Pannexin-1 expression in developing mouse nervous system: new evidence for expression in sensory ganglia

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• 作者：Abdulrahman Raslan ; Nadine Hainz ; Anja Beckmann…
• 关键词：Gap junction ; Panx1 ; Whole ; mount in situ hybridization ; Mouse
• 刊名：Cell and Tissue Research
• 出版年：2016
• 出版时间：April 2016
• 年：2016
• 卷：364
• 期：1
• 页码：29-41
• 全文大小：793 KB
• 参考文献：Ambrosi C, Gassmann O, Pranskevich JN, Boassa D, Smock A, Wang J, Dahl G, Steinem C, Sosinsky GE (2010) Pannexin1 and Pannexin2 channels show quaternary similarities to connexons and different oligomerization numbers from each other. J Biol Chem 285:24420–24431CrossRef PubMed PubMedCentral
  Anselmi F, Hernandez VH, Crispino G, Seydel A, Ortolano S, Roper SD, Kessaris N, Richardson W, Rickheit G, Filippov MA, Monyer H, Mammano F (2008) ATP release through connexin hemichannels and gap junction transfer of second messengers propagate Ca2+ signals across the inner ear. Proc Natl Acad Sci U S A 105:18770–18775CrossRef PubMed PubMedCentral
  Arber S (2012) Motor circuits in action: specification, connectivity, and function. Neuron 74:975–989CrossRef PubMed
  Avendano BC, Montero TD, Chavez CE, von Bernhardi R, Orellana JA (2015) Prenatal exposure to inflammatory conditions increases Cx43 and Panx1 unopposed channel opening and activation of astrocytes in the offspring effect on neuronal survival. Glia (in press)
  Baranova A, Ivanov D, Petrash N, Pestova A, Skoblov M, Kelmanson I, Shagin D, Nazarenko S, Geraymovych E, Litvin O, Tiunova A, Born TL, Usman N, Staroverov D, Lukyanov S, Panchin Y (2004) The mammalian pannexin family is homologous to the invertebrate innexin gap junction proteins. Genomics 83:706–716CrossRef PubMed
  Bargiotas P, Krenz A, Hormuzdi SG, Ridder DA, Herb A, Barakat W, Penuela S, Engelhardt J von, Monyer H, Schwaninger M (2011) Pannexins in ischemia-induced neurodegeneration. Proc Natl Acad Sci U S A 108:20772–20777
  Basson MA, Wingate RJ (2013) Congenital hypoplasia of the cerebellum: developmental causes and behavioural consequences. Front Neuroanat 7:29CrossRef PubMed PubMedCentral
  Bravo D, Ibarra P, Retamal J, Pelissier T, Laurido C, Hernandez A, Constandil L (2014) Pannexin 1: a novel participant in neuropathic pain signaling in the rat spinal cord. Pain 155:2108-2115CrossRef PubMed
  Bruzzone R, Hormuzdi SG, Barbe MT, Herb A, Monyer H (2003) Pannexins, a family of gap junction proteins expressed in brain. Proc Natl Acad Sci U S A 100:13644–13649CrossRef PubMed PubMedCentral
  Casanova JC, Uribe V, Badia-Careaga C, Giovinazzo G, Torres M, Sanz-Ezquerro JJ (2011) Apical ectodermal ridge morphogenesis in limb development is controlled by Arid3b-mediated regulation of cell movements. Development 138:1195–1205CrossRef PubMed
  Celetti SJ, Cowan KN, Penuela S, Shao Q, Churko J, Laird DW (2010) Implications of pannexin 1 and pannexin 3 for keratinocyte differentiation. J Cell Sci 123:1363–1372CrossRef PubMed
  Chang Q, Gonzalez M, Pinter MJ, Balice-Gordon RJ (1999) Gap junctional coupling and patterns of connexin expression among neonatal rat lumbar spinal motor neurons. J Neurosci 19:10813–10828PubMed
  Chen J, Zhu Y, Liang C, Chen J, Zhao HB (2015) Pannexin1 channels dominate ATP release in the cochlea ensuring endocochlear potential and auditory receptor potential generation and hearing. Sci Rep 5:10762CrossRef PubMed PubMedCentral
  Cisneros-Mejorado A, Gottlieb M, Cavaliere F, Magnus T, Koch-Nolte F, Scemes E, Perez-Samartin A, Matute C (2015) Blockade of P2X7 receptors or pannexin-1 channels similarly attenuates postischemic damage. J Cereb Blood Flow Metab 35:843–850CrossRef PubMed
  Cone AC, Ambrosi C, Scemes E, Martone ME, Sosinsky G (2013) A comparative antibody analysis of Pannexin1 expression in four rat brain regions reveals varying subcellular localizations. Front Pharmacol 4:6CrossRef PubMed PubMedCentral
  Cordes SP (2001) Molecular genetics of cranial nerve development in mouse. Nat Rev Neurosci 2:611–623CrossRef PubMed
  Dahl E, Willecke K, Balling R (1997) Segment-specific expression of the gap junction gene connexin31 during hindbrain development. Dev Gene Evol 207:359–361CrossRef
  De Bellard ME, Ching W, Gossler A, Bronner-Fraser M (2002) Disruption of segmental neural crest migration and ephrin expression in delta-1 null mice. Dev Biol 249:121–130CrossRef PubMed
  Hanstein R, Negoro H, Patel NK, Charollais A, Meda P, Spray DC, Suadicani SO, Scemes E (2013) Promises and pitfalls of a Pannexin1 transgenic mouse line. Front Pharmacol 4:61CrossRef PubMed PubMedCentral
  Hartfield EM, Rinaldi F, Glover CP, Wong LF, Caldwell MA, Uney JB (2011) Connexin 36 expression regulates neuronal differentiation from neural progenitor cells. PLoS One 6:e14746CrossRef PubMed PubMedCentral
  Hawkes R (2012) Pattern formation during development of the embryonic cerebellum. Front Neuroanat 6:10PubMed PubMedCentral
  Iacopetti P, Michelini M, Stuckmann I, Oback B, Aaku-Saraste E, Huttner WB (1999) Expression of the antiproliferative gene TIS21 at the onset of neurogenesis identifies single neuroepithelial cells that switch from proliferative to neuron-generating division. Proc Natl Acad Sci U S A 96:4639–4644CrossRef PubMed PubMedCentral
  Jungbluth S, Willecke K, Champagnat J (2002) Segment-specific expression of connexin31 in the embryonic hindbrain is regulated by Krox20. Dev Dyn 223:544–551CrossRef PubMed
  Karatas H, Erdener SE, Gursoy-Ozdemir Y, Lule S, Eren-Kocak E, Sen ZD, Dalkara T (2013) Spreading depression triggers headache by activating neuronal Panx1 channels. Science 339:1092–1095CrossRef PubMed
  Kaufman MH (2003) The atlas of mouse development. Academic Press, New York
  Langlois S, Xiang X, Young K, Cowan BJ, Penuela S, Cowan KN (2014)Pannexin 1 and pannexin 3 channels regulate skeletal muscle myoblast proliferation and differentiation.J Biol Chem 289:30717-30731CrossRef PubMed PubMedCentral
  Mannelli LD, Marcoli M, Micheli L, Zanardelli M, Maura G, Ghelardini C, Cervetto C (2015) Oxaliplatin evokes P2X7-dependent glutamate release in the cerebral cortex: a pain mechanism mediated by Pannexin 1. Neuropharmacology 97:133–141CrossRef
  Martinez S, Andreu A, Mecklenburg N, Echevarria D (2013) Cellular and molecular basis of cerebellar development. Front Neuroanat 7:18CrossRef PubMed PubMedCentral
  Namba K, Sugihara I, Hashimoto M (2011) Close correlation between the birth date of Purkinje cells and the longitudinal compartmentalization of the mouse adult cerebellum. J Comp Neurol 519:2594–2614CrossRef PubMed
  Penuela S, Kelly JJ, Churko JM, Barr KJ, Berger AC, Laird DW (2014) Panx1 regulates cellular properties of keratinocytes and dermal fibroblasts in skin development and wound healing. J Invest Dermatol 134:2026–2035CrossRef PubMed
  Phippard D, Lu L, Lee D, Saunders JC, Crenshaw EB 3rd (1999) Targeted mutagenesis of the POU-domain gene Brn4/Pou3f4 causes developmental defects in the inner ear. J Neurosci 19:5980–5989PubMed
  Prochnow N, Abdulazim A, Kurtenbach S, Wildforster V, Dvoriantchikova G, Hanske J, Petrasch-Parwez E, Shestopalov VI, Dermietzel R, Manahan-Vaughan D, Zoidl G (2012) Pannexin1 stabilizes synaptic plasticity and is needed for learning. PLoS One 7:e51767CrossRef PubMed PubMedCentral
  Rao MS, Jacobson M (2005) Developmental neurobiology. Springer, HeidelbergCrossRef
  Ray A, Zoidl G, Weickert S, Wahle P, Dermietzel R (2005) Site-specific and developmental expression of pannexin1 in the mouse nervous system. Eur J Neurosci 21:3277–3290CrossRef PubMed
  Ray A, Zoidl G, Wahle P, Dermietzel R (2006) Pannexin expression in the cerebellum. Cerebellum 5:189–192CrossRef PubMed
  Retamal MA, Alcayaga J, Verdugo CA, Bultynck G, Leybaert L, Sáez PJ, Fernández R, León LE, Sáez JC (2014) Opening of pannexin- and connexin-based channels increases the excitability of nodose ganglion sensory neurons. Front Cell Neurosci 8:158CrossRef PubMed PubMedCentral
  Rigato C, Swinnen N, Buckinx R, Couillin I, Mangin JM, Rigo JM, Legendre P, Le Corronc H (2012) Microglia proliferation is controlled by P2X7 receptors in a Pannexin-1-independent manner during early embryonic spinal cord invasion. J Neurosci 32:11559–11573CrossRef PubMed
  Sanchez HA, Verselis VK (2014) Aberrant Cx26 hemichannels and keratitis-ichthyosis-deafness syndrome: insights into syndromic hearing loss. Front Cell Neurosci 8:354CrossRef PubMed PubMedCentral
  Sanes DH, Reh TA, Harris WA (2011) Development of the nervous system. Elsevier Science, Amsterdam
  Santiago MF, Veliskova J, Patel NK, Lutz SE, Caille D, Charollais A, Meda P, Scemes E (2011) Targeting pannexin1 improves seizure outcome. PLoS One 6:e25178CrossRef PubMed PubMedCentral
  Sarkar FH, Visscher DW, Crissman JD (1993) Quantitative analysis of Her-2/neu (ERBB2) gene expression using reverse transcriptase polymerase chain reaction. Diagn Mol Pathol 2:210–218CrossRef PubMed
  Tang W, Ahmad S, Shestopalov VI, Lin X (2008) Pannexins are new molecular candidates for assembling gap junctions in the cochlea. Neuroreport 19:1253–1257CrossRef PubMed PubMedCentral
  Vitalis T, Ansorge MS, Dayer AG (2013) Serotonin homeostasis and serotonin receptors as actors of cortical construction: special attention to the 5-HT3A and 5-HT6 receptor subtypes. Front Cell Neurosci 7:93
  Vogt A, Hormuzdi SG, Monyer H (2005) Pannexin1 and Pannexin2 expression in the developing and mature rat brain. Mol Brain Res 141:113–120CrossRef PubMed
  Wang XH, Streeter M, Liu YP, Zhao HB (2009) Identification and characterization of pannexin expression in the mammalian cochlea. J Comp Neurol 512:336–346CrossRef PubMed PubMedCentral
  Wicki-Stordeur LE, Swayne LA (2013) Panx1 regulates neural stem and progenitor cell behaviours associated with cytoskeletal dynamics and interacts with multiple cytoskeletal elements. Cell Commun Signal 11:62CrossRef PubMed PubMedCentral
  Wicki-Stordeur LE, Dzugalo AD, Swansburg RM, Suits JM, Swayne LA (2012) Pannexin 1 regulates postnatal neural stem and progenitor cell proliferation. Neural Dev 7:11CrossRef PubMed PubMedCentral
  Wurst W, Bally-Cuif L (2001) Neural plate patterning: upstream and downstream of the isthmic organizer. Nat Rev Neurosci 2:99–108CrossRef PubMed
  Xu H, Yang Y, Tang X, Zhao M, Liang F, Xu P, Hou B, Xing Y, Bao X, Fan X (2013) Bergmann glia function in granule cell migration during cerebellum development. Mol Neurobiol 47:833–844CrossRef PubMed
  Zappala A, Cicero D, Serapide MF, Paz C, Catania MV, Falchi M, Parenti R, Panto MR, La Delia F, Cicirata F (2006) Expression of pannexin1 in the CNS of adult mouse: cellular localization and effect of 4-aminopyridine-induced seizures. Neuroscience 141:167–178CrossRef PubMed
  Zhang Y, Laumet G, Chen SR, Hittelman WN, Pan HL (2015) Pannexin-1 up-regulation in the dorsal root ganglion contributes to neuropathic pain development. J Biol Chem 290:14647–14655CrossRef PubMed
  Zhao HB, Zhu Y, Liang C, Chen J (2015) Pannexin 1 deficiency can induce hearing loss. Biochem Biophys Res Commun 463:143–147CrossRef PubMed
  
• 作者单位：Abdulrahman Raslan (1)
  Nadine Hainz (1)
  Anja Beckmann (1)
  Thomas Tschernig (1)
  Carola Meier (1)
  
  1. Department of Anatomy and Cell Biology, Saarland University, Building 61, 66424, Homburg, Saar, Germany
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Biomedicine
  Human Genetics
  Proteomics
  Molecular Medicine
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-0878

文摘

Pannexin1 (Panx1) is one of three members of the pannexin protein family. The expression of Panx1 mRNA has been extensively investigated from late embryonic to adult stages. In contrast, expression during early embryonic development is largely unknown. Our aim is to examine the temporal and spatial expression of Panx1 in mouse embryonic development by focusing on embryonic days (E) 9.5 to 12.5. Whole embryos are investigated in order to provide a comprehensive survey. Analyses were performed at the mRNA level by using reverse transcription plus the polymerase chain reaction and whole-mount in situ hybridization. Panx1 mRNA was detected in the heads and bodies of embryos at all developmental stages investigated (E9.5, E10.5, E11.5, E12.5). In particular, the nervous system expressed Panx1 at an early time point. Interestingly, Panx1 expression was found in afferent ganglia of the cranial nerves and spinal cord. This finding is of particular interest in the context of neuropathic pain and other Panx1-related neurological disorders. Our study shows, for the first time, that Panx1 is expressed in the central and peripheral nervous system during early developmental stages. The consequences of Panx1 deficiency or inhibition in a number of experimental paradigms might therefore be predicated on changes during early development.