Prenatal nicotine exposure enhances Cx43 and Panx1 unopposed channel activity in brain cells of adult offspring mice fed a high-fat/cholesterol diet

Frontiers in Cellular Neuroscience

Volumn 8, Issue DEC, 2014, Pages

  Orellana, Juan A ^a   Busso, Dolores ^a   Ramírez, Gigliola ^a   Campos, Marlys ^b   Rigotti, Attilio ^a   Eugenín, Jaime ^b   Bernhardi, Rommyvon ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b UNIVERSIDAD DE SANTIAGO DE CHILE   (Chile)

Author keywords

Brain; Connexins; Fatdiet; Glia; Hemichannels; Nicotine; Pannexins

Indexed keywords

ADENOSINE TRIPHOSPHATE; CHOLESTEROL; CONNEXIN 43; CYCLOOXYGENASE 2; GLUTAMIC ACID; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; IONOTROPIC ATP RECEPTOR TYPE 7; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NICOTINE; PANNEXIN 1; PROSTAGLANDIN E RECEPTOR 1; PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN CELL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FEEDING; GLIA CELL; GLUTAMATERGIC SYNAPSE; HIPPOCAMPUS; LIPID DIET; MICROGLIA; MOUSE; NERVE CELL; NONHUMAN; PREGNANCY; PRENATAL EXPOSURE; PROTEIN ANALYSIS; SIGNAL TRANSDUCTION;

EID: 84937736362     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2014.00403     Document Type: Article

References (76)

1. Amitai, Y. (2010). Physiologic role for “inducible” nitric oxide synthase: a new form of astrocytic-neuronal interface. Glia 58,1775-1781. doi: 10.1002/glia.21057
2. Arbeloa, J., Perez-Samartin, A., Gottlieb, M., and Matute, C. (2012). P2X7 receptor blockade prevents ATP excitotoxicity in neurons and reduces brain damage after ischemia. Neurobiol. Dis. 45, 954-961. doi: 10.1016/j.nbd.2011.12.014
3. Ashpole, N. M., Chawla, A. R., Martin, M. P., Brustovetsky, T., Brustovetsky, N., and Hudmon, A. (2013). Loss of calcium/calmodulin-dependent protein kinase II activity in cortical astrocytes decreases glutamate uptake and induces neurotoxic release of ATP. J. Biol. Chem. 288, 14599-14611. doi: 10.1074/jbc.M113.466235
4. Bilbo, S. D., Levkoff, L. H., Mahoney, J. H., Watkins, L. R., Rudy, J. W., and Maier, S. F. (2005). Neonatal infection induces memory impairments following an immune challenge in adulthood. Behav. Neurosci. 119, 293-301. doi:10.1037/0735-7044.119.1.293
5. Block, M. L., Zecca, L., and Hong, J. S. (2007). Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev. Neurosci. 8, 57-69. doi:10.1038/nrn2038
6. Boksa, P. (2010). Effects of prenatal infection on brain development and behavior: a review of findings from animal models. Brain Behav. Immun. 24, 881-897. doi:10.1016/j.bbi.2010.03.005
7. Bradford, s. T., Stamatovic, S. M., Dondeti, R. S., Keep, R. F., and Andjelkovic, A. V. (2011). Nicotine aggravates the brain postischemic inflammatory response. Am. J. Physiol. Heart Circ. Physiol. 300, H1518-H1529. doi: 10.1152/ajpheart.00928.2010
8. Burkovetskaya, M., Karpuk, N., Xiong, J., Bosch, M., Boska, M. D., Takeuchi,H. ,et al. (2014). Evidence for Aberrant Astrocyte Hemichannel activity in Juvenile Neuronal Ceroid Lipofuscinosis (JNCL). PLoS One 9:e95023. doi: 10.1371/journal.pone.0095023
9. Coddou, C., Bravo, E., and Eugenin, J. (2009). Alterations in cholinergic sensitivity of respiratory neurons induced by pre-natal nicotine: a mechanism for respiratory dysfunction in neonatal mice. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 2527-2535. doi: 10.1098/rstb.2009.0078
10. Contreras, J. E., Sanchez, H. A., Eugenin, E. A., Speidel, D., Theis, M., Willecke, K., et al. (2002). Metabolic inhibition induces opening of unapposed connexin 43 gap junction hemichannels and reduces gap junctional communication in cortical astrocytes in culture. Proc. Natl. Acad. Sci. USA 99, 495-500. doi:10.1073/pnas.012589799
11. DiFranza, J. R., and Lew, R. A. (1995). Effect of maternal cigarette smoking on pregnancy complications and sudden infant death syndrome. J. Fam. Pract. 40, 385-394.
12. Dufour, F., Liu, Q. Y., Gusev, P., Alkon, D., and Atzori, M. (2006). Cholesterol-enriched diet affects spatial learning and synaptic function in hippocampal synapses. Brain Res. 1103, 88-98. doi: 10.1016/j.brainres.2006.05.086
13. Dwyer, J. B., Broide, R. S., and Leslie, F. M. (2008). Nicotine and brain development. Birth Defects Res. C Embryo Today 84, 30-44. doi: 10.1002/bdrc.20118
14. Erickson, M. A., and Banks, W. A. (2011). Cytokine and chemokine responses in serum and brain after single and repeated injections of lipopolysaccharide: multiplex quantification with path analysis. Brain Behav. Immun. 25, 1637-1648. doi:10.1016/j.bbi.2011.06.006
15. Eugenin, J., Otarola, M., Bravo, E., Coddou, C., Cerpa, V., Reyes-Parada, M., et al. (2008). Prenatal to early postnatal nicotine exposure impairs central chemoreception and modifies breathing pattern in mouse neonates: a probable link to sudden infant death syndrome. J. Neurosci. 28, 13907-13917. doi: 10.1523/JNEUROSCI.4441-08.2008
16. Fields, R. D., and Burnstock, G. (2006). Purinergic signalling in neuron-glia interactions. Nat. Rev. Neurosci. 7, 423-436. doi: 10.1038/nrn1928
17. Froger, N., Orellana, J. A., Calvo, C. F., Amigou, E., Kozoriz, M. G., Naus, C. C., et al. (2010). Inhibition of cytokine-induced connexin43 hemichannel activity in astrocytes is neuroprotective. Mol. Cell. Neurosci. 45, 37-46. doi: 10.1016/j.n.2010.05.007
18. Froger, N., Orellana, J. A., Cohen-Salmon, M., Ezan, P., Amigou, E., Saez, J. C., et al. (2009). Cannabinoids prevent the opposite regulation of astroglial connexin43 hemichannels and gap junction channels induced by pro-inflammatory treatments. J. Neurochem. 111, 1383-1397. doi: 10.1111/j.1471-4159.2009.06407.x
19. Garre, J. M., Retamal, M. A., Cassina, P., Barbeito, L., Bukauskas, F. F., Saez, J. C., et al. (2010). FGF-1 induces ATP release from spinal astrocytes in culture and opens pannexin and connexin hemichannels. Proc. Natl. Acad. Sci. U S A 107, 22659-22664. doi:10.1073/pnas.1013793107
20. Gulbransen, B. D., Bashashati, M., Hirota, S. A., Gui, X., Roberts, J. A., Macdonald, J. A., et al. (2012). Activation of neuronal P2X7 receptor-pannexin-1 mediates death of enteric neurons during colitis. Nat. Med.18, 600-604. doi: 10.1038/nm.2679
21. Huckstepp, R. T. R., id Bihi, R., Eason, R., Spyer, K. M., Dicke, N., Willecke, K., et al. (2010). Connexin hemichannel-mediated CO2-dependent release of ATP in the medulla oblongata contributes to central respiratory chemosensitivity. J. Physiol. 588, 3901-3920. doi: 10.1113/jphysiol.2010.192088
22. Iglesias, R., Dahl, G., Qiu, F., Spray, D. C., and Scemes, E. (2009). Pannexin 1: the molecular substrate of astrocyte “hemichannels”. J. Neurosci. 29, 7092-7097. doi: 10.1523/JNEUROSCI.6062-08.2009
23. Jacobsen, L. K., Slotkin, T. A., Westerveld, M., Mencl, W. E., and Pugh, K. R. (2006). Visuospatial memory deficits emerging during nicotine withdrawal in adolescents with prenatal exposure to active maternal smoking. Neuropsychopharmacology 31,1550-1561. doi: 10.1038/sj.npp.1300981
24. Julvez, J., Ribas-Fito, N., Torrent, M., Forns, M., Garcia-Esteban, R., and Sunyer, J. (2007). Maternal smoking habits and cognitive development ofchildren at age 4 years in a population-based birth cohort. Int. J. Epidemiol. 36, 825-832. doi: 10.1093/ije/dym107
25. Karpuk, N., Burkovetskaya, M., Fritz, T., Angle, A., and Kielian, T. (2011). Neuroinflammation leads to region-dependent alterations in astrocyte gap junction communication and hemichannel activity. J. Neurosci. 31,414-425. doi:10.1523/JNEUROSCI.5247-10.2011
26. Lau, P. P., Li, L., Merched, A. J., Zhang, A. L., Ko, K. W., and Chan, L. (2006). Nicotine induces proinflammatory responses in macrophages and the aorta leading to acceleration of atherosclerosis in low-density lipoprotein receptor(-/-) mice. Arterioscler. Thromb. Vasc. Biol. 26,143-149. doi: 10.1161/01.ATV.0000193510.19000.10
27. Lau, A., and Tymianski, M. (2010). Glutamate receptors, neurotoxicity and neurodegeneration. Pflugers Arch. 460, 525-542. doi: 10.1007/s00424-010-0809-1
28. Lewis, D. K., Bake, S., Thomas, K., Jezierski, M. K., and Sohrabji, F. (2010). A high cholesterol diet elevates hippocampal cytokine expression in an age and estrogen-dependent manner in female rats. J. Neuroimmunol. 223, 31-38. doi:10.1016/j.jneuroim.2010.03.024
29. Lin, J. H., Lou, N., Kang, N., Takano, T., Hu, F., Han, X., et al. (2008). A central role of connexin 43 in hypoxic preconditioning. J. Neurosci. 28, 681-695. doi: 10.1523/JNEUROSCI.3827-07.2008
30. Locovei, S., Wang, J., and Dahl, G. (2006). Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium. FEBS Lett. 580, 239-244. doi:10.1016/j.febslet.2005.12.004
31. Luck, W., Nau, H., Hansen, R., and Steldinger, R.(1985). Extent of nicotine and cotinine transfer to the human fetus, placenta and amniotic fluid of smoking mothers. Dev. Pharmacol. Ther. 8, 384-395.
32. Morton, D. B., and Griffiths, P. H. (1985). Guidelines on the recognition of pain, distress and discomfort in experimental animals and an hypothesis for assessment. Vet. Rec. 116, 431-436. doi: 10.1136/vr.116.16.431
33. Muneoka, K., Ogawa, T., Kamei, K., Muraoka, S., Tomiyoshi, R., Mimura, Y., et al. (1997). Prenatal nicotine exposure affects the development of the central serotonergic system as well as the dopaminergic system in rat offspring: involvement of route of drug administrations. Brain Res. Dev. Brain Res. 102, 117-126. doi: 10.1016/S0165-3806(97)00092-8
34. Naeye, R. L., and Peters, E. C. (1984). Mental development of children whose mothers smoked during pregnancy. Obstet. Gynecol. 64, 601-607.
35. Navarro, H. A., Seidler, F. J., Schwartz, R. D., Baker, F. E., Dobbins, S. S., and Slotkin, T. A. (1989). Prenatal exposure to nicotine impairs nervous system development at a dose which does not affect viability or growth. Brain Res. Bull. 23,187-192. doi:10.1016/0361-9230(89)90146-9
36. Orellana, J. A., Froger, N., Ezan, P., Jiang, J. X., Bennett, M. V., Naus, C. C., et al. (2011a). ATP and glutamate released via astroglial connexin 43 hemichannels mediate neuronal death through activation of pannexin 1 hemichannels. J. Neurochem. 118, 826-840. doi: 10.1111/j.1471-4159.2011.07210.x
37. Orellana, J. A., Hernandez, D. E., Ezan, P., Velarde, V., Bennett, M. V., Giaume, C., et al. (2010). Hypoxia in high glucose followed by reoxygenation in normal glucose reduces the viability of cortical astrocytes through increased permeability of connexin 43 hemichannels. Glia 58, 329-343. doi: 10.1002/glia.20926
38. Orellana, J. A., Montero, T. D., and von Bernhardi, R. (2013). Astrocytes inhibit nitric oxide-dependent Ca(2+) dynamics in activated microglia: involvement of ATP released via pannexin 1 channels. Glia 61, 2023-2037. doi: 10.1002/glia.22573
39. Orellana, J. A., Saez, P. J., Cortes-Campos, C., Elizondo, R. J., Shoji, K. F., Contreras- Duarte, S., et al. (2012). Glucose increases intracellular free Ca(2+) in tanycytes via ATP released through connexin 43 hemichannels. Glia 60, 53-68. doi: 10.1002/glia.21246
40. Orellana, J. A., Saez, P. J., Shoji, K. F., Schalper, K. A., Palacios-Prado, N., Velarde, V., et al. (2009). Modulation of brain hemichannels and gap junction channels by pro-inflammatory agents and their possible role in neurodegeneration. Antioxid. Redox Signal.11,369-399. doi: 10.1089/ars.2008.2130
41. Orellana, J. A., Shoji, K. F., Abudara, V., Ezan, P., Amigou, E., Saez, P. J., et al. (2011b). Amyloid v-induced death in neurons involves glial and neuronal hemichannels. J. Neurosci. 31, 4962-4977. doi: 10.1523/JNEUROSCI.6417-10.2011
42. Pelegrin, P., and Surprenant, A. (2006). Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor. EMBO J. 25, 5071-5082. doi: 10.1038/sj.emboj.7601378
43. Perea, G., and Araque, A. (2010). Glia modulates synaptic transmission. Brain Res. Rev. 63, 93-102. doi: 10.1016/j.brainresrev.2009.10.005
44. Perea, G., Navarrete, M., and Araque, A. (2009). Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci. 32, 421-431. doi:10.1016/j.tins.2009.05.001
45. Rantakallio, P., and Koiranen, M. (1987). Neurological handicaps among children whose mothers smoked during pregnancy. Prev. Med. 16, 597-606. doi: 10.1016/0091-7435(87)90043-0
46. Retamal, M. A., Froger, N., Palacios-Prado, N., Ezan, P., Saez, P. J., Saez, J. C., et al. (2007). Cx43 hemichannels and gap junction channels in astrocytes are regulated oppositely by proinflammatory cytokines released from activated microglia. J. Neurosci. 27,13781-13792. doi: 10.1523/JNEUR0SCI.2042-07.2007
47. Rouach, N., Avignone, E., Meme, W., Koulakoff, A., Venance, L., Blomstrand, F., et al. (2002). Gap junctions and connexin expression in the normal and pathological central nervous system. Biol. Cell 94, 457-475. doi: 10.1016/S0248-4900(02)00016-3
48. Roy, T. S., and Sabherwal, U.(1994). Effects of prenatal nicotine exposure on the morphogenesis of somatosensory cortex. Neurotoxicol. Teratol.16, 411-421. doi: 10.1016/0892-0362(94)90030-2
49. Roy, T. S., and Sabherwal, U.(1998). Effects of gestational nicotine exposure on hippocampal morphology. Neurotoxicol. Teratol. 20, 465-473. doi: 10.1016/S0892-0362(97)00137-2
50. Roy, T. S., Seidler, F. J., and Slotkin, T. A. (2002). Prenatal nicotine exposure evokes alterations of cell structure in hippocampus and somatosensory cortex. J. Pharmacol. Exp. Ther. 300, 124-133. doi: 10.1124/jpet.300.1.124
51. Saez, J. C., and Leybaert, L. (2014). Hunting for connexin hemichannels. FEBS Lett. 588, 1205-1211. doi: 10.1016/j.febslet.2014.03.004
52. Saez, P. J., Shoji, K. F., Retamal, M. A., Harcha, P. A., Ramirez, G., Jiang, J. X., et al. (2013). ATP is required and advances cytokine-induced gap junction formation in microglia in vitro. Mediators Inflamm. 2013:216-402. doi:10.1155/2013/216402
53. Salvemini, D., Misko, T. P., Masferrer, J. L., Seibert, K., Currie, M. G., and Needleman, P. (1993). Nitric oxide activates cyclooxygenase enzymes. Proc. Natl. Acad. Sci. USA 90, 7240-7244. doi: 10.1073/pnas.90.15.7240
54. Samy, A. S., and Igwe, O. J. (2012). Regulation of IL-1beta-induced cyclooxygenase- 2 expression byinteractions ofAbeta peptide, apolipoprotein E and nitric oxide in human neuroglioma. J. Mol. Neurosci. 47, 533-545. doi: 10.1007/s12031-011-9670-8
55. Schalper, K. A., Palacios-Prado, N., Orellana, J. A., and Saez, J. C. (2008). Currently used methods for identification and characterization of hemichannels. Cell Commun. Adhes.15, 207-218. doi: 10.1080/15419060802014198
56. Schneider, T., Ilott, N., Brolese, G., Bizarro, L., Asherson, P. J.,andStolerman,I. P. (2011). Prenatal exposure to nicotine impairs performance of the 5-choice serial reaction time task in adult rats. Neuropsychopharmacology 36,1114-1125. doi: 10.1038/npp.2010.249
57. Sheng, W., zong, Y., Mohammad, A., Ajit, D., Cui, J., Han, D., et al. (2011). Pro-inflammatory cytokines and lipopolysaccharide induce changes in cell morphology and upregulation of ERK1/2, iNOS and sPLA(2)-IIA expression in astrocytes and microglia. J. Neuroinflammation 8:121. doi: 10.1186/1742-20948-121
58. Shestopalov, V. I., and Slepak, V. Z. (2014). Molecular pathways of pannexin1- mediated neurotoxicity. Front. Physiol. 5:23. doi: 10.3389/fphys.2014.00023
59. Silverman, W., Locovei, S., and Dahl, G. (2008). Probenecid, a gout remedy, inhibits pannexin 1 channels. Am. J. Physiol. Cell Physiol. 295, C761-C767. doi:10.1152/ajpcell.00227.2008
60. Slotkin, T. A., Lappi, S. E., Tayyeb, M. I., and Seidler, F. J. (1991). Chronic prenatal nicotine exposure sensitizes rat brain to acute postnatal nicotine challenge as assessed with ornithine decarboxylase. Life Sci. 49, 665-670. doi: 10.1016/0024-3205(91)90113
61. P Stehberg, J., Moraga-Amaro, R., Salazar, C., Becerra, A., Echeverria, C., Orellana, J. A., et al. (2012). Release of gliotransmitters through astroglial connexin 43 hemichannels is necessary for fear memory consolidation in the basolateral amygdala. FASEB J. 26, 3649-3657. doi: 10.1096/fj.11-198416
62. Takeuchi, H., Jin, S., Wang, J., Zhang, G., Kawanokuchi, J., Kuno, R., et al. (2006). Tumor necrosis factor-alpha induces neurotoxicity via glutamate release from hemichannels ofactivated microglia in an autocrine manner. J. Biol. Chem. 281, 21362-21368. doi: 10.1074/jbc.M600504200
63. Thirumangalakudi, L., Prakasam, A., Zhang, R., Bimonte-Nelson, H., Sambamurti, K., Kindy, M. S., et al. (2008). High cholesterol-induced neuroinflammation and amyloid precursor protein processing correlate with loss of working memory in mice. J. Neurochem. 106, 475-485. doi: 10.1111/j.1471-4159.2008.05415.x
64. Thompson, R. J., Jackson, M. F., Olah, M. E., Rungta, R. L., Hines, D. J., Beazely, M. A., et al. (2008). Activation of pannexin-1 hemichannels augments aberrant bursting in the hippocampus. Science 322, 1555-1559. doi: 10.1126/science.1165209
65. Thompson, R. J. R., Zhou, N. N., and Macvicar, B. A. (2006). Ischemia opens neuronal gap junction hemichannels. Science 312, 924-927. doi: 10.1126/science.1126241
66. Toledo-Rodriguez, M., Lotfipour, S., Leonard, G., Perron, M., Richer, L., Veillette, S., et al. (2010). Maternal smoking during pregnancy is associated with epigenetic modifications of the brain-derived neurotrophic factor-6 exon in adolescent offspring. Am. J. Med. Genet. B Neuropsychiatr. Genet. 153B, 1350-1354. doi: 10.1002/ajmg.b.31109
67. Torres, A., Wang, F., Xu, Q., Fujita, T., Dobrowolski, R., Willecke, K., et al. (2012). Extracellular Ca(2)(+) acts as a mediator of communication from neurons to glia. Sci. Signal. 5:ra8. doi: 10.1126/scisignal.2002160
68. Trivino, A., Ramirez, A. I., Salazar, J. J., De Hoz, R., Rojas, B., Padilla, E., et al. (2006). A cholesterol-enriched diet induces ultrastructural changes in retinal and macroglial rabbit cells. Exp. Eye Res. 83, 357-366. doi: 10.1016/j.exer.2005.12.020
69. Tzeng, S. F., Hsiao, H. Y., and Mak, O. T. (2005). Prostaglandins and cyclooxy- genases in glial cells during brain inflammation. Curr. Drug Targets Inflamm. Allergy 4, 335-340. doi: 10.2174/1568010054022051
70. van de Kamp, J. L., and Collins, A. C. (1994). Prenatal nicotine alters nicotinic receptor development in the mouse brain. Pharmacol. Biochem. Behav. 47, 889-900. doi: 10.1016/0091-3057(94)90293-3
71. Vinukonda, G., Csiszar, A., Hu, F., Dummula, K., Pandey, N. K., Zia, M. T., et al. (2010). Neuroprotection in a rabbit model of intraventricular haemorrhage by cyclooxygenase-2, prostanoid receptor-1 or tumour necrosis factor-alpha inhibition. Brain 133, 2264-2280. doi: 10.1093/brain/awq107
72. Wang, N., De Bock, M., Decrock, E., Bol, M., Gadicherla, A., Bultynck, G., et al. (2013a). Connexin targeting peptides as inhibitors of voltage- and intracellular Ca2+-triggered Cx43 hemichannel opening. Neuropharmacology 75, 506-516. doi: 10.1016/j.neuropharm.2013.08.021
73. Wang, N., De Bock, M., Decrock, E., Bol, M., Gadicherla, A., Vinken, M., et al. (2013b). Paracrine signaling through plasma membrane hemichannels. Biochim. Biophys. Acta 1828, 35-50. doi: 10.1016/j.bbamem.2012.07.002
74. Woodward, D. F., Jones, R. L., and Narumiya, S. (2011). International Union of Basic and Clinical Pharmacology. LXXXIII: classification of prostanoid receptors, updating 15 years of progress. Pharmacol. Rev. 63,471-538. doi: 10.1124/pr.110.003517
75. Xiong, J., Burkovetskaya, M., Karpuk, N., and Kielian, T. (2012). IL-1RI (interleukin-1 receptor type I) signalling is essential for host defence and hemichannel activity during acute central nervous system bacterial infection. ASNNeuro 4:e00085. doi: 10.1042/AN20120008
76. Ya, B. L., Liu, W. Y., Ge, F., Zhang, Y. X., Zhu, B. L., and Bai, B. (2013). Dietary cholesterol alters memory and synaptic structural plasticity in young rat brain. Neurol. Sci. 34,1355-1365. doi: 10.1007/s10072-012-1241-4