Gap junction-mediated cell-to-cell communication in oral development and oral diseases: a concise review of research progress

Wenjing Liu , Yujia Cui , Jieya Wei , Jianxun Sun , Liwei Zheng , Jing Xie

International Journal of Oral Science ›› 2020, Vol. 12 ›› Issue (1) : 17

PDF
International Journal of Oral Science ›› 2020, Vol. 12 ›› Issue (1) : 17 DOI: 10.1038/s41368-020-0086-6
Review Article

Gap junction-mediated cell-to-cell communication in oral development and oral diseases: a concise review of research progress

Author information +
History +
PDF

Abstract

Homoeostasis depends on the close connection and intimate molecular exchange between extracellular, intracellular and intercellular networks. Intercellular communication is largely mediated by gap junctions (GJs), a type of specialized membrane contact composed of variable number of channels that enable direct communication between cells by allowing small molecules to pass directly into the cytoplasm of neighbouring cells. Although considerable evidence indicates that gap junctions contribute to the functions of many organs, such as the bone, intestine, kidney, heart, brain and nerve, less is known about their role in oral development and disease. In this review, the current progress in understanding the background of connexins and the functions of gap junctions in oral development and diseases is discussed. The homoeostasis of tooth and periodontal tissues, normal tooth and maxillofacial development, saliva secretion and the integrity of the oral mucosa depend on the proper function of gap junctions. Knowledge of this pattern of cell–cell communication is required for a better understanding of oral diseases. With the ever-increasing understanding of connexins in oral diseases, therapeutic strategies could be developed to target these membrane channels in various oral diseases and maxillofacial dysplasia.

Cite this article

Download citation ▾
Wenjing Liu, Yujia Cui, Jieya Wei, Jianxun Sun, Liwei Zheng, Jing Xie. Gap junction-mediated cell-to-cell communication in oral development and oral diseases: a concise review of research progress. International Journal of Oral Science, 2020, 12(1): 17 DOI:10.1038/s41368-020-0086-6

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Brucher BL, Jamall IS. Cell-cell communication in the tumor microenvironment, carcinogenesis, and anticancer treatment. Cell. Physiol. Biochem., 2014, 34: 213-243.

[2]

McCrea PD, Gu D, Balda MS. Junctional music that the nucleus hears: cell-cell contact signaling and the modulation of gene activity. Cold Spring Harb. Perspect. Biol., 2009, 1: a002923.

[3]

Wiener J, Spiro D, Loewenstein WR. Studies on an epithelial (gland) cell junction. II. Surface structure. J. Cell Biol., 1964, 22: 587-598.

[4]

Barbe MT, Monyer H, Bruzzone R. Cell-cell communication beyond connexins: the pannexin channels. Physiology, 2006, 21: 103-114.

[5]

Weidmann S. The electrical constants of Purkinje fibres. J. Physiol., 1952, 118: 348-360.

[6]

Furshpan EJ, Potter DD. Mechanism of nerve-impulse transmission at a crayfish synapse. Nature, 1957, 17: 342-343.

[7]

Epifantseva I, Shaw RM. Intracellular trafficking pathways of Cx43 gap junction channels. Biochim. Biophys. Acta Biomembr., 2018, 1860: 40-47.

[8]

Spray DC, . Gap junction mediated signaling between satellite glia and neurons in trigeminal ganglia. Glia, 2019, 67: 791-801.

[9]

Meda P. Gap junction proteins are key drivers of endocrine function. Biochimica Biophysica. Acta Biomembranes., 2018, 1860: 124-140.

[10]

Jagger DJ, Forge A. Connexins and gap junctions in the inner ear—it’s not just about K+ recycling. Cell Tissue Res., 2015, 360: 633-644.

[11]

Laird DW, Lampe PD. Therapeutic strategies targeting connexins. Nat. Rev. Drug Discov., 2018, 17: 905-921.

[12]

Neijssen J, Pang B, Neefjes J. Gap junction-mediated intercellular communication in the immune system. Prog. Biophys. Mol. Biol., 2007, 94: 207-218.

[13]

Wong P, Laxton V, Srivastava S, Chan YW, Tse G. The role of gap junctions in inflammatory and neoplastic disorders (Review). Int. J. Mol. Med., 2017, 39: 498-506.

[14]

Moorer MC, Stains JP. Connexin43 and the intercellular signaling network regulating skeletal remodeling. Curr. Osteoporos. Rep., 2017, 15: 24-31.

[15]

Chen Q, . Carcinoma-astrocyte gap junctions promote brain metastasis by cGAMP transfer. Nature, 2016, 533: 493-498.

[16]

Samiei M, . Cell junctions and oral health. EXCLI J., 2019, 18: 317-330.

[17]

Groeger SE, Meyle J. Epithelial barrier and oral bacterial infection. Periodontology, 2015, 69: 46-67.

[18]

Hervé JC, Derangeon M. Gap-junction-mediated cell-to-cell communication. Cell Tissue Res., 2013, 352: 21-31.

[19]

Roy S, Jiang JX, Li AF, Kim D. Connexin channel and its role in diabetic retinopathy. Prog. Retin. Eye. Res., 2017, 61: 35-59.

[20]

Beyer EC, Berthoud M. Gap junction gene and protein families: connexins, innexins, and pannexins. Biochim. Biophys. Acta Biomembr., 2018, 1860: 5-8.

[21]

Meşe G, Richard G, White TW. Gap junctions: basic structure and function. J. Invest. Dermatol., 2007, 127: 2516-2524.

[22]

Krutovskikh V, Yamasaki H. Connexin gene mutations in human genetic diseases. Mutat. Res., 2000, 462: 197-207.

[23]

Rodríguez-Sinovas A, Ruiz-Meana M, Denuc A, García-Dorado D. Mitochondrial Cx43, an important component of cardiac preconditioning. Biochim Biophys. Acta Biomembr., 2018, 1860: 174-181.

[24]

Liu, W. et al. Transforming growth factor-beta1 up-regulates connexin43 expression in osteocytes via canonical Smad-dependent signaling pathway. Biosci. Rep. 38, BSR20181678 (2018).

[25]

Lampe PD, Lau AF. The effects of connexin phosphorylation on gap junctional communication. Int. J. Biochem. Cell Biol., 2004, 36: 1171-1186.

[26]

Berthoud VM, Beyer EC, Kurata WE, Lau AF, Lampe PD. The gap-junction protein connexin 56 is phosphorylated in the intracellular loop and the carboxy-terminal region. Eur. J. Biochem., 1997, 244: 89-97.

[27]

Traub O, Look J, Dermietzel R. Comparative characterization of the 21-kD and 26-kD gap junction proteins in murine liver and cultured hepatocytes. J. Cell. Biol., 1989, 108: 1039-1051.

[28]

Goodenough DA, Paul DL. Gap junctions. Cold Spring Harb. Perspect. Biol., 2009, 1: a002576.

[29]

Solan JL, Lampe PD. Specific Cx43 phosphorylation events regulate gap junction turnover in vivo. Febs. Lett., 2014, 588: 1423-1429.

[30]

Fernandes R, Girão H, Pereira P. High glucose down-regulates intercellular communication in retinal endothelial cells by enhancing degradation of connexin 43 by a proteasome-dependent mechanism. J. Biol. Chem., 2004, 279: 27219-27224.

[31]

John S, Cesario D, Weiss JN. Gap junctional hemichannels in the heart. Acta Physiol. Scand., 2003, 179: 23-31.

[32]

Lilly E, Sellitto C, Milstone LM, White TW. Connexin channels in congenital skin disorders. Semin. Cell Dev. Biol., 2016, 50: 4-12.

[33]

Evans WH, Martin PE. Gap junctions: structure and function. Mol. Membr. Biol., 2002, 19: 121-136.

[34]

Zappitelli T, Aubin JE. The “connexin” between bone cells and skeletal functions. J. Cell. Biochem., 2014, 115: 1646-1658.

[35]

Pereda AE, . Gap junction-mediated electrical transmission: regulatory mechanisms and plasticity. Biochim Biophys. Acta, 2013, 1828: 134-146.

[36]

Dupont G, Combettes L, Leybaert L. Calcium dynamics: spatio-temporal organization from the subcellular to the organ level. Int. Rev. Cytol., 2007, 261: 193-245.

[37]

Zhang D, . Extracellular matrix elasticity regulates osteocyte gap junction elongation: involvement of paxillin in intracellular signal transduction. Cell. Physiol. Biochem., 2018, 51: 1013-1026.

[38]

Xie J, . Compliant substratum changes osteocyte functions: the role of ITGB3/FAK/β-catenin signaling matters. ACS Appl. Bio. Mater., 2018, 1: 792-801.

[39]

Kanemitsu MY, Lau AF. Epidermal growth factor stimulates the disruption of gap junctional communication and connexin43 phosphorylation independent of 12-0-tetradecanoylphorbol 13-acetate-sensitive protein kinase C: the possible involvement of mitogen-activated protein kinase. Mol. Biol. Cell., 1993, 4: 837-848.

[40]

Ueki T, . Epidermal growth factor down-regulates connexin-43 expression in cultured rat cortical astrocytes. Neurosci. Lett., 2001, 313: 53-56.

[41]

Rivedal E, Opsahl H. Role of PKC and MAP kinase in EGF- and TPA-induced connexin43 phosphorylation and inhibition of gap junction intercellular communication in rat liver epithelial cells. Carcinogenesis, 2001, 22: 1543-1550.

[42]

Kennedy KL, Floyd AA, Clarkson AM, Lee VH. Epidermal growth factor regulation of connexin 43 in cultured granulosa cells from preantral rabbit follicles. Mol. Reprod. Dev., 2003, 64: 61-69.

[43]

Kojima T, Mitaka T, Paul DL, Mori M, Mochizuki Y. Reappearance and long-term maintenance of connexin32 in proliferated adult rat hepatocytes: use of serum-free L-15 medium supplemented with EGF and DMSO. J. Cell. Sci., 1995, 108: 1347-1357.

[44]

Yao J, Morioka T, Oite T. PDGF regulates gap junction communication and connexin43 phosphorylation by PI 3-kinase in mesangial cells. Kidney Int., 2000, 57: 1915-1926.

[45]

Hossain MZ, Ao P, Boynton AL. Rapid disruption of gap junctional communication and phosphorylation of connexin43 by platelet-derived growth factor in T51B rat liver epithelial cells expressing platelet-derived growth factor receptor. J. Cell. Physiol., 1998, 174: 66-77.

[46]

Moorby CD, Gherardi E. Expression of a Cx43 deletion mutant in 3T3 A31 fibroblasts prevents PDGF-induced inhibition of cell communication and suppresses cell growth. Exp. Cell Res., 1999, 249: 367-376.

[47]

Zhang X, . PDGF-mediated PI3K/AKT/β-catenin signaling regulates gap junctions in corpus cavernosum smooth muscle cells. Exp. Cell Res., 2018, 362: 252-259.

[48]

Doble BW, Kardami E. Basic fibroblast growth factor stimulates connexin-43 expression and intercellular communication of cardiac fibroblasts. Mol. Cell. Biochem., 1995, 143: 81-87.

[49]

Reuss B, Hertel M, Werner S, Unsicker K. Fibroblast growth factors-5 and -9 distinctly regulate expression and function of the gap junction protein connexin43 in cultured astroglial cells from different brain regions. Glia, 2000, 30: 231-241.

[50]

Schalper KA, . Modulation of gap junction channels and hemichannels by growth factors. Mol. Biosyst., 2012, 8: 685-698.

[51]

Sakurai T, Tsuchida M, Lampe PD, Murakami M. Cardiomyocyte FGF signaling is required for Cx43 phosphorylation and cardiac gap junction maintenance. Exp. Cell Res., 2013, 319: 2152-2165.

[52]

Liu XY, . FGF-7 dictates osteocyte cell processes through beta-catenin transduction. Sci. Rep., 2018, 8

[53]

Liu W, . TGF-β1 facilitates cell-cell communication in osteocytes via connexin43- and pannexin1-dependent gap junctions. Cell Death Discov., 2019, 5: 141.

[54]

Wang Q, . The involvement of the ERK-MAPK pathway in TGF-β1-mediated connexin43-gap junction formation in chondrocytes. Connect. Tissue Res., 2019, 60: 477-486.

[55]

Wang Q, . TGF-β1 promotes gap junctions formation in chondrocytes via Smad3/Smad4 signalling. Cell Prolif., 2018, 52

[56]

Chen YC, . Transforming growth factor-beta1 up-regulates connexin43 expression in human granulosa cells. Hum. Reprod., 2015, 30: 2190-2201.

[57]

Cheng JC, Chang HM, Fang L, Sun YP, Leung PC. TGF-beta1 up-regulates connexin43 expression: a potential mechanism for human trophoblast cell differentiation. J. Cell. Physiol., 2015, 230: 1558-1566.

[58]

Lim MC, Maubach G, Zhuo L. TGF-beta1 down-regulates connexin 43 expression and gap junction intercellular communication in rat hepatic stellate cells. Eur. J. Cell Biol., 2009, 88: 719-730.

[59]

Neuhaus J, Heinrich M, Schwalenberg T, Stolzenburg J-U. TGF-β1 inhibits Cx43 expression and formation of functional syncytia in cultured smooth muscle cells from human detrusor. Eur. Urol., 2009, 55: 491-498.

[60]

Theodossiou SK, Tokle J, Schiele NR. TGFβ2-induced tenogenesis impacts cadherin and connexin cell-cell junction proteins in mesenchymal stem cells. Biochem. Biophys. Res. Commun., 2019, 508: 889-893.

[61]

Kabir N, Chaturvedi K, Liu LS, Sarkar DK. Transforming growth factor-beta3 increases gap-junctional communication among folliculostellate cells to release basic fibroblast growth factor. Endocrinology, 2005, 146: 4054-4060.

[62]

Hervé JC, Derangeon M, Sarrouilhe D, Giepmans BN, Bourmeyster N. Gap junctional channels are parts of multiprotein complexes. Biochim. Biophys. Acta, 2012, 1818: 1844-1865.

[63]

Squecco R, . Sphingosine 1-phosphate induces myoblast differentiation through Cx43 protein expression: a role for a gap junction-dependent and -independent function. Mol. Biol. Cell., 2006, 17: 4896-4910.

[64]

Giepmans BN, Verlaan I, Moolenaar WH. Connexin-43 interactions with ZO-1 and alpha- and beta-tubulin. Cell Commun. Adhes., 2001, 8: 219-223.

[65]

Paris L, Tonutti L, Vannini C, Bazzoni G. Structural organization of the tight junctions. Biochim. Biophys. Acta, 2008, 1778: 646-659.

[66]

Singh D, Solan JL, Taffet SM, Javier R, Lampe PD. Connexin 43 interacts with zona occludens-1 and -2 proteins in a cell cycle stage-specific manner. J. Biol. Chem., 2005, 280: 30416-30421.

[67]

Toyofuku T, . c-Src regulates the interaction between connexin-43 and ZO-1 in cardiac myocytes. J. Biol. Chem., 2001, 276: 1780-1788.

[68]

Azarnia R, Reddy S, Kmiecik TE, Shalloway D, Loewenstein WR. The cellular src gene product regulates junctional cell-to-cell communication. Science, 1988, 239: 398-401.

[69]

Kojima T, . Induction of tight junctions in human connexin 32 (hCx32)-transfected mouse hepatocytes: connexin 32 interacts with occludin. Biochem. Biophys. Res. Commun., 1999, 266: 222-229.

[70]

Nusrat A, Chen JA, Foley CS. The coiled-coil domain of occludin can act to organize structural and functional elements of the epithelial tight junction. J. Biol. Chem., 2000, 275: 29816-29822.

[71]

Kojima T, . Cx32 but not Cx26 is associated with tight junctions in primary cultures of rat hepatocytes. Exp. Cell Res., 2001, 263: 193-201.

[72]

Nagasawa K, . Possible involvement of gap junctions in the barrier function of tight junctions of brain and lung endothelial cells. J. Cell. Physiol., 2006, 208: 123-132.

[73]

Wei CJ, Francis R, Xu X, Lo CW. Connexin43 associated with an N-cadherin-containing multiprotein complex is required for gap junction formation in NIH3T3 cells. J. Biol. Chem., 2005, 280: 19925-19936.

[74]

Luo Y, Radice GL. Cadherin-mediated adhesion is essential for myofibril continuity across the plasma membrane but not for assembly of the contractile apparatus. J. Cell Sci., 2003, 116: 14711-14719.

[75]

Govindarajan R, . Assembly of connexin43 into gap junctions is regulated differentially by E-cadherin and N-cadherin in rat liver epithelial cells. Mol. Biol. Cell., 2010, 21: 4089-4107.

[76]

Malhotra JD, Thyagarajan V, Chen C, Isom LL. Tyrosine-phosphorylated and nonphosphorylated sodium channel beta1 subunits are differentially localized in cardiac myocytes. J. Biol. Chem., 2004, 279: 40748-40754.

[77]

Liu J, Xu J, Gu S, Nicholson BJ, Jiang JX. Aquaporin 0 enhances gap junction coupling via its cell adhesion function and interaction with connexin 50. J. Cell. Sci., 2011, 124: 198-206.

[78]

Leithe E, Mesnil M, Aasen T. The connexin 43 C-terminus: a tail of many tales. Biochim. Biophys. Acta Biomembr., 2018, 1860: 48-64.

[79]

Park DJ, . Akt phosphorylates Connexin43 on Ser373, a “mode-1” binding site for 14-3-3. Cell Commun. Adhes., 2007, 14: 211-226.

[80]

Johnstone SR, . MAPK phosphorylation of connexin 43 promotes binding of cyclin E and smooth muscle cell proliferation. Circ. Res., 2012, 111: 201-211.

[81]

Lampe PD, . Phosphorylation of connexin43 on serine368 by protein kinase C regulates gap junctional communication. J. Cell. Biol., 2000, 149: 1503-1512.

[82]

About I, Proust JP, Raffo S, Mitsiadis TA, Franquin JC. In vivo and in vitro expression of connexin 43 in human teeth. Connect. Tissue Res., 2002, 43: 232-237.

[83]

Kagayama M, Akita H, Sasano Y. Immunohistochemical localization of connexin 43 in the developing tooth germ of rat. Anat. Embryol., 1995, 191: 561-568.

[84]

Pinero GJ, Parker S, Rundus V, Hertzberg EL, Minkoff R. Immunolocalization of connexin 43 in the tooth germ of the neonatal rat. Histochem J., 1994, 26: 765-770.

[85]

Murakami S, Muramatsu T, Shimono M. Expression and localization of connexin 43 in rat incisor odontoblasts. Anat. Embryol., 2001, 203: 367-374.

[86]

Inai T, Nakamura K, Kurisu K, Shibata Y. Immunohistochemical localization of connexin43 in the enamel organ of the rat upper incisor during ameloblast development. Arch. Histol. Cytol., 1997, 60: 297-306.

[87]

Al-Ansari, S. et al. The importance of connexin 43 in enamel development and mineralization. Front. Physiol. https://doi.org/10.3389/fphys.2018.00750 (2018).

[88]

Toth K, Shao Q, Lorentz R, Laird DW. Decreased levels of Cx43 gap junctions result in ameloblast dysregulation and enamel hypoplasia in Gja1Jrt/+ mice. J. Cell. Physiol., 2010, 223: 601-609.

[89]

Uribe P, . Study on site-specific expression of bone formation and resorption factors in human dental follicles. Eur. J. Oral. Sci., 2018, 126: 439-448.

[90]

Fried K, Mitsiadis TA, Guerrier A, Haegerstrand A, Meister B. Combinatorial expression patterns of the connexins 26, 32, and 43 during development, homeostasis, and regeneration of rat teeth. Int. J. Dev. Biol., 1996, 40: 985-995.

[91]

Amano K, . Cleft lip in oculodentodigital dysplasia suggests novel roles for connexin43. J. Dent. Res., 2012, 91: 38S-44S.

[92]

Yamada A, . Connexin 43 is necessary for salivary gland branching morphogenesis and FGF10-induced ERK1/2 phosphorylation. J. Biol. Chem., 2016, 291: 904-912.

[93]

Ihara A, Muramatsu T, Shimono M. Expression of connexin 32 and 43 in developing rat submandibular salivary glands. Arch. Oral. Biol., 2000, 45: 227-235.

[94]

Kim JY, Cho SW, Lee MJ. Inhibition of connexin 43 alters Shh and Bmp-2 expression patterns in embryonic mouse tongue. Cell Tissue Res., 2005, 320: 409-415.

[95]

Lee MJ, . Association of Shh and Ptc with keratin localization in the initiation of the formation of circumvallate papilla and von Ebner’s gland. Cell Tissue Res., 2006, 325: 253-261.

[96]

Kato R, . Gap-junction-mediated communication in human periodontal ligament cells. J. Dent. Res., 2013, 92: 635-640.

[97]

Yamaoka Y, . Double expressions of connexin 43 and 32 in human periodontal ligament fibroblasts. Tissue Cell., 2000, 32: 328-335.

[98]

Li S, . Connexin 43 and ERK regulate tension-induced signal transduction in human periodontal ligament fibroblasts. J. Orthop. Res., 2015, 33: 1008-1014.

[99]

Yamaoka Y, Sawa Y, Ebata N, Ibuki N, Yoshida S. Cultured periodontal ligament fibroblasts express diverse connexins. Tissue Cell., 2002, 34: 375-380.

[100]

Su M, . Expression of connexin 43 in rat mandibular bone and periodontal ligament (PDL) cells during experimental tooth movement. J. Dent. Res., 1997, 76: 1357-1366.

[101]

Xu C, . Cyclic stretch influenced expression of membrane connexin 43 in human periodontal ligament cell. Arch. Oral. Biol., 2012, 57: 1602-1608.

[102]

Ye P, Chapple CC, Kumar RK, Hunter N. Expression patterns of E-cadherin, involucrin, and connexin gap junction proteins in the lining epithelia of inflamed gingiva. J. Pathol., 2000, 192: 58-66.

[103]

Hatakeyama S, . Expression pattern of adhesion molecules in junctional epithelium differs from that in other gingival epithelia. J. Periodontal Res., 2006, 41: 322-328.

[104]

Fujita T, . Irsogladine maleate counters the interleukin-1 beta-induced suppression in gap-junctional intercellular communication but does not affect the interleukin-1 beta-induced zonula occludens protein-1 levels in human gingival epithelial cells. J. Periodontal Res., 2008, 43: 96-102.

[105]

Muramatsu T, Uekusa T, Masaoka T. Differential expression and localization of connexins 26 and 43 in the rat gingival epithelium. Arch. Histol. Cytol., 2008, 71: 147-154.

[106]

Tarzemany R, Jiang G, Larjava H, Häkkinen L. Expression and function of connexin 43 in human gingival wound healing and fibroblasts. PLoS ONE, 2015, 10

[107]

Ibuki N, Yamaoka Y, Sawa Y, Kawasaki T, Yoshida S. Different expressions of connexin 43 and 32 in the fibroblasts of human dental pulp. Tissue Cell., 2002, 34: 170-176.

[108]

Chung CK, Muramatsu T, Uekusa T, Sasaki H, Shimono M. Inhibition of connexin 43 expression and function in cultured rat dental pulp cells by antisense oligonucleotide. Cell Tissue Res., 2007, 329: 295-300.

[109]

Li S, . Connexin43-containing gap junctions potentiate extracellular Ca(2)(+)-induced odontoblastic differentiation of human dental pulp stem cells via Erk1/2. Exp. Cell Res., 2015, 338: 1-9.

[110]

Muramatsu T, . Reduction of connexin 43 expression in aged human dental pulp. Int. Endod. J., 2004, 37: 814-818.

[111]

Amano T, Muramatsu T, Amemiya K, Kubo K, Shimono M. Responses of rat pulp cells to heat stress in vitro. J. Dent. Res., 2006, 85: 432-435.

[112]

Köling A, Rask-Andersen H. Membrane junctions between odontoblasts and associated cells. A freeze-fracture study of the human odontoblastic cell layer with special reference to its nerve supply. Acta Odontol. Scand., 1984, 42: 13-22.

[113]

Muramatsu T, . Immunoelectron microscopic observation of connexin43 in rat odontoblasts. Microsc. Res. Tech., 2013, 76: 988-991.

[114]

Farahani RM, Nguyen KA, Simonian M, Hunter N. Adaptive calcified matrix response of dental pulp to bacterial invasion is associated with establishment of a network of glial fibrillary acidic protein + /glutamine synthetase+ cells. Am. J. Pathol., 2010, 177: 1901-1914.

[115]

Couve E, . Reactionary dentinogenesis and neuroimmune response in dental caries. J. Dent. Res., 2014, 93: 788-793.

[116]

Centeno VA, Fontanetti PA, Interlandi V, Ponce RH, Gallará RV. Fluoride alters connexin expression in rat incisor pulp. Arch. Oral. Biol., 2015, 60: 313-319.

[117]

Azarnia R, Loewenstein WR. Intercellular communication and tissue growth: V. A cancer cell strain that fails to make permeable membrane junctions with normal cells. J. Membr. Biol., 1971, 6: 368-385.

[118]

Trosko JE, Chang CC, Upham BL, Tai MH. Ignored hallmarks of carcinogenesis: stem cells and cell-cell communication. Ann. N. Y Acad. Sci., 2004, 1028: 192-201.

[119]

McLachlan E, Shao Q, Wang HL, Langlois S, Laird DW. Connexins act as tumor suppressors in three-dimensional mammary cell organoids by regulating differentiation and angiogenesis. Cancer Res., 2006, 66: 9886-9894.

[120]

Sirnes S, . Connexins in colorectal cancer pathogenesis. Int. J. Cancer, 2015, 137: 1-11.

[121]

Czyż J, Szpak K, Madeja Z. The role of connexins in prostate cancer promotion and progression. Nat. Rev. Urol., 2012, 9: 274-282.

[122]

Yost S, . Increased virulence of the oral microbiome in oral squamous cell carcinoma revealed by metatranscriptome analyses. Int. J. Oral. Sci., 2018, 10: 32.

[123]

Brockmeyer P, Jung K, Perske C, Schliephake H, Hemmerlein B. Membrane connexin 43 acts as an independent prognostic marker in oral squamous cell carcinoma. Int. J. Oncol., 2014, 45: 273-281.

[124]

Essa AA, Yamazaki M, Maruyama S. Tumour-associated macrophages are recruited and differentiated in the neoplastic stroma of oral squamous cell carcinoma. Pathology, 2016, 48: 219-227.

[125]

Zhong WQ, . Down-regulation of connexin43 and connexin32 in keratocystic odontogenic tumours: potential association with clinical features. Histopathology, 2015, 66: 798-807.

[126]

Saitoh M, Oyamada M, Oyamada Y, Kaku T, Mori M. Changes in the expression of gap junction proteins (connexins) in hamster tongue epithelium during wound healing and carcinogenesis. Carcinogenesis, 1997, 18: 1319-1328.

[127]

Ozawa H, Matsunaga T, Kamiya K. Decreased expression of connexin-30 and aberrant expression of connexin-26 in human head and neck cancer. Anticancer Res., 2007, 27: 2189-2195.

[128]

Wang J, Dai Y, Huang Y. All-trans retinoic acid restores gap junctional intercellular communication between oral cancer cells with upregulation of Cx32 and Cx43 expressions in vitro. Med. Oral. Patol. Oral. Cir. Bucal, 2013, 18: e569-e577.

[129]

Piechocki MP, Lonardo F, Ensley JF. Anticancer activity of docetaxel in murine salivary gland carcinoma. Clin. Cancer Res., 2002, 8: 870-877.

[130]

Livny O, . Lycopene inhibits proliferation and enhances gap-junction communication of KB-1 human oral tumor cell. J. Nutr., 2002, 132: 3754-3759.

[131]

Rednam S, Hicks J, Levy ML, Pappo AS. Metastatic squamous cell carcinoma of the oropharynx in a child with a mutation in the connexin 26 gene. J. Pediatr. Hematol. Oncol., 2011, 33: 387-389.

[132]

van Steensel MA, van Geel. M, Nahuys M, Smitt JH, Steijlen PM. A novel connexin 26 mutation in a patient diagnosed with keratitis-ichthyosis-deafness syndrome. J. Invest. Dermatol., 2002, 118: 724-727.

[133]

Hadjichristou C, . Oculo-dento-digital dysplasia (ODDD) due to a GJA1 mutation: report of a case with emphasis on dental manifestations. Int. J. Prosthodont., 2017, 30: 280-285.

[134]

Paznekas WA, . GJA1 mutations, variants, and connexin 43 dysfunction as it relates to the oculodentodigital dysplasia phenotype. Hum. Mutat., 2009, 30: 724-733.

[135]

Tarzemany R, Jiang G, Jiang JX, Larjava H, Häkkinen L. Connexin 43 hemichannels regulate the expression of wound healing-associated genes in human gingival fibroblasts. Sci. Rep., 2017, 7

[136]

Tarzemany R, . Connexin 43 regulates the expression of wound healing-related genes in human gingival and skin fibroblasts. Exp. Cell Res., 2018, 367: 150-161.

[137]

Li, X. et al. TGF-beta1-induced connexin43 promotes scar formation via the Erk/MMP-1/collagen III pathway. J. Oral Rehabil. https://doi.org/10.1111/joor.12829 (2019).

[138]

Hsu JC, Yamada KM. Salivary gland branching morphogenesis–recent progress and future opportunities. Int. J. Oral. Sci., 2010, 2: 117-126.

[139]

Shimono M, Young, Lee. C, Matsuzaki H. Connexins in salivary glands. Eur. J. Morphol., 2000, 38: 257-261.

[140]

Actis AB, Lampe PD, Eynard AR. Cellular basis and clinical implications of biological markers in salivary tissues their topological distribution in murine submandibular gland. Oral. Oncol., 2002, 38: 441-449.

[141]

Muramatsu T, Hashimoto S, Shimono M. Differential expression of gap junction proteins connexin32 and 43 in rat submandibular and sublingual glands. J. Histochem. Cytochem., 1996, 44: 49-56.

[142]

Kuraoka A, Yamanaka I, Miyahara A, Shibata Y, Uemura T. Immunocytochemical studies of major gap junction proteins in rat salivary glands. Eur. Arch. Otorhinolaryngol., 1994, 251(Suppl 1): S95-S99.

Funding

National Natural Science Foundation of China (National Science Foundation of China)(81600840)

AI Summary AI Mindmap
PDF

149

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/