Pannexin channels increase propidium iodide permeability in frozen–thawed dog spermatozoa
J. L. Torres B , J. Palomino A , R. D. Moreno B and M. De los Reyes A C
+ Author Affiliations
- Author Affiliations
A Laboratory of Animal Reproduction, Faculty of Veterinary Sciences, University of Chile, Casilla 2, Correo 14, La Granja, Santiago, Chile.
B Physiology Department, Biological Sciences Faculty, Pontifical Catholic University of Chile, Alameda 340, Santiago, Chile.
C Corresponding author. Email: mdlreyes@uchile.cl
Reproduction, Fertility and Development 29(11) 2269-2276 https://doi.org/10.1071/RD16267
Submitted: 5 July 2016 Accepted: 28 February 2017 Published: 10 April 2017
Abstract
Pannexins (Panx) are proteins that form functional single membrane channels, but they have not yet been described in dogs. The aim of the present study was to detect Panx1, Panx2 and Panx3 in frozen–thawed dog spermatozoa using flow cytometry and immunofluorescence analyses, evaluating the relationship of these proteins with propidium iodide (PI) in frozen–thawed spermatozoa. Fresh and frozen–thawed dog spermatozoa from eight dogs were preincubated with 3 μM PI with or without 15 μM carbenoxolone (CBX) or 1 mM probenecid (PBD), two Panx channel inhibitors, and then incubated with rabbit anti-Panx1, anti-Panx2 and anti-Panx3 antibodies (1 : 200). Panx immunolocalisation was assessed by fluorescence microscopy. Flow cytometry data were evaluated by analysis of variance. All three Panx proteins were found in dog spermatozoa: Panx1 was mostly localised to the acrosomal and equatorial segment, Panx2 was found in the posterior region of the head and tail and Panx3 was localised to the equatorial and posterior head segment. The percentage of PI-positive cells determined by flow cytometry was reduced (P < 0.05) in the presence of Panx inhibitors. These results show that Panx proteins are present in dog spermatozoa and increase PI permeability in frozen–thawed dog sperm, suggesting that the percentage of PI-positive spermatozoa used as an indicator of non-viable cells may lead to overestimation of non-viable cells.
Additional keywords: acrosome, cryopreservation, protein.
References
Ambrosi, C., Gassmann, O., Pranskevich, J. N., Boassa, D., Smock, A., Wang, J., Dahl, G., Steinem, C., and Sosinsky, G. E. (2010). Pannexin1 and Pannexin2 channels show quaternary similarities to connexons and different oligomerization numbers from each other. J. Biol. Chem. 285, 24420–24431.| Pannexin1 and Pannexin2 channels show quaternary similarities to connexons and different oligomerization numbers from each other.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpsFems7w%3D&md5=dbe24a5b80d5a5c59777bd04d073edcdCAS |
Bao, L., Locovei, S., and Dahl, G. (2004). Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett. 572, 65–68.
| Pannexin membrane channels are mechanosensitive conduits for ATP.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmsVGhsL4%3D&md5=41fe5a83529c29e1cd4066fe1f26f63dCAS |
Baranova, A., Ivanov, D., Petrash, N., Pestova, A., Skoblov, M., Kelmanson, I., Shagin, D., Nazarenko, S., Geraymovych, E., Litvin, O., Tiunova, A., Born, T., Usman, N., Staroverov, D., Lukyanov, S., and Panchin, Y. (2004). The mammalian pannexin family is homologous to the invertebrate innexin gap junction proteins. Genomics 83, 706–716.
| The mammalian pannexin family is homologous to the invertebrate innexin gap junction proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXitVGqs74%3D&md5=fbed309bc08d97a73dc2094c706a47caCAS |
Bargiotas, P., Krenz, A., Monyer, H., and Schwaninger, M. (2012). Functional outcome of pannexin-deficient mice after cerebral ischemia. Channels (Austin) 6, 453–456.
| Functional outcome of pannexin-deficient mice after cerebral ischemia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXivFeiur8%3D&md5=8d2466a8546d26273a8b8357b8d8efc8CAS |
Beckel, J. M., Argall, A. J., Lim, J. C., Xia, J., Lu, W., Coffey, E. E., Macarak, E. J., Shahidullah, M., Delamere, N. A., Zode, G. S., Sherffield, V. C., Shestopalov, V. I., Laties, A. M., and Mitchell, C. H. (2014). Mechanosensitive release of adenosine 5′-triphosphate through pannexin channels and mechanosensitive upregulation of pannexin channels in optic nerve head astrocytes: a mechanism for purinergic involvement in chronic strain. Glia 62, 1486–1501.
| Mechanosensitive release of adenosine 5′-triphosphate through pannexin channels and mechanosensitive upregulation of pannexin channels in optic nerve head astrocytes: a mechanism for purinergic involvement in chronic strain.Crossref | GoogleScholarGoogle Scholar |
Bond, S. R., and Naus, C. C. (2014). The pannexins: past and present. Front. Physiol. 5, 58.
| The pannexins: past and present.Crossref | GoogleScholarGoogle Scholar |
Boyce, A. K., Wicki-Stordeur, L. E., and Swayne, L. A. (2014). Powerful partnership: crosstalk between pannexin 1 and the cytoskeleton. Front. Physiol. 5, 27.
| Powerful partnership: crosstalk between pannexin 1 and the cytoskeleton.Crossref | GoogleScholarGoogle Scholar |
Bruzzone, R., Hormuzdi, S., Barbe, M., and Monyer, H. (2003). Pannexins, a family of gap junction proteins expressed in brain. Proc. Natl Acad. Sci. USA 100, 13644–13649.
| Pannexins, a family of gap junction proteins expressed in brain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptFOitb0%3D&md5=a6b0b032d2fb79af3072417135aa8fd1CAS |
Chekeni, F. B., Elliott, M. R., Sandilos, J. K., Walk, S. F., Kinchen, J. M., Lazarowski, E. R., Armstrong, A. J., Penuela, S., Laird, D. W., Salvesen, G. S., Isakson, B. E., Bayliss, D. A., and Ravichandran, K. S. (2010). Pannexin 1 channels mediate ‘find-me’ signal release and membrane permeability during apoptosis. Nature 467, 863–867.
| Pannexin 1 channels mediate ‘find-me’ signal release and membrane permeability during apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1yhsLbN&md5=a011132b2c82f58919e0353c3b5e7bdeCAS |
Corcini, C. D., Goularte, K. L., Bongalhardo, D. C., Lucia, T., Jardim, R. D., and Varela, A. S. (2016). Effect of egg yolk plasma on dog sperm cryopreservation. Andrologia 48, 114–115.
| Effect of egg yolk plasma on dog sperm cryopreservation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2Mngs1ektA%3D%3D&md5=69171a547436fb883a3c4ea4459f6f42CAS |
Cuasnicú, P. S., Da Ros, V. G., Weigel-Muñoz, M., and Cohen, D. J. (2016). Acrosome reaction as a preparation for gamete fusion. Adv. Anat. Embryol. Cell Biol. 220, 159–172.
| Acrosome reaction as a preparation for gamete fusion.Crossref | GoogleScholarGoogle Scholar |
De los Reyes, M., Carrion, R., and Barros, C. (2006). In vitro fertilization of in vitro matured canine oocytes using frozen–thawed dog semen. Theriogenology 66, 1682–1684.
| In vitro fertilization of in vitro matured canine oocytes using frozen–thawed dog semen.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28rlsFelug%3D%3D&md5=f25477af547bdfb251c9eca70afe75a5CAS |
De los Reyes, M., de Lange, J., Anguita, C., Palomino, J., and Barros, C. (2009). In vitro sperm penetration through the zona pellucida of immature and in vitro mature canine oocytes using fresh, chilled and frozen dog semen. Anim. Reprod. Sci. 110, 37–45.
| In vitro sperm penetration through the zona pellucida of immature and in vitro mature canine oocytes using fresh, chilled and frozen dog semen.Crossref | GoogleScholarGoogle Scholar |
Dorado, J., Gálvez, M. J., Morrell, J. M., Alcaráz, L., and Hidalgo, M. (2013). Use of single-layer centrifugation with Androcoll-C to enhance sperm quality in frozen–thawed dog semen. Theriogenology 80, 955–962.
| Use of single-layer centrifugation with Androcoll-C to enhance sperm quality in frozen–thawed dog semen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlektrbL&md5=38eea916b566842c4234002739648bfaCAS |
Dourado, M., Wong, E., and Hackos, D. H. (2014). Pannexin-1 is blocked by its C-terminus through a delocalized non-specific interaction surface. PLoS One 9, e99596.
| Pannexin-1 is blocked by its C-terminus through a delocalized non-specific interaction surface.Crossref | GoogleScholarGoogle Scholar |
Felipe-Pérez, Y. E., Valencia, J., Juárez-Mosqueda, Mde. L., Pescador, N., Roa-Espitia, A. L., and Hernández-González, E. O. (2012). Cytoskeletal proteins F-actin and β-dystrobrevin are altered by the cryopreservation process in bull sperm. Cryobiology 64, 103–109.
| Cytoskeletal proteins F-actin and β-dystrobrevin are altered by the cryopreservation process in bull sperm.Crossref | GoogleScholarGoogle Scholar |
Graham, J. K., Kunze, E., and Hammerstedt, R. H. (1990). Analysis of sperm cell viability, acrosomal integrity, and mitochondrial function using flow cytometry. Biol. Reprod. 43, 55–64.
| Analysis of sperm cell viability, acrosomal integrity, and mitochondrial function using flow cytometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXkslGltLs%3D&md5=9c7b12567927f4b8fa4dae150007468aCAS |
Gutiérrez-Pérez, O., Juárez-Mosqueda, M. L., Mota, D., and Trujillo, M. E. (2011). The disruption in actin–perinuclear theca interactions are related with changes induced by cryopreservation observed on sperm chromatin nuclear decondensation of boar semen. Cryobiology 62, 32–39.
| The disruption in actin–perinuclear theca interactions are related with changes induced by cryopreservation observed on sperm chromatin nuclear decondensation of boar semen.Crossref | GoogleScholarGoogle Scholar |
Ishijima, S. (2015). Ca2+ and cAMP regulations of microtubule sliding in hyperactivated motility of bull spermatozoa. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 91, 99–108.
| Ca2+ and cAMP regulations of microtubule sliding in hyperactivated motility of bull spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXnt1Shs7c%3D&md5=96a5290f5f421005c25a75fd23d05e0fCAS |
Jewgenow, K., and Songsasen, N. (2014). Reproduction and advances in reproductive studies in carnivores. Adv. Exp. Med. Biol. 753, 205–239.
| Reproduction and advances in reproductive studies in carnivores.Crossref | GoogleScholarGoogle Scholar |
Jiang, H., Zhu, A. G., Mamczur, M., Falck, J. R., Lerea, K. M., and McGiff, J. C. (2007). Stimulation of rat erythrocyte P2X7 receptor induces the release of epoxyeicosatrienoic acids. Br. J. Pharmacol. 151, 1033–1040.
| Stimulation of rat erythrocyte P2X7 receptor induces the release of epoxyeicosatrienoic acids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXot1ylsLw%3D&md5=2c01cefdc79431e099b30b20c365f14dCAS |
Kawakami, E., Vandevoort, C. A., Mahi-Brown, C. A., and Overstreet, J. W. (1993). Induction of acrosome reactions of canine sperm by homologous zona pellucida. Biol. Reprod. 48, 841–845.
| Induction of acrosome reactions of canine sperm by homologous zona pellucida.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s3ltVWltw%3D%3D&md5=2760961d3ed2e5c78b790b4fffb419a1CAS |
Kim, S. H., Yu, D. H., and Kim, Y. J. (2010). Effects of cryopreservation on phosphatidylserine translocation, intracellular hydrogen peroxide, and DNA integrity in canine sperm. Theriogenology 73, 282–292.
| Effects of cryopreservation on phosphatidylserine translocation, intracellular hydrogen peroxide, and DNA integrity in canine sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1Wgt7fO&md5=33f65403b085bb62dda5d8a26edcac6dCAS |
Kim, H. H., Funaro, M., Mazel, S., Goldstein, M., Schlegel, P. N., and Paduch, D. A. (2013). Flow cytometric characterization of apoptosis and chromatin damage in spermatozoa. Reprod. Biomed. Online 26, 393–395.
| Flow cytometric characterization of apoptosis and chromatin damage in spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXisVOmtrc%3D&md5=23fd0814f3398480a7cb29d5431c1e62CAS |
Kranz, K., Dorgau, B., Pottek, M., Herrling, R., Schultz, K., Bolte, P., Monyer, H., Penuela, S., Laird, D. W., Dedek, K., Weiler, R., and Janssen-Bienhold, U. (2013). Expression of Pannexin1 in the outer plexiform layer of the mouse retina and physiological impact of its knockout. J. Comp. Neurol. 521, 1119–1135.
| Expression of Pannexin1 in the outer plexiform layer of the mouse retina and physiological impact of its knockout.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFCisrk%3D&md5=1a1b632a23688f913680c8bc1c16f2e6CAS |
Krick, S., Wang, J., St-Pierre, M., Gonzalez, C., Dahl, G., and Salathe, M. (2016). Dual oxidase 2 (Duox2) regulates pannexin 1-mediated ATP release in primary human airway epithelial cells via changes in intracellular pH and not H2O2 production. J. Biol. Chem. 291, 6423–6432.
| Dual oxidase 2 (Duox2) regulates pannexin 1-mediated ATP release in primary human airway epithelial cells via changes in intracellular pH and not H2O2 production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XksVShsL4%3D&md5=af39e8594de31520605da79cb69cf61eCAS |
Li, Y., Du, X. F., Liu, C. S., Wen, Z. L., and Du, J. L. (2012). Reciprocal regulation between resting microglial dynamics and neuronal activity in vivo. Dev. Cell 23, 1189–1202.
| Reciprocal regulation between resting microglial dynamics and neuronal activity in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslKqsb7F&md5=8c3e19dad5a71d197cdf813c2a3d281cCAS |
Lizama, C., Lagos, C. F., Lagos-Cabré, R., Cantuarias, L., Rivera, F., Huenchuñir, P., Pérez-Acle, T., Carrión, F., and Moreno, R. D. (2009). Calpain inhibitors prevent p38 MAPK activation and germ cell apoptosis after heat stress in pubertal rat testes. J. Cell. Physiol. 221, 296–305.
| Calpain inhibitors prevent p38 MAPK activation and germ cell apoptosis after heat stress in pubertal rat testes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVGrsrrK&md5=30373b6b7db767df5995780d196759f3CAS |
Martins, M. I. M., Padilha, L. C., Souza, F. F., and Lopes, M. D. (2009). Fertilizing capacity of frozen epididymal sperm collected from dogs. Reprod. Domest. Anim. 44, 342–344.
| Fertilizing capacity of frozen epididymal sperm collected from dogs.Crossref | GoogleScholarGoogle Scholar |
Mogas, M. T., Alamo, M. R., and Rodríguez-Gil, J. E. (2011). Roles of Na+/K+-dependent ATPase, Na+/H+ antiporter and GLUT hexose transporters in the cryosurvival of dog spermatozoa: effects on viability, acrosome state and motile sperm subpopulation structure. Theriogenology 75, 1669–1681.
| Roles of Na+/K+-dependent ATPase, Na+/H+ antiporter and GLUT hexose transporters in the cryosurvival of dog spermatozoa: effects on viability, acrosome state and motile sperm subpopulation structure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXotFWgt7Y%3D&md5=627ff6fb4536886a97601ed3cce4ae12CAS |
Orellana, J. A., Díaz, E., Schalper, K. A., Vargas, A. A., Bennett, M. V., and Sáez, J. C. (2011). Cation permeation through connexin 43 hemichannels is cooperative, competitive and saturable with parameters depending on the permeant species. Biochem. Biophys. Res. Commun. 409, 603–609.
| Cation permeation through connexin 43 hemichannels is cooperative, competitive and saturable with parameters depending on the permeant species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnslyru70%3D&md5=d59fcd9a9538384a24b371acf149eadeCAS |
Ortiz, R. J., Lizama, C., Codelia, V. A., and Moreno, R. D. (2009). A molecular evaluation of germ cell death induced by etoposide in pubertal rat testes. Mol. Hum. Reprod. 15, 363–371.
| A molecular evaluation of germ cell death induced by etoposide in pubertal rat testes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvVWktb0%3D&md5=e7383d1443c67f701c13230de1711630CAS |
Palomino, J., and De los Reyes, M. (2009). A scanning electron microscope study of frozen/thawed dog sperm during in vitro gamete interaction. Reprod. Domest. Anim. 44, 278–283.
| A scanning electron microscope study of frozen/thawed dog sperm during in vitro gamete interaction.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38zitVKqsQ%3D%3D&md5=3daa7bba54d26a952d53e7a2e1a6fb76CAS |
Panchina, Y., Kelmanson, I., Matz, M., Lukyanov, K., Usman, N., and Lukyanov, S. (2000). A ubiquitous family of putative gap junction molecules. Curr. Biol. 10, R473–R474.
| A ubiquitous family of putative gap junction molecules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkslSitLg%3D&md5=49ffcb6dfc1d87265b8c29f783caa9f4CAS |
Parrish, J. J., Susko-Parrish, J., Winer, M. A., and First, N. L. (1988). Capacitation of bovine sperm by heparin. Biol. Reprod. 38, 1171–1180.
| Capacitation of bovine sperm by heparin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXkslWit7g%3D&md5=0ac0f575acccca1e7b1e8a11e9e41f46CAS |
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.
| Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFChsrzM&md5=828e496f10cece85e8d9d6045caa21a0CAS |
Peña, A. I., Barrio, M., Becerra, J. J., Quintela, P. G., and Herradón, P. G. (2004). Zona pellucida binding ability and responsiveness to ionophore challenge of cryopreserved dog spermatozoa after different periods of capacitation in vitro. Anim. Reprod. Sci. 84, 193–210.
| Zona pellucida binding ability and responsiveness to ionophore challenge of cryopreserved dog spermatozoa after different periods of capacitation in vitro.Crossref | GoogleScholarGoogle Scholar |
Prochowska, S., Niżański, W., Ochota, M., and Partyka, A. (2014). Effect of dilution rate on feline urethral sperm motility, viability, and DNA integrity. Theriogenology 82, 1273–1280.
| Effect of dilution rate on feline urethral sperm motility, viability, and DNA integrity.Crossref | GoogleScholarGoogle Scholar |
Ray, A., Zoidl, G., Wahle, P., and Dermietzel, R. (2006). Pannexin expression in the cerebellum. Cerebellum 5, 189–192.
| Pannexin expression in the cerebellum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFOrt77F&md5=a60db940d37f0548e041d93ce6d552aaCAS |
Sánchez-Cárdenas, C., Servín-Vences, M. R., José, O., Treviño, C. L., Hernández-Cruz, A., and Darszon, A. (2014). Acrosome reaction and Ca2+ imaging in single human spermatozoa: new regulatory roles of [Ca2+]i. Biol. Reprod. 91, 67.
| Acrosome reaction and Ca2+ imaging in single human spermatozoa: new regulatory roles of [Ca2+]i.Crossref | GoogleScholarGoogle Scholar |
Santi, C. M., Orta, G., Salkoff, L., Visconti, P. E., Darszon, A., and Treviño, C. L. (2013). K+ and Cl− channels and transporters in sperm function. Curr. Top. Dev. Biol. 102, 385–421.
| K+ and Cl− channels and transporters in sperm function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtV2lsrjF&md5=43eb0bde735d747a09a5ecf90f3a8a14CAS |
Seminario-Vidal, L., Okada, S. F., Sesma, J. I., Kreda, S. M., van Heusden, C. A., Zhu, Y., Jones, L. C., O’Neal, W. K., Penuela, S., Laird, D. W., Boucher, R. C., and Lazarowski, E. R. (2011). Rho signaling regulates pannexin 1-mediated ATP release from airway epithelia. J. Biol. Chem. 286, 26277–26286.
| Rho signaling regulates pannexin 1-mediated ATP release from airway epithelia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpt1Kkt70%3D&md5=f13103cc6892b3a59d639492cc8a01f1CAS |
Stival, C., Puga Molina, Ldel. C., Paudel, B., Buffone, M. G., Visconti, P. E., and Krapf, D. (2016). Sperm capacitation and acrosome reaction in mammalian sperm. Adv. Anat. Embryol. Cell Biol. 220, 93–106.
| Sperm capacitation and acrosome reaction in mammalian sperm.Crossref | GoogleScholarGoogle Scholar |
Thompson, R. J., Zhou, N., and MacVicar, B. A. (2006). Ischemia opens neuronal gap junction hemichannels. Science 312, 924–927.
| Ischemia opens neuronal gap junction hemichannels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xktlyhs7k%3D&md5=3e6c9ed6a8907542e65fe8ab461ccce5CAS |
Turmel, P., Dufresne, J., Hermo, L., Smith, C., Penuela, S., Laird, D., and Cyr, D. (2011). Characterization of pannexin1 and pannexin3 and their regulation by androgens in the male reproductive tract of the adult rat. Mol. Reprod. Dev. 78, 124–138.
| Characterization of pannexin1 and pannexin3 and their regulation by androgens in the male reproductive tract of the adult rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXitVyltbw%3D&md5=06027dd47071fd8347ba16136c3858b1CAS |
Vogt, A., Hormuzdi, S., and Monyer, H. (2005). Pannexin1 and Pannexin2 expression in the developing and mature rat brain. Brain Res. Mol. Brain Res. 141, 113–120.
| Pannexin1 and Pannexin2 expression in the developing and mature rat brain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFylurjP&md5=f2c674f5e6353978722116ab4b962e1fCAS |
Voigt, J., Grosche, A., Vogler, S., Pannicke, Y., Hollborn, M., Kohen, L., Wiedemann, P., Reinchenbach, A., and Bringmann, A. (2015). Nonvesicular release of ATP from rat retinal glial (Müller) cells is differentially mediated in response to osmotic stress and glutamate. Neurochem. Res. 40, 651–660.
| Nonvesicular release of ATP from rat retinal glial (Müller) cells is differentially mediated in response to osmotic stress and glutamate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXmsl2kug%3D%3D&md5=976404caa9a468e31834de8413c3c607CAS |
Xiao, F., Waldrop, S. L., Khimji, A. K., and Kilic, G. (2012). Pannexin1 contributes to pathophysiological ATP release in lipoapoptosis induced by saturated free fatty acids in liver cells. Am. J. Physiol. Cell Physiol. 303, C1034–C1044.
| Pannexin1 contributes to pathophysiological ATP release in lipoapoptosis induced by saturated free fatty acids in liver cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVKmtLjJ&md5=6314c22feddccc654505b01096189fedCAS |
Xiong, X. X., Gu, L. J., Shen, J., Kang, X. H., Zheng, Y. Y., Yue, S. B., and Zhu, S. M. (2014). Probenecid protects against transient focal cerebral ischemic injury by inhibiting HMGB1 release and attenuating AQP4 expression in mice. Neurochem. Res. 39, 216–224.
| Probenecid protects against transient focal cerebral ischemic injury by inhibiting HMGB1 release and attenuating AQP4 expression in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVyqt7jF&md5=9ebadcaba0089f766b88fa36eab2a62bCAS |
Yeh, C. J., Hsi, B. L., and Faulk, W. P. (1981). Propidium iodide as a nuclear marker in immunofluorescence. II. Use with cellular identification and viability studies. J. Immunol. Methods 43, 269–275.
| Propidium iodide as a nuclear marker in immunofluorescence. II. Use with cellular identification and viability studies.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M3ktVyltw%3D%3D&md5=3ed0402c221e45084c92bed0e68adf1dCAS |
Yen, M. R., and Saier, M. H. (2007). Gap junctional proteins of animals: the innexin/pannexin superfamily. Prog. Biophys. Mol. Biol. 94, 5–14.
| Gap junctional proteins of animals: the innexin/pannexin superfamily.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlvVOmu7c%3D&md5=c348bbfd2fa38111168e20ea604311feCAS |
