22. Gascon M, Vrijheid M, Martínez D, Forns J, Grimalt JO, Torrent M, Sunyer J (2011) Effects of pre and postnatal exposure to low levels of polybromodiphenyl ethers on neurodevelopment and thyroid hormone levels at 4 years of age. Environ Int 37:605-611
23. Gassmann K, Abel J, Bothe H, Haarmann-Stemmann T, Merk HF, Quasthoff KN, Rockel TD, Schreiber T, Fritsche E (2010) Species-specific differential AhR expression protects human neural progenitor cells against developmental neurotoxicity of PAHs. Environ Health Perspect 118(11):1571-1577
24. Haak L, Song LS, Molinski TF, Pessah IN, Cheng H, Russell JT (2001) Sparks and puffs in oligodendrocyte progenitors: cross talk between ryanodine receptors and inositol trisphosphate receptors. J Neurosci 21:3860-3870 (Pubitemid 32466478)
25. Harishchandra RK, Wulff S, Lentzen G, Neuhaus T, Galla HJ (2010) The effect of compatible solute ectoines on the structural organization of lipid monolayer and bilayer membranes. Biophys Chem 150:37-46
26. He M, McCarthy KD (1994) Oligodendroglial signal transduction systems are developmentally regulated. J Neurochem 63:501-508 (Pubitemid 24233682)
27. Herbstman JB, Sjodin A, Kurzon M, Lederman SA, Jones RS, Rauh V, Needham L, Tang D, Niedzwiecki M, Wang RY, Perera F (2010) Prenatal exposure to PBDEs and neurodevelopment. Environ Health Perspect 118(5):712-719
28. Inglefield JR, Shafer TJ (2000a) Polychlorinated biphenyl-stimulation of Ca(2+) oscillations in developing neocortical cells: a role for excitatory transmitters and L-type voltage-sensitive Ca(2+) channels. J Pharmacol Exp Ther 295:105-113
29. Inglefield JR, Shafer TJ (2000b) Perturbation by the PCB mixture Aroclor 1254 of GABA(A) receptor-mediated calcium and chloride responses during maturation in vitro of rat neocortical cells. Toxicol Appl Pharmacol 164:184-195 (Pubitemid 30238538)
30. Inglefield JR, Mundy WR, Shafer TJ (2001) Inositol 1,4,5-triphosphate receptor-sensitive Ca(2+) release, store-operated Ca(2+) entry, and cAMP responsive element binding protein phosphorylation in developing cortical cells following exposure to polychlorinated biphenyls. J Pharmacol Exp Ther 297:762-773 (Pubitemid 32378010)
31. Kafitz KW, Meier SD, Stephan J, Rose CR (2008) Developmental profile and properties of sulforhodamine 101 - labeled glial cells in acute brain slices of rat hippocampus. J Neurosci Methods 169:84-92
32. Kiciński M, Viaene MK, Den Hond E, Schoeters G, Covaci A, Dirtu AC, Nelen V, Bruckers L, Croes K, Sioen I, Baeyens W, Van Larebeke N, Nawrot TS (2012) Neurobehavioral function and low-level exposure to brominated flame retardants in adolescents: a cross-sectional study. Environ Health 11:86. doi:10.1186/1476-069X-11-86
33. Kim KH, Bose DD, Ghogha A, Riehl J, Zhang R, Barnhart CD, Lein PJ, Pessah IN (2011) Para- and ortho-substitutions are key determinants of polybrominated diphenyl ether activity toward ryanodine receptors and neurotoxicity. Envrion Health Perspect 119:519-526
34. Kodavanti PR, Ward TR (2005) Differential effects of commercial polybrominated diphenyl ether and polychlorinated biphenyl mixtures on intracellular signaling in rat brain in vitro. Toxicol Sci 85:952-962 (Pubitemid 40846870)
35. Lentzen G, Schwarz T (2006) Extremolytes: natural compounds from extremophiles for versatile applications. Appl Microbiol Biotechnol 72:623-634 (Pubitemid 44454921)
36. Maric D, Maric I, Barker JL (2000) Developmental changes in cell calcium homeostasis during neurogenesis of the embryonic rat cerebral cortex. Cereb Cortex 10:561-573 (Pubitemid 30387835)
37. Marsh G, Hu J, Jakobsson E, Rahm S, Bergman A (1999) Synthesis and characterization of 32 polybrominated diphenyl ethers. Environ Sci Technol 33:3033-3037 (Pubitemid 29422459)
38. Marsh G, Athanasiadou M, Athanassiadis I, Sandholm A (2006) Identification of hydroxylated metabolites in 2,2',4,4'-tetrabromodiphenyl ether exposed rats. Chemosphere 63:690-697
39. Matyash M, Matyash V, Nolte C, Sorrentino V, Kettenmann H (2002) Requirement of functional ryanodine receptor type 3 for astrocyte migration. FASEB J 16:84-86
40. Meier SD, Kafitz KW, Rose CR (2008) Developmental profile and mechanisms of GABA-induced calcium signaling in hippocampal astrocytes. Glia 56:1127-1137
41. Moors M, Cline JE, Abel J, Fritsche E (2007) ERK-dependent and -independent pathways trigger human neural progenitor cell migration. Toxicol Appl Pharmacol 221:57-67 (Pubitemid 46702273)
42. Moors M, Rockel TD, Abel J, Cline JE, Gassmann K, Schreiber T, Schuwald J, Weinmann N, Fritsche E (2009) Human neurospheres as three-dimensional cellular systems for developmental neurotoxicity testing. Environ Health Perspect 117:1131-1138
43. Moors M, Vudattu NK, Abel J, Kramer U, Rane L, Ulfig N, Ceccatelli S, Seyfert-Margolies V, Fritsche E, Maeurer MJ (2010) Interleukin-7 (IL-7) and IL-7 splice variants affect differentiation of human neural progenitor cells. Genes Immun 11:11-20
44. Owens DF, Flint AC, Dammerman RS, Kriegstein AR (2000) Calcium dynamics of neocortical ventricular zone cells. Dev Neurosci 22:25-33 (Pubitemid 30098903)
45. Pessah IN, Cherednichenko G, Lein PJ (2010) Minding the calcium store: ryanodine receptor activation as a convergent mechanism of PCB toxicity. Pharmacol Ther 125:260-285
46. Piper DR, Mujtaba T, Rao MS, Lucero MT (2000) Immunocytochemical and physiological characterization of a population of cultured human neural precursors. J Neurophysiol 84(1):534-548 (Pubitemid 30490071)
47. Qiu X, Bigsby RM, Hites RA (2009) Hydroxylated metabolites of polybrominated diphenyl ethers in human blood samples from the United States. Environ Health Perspect 117:93-98
48. Reynolds BA, Weiss S (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707-1710
49. Reynolds BA, Tetzlaff W, Weiss S (1992) A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J Neurosci 12:4565-4574
50. Rice D, Barone S Jr (2000) Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 108(Suppl 3):511-533 (Pubitemid 30466179)
51. Roze E, Meijer L, Bakker A, Van Braeckel KN, Sauer PJ, Bos AF (2009) Prenatal exposure to organohalogens, including brominated flame retardants, influences motor, cognitive, and behavioral performance at school age. Environ Health Perspect 117:1953-1958
52. Schreiber T, Gassmann K, Götz C, Hübenthal U, Moors M, Krause G, Merk HF, Nguyen NH, Scanlan TS, Abel J, Rose CR, Fritsche E (2010) Polybrominated diphenyl ethers induce developmental neurotoxicity in a human in vitro model: evidence for endocrine disruption. Environ Health Perpect 118:572-578
53. Staskal DF, Hakk H, Bauer D, Diliberto JJ, Birnbaum LS (2006) Toxicokinetics of polybrominated diphenyl ether congeners 47, 99, 100, and 153 in mice. Toxicol Sci 94:28-37 (Pubitemid 44542327)
54. Svendsen CN, ter Borg MG, Armstrong RJ, Rosser AE, Chandran S, Ostenfeld T, Caldwell MA (1998) A new method for the rapid and long term growth of human neural precursor cells. J Neurosci Methods 85:141-152 (Pubitemid 29003064)
55. Takeda M, Nelson DJ, Soliven B (1995) Calcium signaling in cultured rat oligodendrocytes. Glia 14:225-236
56. Tan Y, Chen CH, Lawrence D, Carpenter DO (2004) Ortho-substituted PCBs kill cells by altering membrane structure. Toxicol Sci 80:54-59 (Pubitemid 38967396)
57. Tegenge MA, Rockel TD, Fritsche E, Bicker G (2011) Nitric oxide stimulates human neural progenitor cell migration via cGMPmediated signal transduction. Cell Mol Life Sci 68:2089-2099
58. Ward CW, Protasi F, Castillo D, Wang Y, Chen SR, Pessah IN, Allen PD, Schneider MF (2001) Type 1 and type 3 ryanodine receptors generate different Ca(2+) release event activity in both intact and permeabilized myotubes. Biophys J 81:3216-3230 (Pubitemid 33111471)
59. Xu G, Broadbelt KG, Haynes RL, Folkerth RD, Borenstein NS, Belliveau RA, Trachtenberg FL, Volpe JJ, Kinney HC (2011) Late development of the GABAergic system in the human cerebral cortex and white matter. J Neuropathol Exp Neurol 70:841-858
60. Yu K, He Y, Yeung LW, Lam PK, Wu RS, Zhou B (2008) DE-71-induced apoptosis involving intracellular calcium and the Baxmitochondria-caspase protease pathway in human neuroblastoma cells in vitro. Toxicol Sci 104:341-351 (Pubitemid 352038257)