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Intercellular Network of Junctions of the Gastrointestinal Tract

  • Menizibeya Osain Welcome
Chapter

Abstract

The peculiar organization of cells of the gastrointestinal tract, in part, is due to the integrity of the anatomical architecture of the linkages or junctions between the neighboring cells. In this chapter, the structural and functional characteristics of these junctions are discussed.

Keywords

Epithelium Epithelial cells Intercellular junction Intercellular network Intercellular linkage Gap junction (macula communicansNexus Connexin Pannexin Innexin Tight junction (zonula occludensOccludin Cadherins Intermediate junction Adherens junction (zonula adherensCatenin Plakins (plakophilin, plakoglobin) Desmoglein Desmocollin Desmosome (macula adhaerens) 

Abbreviations

ADP

Adenosine diphosphate

AMP

Adenosine monophosphate

ATP

Adenosine triphosphate

Bves

Blood vessel epicardial substance

cAMP

Cyclic adenosine monophosphate

CAR

Coxsackievirus and adenovirus receptor

CaSR

Ca2+-sensing receptor

cGMP

Cyclic guanosine monophosphate

Cx

Connexin

GK

Guanylate kinase

GTP

Guanosine triphosphate

Inx

Innexin

IP3

Inositol 1,4,5-triphosphate

JAM

Junctional adhesion molecule

MAGUK

Membrane-associated guanylate kinase

MARVEL

MAL (myelin and lymphocyte) and related proteins for vesicle trafficking and membrane link

NAD

Nicotinamide adenine dinucleotide

Panx

Pannexin

PDZ

Postsynaptic density, disk-large, ZO

PKC

Protein kinase type C

Popdc

Popeye domain-containing gene family of proteins

SH3

Src (sarcoma) homology-3

ZO

Zona occludens protein

Bibliography

  1. 1.
    Fasano A (2012) Zonulin, regulation of tight junctions, and autoimmune diseases. Ann N Y Acad Sci 1258(1):25–33PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Lerner A, Matthias T (2015) Changes in intestinal tight junction permeability associated with industrial food additives explain the rising incidence of autoimmune disease. Autoimm Rev 14(6):479–489CrossRefGoogle Scholar
  3. 3.
    Lee SH (2015) Intestinal permeability regulation by tight junction: implication on inflammatory bowel diseases. Intest Res 13(1):11–18PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Ugalde-Silva P, Gonzalez-Lugo O, Navarro-Garcia F (2016) Tight junction disruption induced by type 3 secretion system effectors injected by enteropathogenic and enterohemorrhagic Escherichia coli. Front Cell Infect Microbiol 6:87PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Sharma R, Young C, Neu J (2010) Molecular modulation of intestinal epithelial barrier: contribution of microbiota. J Biomed Biotechnol 2010:305879PubMedPubMedCentralGoogle Scholar
  6. 6.
    Blaskewicz CD, Pudney J, Anderson DJ (2011) Structure and function of intercellular junctions in human cervical and vaginal mucosal epithelia. Biol Reprod 85(1):97–104PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Giepmans BNG, van IJzendoorn SCD (2009) Epithelial cell–cell junctions and plasma membrane domains. BBA—Biomembr 1788(4):820–831CrossRefGoogle Scholar
  8. 8.
    Günzel D, Yu ASL (2013) Claudins and the modulation of tight junction permeability. Physiol Rev 93(2):525–569PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Palade GE (1974) Intracellular aspects of the process of protein secretion. In: Nobel Lecture physiology or medicine. Almqvist & Wiksell International, StockholmGoogle Scholar
  10. 10.
    Farquhar MG, Palade GE (1963) Junctional complexes in various epithelia. J Cell Biol 17:375–412PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Diamond JM (1977) Twenty-first Bowditch Lecture. The epithelial junction: Bridge, gate, and fence. Physiol 20(1):10–18Google Scholar
  12. 12.
    Goodenough DA, Paul DL (2009) Gap Junctions. Cold Spring Harb Symp Quant Biol 1(1):a002576Google Scholar
  13. 13.
    Retamal MA, Reyes EP, García IE, Pinto B, Martínez AD, González C (2015) Diseases associated with leaky hemichannels. Front Cell Neurosci 9:267PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Mee G, Richard G, White TW (2007) Gap junctions: basic structure and function. J Invest Dermatol 127:2516–2524CrossRefGoogle Scholar
  15. 15.
    Scemes E, Spray DC, Meda P (2009) Connexins, pannexins, innexins: novel roles of “hemi-channels”. Pflugers Arch 457(6):1207–1226PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Söhl G, Willecke K (2004) Gap junctions and the connexin protein family. Cardiovasc Res 62:228–232PubMedCrossRefPubMedCentralGoogle Scholar
  17. 17.
    Dahl G, Locovei S (2006) Pannexin: to gap or not to gap, is that a question? IUBMB Life 58(7):409–419PubMedCrossRefPubMedCentralGoogle Scholar
  18. 18.
    Frinchi M, Di Liberto V, Turimella S, D’Antoni F, Theis M, Belluardo N, Mudò G (2013) Connexin36 (Cx36) expression and protein detection in the mouse carotid body and myenteric plexus. Acta Histochem 115(3):252–256PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Kumar NM, Gilula NB (1996) The gap junction communication channel. Cell 84(3):381–388PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Sohl G, Willecke K (2003) An update on connexin genes and their nomenclature in mouse and man. Cell Commun Adhes 10:173–180PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Le Vasseur M, Lelowski J, Bechberger JF, Sin W-C, Naus CC (2014) Pannexin 2 protein expression is not restricted to the CNS. Front Cell Neurosci 8:392PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Diezmos EF, Sandow SL, Markus I, Perera DS, Lubowski DZ, King DW et al (2013) Expression and localization of pannexin-1 hemichannels in human colon in health and disease. Neurogastroenterol Motil 25(6):e395–e405PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Kanczuga-Koda L, Sulkowski S, Koda M, Sobaniec-Lotowska M, Sulkowska M (2004) Expression of connexins 26, 32 and 43 in the human colon–an immunohistochemical study. Folia Histochem Cytobiol 42(4):203–217PubMedPubMedCentralGoogle Scholar
  24. 24.
    Wang YF, Daniel EE (2001) Gap junctions in gastrointestinal muscle contain multiple connexins. Am J Physiol Gastrointest Liver Physiol 281(2):G533–G543PubMedCrossRefPubMedCentralGoogle Scholar
  25. 25.
    Nagy JI, Urena-Ramirez V, Ghia JE (2014) Functional alterations in gut contractility after connexin36 ablation and evidence for gap junctions forming electrical synapses between nitrergic enteric neurons. FEBS Lett 588(8):1480–1490PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Palade GE (1975) Intracellular aspects of the process of protein synthesis. Sci 189:347–358CrossRefGoogle Scholar
  27. 27.
    Saucan L, Palade GE (1994) Membrane and secretory proteins are transported from the Golgi complex to the sinusoidal plasmalemma of hepatocytes by distinct vesicular carriers. J Cell Biol 125:733–741PubMedCrossRefPubMedCentralGoogle Scholar
  28. 28.
    Connors BW (2012) Tales of a dirty drug: carbenoxolone, gap junctions, and seizures. Epilepsy Curr 12(2):66–68PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Srinivas M, Hopperstad MG, Spray DC (2001) Quinine blocks specific gap junction channel subtypes. PNAS 98(19):10942–10947PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Qi X, Varma P, Newman D, Dorian P (2001) Gap junction blockers decrease defibrillation thresholds without changes in ventricular refractoriness in isolated rabbit hearts. Circ 104:1544–1549CrossRefGoogle Scholar
  31. 31.
    Bai D, del Corsso C, Srinivas M, Spray DC (2006) Block of specific gap junction channel subtypes by 2-aminoethoxydiphenyl borate (2-APB). JPET 319(3):1452–1458CrossRefGoogle Scholar
  32. 32.
    Chiba H, Osanai M, Murata M, Kojima T, Sawada N (2008) Transmembrane proteins of tight junctions. BBA Biomembr 1778(3):588–600CrossRefGoogle Scholar
  33. 33.
    Hou J (2014) The kidney tight junction (Review). Int J Mol Med 34(6):1451–1457PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Förster C (2008) Tight junctions and the modulation of barrier function in disease. Histochem Cell Biol 130(1):55–70PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Anderson JM, Van Itallie CM (2009) Physiology and function of the tight junction. Cold Spring Harb Perspect Biol 1(2):a002584PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Baumgartner S, Littleton JT, Broadie K, Bhat MA, Harbecke R, Lengyel JA et al (1996) A Drosophila neurexin is required for septate junction and blood-nerve barrier formation and function. Cell 87(6):1059–1068PubMedCrossRefPubMedCentralGoogle Scholar
  37. 37.
    Oshima K, Fehon RG (2011) Analysis of protein dynamics within the septate junction reveals a highly stable core protein complex that does not include the basolateral polarity protein Discs large. J Cell Sci 124(Pt 16):2861–2871PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Juang JL, Carlson SD (1994) Analog of vertebrate anionic sites in blood-brain interface of larval Drosophila. Cell Tissue Res 277(1):87–95PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    Abbott NJ, Rönnbäck L, Hansson E (2006) Astrocyte–endothelial interactions at the blood–brain barrier. Nat Rev Neurosci 7:41–53PubMedCrossRefPubMedCentralGoogle Scholar
  40. 40.
    Willis CL (2011) Glia-induced reversible disruption of blood–brain barrier integrity and neuropathological response of the neurovascular unit. Toxicol Patholvol 39(1):172–185CrossRefGoogle Scholar
  41. 41.
    Balda MS, Matter K (2008) Tight junctions at a glance. J Cell Sci 121:3677–3682PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    Mandel LJ, Bacallao R, Zampighi G (1993) Uncoupling of the molecular ‘fence’ and paracellular ‘gate’ functions in epithelial tight junctions. Nat 361(6412):552–555CrossRefGoogle Scholar
  43. 43.
    Landy J, Ronde E, English N, Clark SK, Hart AL, Knight SC et al (2016) Tight junctions in inflammatory bowel diseases and inflammatory bowel disease associated colorectal cancer. World J Gastroenterol 22(11):3117–3126PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Sánchez-Pulido L, Martín-Belmonte F, Valencia A, Alonso MA (2002) MARVEL: a conserved domain involved in membrane apposition events. Trends Biochem Sci 27(12):599–601PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Raleigh DR, Marchiando AM, Zhang Y, Shen L, Sasaki H, Wang Y et al (2010) Tight junction–associated MARVEL proteins MarvelD3, tricellulin, and occludin have distinct but overlapping functions. Mol Biol Cell 21(7):1200–1213PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Wu Y-C, Liu C-Y, Chen Y-H, Chen R-F, Huang C-J, Wang I-J (2012) Blood vessel epicardial substance (Bves) regulates epidermal tight junction integrity through atypical protein kinase C. J Biol Chem 287:39887–39897PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Abe K, Takeichi M (2008) EPLIN mediates linkage of the cadherin—catenin complex to F-actin and stabilizes the circumferential actin belt. PNAS 105(1):13–19PubMedCrossRefPubMedCentralGoogle Scholar
  48. 48.
    Cho KO, Hunt CA, Kennedy MB (1992) The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron 9(5):929–942PubMedCrossRefPubMedCentralGoogle Scholar
  49. 49.
    Woods DF, Bryant PJ (1993) ZO-1, DlgA, PSD-95/SAP90: homologous proteins in tight, septate and synaptic cell junctions. Mech Dev 44:85–89PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Overgaard CE, Daugherty BL, Mitchell LA, Koval M (2011) Claudins: control of barrier function and regulation in response to oxidant stress. Antioxid Redox Signal 15(5):1179–1193PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Shen L, Weber CR, Raleigh DR, Yu D, Turner JR (2011) Tight junction pore and leak pathways: a dynamic duo. Annu Rev Physiol 73:283–309PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Pei L (2016) Paracellular epithelial transport maximizes energy efficiency in the kidney. University of Kansas, Kansas, USAGoogle Scholar
  53. 53.
    Anderson JM, Van Itallie CM (2009) Physiology and function of the tight junction. Cold Spring Harb Perspect Biol 1(2):a002584PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Markov AG, Amasheh S (2011) Barrier properties and tight junction protein expression along the longitudinal axis of rat intestine. Ross Fiziol Zh Im I M Sechenova 97(10):1066–1083PubMedPubMedCentralGoogle Scholar
  55. 55.
    Hou J (2012) Lecture: new light on the role of claudins in the kidney. Organogenesis 8(1):1–9PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Gong Y, Hou J (2014) Claudin-14 underlies Ca++-sensing receptor-mediated Ca++ metabolism via NFAT-microRNA-based mechanisms. J Am Soc Nephrol 25(4):745–760PubMedCrossRefPubMedCentralGoogle Scholar
  57. 57.
    Amasheh S, Fromm M, Günzel D (2011) Claudins of intestine and nephron—a correlation of molecular tight junction structure and barrier function. Acta Physiol (Oxf) 201(1):133–140CrossRefGoogle Scholar
  58. 58.
    Markov AG, Falchuk EL, Kruglova NM, Rybalchenko OV, Fromm M, Amasheh S (2014) Comparative analysis of theophylline and cholera toxin in rat colon reveals an induction of sealing tight junction proteins. Pflugers Arch 466(11):2059–2065PubMedCrossRefPubMedCentralGoogle Scholar
  59. 59.
    Zeissig S, Bürgel N, Günzel D, Richter J, Mankertz J, Wahnschaffe U et al (2007) Changes in expression and distribution of claudin 2, 5 and 8 lead to discontinuous tight junctions and barrier dysfunction in active Crohn’s disease. Gut 56(1):61–72PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Mankertz J, Schulzke JD (2007) Altered permeability in inflammatory bowel disease: pathophysiology and clinical implications. Curr Opin Gastroenterol 23(4):379–383PubMedCrossRefPubMedCentralGoogle Scholar
  61. 61.
    Heller F, Florian P, Bojarski C, Richter J, Christ M, Hillenbrand B et al (2005) Interleukin-13 is the key effector Th2 cytokine in ulcerative colitis that affects epithelial tight junctions, apoptosis, and cell restitution. Gastroenterol 129(2):550–564CrossRefGoogle Scholar
  62. 62.
    Schulzke JD, Ploeger S, Amasheh M, Fromm A, Zeissig S, Troeger H et al (2009) Epithelial tight junctions in intestinal inflammation. Ann N Y Acad Sci 1165:294–300PubMedCrossRefPubMedCentralGoogle Scholar
  63. 63.
    Hou J, Goodenough DA (2010) Claudin-16 and claudin-19 function in the thick ascending limb. Curr Opin Nephrol Hypertens 19(5):483–488PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Bauer H, Zweimueller-Mayer J, Steinbacher P, Lametschwandtner A, Bauer HC (2010) The dual role of zonula occludens (ZO) proteins. J Biomed Biotechnol 2010:402593PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Itoh M, Nagafuchi A, Moroi S, Tsukita S (1997) Involvement of ZO-1 in cadherin-based cell adhesion through its direct binding to alpha catenin and actin filaments. J Cell Biol 138(1):181–192PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Itoh M, Furuse M, Morita K, Kubota K, Saitou M, Tsukita S (1999) Direct binding of three tight junction-associated MAGUKs, ZO-1, ZO-2, and ZO-3, with the COOH termini of claudins. J Cell Biol 147(6):1351–1363PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Woods DF, Bryant PJ (1993) ZO-1, DlgA and PSD-95/SAP90: homologous proteins in tight, septate and synaptic cell junctions. Mech Dev 44(2–3):85–89PubMedCrossRefPubMedCentralGoogle Scholar
  68. 68.
    Guillemot L, Paschoud S, Pulimeno P, Foglia A, Citi S (2008) The cytoplasmic plaque of tight junctions: a scaffolding and signalling center. BBA Biomembranes 1778(3):601–613PubMedCrossRefPubMedCentralGoogle Scholar
  69. 69.
    Mariano C, Sasaki H, Brites D, Brito MA (2011) A look at tricellulin and its role in tight junction formation and maintenance. Eur J Cell Biol 90(10):787–796PubMedCrossRefPubMedCentralGoogle Scholar
  70. 70.
    Fanning AS, Jameson BJ, Jesaitis LA, Anderson JM (1998) The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. J Biol Chem 273(45):29745–29753PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Kale G, Naren AP, Sheth P, Rao RK (2003) Tyrosine phosphorylation of occludin attenuates its interactions with ZO-1, ZO-2, and ZO-3. Biochem Biophys Res Commun 302(2):324–329PubMedCrossRefPubMedCentralGoogle Scholar
  72. 72.
    Choi W, Acharya BR, Peyret G, Fardin M-A, Mège R-M, Ladoux B et al (2016) Remodeling the zonula adherens in response to tension and the role of afadin in this response. J Cell Biol 213(2):243–260PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Kamitani T, Sakaguchi H, Tamura A, Miyashita T, Yamazaki Y, Tokumasu R et al (2015) Deletion of tricellulin causes progressive hearing loss associated with degeneration of cochlear hair cells. Sci Rep 5:18402PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Krug SM, Amasheh S, Richter JF, Milatz S, Günzel D, Westphal JK et al (2009) Tricellulin forms a barrier to macromolecules in tricellular tight junctions without affecting ion permeability. Mol Biol Cell 20(16):3713–3724PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Riazuddin S, Ahmed ZM, Fanning AS, Lagziel A, Kitajiri S-I, Ramzan K et al (2006) Tricellulin is a tight-junction protein necessary for hearing. Am J Hum Genet 79(6):1040–1051PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Brand T (2005) The Popeye domain-containing gene family. Cell Biochem Biophys 43(1):95–103PubMedCrossRefPubMedCentralGoogle Scholar
  77. 77.
    Osler ME, Smith TK, Bader DM (2006) Bves, a member of the Popeye domain-containing gene family. Dev Dynam 235(3):586–593CrossRefGoogle Scholar
  78. 78.
    Hager HA, Bader DM (2009) Bves: ten years after. Histol Histopathol 24(6):777–787PubMedPubMedCentralGoogle Scholar
  79. 79.
    Wu Y-C, Chen R-F, Liu C-Y, Hu FR, Huang C-J, Wang I-J (2014) Knockdown of Zebrafish blood vessel epicardial substance results in incomplete retinal lamination. Sci World J 2014:803718Google Scholar
  80. 80.
    Andrée B, Hillemann T, Kessler-icekson G, Schmitt-john T, Jockusch H, Arnold HH, Brand T (2000) Isolation and characterization of the novel popeye gene family expressed in skeletal muscle and heart. Dev Biol 223(2):371–382PubMedCrossRefPubMedCentralGoogle Scholar
  81. 81.
    Schindler RFR, Brand T (2016) The Popeye domain containing protein family—a novel class of cAMP effectors with important functions in multiple tissues. Prog Biophys Mol Biol 120(1–3):28–36PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Froese A, Breher SS, Waldeyer C, Schindler RF, Nikolaev VO, Rinné S et al (2012) Popeye domain containing proteins are essential for stress-mediated modulation of cardiac pacemaking in mice. J Clin Invest 122(3):1119–1130PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Smith TK, Bader DM (2006) Characterization of Bves expression during mouse development using newly generated immunoreagents. Dev Dynam 235:1701–1708CrossRefGoogle Scholar
  84. 84.
    Pardo JV, Craig SW (1979) alpha-Actinin localization in the junctional complex of intestinal epithelial cells. J Cell Biol 80:203–210PubMedCrossRefPubMedCentralGoogle Scholar
  85. 85.
    Renyong G, Hiroshi S, Shigeki S (2006) Endothelial cell motility is compatible with junctional integrity. J Cell Physiol 211:327–335Google Scholar
  86. 86.
    Meng W, Takeichi M (2009) Adherens junction: molecular architecture and regulation. Cold Spring Harb Perspect Biol 1(6):a002899PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Harrison OJ, Jin X, Hong S, Bahna F, Ahlsen G, Brasch J et al (2011) The extracellular architecture of adherens junctions revealed by crystal structures of type I cadherins. Struct 19(2):244–256CrossRefGoogle Scholar
  88. 88.
    Hartsock A, Nelson WJ (2008) Adherens and tight junctions: structure, function and connections to the actin cytoskeleton. Biochim Biophys Acta 1778(3):660–669PubMedCrossRefPubMedCentralGoogle Scholar
  89. 89.
    Straub BK, Rickelt S, Zimbelmann R, Grund C, Kuhn C, Iken M et al (2011) E-N-cadherin heterodimers define novel adherens junctions connecting endoderm-derived cells. J Cell Biol 195(5):873–887PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Coopman P, Djiane A (2016) Adherens junction and E-Cadherin complex regulation by epithelial polarity. Cell Mol Life Sci 73(18):3535–3553PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    Hoffmann B, Schäfer C (2010) Filopodial focal complexes direct adhesion and force generation towards filopodia outgrowth. Cell Adh Migr 4(2):190–193PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Vasioukhin V, Fuchs E (2001) Actin dynamics and cell-cell adhesion in epithelia. Curr Opin Cell Biol 13(1):76–84PubMedCrossRefPubMedCentralGoogle Scholar
  93. 93.
    Green KJ, Simpson CL (2007) Desmosomes: new perspectives on a classic. J Invest Dermatol 127(11):2499–2515PubMedCrossRefPubMedCentralGoogle Scholar
  94. 94.
    Waschke J (2008) The desmosome and pemphigus. Histochem Cell Biol 130(1):21–54PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Green KJ, Gaudry CA (2000) Are desmosomes more than tethers for intermediate filaments? Nat Rev Mol Cell Biol 1:208–216PubMedCrossRefPubMedCentralGoogle Scholar
  96. 96.
    Garrod D, Chidgey M (2008) Desmosome structure, composition and function. Biochim Biophys Acta 1778(3):572–587PubMedCrossRefPubMedCentralGoogle Scholar
  97. 97.
    Kitajima Y (2013) New insights into desmosome regulation and pemphigus blistering as a desmosome-remodeling disease. Kaohsiung J Med Sci 29(1):1–13PubMedCrossRefPubMedCentralGoogle Scholar
  98. 98.
    Sumigray KD, Lechler T (2012) Desmoplakin controls microvilli length but not cell adhesion or keratin organization in the intestinal epithelium. Mol Biol Cell 23(5):792–799PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Acehan D, Petzold C, Gumper I, Sabatini DD, Müller EJ, Cowin P, Stokes DL (2008) Plakoglobin is required for effective intermediate filament anchorage to desmosomes. J Invest Dermatol 128(11):2665–2675PubMedCrossRefPubMedCentralGoogle Scholar
  100. 100.
    Bornslaeger EA, Godsel LM, Corcoran CM, Park JK, Hatzfeld M, Kowalczyk AP, Green KJ (2001) Plakophilin 1 interferes with plakoglobin binding to desmoplakin, yet together with plakoglobin promotes clustering of desmosomal plaque complexes at cell-cell borders. J Cell Sci 114(Pt 4):727–738PubMedPubMedCentralGoogle Scholar
  101. 101.
    Holthöfer B, Windoffer R, Troyanovsky S, Leube RE (2007) Structure and function of desmosomes. Int Rev Cytol 264:65–163PubMedCrossRefPubMedCentralGoogle Scholar
  102. 102.
    Windoffer R, Borchert-Stuhlträger M, Leube RE (2002) Desmosomes: interconnected calcium-dependent structures of remarkable stability with significant integral membrane protein turnover. J Cell Sci 115(Pt 8):1717–1732PubMedPubMedCentralGoogle Scholar
  103. 103.
    Kowalczyk AP, Navarro P, Dejana E, Bornslaeger EA, Green KJ, Kopp DS, Borgwardt JE (1998) VE-cadherin and desmoplakin are assembled into dermal microvascular endothelial intercellular junctions: a pivotal role for plakoglobin in the recruitment of desmoplakin to intercellular junctions. J Cell Sci 111(Pt 20):3045–3057PubMedPubMedCentralGoogle Scholar
  104. 104.
    Hull BE, Staehelin LA (1979) The terminal web. A reevaluation of its structure and function. J Cell Biol 81(1):67–82PubMedCrossRefPubMedCentralGoogle Scholar
  105. 105.
    Brooke MA, Nitoiu D, Kelsell DP (2012) Cell-cell connectivity: desmosomes and disease. J Pathol 226(2):158–171PubMedCrossRefPubMedCentralGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Physiology, Faculty of Basic Medical SciencesCollege of Health Sciences, Nile University of NigeriaFCT-AbujaNigeria

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