PCB-95 modulates the calcium-dependent signaling pathway responsible for activity-dependent dendritic growth

Environmental Health Perspectives

Volumn 120, Issue 7, 2012, Pages 1003-1009

  Wayman, Gary A ^a   Bose, Diptiman D ^b   Yang, Dongren ^b   Lesiak, Adam ^a   Bruun, Donald ^b   Impey, Soren ^c   Ledoux, Veronica ^c   Pessah, Isaac N ^b   Lein, Pamela J ^b,c  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Ca2+; CaMKI; CREB; Dendrites; Developmental neurotoxicity; Hippocampal MEK; Neuronal connectivity; Neurons; Non dioxin like PCBs; Ryanodine receptor; Utism; Wnt2

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; BICUCULLINE; CALCIUM; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE I; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE; POLYCHLORINATED BIPHENYL; RYANODINE; RYANODINE RECEPTOR; SMALL INTERFERING RNA; WNT2 PROTEIN;

ANIMAL CELL; ARTICLE; CALCIUM SIGNALING; CONTROLLED STUDY; CYTOARCHITECTURE; DENDRITE GROWTH; DEVELOPMENTAL DISORDER; ENVIRONMENTAL FACTOR; EXPOSURE; NERVE CELL GROWTH; NONHUMAN; PERIKARYON; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RAT; RISK FACTOR; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; WNT SIGNALING PATHWAY;

ANIMALS; CALCIUM; CELLS, CULTURED; DENDRITES; HIPPOCAMPUS; NEURONS; POLYCHLORINATED BIPHENYLS; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

RATTUS;

EID: 84864134381     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.1104833     Document Type: Article

References (57)

1. Adasme T, Haeger P, Paula-Lima AC, Espinoza I, Casas-AlarconMM, Carrasco MA, et al. 2011. Involvement of ryanodine receptors in neurotrophin-induced hippocampal synaptic plasticity and spatial memory formation. Proc Natl Acad Sci USA 108(7):3029-3034.
2. 2+signaling and associative memory: steps through a calexcitin, ryanodine receptor, K+ channel cascade. Trends Neurosci 21(12):529-537.
3. Baker KD, Edwards TM, Rickard NS. 2010. A ryanodine receptor agonist promotes the consolidation of long-term memory in young chicks. Behav Brain Res 206(1):143-146.
4. 2+store in the plasticity of central neurons. Trends Pharmacol Sci 27(2):78-84.
5. Berridge MJ. 2006. Calcium microdomains: organization and function. Cell Calcium 40(5-6):405-412.
6. Bourgeron T. 2009. A synaptic trek to autism. Curr Opin Neurobiol 19(2):231-234.
7. Buck E, Zimanyi I, Abramson JJ, Pessah IN. 1992. Ryanodine stabilizes multiple conformational states of the skeletal. muscle calcium release channel. J Biol Chem 267(33):23560-23567.
8. Cavallaro S, Meiri N, Yi CL, Musco S, Ma W, Goldberg J, et al. 1997. Late memory-related genes in the hippocampus revealed by RNA fingerprinting. Proc Natl Acad Sci USA 94(18):9669-9673.
9. Dolmetsch RE, Xu K, Lewis RS. 1998. Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392(6679):933-936.
10. Edwards TM, Rickard NS. 2006. Pharmaco-behavioural evidence indicating a complex role for ryanodine receptor calcium release channels in memory processing for a passive avoidance task. Neurobiol Learning Mem 86(1):1-8.
11. Emptage N, Bliss TV, Fine A. 1999. Single synaptic events evoke NMDA receptor-mediated release of calcium from internal stores in hippocampal dendritic spines. Neuron 22(1):115-124.
12. Fessenden JD, Perez CF, Goth S, Pessah IN, Allen PD. 2003. Identification of a key determinant of ryanodine receptor type 1 required for activation by 4-chloro-m-cresol. J Biol Chem 278(31):28727-28735.
13. Futatsugi A, Kato K, Ogura H, Li ST, Nagata E, Kuwajima G, et al. 1999. Facilitation of NMDAR-independent LTP and spatial learning in mutant mice lacking ryanodine receptor type 3. Neuron 24(3):701-713.
14. Gafni J, Wong PW, Pessah IN. 2004. Non-coplanar 2,2',3,5',6-pentachlorobiphenyl (PCB95) amplifies ionotropic glutamate receptor signaling in embryonic cerebellar granule neurons by a mechanism involving ryanodine receptors. Toxicol Sci 77(1):72-82.
15. Galeotti N, Quattrone A, Vivoli E, Norcini M, Bartolini A, Ghelardini C. 2008. Different involvement of type 1, 2, and 3 ryanodine receptors in memory processes. Learn Memory 15(5):315-323.
16. Geschwind DH, Levitt P. 2007. Autism spectrum disorders: developmental disconnection syndromes. Curr Opin Neurobiol 17(1):103-111.
17. Han C, Lin X. 2005. Shifted from Wnt to Hedgehog signaling pathways [Preview]. Mol Cell 17(3):321-322.
18. 2+entry, and cAMP responsive element binding protein phosphorylation in developing cortical cells following exposure to polychlorinated biphenyls. JPharmacol Exp Ther 297(2):762-773.
19. Jolous-Jamshidi B, Cromwell HC, McFarland AM, Meserve LA. 2010. Perinatal exposure to polychlorinated biphenyls alters social behaviors in rats. Toxicol Lett 199(2):136-143.
20. Kemmerling U, Munoz P, Muller M, Sanchez G, Aylwin ML, Klann E, et al. 2007. Calcium release by ryanodine receptors mediates hydrogen peroxide-induced activation of ERK and CREB phosphorylation in N2a cells and hippocampal neurons. Cell Calcium 41(5):491-502.
21. Kenet T, Froemke RC, Schreiner CE, Pessah IN, Merzenich MM. 2007. Perinatal exposure to a noncoplanar polychlorinated biphenyl alters tonotopy, receptive fields, and plasticity in rat primary auditory cortex. Proc Natl Acad Sci USA 104(18):7646-7651.
22. Korkotian E, Segal M. 1999. Release of calcium from stores alters the morphology of dendritic spines in cultured hippocampal neurons. Proc Natl Acad Sci USA 96(21):12068-12072.
23. Kouzu Y, Moriya T, Takeshima H, Yoshioka T, Shibata S. 2000. Mutant mice lacking ryanodine receptor type 3 exhibit deficits of contextual fear conditioning and activation of calcium/calmodulin-dependent protein kinase II in the hippocampus. Brain Res Mol Brain Res 76(1):142-150.
24. 2+signaling. Curr Opin Neurobiol 17(1):112-119.
25. Lein PJ, Barnhart CD, Pessah IN. 2011. Acute hippocampal slice preparation and hippocampal slice cultures. Methods Mol Biol 758:115-134.
26. Lein PJ, Yang D, Bachstetter AD, Tilson HA, Harry GJ, MervisRF, et al. 2007. Ontogenetic alterations in molecular and structural correlates of dendritic growth after developmental exposure to polychlorinated biphenyls. Environ Health Perspect 115:556-563.
27. Levitt P, Campbell DB. 2009. The genetic and neurobiologic compass points toward common signaling dysfunctions in autism spectrum disorders. J Clin Invest 119(4):747-754.
28. Li ST, Kato K, Mikoshiba K. 1998. Effect of calcineurin inhibitors on long-term depression in CA1 rat hippocampal neurons. 28th Annu Meet Soc Neurosci Abs 24:1815.
29. 2+spike frequency can optimize gene expression. Nature 392(6679):936-941.
30. Lohmann C. 2009. Calcium signaling and the development of specific neuronal connections. Prog Brain Res 175:443-452.
31. Lohmann C, Finski A, Bonhoeffer T. 2005. Local calcium transients regulate the spontaneous motility of dendritic filopodia. Nat Neurosci 8(3):305-312.
32. Lohmann C, Myhr KL, Wong RO. 2002. Transmitter-evoked local calcium release stabilizes developing dendrites. Nature 418(6894):177-181.
33. Lohmann C, Wong RO. 2005. Regulation of dendritic growth and plasticity by local and global calcium dynamics. Cell Calcium 37(5):403-409.
34. Lu YF, Hawkins RD. 2002. Ryanodine receptors contribute to cGMP-induced late-phase LTP and CREB phosphorylation in the hippocampus. JNeurophysiol 88(3):1270-1278.
35. Matsuo N, Tanda K, Nakanishi K, Yamasaki N, Toyama K, Takao K, et al. 2009. Comprehensive behavioral pheno-typing of ryanodine receptor type 3 (RyR3) knockout mice: decreased social contact duration in two social interaction tests. Front Behav Neurosci 3:3; doi 10.3389/neuro.08.003.2009 [Online 7 May 2009].
36. Meijering E, Jacob M, Sarria JC, Steiner P, Hirling H, Unser M. 2004. Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images. Cytometry A 58(2):167-176.
37. 2+release from ryanodine receptors in rat spiral ganglion neurons. Cell Calcium 43(4):356-366.
38. Pasca SP, Portmann T, Voineagu I, Yazawa M, Shcheglovitov A, Pasca AM, et al. 2011. Using iPSC-derived neurons to uncover cellular phenotypes associated with Timothy syndrome [Letter]. Nat Med 17(12):1657-1662.
39. Pessah IN, Cherednichenko G, Lein PJ. 2010. Minding the calcium store: ryanodine receptor activation as a convergent mechanism of PCBtoxicity. Pharmacol Ther 125(2):260-285.
40. Pessah IN, Lein PJ. 2008. Evidence for environmental susceptibility in autism: What we need to know about gene × environment interactions. In: Autism: Current Theories and Evidence (Zimmerman A, ed). Totawa, NJ:Humana Press, 409-428.
41. Pittenger C, Kandel ER. 2003. In search of general mechanisms for long-lasting plasticity: aplysia and the hippocampus. Philos Trans R Soc Lond B Biol Sci 358(1432):757-763.
42. 2+release and generates hydrogen peroxide, which jointly stimulate NF-kB activity. Antioxid Redox Signaling 14(7):1245-1259.
43. Rosso SB, Sussman D, Wynshaw-Boris A, Salinas PC. 2005. Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development. Nat Neurosci 8(1):34-42.
44. Rubenstein JL, Merzenich MM. 2003. Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav 2(5):255-267.
45. Segal M, Korkotian E, Murphy DD. 2000. Dendritic spine formation and pruning: common cellular mechanisms? Trends Neurosci 23(2):53-57.
46. V1.2 calcium channel dysfunction causes a multisystem disorder including arrhythmia and autism. Cell 119(1):19-31.
47. 2+from intracellular stores. J Neurophysiol 77(2):812-825.
48. Wang Y, Wu J, Rowan MJ, Anwyl R. 1996. Ryanodine produces a low frequency stimulation-induced NMDA receptor-independent long-term potentiation in the rat dentate gyrus in vitro. J Physiol 495 (Pt 3):755-767.
49. Wayman GA, Impey S, Marks D, Saneyoshi T, Grant WF, Derkach V, et al. 2006. Activity-dependent dendritic arborization mediated by CaM-kinase I activation and enhanced CREB-dependent transcription of Wnt-2. Neuron 50(6):897-909.
50. Wayman GA, Kaech S, Grant WF, Davare M, Impey S, Tokumitsu H, et al. 2004. Regulation of axonal extension and growth cone motility by calmodulin-dependent protein kinase I. J Neurosci 24(15):3786-3794.
51. Wayman GA, Yang D, Bose DD, Lesiak A, Ledoux V, BruunD, et al. 2012. PCB-95 promotes dendritic growth via ryanodine receptor-dependent mechanisms. Environ Health Perspect 120:997-1002.
52. Wong PW, Brackney WR, Pessah IN. 1997. ortho-Substituted polychlorinated biphenyls alter microsomal calcium transport by direct interaction with ryanodine receptors of mammalian brain. J Biol Chem 272(24):15145-15153.
53. Wong PW, Garcia EF, Pessah IN. 2001. ortho-Substituted PCB95 alters intracellular calcium signaling and causes cellular acidification in PC12 cells by an immunophilin-dependent mechanism. J Neurochem 76(2):450-463.
54. Yang D, Kim KH, Phimister A, Bachstetter AD, Ward TR, Stackman RW, et al. 2009. Developmental exposure to polychlorinated biphenyls interferes with experience-dependent dendritic plasticity and ryanodine receptor expression in weanling rats. Environ Health Perspect 117:426-435.
55. Yu X, Malenka RC. 2003. b-catenin is critical for dendritic morphogenesis. Nat Neurosci 6(11):1169-1177.
56. Zhao W, Meiri N, Xu H, Cavallaro S, Quattrone A, Zhang L, et al. 2000. Spatial learning induced changes in expression of the ryanodine type II receptor in the rat hippocampus. FASEB J 14(2):290-300.
57. 2+release channel from skeletal. muscle sarcoplasmic reticulum. MolPharmacol 42(6):1049-1057.