Connexins: a myriad of functions extending beyond assembly of gap junction channels

Dbouk, Hashem A.; Mroue, Rana M.; El-Sabban, Marwan E.; Talhouk, Rabih S.

doi:10.1186/1478-811x-7-4

Title: Connexins: a myriad of functions extending beyond assembly of gap junction channels

Journal Article · 01 January 2009 · Cell Communication and Signaling

DOI: https://doi.org/10.1186/1478-811x-7-4 · OSTI ID:1626579

Dbouk, Hashem A. ^[1]; Mroue, Rana M. ^[2]; El-Sabban, Marwan E. ^[3]; Talhouk, Rabih S. ^[4]

American Univ. of Beirut (Lebanon). Faculty of Arts and Sciences, Dept. of Biology; Albert Einstein College of Medicine, Bronx, NY (United States). Dept. of Molecular Pharmacology; DOE/OSTI
American Univ. of Beirut (Lebanon). Faculty of Arts and Sciences, Dept. of Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Division of Life Sciences
American Univ. of Beirut (Lebanon). Faculty of Medicine, Dept. of Human Morphology
American Univ. of Beirut (Lebanon). Faculty of Arts and Sciences, Dept. of Biology

Connexins constitute a large family of trans-membrane proteins that allow intercellular communication and the transfer of ions and small signaling molecules between cells. Recent studies have revealed complex translational and post-translational mechanisms that regulate connexin synthesis, maturation, membrane transport and degradation that in turn modulate gap junction intercellular communication. With the growing myriad of connexin interacting proteins, including cytoskeletal elements, junctional proteins, and enzymes, gap junctions are now perceived, not only as channels between neighboring cells, but as signaling complexes that regulate cell function and transformation. Connexins have also been shown to form functional hemichannels and have roles altogether independent of channel functions, where they exert their effects on proliferation and other aspects of life and death of the cell through mostly-undefined mechanisms. This review provides an updated overview of current knowledge of connexins and their interacting proteins, and it describes connexin modulation in disease and tumorigenesis.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: Lebanese National Council for Scientific Research; USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1626579

Journal Information:: Cell Communication and Signaling, Journal Name: Cell Communication and Signaling Journal Issue: 1 Vol. 7; ISSN 1478-811X

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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A Self-restricted CD38-connexin 43 Cross-talk Affects NAD+ and Cyclic ADP-ribose Metabolism and Regulates Intracellular Calcium in 3T3 Fibroblasts Bruzzone, Santina; Franco, Luisa; Guida, Lucrezia Journal of Biological Chemistry, Vol. 276, Issue 51 https://doi.org/10.1074/jbc.M107308200	journal	December 2001
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Retroviral Delivery of Connexin Genes to Human Breast Tumor Cells Inhibits in Vivo Tumor Growth by a Mechanism That Is Independent of Significant Gap Junctional Intercellular Communication Qin, Hong; Shao, Qing; Curtis, Heather Journal of Biological Chemistry, Vol. 277, Issue 32 https://doi.org/10.1074/jbc.M200797200	journal	August 2002
Impaired Trafficking of Connexins in Androgen-independent Human Prostate Cancer Cell Lines and Its Mitigation by α-Catenin Govindarajan, Rajgopal; Zhao, Sumin; Song, Xiao-Hong Journal of Biological Chemistry, Vol. 277, Issue 51 https://doi.org/10.1074/jbc.M202652200	journal	December 2002
Gap Junctional Communication Modulates Gene Transcription by Altering the Recruitment of Sp1 and Sp3 to Connexin-response Elements in Osteoblast Promoters Stains, Joseph P.; Lecanda, Fernando; Screen, Joanne Journal of Biological Chemistry, Vol. 278, Issue 27 https://doi.org/10.1074/jbc.M212554200	journal	July 2003
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Evolutionary selection pressure and family relationships among connexin genes Cruciani, Véronique; Mikalsen, Svein-Ole Biological Chemistry, Vol. 388, Issue 3 https://doi.org/10.1515/BC.2007.028	journal	March 2007
Functional Coupling between Neurons and Glia Alvarez-Maubecin, Veronica; García-Hernández, Fernando; Williams, John T. The Journal of Neuroscience, Vol. 20, Issue 11 https://doi.org/10.1523/JNEUROSCI.20-11-04091.2000	journal	June 2000
Calmodulin Kinase Pathway Mediates the K ⁺ -Induced Increase in Gap Junctional Communication between Mouse Spinal Cord Astrocytes De Pina-Benabou, Mara H.; Srinivas, Miduturu; Spray, David C. The Journal of Neuroscience, Vol. 21, Issue 17 https://doi.org/10.1523/JNEUROSCI.21-17-06635.2001	journal	September 2001
Role of gap junctions during early embryo development Houghton, Franchesca D. Reproduction, Vol. 129, Issue 2 https://doi.org/10.1530/rep.1.00277	journal	February 2005
Identification of a protein kinase activity that phosphorylates connexin43 in a pH-dependent manner Yahuaca, P.; Ek-Vitorin, J. F.; Rush, P. Brazilian Journal of Medical and Biological Research, Vol. 33, Issue 4 https://doi.org/10.1590/S0100-879X2000000400005	journal	April 2000
Gap Junctions and Connexon Hemichannels in Human Embryonic Stem Cells Huettner, James E.; Lu, Aiwu; Qu, Yun Stem Cells, Vol. 24, Issue 7 https://doi.org/10.1634/stemcells.2005-0003	journal	July 2006
The function of connexin 43 on the differentiation of rat bone marrow cells in culture Kamijo, Minoru; Haraguchi, Takayuki; Tonogi, Morio Biomedical Research, Vol. 27, Issue 6 https://doi.org/10.2220/biomedres.27.289	journal	January 2006
Connexin Genes in the Mouse and Human Genome Eiberger, JÜRgen; Degen, Joachim; Romualdi, Alessandro Cell Communication & Adhesion, Vol. 8, Issue 4-6 https://doi.org/10.3109/15419060109080717	journal	January 2001
Connexin45 Interacts with Zonula Occludens-1 in Osteoblastic Cells Laing, James G.; Manley-Markowski, RenÉE N.; Koval, Michael Cell Communication & Adhesion, Vol. 8, Issue 4-6 https://doi.org/10.3109/15419060109080725	journal	January 2001
Connexin-43 Interactions with ZO-1 and α- and β-tubulin Giepmans, Ben N. G.; Verlaan, Ingrid; Moolenaar, Wouter H. Cell Communication & Adhesion, Vol. 8, Issue 4-6 https://doi.org/10.3109/15419060109080727	journal	January 2001
v-Src-Mediated Phosphorylation of Connexin43 on Tyrosine Disrupts Gap Junctional Communication in Mammalian Cells Lin, Rui; Warn-Cramer, Bonnie J.; Kurata, Wendy E. Cell Communication & Adhesion, Vol. 8, Issue 4-6 https://doi.org/10.3109/15419060109080735	journal	January 2001
N-Cadherin and Cx43α1 Gap Junctions Modulates Mouse Neural Crest Cell Motility via Distinct Pathways Xu, X.; Li, W. E. I.; Huang, G. Y. Cell Communication & Adhesion, Vol. 8, Issue 4-6 https://doi.org/10.3109/15419060109080746	journal	January 2001
Proliferation and Polarity in Breast Cancer: Untying the Gordian Knot Liu, Hong; Radisky, Derek C.; Bissell, Mina J. Cell Cycle, Vol. 4, Issue 5 https://doi.org/10.4161/cc.4.5.1674	journal	March 2005

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Connexin 43 Hemichannel as a Novel Mediator of Sterile and Infectious Inflammatory Diseases Li, Wei; Bao, Guoqiang; Chen, Weiqiang Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-017-18452-1	journal	January 2018
Cross-talk between intestinal epithelial cells and immune cells in inflammatory bowel disease Al-Ghadban, Sara; Kaissi, Samira; Homaidan, Fadia R. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep29783	journal	July 2016
The Loss of Cellular Junctions in Epithelial Lung Cells Induced by Cigarette Smoke Is Attenuated by Corilagin Muresan, Ximena M.; Cervellati, Franco; Sticozzi, Claudia Oxidative Medicine and Cellular Longevity, Vol. 2015 https://doi.org/10.1155/2015/631758	journal	January 2015
Connexin’s Connection in Breast Cancer Growth and Progression Banerjee, Debarshi International Journal of Cell Biology, Vol. 2016 https://doi.org/10.1155/2016/9025905	journal	January 2016
A low-protein diet during pregnancy prevents modifications in intercellular communication proteins in rat islets Marçal-Pessoa, Ana Flávia; Bassi-Branco, Carmen Lucia; Salvatierra, Cristiana dos Santos Barbosa Biological Research, Vol. 48, Issue 1 https://doi.org/10.1186/0717-6287-48-3	journal	January 2015
Transcellular communication at the immunological synapse: a vesicular traffic-mediated mutual exchange Finetti, Francesca; Cassioli, Chiara; Baldari, Cosima T. F1000Research, Vol. 6 https://doi.org/10.12688/f1000research.11944.1	journal	October 2017
Function of Connexin-43 in Macrophages Rodjakovic, Daniel; Salm, Lilian; Beldi, Guido International Journal of Molecular Sciences https://doi.org/10.20944/preprints202012.0272.v1	journal	December 2020
PASE: a novel method for functional prediction of amino acid substitutions based on physicochemical properties Li, Xidan; Kierczak, Marcin; Shen, Xia Frontiers in Genetics, Vol. 4 https://doi.org/10.3389/fgene.2013.00021	journal	January 2013
Cancer Connectors: Connexins, Gap Junctions, and Communication Sinyuk, Maksim; Mulkearns-Hubert, Erin E.; Reizes, Ofer Frontiers in Oncology, Vol. 8 https://doi.org/10.3389/fonc.2018.00646	journal	December 2018
Protein–Protein Interactions with Connexin 43: Regulation and Function Sorgen, Paul; Trease, Andrew; Spagnol, Gaelle International Journal of Molecular Sciences, Vol. 19, Issue 5 https://doi.org/10.3390/ijms19051428	journal	May 2018
Vascularization in the Bone Repair Zhou, Jian; Dong, Jian Osteogenesis https://doi.org/10.5772/36325	book	February 2012
Connexin 43 in astrocytes contributes to motor neuron toxicity in amyotrophic lateral sclerosis: Connexin 43 Plays a Role in Loss of Motor Neurons in ALS Almad, Akshata A.; Doreswamy, Arpitha; Gross, Sarah K. Glia, Vol. 64, Issue 7 https://doi.org/10.1002/glia.22989	journal	April 2016
Shifting Paradigms on the Role of Connexin43 in the Skeletal Response to Mechanical Load: CONNEXIN43 AND MECHANICAL SIGNALS Lloyd, Shane A.; Loiselle, Alayna E.; Zhang, Yue Journal of Bone and Mineral Research, Vol. 29, Issue 2 https://doi.org/10.1002/jbmr.2165	journal	January 2014
BMP Signaling Mediated by BMPR1A in Osteoclasts Negatively Regulates Osteoblast Mineralization Through Suppression of Cx43: BMP S IGNALING IN OC R EGULATES OC-OB C ROSSTALK Shi, Ce; Zhang, Honghao; Louie, Ke'ale Journal of Cellular Biochemistry, Vol. 118, Issue 3 https://doi.org/10.1002/jcb.25746	journal	September 2016
Molecular dissection of cone photoreceptor-enriched genes encoding transmembrane and secretory proteins: XXXX Papal, Samantha; Monti, Christopher E.; Tennison, Mackenzie E. Journal of Neuroscience Research, Vol. 97, Issue 1 https://doi.org/10.1002/jnr.24329	journal	September 2018
The pleiotropic effects of Innexin genes expressed in Drosophila glia encompass wing chemosensory sensilla Raad, Hussein; Robichon, Alain Journal of Neuroscience Research, Vol. 97, Issue 10 https://doi.org/10.1002/jnr.24485	journal	June 2019
Roles of connexins and pannexins in digestive homeostasis Maes, Michaël; Cogliati, Bruno; Crespo Yanguas, Sara Cellular and Molecular Life Sciences, Vol. 72, Issue 15 https://doi.org/10.1007/s00018-015-1961-8	journal	June 2015
Gap Junctions and Wnt Signaling in the Mammary Gland: a Cross-Talk? Fostok, Sabreen F.; El-Sibai, Mirvat; El-Sabban, Marwan Journal of Mammary Gland Biology and Neoplasia, Vol. 24, Issue 1 https://doi.org/10.1007/s10911-018-9411-5	journal	September 2018
Gap junction and hemichannel-independent actions of connexins on cell and tissue functions - An update Zhou, Jade Z.; Jiang, Jean X. FEBS Letters, Vol. 588, Issue 8 https://doi.org/10.1016/j.febslet.2014.01.001	journal	January 2014
Connexins modulate autophagosome biogenesis Bejarano, Eloy; Yuste, Andrea; Patel, Bindi Nature Cell Biology, Vol. 16, Issue 5 https://doi.org/10.1038/ncb2934	journal	April 2014
Evidence of decreased gap junction coupling between astrocytes and oligodendrocytes in the anterior cingulate cortex of depressed suicides Tanti, Arnaud; Lutz, Pierre-Eric; Kim, John Neuropsychopharmacology, Vol. 44, Issue 12 https://doi.org/10.1038/s41386-019-0471-z	journal	August 2019
Connexin 43 Hemichannel as a Novel Mediator of Sterile and Infectious Inflammatory Diseases Li, Wei; Bao, Guoqiang; Chen, Weiqiang Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-017-18452-1	journal	January 2018
Cross-talk between intestinal epithelial cells and immune cells in inflammatory bowel disease Al-Ghadban, Sara; Kaissi, Samira; Homaidan, Fadia R. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep29783	journal	July 2016
Ischaemia-induced autophagy leads to degradation of gap junction protein connexin43 in cardiomyocytes Martins-Marques, Tania; Catarino, Steve; Zuzarte, Monica Biochemical Journal, Vol. 467, Issue 2 https://doi.org/10.1042/bj20141370	journal	April 2015
Connexin 43 is critical to maintain the homeostasis of the blood-testis barrier via its effects on tight junction reassembly Li, M. W. M.; Mruk, D. D.; Lee, W. M. Proceedings of the National Academy of Sciences, Vol. 107, Issue 42 https://doi.org/10.1073/pnas.1007047107	journal	October 2010
MicroRNA 320a Functions as a Novel Endogenous Modulator of Aquaporins 1 and 4 as Well as a Potential Therapeutic Target in Cerebral Ischemia* Sepramaniam, Sugunavathi; Armugam, Arunmozhiarasi; Lim, Kai Ying Journal of Biological Chemistry, Vol. 285, Issue 38 https://doi.org/10.1074/jbc.m110.144576	journal	September 2010
Oligomeric Structure and Functional Characterization of Caenorhabditis elegans Innexin-6 Gap Junction Protein* Oshima, Atsunori; Matsuzawa, Tomohiro; Nishikawa, Kouki Journal of Biological Chemistry, Vol. 288, Issue 15 https://doi.org/10.1074/jbc.m112.428383	journal	April 2013
Human cell responses to ionizing radiation are differentially affected by the expressed connexins Autsavapromporn, N.; De Toledo, S. M.; Jay-Gerin, J. -P. Journal of Radiation Research, Vol. 54, Issue 2 https://doi.org/10.1093/jrr/rrs099	journal	November 2012
Connexin 43 impacts the chick premigratory cranial neural crest cell population without affecting the neural crest cell epithelial-to-mesenchymal transition Jourdeuil, Karyn; Taneyhill, Lisa A. Journal of Cell Science https://doi.org/10.1101/673921	posted_content	January 2019
Neuroependymal Denudation is in Progress in Full-term Human Foetal Spina Bifida Aperta: Ependymal Disruption in Human Spina Bifida Sival, Deborah A.; Guerra, Montserrat; den Dunnen, Wilfred F. A. Brain Pathology, Vol. 21, Issue 2 https://doi.org/10.1111/j.1750-3639.2010.00432.x	journal	January 2011
Connexins in Cardiovascular and Neurovascular Health and Disease: Pharmacological Implications Leybaert, Luc; Lampe, Paul D.; Dhein, Stefan Pharmacological Reviews, Vol. 69, Issue 4 https://doi.org/10.1124/pr.115.012062	journal	September 2017
Connexin 37 is localized in renal epithelia and responds to changes in dietary salt intake Stoessel, Adelina; Himmerkus, Nina; Bleich, Markus American Journal of Physiology-Renal Physiology, Vol. 298, Issue 1 https://doi.org/10.1152/ajprenal.00295.2009	journal	January 2010
Tight Junctions in Salivary Epithelium Baker, Olga J. Journal of Biomedicine and Biotechnology, Vol. 2010 https://doi.org/10.1155/2010/278948	journal	January 2010
The Loss of Cellular Junctions in Epithelial Lung Cells Induced by Cigarette Smoke Is Attenuated by Corilagin Muresan, Ximena M.; Cervellati, Franco; Sticozzi, Claudia Oxidative Medicine and Cellular Longevity, Vol. 2015 https://doi.org/10.1155/2015/631758	journal	January 2015
Connexin’s Connection in Breast Cancer Growth and Progression Banerjee, Debarshi International Journal of Cell Biology, Vol. 2016 https://doi.org/10.1155/2016/9025905	journal	January 2016
Mena/VASP and αII-Spectrin complexes regulate cytoplasmic actin networks in cardiomyocytes and protect from conduction abnormalities and dilated cardiomyopathy Benz, Peter M.; Merkel, Carla J.; Offner, Kristin Cell Communication and Signaling, Vol. 11, Issue 1 https://doi.org/10.1186/1478-811x-11-56	journal	January 2013
Distinctive actions of connexin 46 and connexin 50 in anterior pituitary folliculostellate cells Vitale, María Leiza; Garcia, Christopher J.; Akpovi, Casimir D. PLOS ONE, Vol. 12, Issue 7 https://doi.org/10.1371/journal.pone.0182495	journal	July 2017
Cell surface membrane proteins as personalized biomarkers: where we stand and where we are headed Várady, György; Cserepes, Judit; Németh, Adrienn Biomarkers in Medicine, Vol. 7, Issue 5 https://doi.org/10.2217/bmm.13.90	journal	October 2013
Impaired membrane targeting and aberrant cellular localization of human Cx26 mutants associated with inherited recessive hearing loss Xiao, Zian; Yang, Zhongchun; Liu, Xuezhong Acta Oto-Laryngologica, Vol. 131, Issue 1 https://doi.org/10.3109/00016489.2010.506885	journal	August 2010
Cancer Connectors: Connexins, Gap Junctions, and Communication Sinyuk, Maksim; Mulkearns-Hubert, Erin E.; Reizes, Ofer Frontiers in Oncology, Vol. 8 https://doi.org/10.3389/fonc.2018.00646	journal	December 2018
Tight Junction Proteins and Signaling Pathways in Cancer and Inflammation: A Functional Crosstalk Bhat, Ajaz A.; Uppada, Srijayaprakash; Achkar, Iman W. Frontiers in Physiology, Vol. 9 https://doi.org/10.3389/fphys.2018.01942	journal	January 2019
Protein–Protein Interactions with Connexin 43: Regulation and Function Sorgen, Paul; Trease, Andrew; Spagnol, Gaelle International Journal of Molecular Sciences, Vol. 19, Issue 5 https://doi.org/10.3390/ijms19051428	journal	May 2018
A Cell Junctional Protein Network Associated with Connexin-26 Batissoco, Ana; Salazar-Silva, Rodrigo; Oiticica, Jeanne International Journal of Molecular Sciences, Vol. 19, Issue 9 https://doi.org/10.3390/ijms19092535	journal	August 2018
Fenofibrate Reduces the Asthma-Related Fibroblast-To-Myofibroblast Transition by TGF-Β/Smad2/3 Signaling Attenuation and Connexin 43-Dependent Phenotype Destabilization Paw, Milena; Wnuk, Dawid; Kądziołka, Dominika International Journal of Molecular Sciences, Vol. 19, Issue 9 https://doi.org/10.3390/ijms19092571	journal	August 2018
The putative role of lutein and zeaxanthin as protective agents against age-related macular degeneration: promise of molecular genetics for guiding mechanistic and translational research in the field SanGiovanni, John Paul; Neuringer, Martha The American Journal of Clinical Nutrition, Vol. 96, Issue 5 https://doi.org/10.3945/ajcn.112.038240	journal	October 2012

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