Disruption in Connexin-Based Communication Is Associated with Intracellular Ca2+ Signal Alterations in Astrocytes from Niemann-Pick Type C Mice

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Sáez, Pablo J ^a   Orellana, Juan A ^b   Vega Riveros, Natalia ^a   Figueroa, Vania A ^a,c   Hernández, Diego E ^a   Castro, Juan F ^b   Klein, Andrés D ^b   Jiang, Jean X ^d   Zanlungo, Silvana ^b,e   Sáez, Juan C ^a,c  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^c Centro Interdisciplinario de Neurociencias de Valparaíso   (Chile)

^d UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^e FONDAP Center for Genome Regulation (CGR)   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CONNEXIN 43; GAP JUNCTION PROTEIN; MEMBRANE PROTEIN; PANNEXIN 1; PURINERGIC P2Y1 RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AUTOSOMAL DISORDER; BRAIN SLICE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL COMMUNICATION; CONTROLLED STUDY; DEGENERATIVE DISEASE; DRUG TARGETING; GAP JUNCTION; GENE; GENE EXPRESSION; GENE MUTATION; HIPPOCAMPUS; KNOCKOUT MOUSE; MACROGLIA; MOUSE; NERVE CELL; NERVE CELL CULTURE; NERVOUS SYSTEM INFLAMMATION; NIEMANN PICK DISEASE; NONHUMAN; NPC1 GENE; PATHOGENESIS;

ADENOSINE DIPHOSPHATE; ANIMALS; ANIMALS, NEWBORN; ANTIBODIES; ASTROCYTES; CALCIUM; CALCIUM SIGNALING; CELL COMMUNICATION; CELLS, CULTURED; CONNEXIN 43; CONNEXINS; DISEASE MODELS, ANIMAL; GAP JUNCTIONS; GENE DELETION; GENE EXPRESSION REGULATION; HIPPOCAMPUS; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NIEMANN-PICK DISEASE, TYPE C; PROTEINS; RECEPTORS, PURINERGIC P2Y1; TISSUE CULTURE TECHNIQUES;

EID: 84881601333     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071361     Document Type: Article

References (87)

1. Carstea ED, Morris JA, Coleman KG, Loftus SK, Zhang D, et al. (1997) Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science 277: 228-231.
2. Rosenbaum AI, Maxfield FR, (2011) Niemann-Pick type C disease: molecular mechanisms and potential therapeutic approaches. J Neurochem 116: 789-795.
3. Liscum L, Ruggiero RM, Faust JR, (1989) The intracellular transport of low density lipoprotein-derived cholesterol is defective in Niemann-Pick type C fibroblasts. J Cell Biol 108: 1625-1636.
4. Loftus SK, Morris JA, Carstea ED, Gu JZ, Cummings C, et al. (1997) Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science 277: 232-235.
5. Pressey SN, Smith DA, Wong AM, Platt FM, Cooper JD, (2012) Early glial activation, synaptic changes and axonal pathology in the thalamocortical system of Niemann-Pick type C1 mice. Neurobiol Dis 45: 1086-1100.
6. Xu S, Chen X, Wei X, Liu G, Wang Q, (2011) Presynaptic impairment in Niemann-Pick C1-deficient neurons: not dependent on presence of glial cells. Neurosci Lett 496: 54-59.
7. Xu S, Zhou S, Xia D, Xia J, Chen G, et al. (2010) Defects of synaptic vesicle turnover at excitatory and inhibitory synapses in Niemann-Pick C1-deficient neurons. Neuroscience 167: 608-620.
8. Klein A, Maldonado C, Vargas LM, Gonzalez M, Robledo F, et al. (2011) Oxidative stress activates the c-Abl/p73 proapoptotic pathway in Niemann-Pick type C neurons. Neurobiol Dis 41: 209-218.
9. Walkley SU, Suzuki K, (2004) Consequences of NPC1 and NPC2 loss of function in mammalian neurons. Biochim Biophys Acta 1685: 48-62.
10. Zaaraoui W, Crespy L, Rico A, Faivre A, Soulier E, et al. (2011) In vivo quantification of brain injury in adult Niemann-Pick Disease Type C. Mol Genet Metab. 103: 138-141.
11. Patel SC, Suresh S, Kumar U, Hu CY, Cooney A, et al. (1999) Localization of Niemann-Pick C1 protein in astrocytes: implications for neuronal degeneration in Niemann- Pick type C disease. Proc Natl Acad Sci U S A 96: 1657-1662.
12. Suzuki H, Sakiyama T, Harada N, Abe M, Tadokoro M, (2003) Pathologic changes of glial cells in murine model of Niemann-Pick disease type C: immunohistochemical, lectin-histochemical and ultrastructural observations. Pediatr Int 45: 1-4.
13. Yu T, Shakkottai VG, Chung C, Lieberman AP, (2011) Temporal and cell-specific deletion establishes that neuronal Npc1 deficiency is sufficient to mediate neurodegeneration. Hum Mol Genet 20: 4440-4451.
14. Zhang M, Strnatka D, Donohue C, Hallows JL, Vincent I, et al. (2008) Astrocyte-only Npc1 reduces neuronal cholesterol and triples life span of Npc1-/- mice. J Neurosci Res 86: 2848-2856.
15. Baudry M, Yao Y, Simmons D, Liu J, Bi X, (2003) Postnatal development of inflammation in a murine model of Niemann-Pick type C disease: immunohistochemical observations of microglia and astroglia. Exp Neurol 184: 887-903.
16. Giaume C, Koulakoff A, Roux L, Holcman D, Rouach N, (2010) Astroglial networks: a step further in neuroglial and gliovascular interactions. Nat Rev Neurosci 11: 87-99.
17. Sáez JC, Berthoud VM, Brañes MC, Martínez AD, Beyer EC, (2003) Plasma membrane channels formed by connexins: their regulation and functions. Physiol Rev 83: 1359-1400.
18. Orellana JA, Sáez PJ, Shoji KF, Schalper KA, Palacios-Prado N, 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.
19. Koulakoff A, Mei X, Orellana JA, Sáez JC, Giaume C (2011) Glial connexin expression and function in the context of Alzheimer's disease. Biochim Biophys Acta.
20. Orellana JA, von Bernhardi R, Giaume C, Sáez JC, (2012) Glial hemichannels and their involvement in aging and neurodegenerative diseases. Rev Neurosci 23: 163-177.
21. Orellana JA, Hernandez DE, Ezan P, Velarde V, Bennett MV, 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.
22. Orellana JA, Shoji KF, Abudara V, Ezan P, Amigou E, et al. (2011) Amyloid beta-induced death in neurons involves glial and neuronal hemichannels. J Neurosci 31: 4962-4977.
23. Retamal MA, Froger N, Palacios-Prado N, Ezan P, Sáez PJ, 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.
24. Contreras JE, Sanchez HA, Eugenin EA, Speidel D, Theis M, 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 U S A 99: 495-500.
25. Siller-Jackson AJ, Burra S, Gu S, Xia X, Bonewald LF, et al. (2008) Adaptation of connexin 43-hemichannel prostaglandin release to mechanical loading. J Biol Chem 283: 26374-26382.
26. Amigo L, Mendoza H, Castro J, Quinones V, Miquel JF, et al. (2002) Relevance of Niemann-Pick type C1 protein expression in controlling plasma cholesterol and biliary lipid secretion in mice. Hepatology 36: 819-828.
27. Orellana JA, Froger N, Ezan P, Jiang JX, Bennett MV, et al. (2011) ATP and glutamate released via astroglial connexin 43 hemichannels mediate neuronal death through activation of pannexin 1 hemichannels. J Neurochem.
28. Liao CK, Wang SM, Chen YL, Wang HS, Wu JC, (2010) Lipopolysaccharide-induced inhibition of connexin43 gap junction communication in astrocytes is mediated by downregulation of caveolin-3. Int J Biochem Cell Biol 42: 762-770.
29. Martínez AD, Sáez JC, (2000) Regulation of astrocyte gap junctions by hypoxia-reoxygenation. Brain Res Brain Res Rev 32: 250-258.
30. Même W, Calvo CF, Froger N, Ezan P, Amigou E, et al. (2006) Proinflammatory cytokines released from microglia inhibit gap junctions in astrocytes: potentiation by beta-amyloid. Faseb J 20: 494-496.
31. Gandhi GK, Ball KK, Cruz NF, Dienel GA, (2010) Hyperglycaemia and diabetes impair gap junctional communication among astrocytes. ASN Neuro 2: e00030.
32. Karpuk N, Burkovetskaya M, Fritz T, Angle A, Kielian T, (2011) Neuroinflammation leads to region-dependent alterations in astrocyte gap junction communication and hemichannel activity. J Neurosci 31: 414-425.
33. Glass CK, Saijo K, Winner B, Marchetto MC, Gage FH, (2010) Mechanisms underlying inflammation in neurodegeneration. Cell 140: 918-934.
34. Dermietzel R, Traub O, Hwang TK, Beyer E, Bennett MV, et al. (1989) Differential expression of three gap junction proteins in developing and mature brain tissues. Proc Natl Acad Sci U S A 86: 10148-10152.
35. Giaume C, Fromaget C, el Aoumari A, Cordier J, Glowinski J, et al. (1991) Gap junctions in cultured astrocytes: single-channel currents and characterization of channel-forming protein. Neuron 6: 133-143.
36. Schalper KA, Palacios-Prado N, Orellana JA, Sáez JC, (2008) Currently used methods for identification and characterization of hemichannels. Cell Commun Adhes 15: 207-218.
37. Iglesias R, Dahl G, Qiu F, Spray DC, Scemes E, (2009) Pannexin 1: the molecular substrate of astrocyte "hemichannels". J Neurosci 29: 7092-7097.
38. Suadicani SO, Iglesias R, Wang J, Dahl G, Spray DC, et al. (2012) ATP signaling is deficient in cultured pannexin1-null mouse astrocytes. Glia 60: 1106-1116.
39. Retamal MA, Schalper KA, Shoji KF, Bennett MV, Sáez JC, (2007) Opening of connexin 43 hemichannels is increased by lowering intracellular redox potential. Proc Natl Acad Sci U S A 104: 8322-8327.
40. Fu R, Yanjanin NM, Bianconi S, Pavan WJ, Porter FD, (2010) Oxidative stress in Niemann-Pick disease, type C. Mol Genet Metab. 101: 214-218.
41. Vázquez MC, del Pozo T, Robledo FA, Carrasco G, Pavez L, et al. (2011) Alteration of gene expression profile in Niemann-Pick type C mice correlates with tissue damage and oxidative stress. PLoS One 6: e28777.
42. Yu W, Gong JS, Ko M, Garver WS, Yanagisawa K, et al. (2005) Altered cholesterol metabolism in Niemann-Pick type C1 mouse brains affects mitochondrial function. J Biol Chem 280: 11731-11739.
43. Zampieri S, Mellon SH, Butters TD, Nevyjel M, Covey DF, et al. (2009) Oxidative stress in NPC1 deficient cells: protective effect of allopregnanolone. J Cell Mol Med 13: 3786-3796.
44. Liscum L, Faust JR, (1989) The intracellular transport of low density lipoprotein-derived cholesterol is inhibited in Chinese hamster ovary cells cultured with 3-beta-[2-(diethylamino)ethoxy]androst-5-en-17-one. J Biol Chem 264: 11796-11806.
45. Marambaud P, Dreses-Werringloer U, Vingtdeux V, (2009) Calcium signaling in neurodegeneration. Mol Neurodegener 4: 20.
46. Nedergaard M, Rodriguez JJ, Verkhratsky A, (2010) Glial calcium and diseases of the nervous system. Cell Calcium 47: 140-149.
47. Kang J, Kang N, Lovatt D, Torres A, Zhao Z, et al. (2008) Connexin 43 hemichannels are permeable to ATP. J Neurosci 28: 4702-4711.
48. Baroja-Mazo A, Barbera-Cremades M, Pelegrin P (2012) The participation of plasma membrane hemichannels to purinergic signaling. Biochim Biophys Acta.
49. Cotrina ML, Lin JH, Alves-Rodrigues A, Liu S, Li J, et al. (1998) Connexins regulate calcium signaling by controlling ATP release. Proc Natl Acad Sci U S A 95: 15735-15740.
50. Orellana JA, Sáez PJ, Cortes-Campos C, Elizondo RJ, Shoji KF, et al. (2012) Glucose increases intracellular free Ca2+ in tanycytes via ATP released through connexin 43 hemichannels. Glia 60: 53-68.
51. Skaper SD, Debetto P, Giusti P, (2010) The P2X7 purinergic receptor: from physiology to neurological disorders. Faseb J 24: 337-345.
52. Di Castro MA, Chuquet J, Liaudet N, Bhaukaurally K, Santello M, et al. (2011) Local Ca2+ detection and modulation of synaptic release by astrocytes. Nat Neurosci 14: 1276-1284.
53. Koizumi S, (2010) Synchronization of Ca2+ oscillations: involvement of ATP release in astrocytes. FEBS J 277: 286-292.
54. Scemes E, (2008) Modulation of astrocyte P2Y1 receptors by the carboxyl terminal domain of the gap junction protein Cx43. Glia 56: 145-153.
55. Falk MM, Baker SM, Gumpert AM, Segretain D, Buckheit RW 3rd, (2009) Gap junction turnover is achieved by the internalization of small endocytic double-membrane vesicles. Mol Biol Cell 20: 3342-3352.
56. Gaietta G, Deerinck TJ, Adams SR, Bouwer J, Tour O, et al. (2002) Multicolor and electron microscopic imaging of connexin trafficking. Science 296: 503-507.
57. Elrick MJ, Pacheco CD, Yu T, Dadgar N, Shakkottai VG, et al. (2010) Conditional Niemann-Pick C mice demonstrate cell autonomous Purkinje cell neurodegeneration. Hum Mol Genet 19: 837-847.
58. Ko DC, Milenkovic L, Beier SM, Manuel H, Buchanan J, et al. (2005) Cell-autonomous death of cerebellar purkinje neurons with autophagy in Niemann-Pick type C disease. PLoS Genet 1: 81-95.
59. López ME, Klein AD, Dimbil UJ, Scott MP, (2011) Anatomically defined neuron-based rescue of neurodegenerative Niemann-Pick type C disorder. J Neurosci 31: 4367-4378.
60. Alvarez AR, Klein A, Castro J, Cancino GI, Amigo J, et al. (2008) Imatinib therapy blocks cerebellar apoptosis and improves neurological symptoms in a mouse model of Niemann-Pick type C disease. FASEB J 22: 3617-3627.
61. Ordoñez MP, Roberts EA, Kidwell CU, Yuan SH, Plaisted WC, et al. (2012) Disruption and therapeutic rescue of autophagy in a human neuronal model of Niemann Pick type C1. Hum Mol Genet 21: 2651-2662.
62. Pacheco CD, Kunkel R, Lieberman AP, (2007) Autophagy in Niemann-Pick C disease is dependent upon Beclin-1 and responsive to lipid trafficking defects. Hum Mol Genet 16: 1495-1503.
63. Rubinsztein DC, Codogno P, Levine B, (2012) Autophagy modulation as a potential therapeutic target for diverse diseases. Nat Rev Drug Discov 11: 709-730.
64. Elrick MJ, Yu T, Chung C, Lieberman AP, (2012) Impaired proteolysis underlies autophagic dysfunction in Niemann-Pick type C disease. Hum Mol Genet 21: 4876-4887.
65. Borbon I, Totenhagen J, Fiorenza MT, Canterini S, Ke W, et al. (2012) Niemann-Pick C1 mice, a model of "juvenile Alzheimer's disease". with normal gene expression in neurons and fibrillary astrocytes show long term survival and delayed neurodegeneration. J Alzheimers Dis 30: 875-887.
66. Zhan H, Moore CS, Chen B, Zhou X, Ma XM, et al. (2012) Stomatin inhibits pannexin-1-mediated whole-cell currents by interacting with its carboxyl terminal. PLoS One 7: e39489.
67. Borbon IA, Erickson RP, (2011) Interactions of Npc1 and amyloid accumulation/deposition in the APP/PS1 mouse model of Alzheimer's. J Appl Genet 52: 213-218.
68. Jelinek D, Heidenreich RA, Erickson RP, Garver WS, (2010) Decreased Npc1 gene dosage in mice is associated with weight gain. Obesity (Silver Spring) 18: 1457-1459.
69. Morales MG, Amigo L, Balboa E, Acuna M, Castro J, et al. (2010) Deficiency of Niemann-Pick C1 protein protects against diet-induced gallstone formation in mice. Liver Int 30: 887-897.
70. Garver WS, Erickson RP, Wilson JM, Colton TL, Hossain GS, et al. (1997) Altered expression of caveolin-1 and increased cholesterol in detergent insoluble membrane fractions from liver in mice with Niemann-Pick disease type C. Biochim Biophys Acta. 1361: 272-280.
71. Garver WS, Hsu SC, Erickson RP, Greer WL, Byers DM, et al. (1997) Increased expression of caveolin-1 in heterozygous Niemann-Pick type II human fibroblasts. Biochem Biophys Res Commun 236: 189-193.
72. Kodam A, Maulik M, Peake K, Amritraj A, Vetrivel KS, et al. (2010) Altered levels and distribution of amyloid precursor protein and its processing enzymes in Niemann-Pick type C1-deficient mouse brains. Glia 58: 1267-1281.
73. López ME, Klein AD, Hong J, Dimbil UJ, Scott MP, (2012) Neuronal and epithelial cell rescue resolves chronic systemic inflammation in the lipid storage disorder Niemann-Pick C. Hum Mol Genet. 21: 2946-2960.
74. López ME, Klein AD, Scott MP, (2012) Complement is dispensable for neurodegeneration in Niemann-Pick disease type C. J Neuroinflammation. 9: 216.
75. Smith D, Wallom KL, Williams IM, Jeyakumar M, Platt FM, (2009) Beneficial effects of anti-inflammatory therapy in a mouse model of Niemann-Pick disease type C1. Neurobiol Dis 36: 242-251.
76. Schalper KA, Sánchez HA, Lee SC, Altenberg GA, Nathanson MH, et al. (2010) Connexin 43 hemichannels mediate the Ca2+ influx induced by extracellular alkalinization. Am J Physiol Cell Physiol 299: C1504-1515.
77. Byun K, Kim JM, Kim N, Kang JA, Won MH, et al. (2011) Alteration of the CNS pathway to the hippocampus in a mouse model of Niemann-Pick, type C disease. J Chem Neuroanat 42: 39-44.
78. Peake KB, Vance JE, (2010) Defective cholesterol trafficking in Niemann-Pick C-deficient cells. FEBS Lett 584: 2731-2739.
79. Koh CH, Cheung NS, (2006) Cellular mechanism of U18666A-mediated apoptosis in cultured murine cortical neurons: bridging Niemann-Pick disease type C and Alzheimer's disease. Cell Signal 18: 1844-1853.
80. Lange Y, Steck TL, (1994) Cholesterol homeostasis. Modulation by amphiphiles. J Biol Chem 269: 29371-29374.
81. Peake KB, Vance JE, (2012) Normalization of cholesterol homeostasis by 2-hydroxypropyl-beta-cyclodextrin in neurons and glia from Niemann-Pick C1 (NPC1)-deficient mice. J Biol Chem 287: 9290-9298.
82. Iftakhar EKI, Koide N, Hassan F, Noman AS, Dagvadorj J, et al. (2009) Novel mechanism of U18666A-induced tumour necrosis factor-alpha production in RAW 264.7 macrophage cells. Clin Exp Immunol 155: 552-558.
83. Lloyd-Evans E, Morgan AJ, He X, Smith DA, Elliot-Smith E, et al. (2008) Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat Med 14: 1247-1255.
84. Shen D, Wang X, Li X, Zhang X, Yao Z, et al. (2012) Lipid storage disorders block lysosomal trafficking by inhibiting a TRP channel and lysosomal calcium release. Nat Commun 3: 731.
85. Zwijsen RM, Oudenhoven IM, de Haan LH, (1992) Effects of cholesterol and oxysterols on gap junctional communication between human smooth muscle cells. Eur J Pharmacol 228: 115-120.
86. Garver WS, Krishnan K, Gallagos JR, Michikawa M, Francis GA, et al. (2002) Niemann-Pick C1 protein regulates cholesterol transport to the trans-Golgi network and plasma membrane caveolae. J Lipid Res 43: 579-589.
87. Langlois S, Cowan KN, Shao Q, Cowan BJ, Laird DW, (2008) Caveolin-1 and-2 interact with connexin43 and regulate gap junctional intercellular communication in keratinocytes. Mol Biol Cell 19: 912-928.