Abstract
Invertebrate diversity and architecture is immense. This is achieved by the organization and function of four tissue types found in most metazoan phyla—epithelial, connective, muscle and nervous tissue. Epithelial tissue is found in all extant animals (parazoan and metazoan alike). Epithelial cells form cellular sheets that cover internal or external surfaces and regulate the passage of material between separated compartments. The transepithelial movement of biological material between compartments can occur across the transcellular pathway (i.e. across cells) or the paracellular pathway (i.e. between cells) and the latter is regulated by occluding junctions that typically link cells in a subapical domain. In this review, information on occluding junctions of invertebrate epithelia is consolidated and discussed in the context of morphology, ultrastructure and physiology. In addition, an overview of what is currently known about invertebrate occluding junction proteins and their role in maintaining the integrity of invertebrate epithelia and regulating the barrier properties of these tissues is presented.
Similar content being viewed by others
References
Adams EDM, Goss GG, Leys SP (2010) Freshwater sponges have functional, sealing epithelia with high transepithelial resistance and negative transepithelial potential. PLoS One 5(11):e15040
Adell T, Gamulin V, Perović-Ottstadt S, Wiens M, Korzhev M, Müller IM, Müller WE (2004) Evolution of metazoan cell junction proteins: the scaffold protein MAGI and the transmembrane receptor tetraspanin in the demosponge Suberites domuncula. J Mol Evol 59(1):41–50
Aguinaldo AM, Turbeville JM, Linford LS, Rivera MC, Garey JR, Raff RA, Lake JA (1997) Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387:489–493
Ahearn GA (1980) Intestinal electrophysiology and transmural ion transport in freshwater prawns. Am J Physiol 239(1):C1–C10
Aladin NV, Potts WTW (1995) Osmoregulatory capacity of the cladocera. J Comp Physiol B 164:671–683
Albrecht EA, Cavicchia JC (2001) Permeability barrier in the mantle epithelium lining the testis in the apple-snail Pomacea canaliculata (Gastropoda: Ampullariidae). Tissue Cell 33(2):148–153
Anderson JM, Van Itallie M (2009) Physiology and function of the tight junction. Cold Spring Harb Perspect Biol. doi:10.1101/a002584
Armenti ST, Nance J (2012) Adherens junctions in C. elegans embryonic morphogenesis. Subcell Biochem 60:279–299. doi:10.1007/978-94-007-4186-7_12
Asano A, Asano K, Sasaki H, Furuse M, Tsukita S (2003) Claudins in Caenorhabditis elegans: their distribution and barrier function in the epithelium. Curr Biol 13:1042–1046
Aschenbrenner S, Walz B (1998) Pleated septate junctions in leech photoreceptors: ultrastructure, arrangement of septa, gate and fence function. Cell Tissue Res 293(253):269
Bagby RM (1970) The fine structure of pinacocytes in the marine sponge Microciona prolifera (Ellis and Solander). Z Zellforsch 105:579–594
Bairati A, Gioria M (2008) An ultrastructural study of cell junctions and the cytoskeleton in epithelial cells of the molluscan integument. J Morphol 269(3):319–331
Baldwin KM, Hakim RS (1999) Evidence for high molecular weight proteins in arthropod gap and smooth septate junctions. Tissue Cell 31:195–201
Baltzegar DA, Reading BJ, Brune ES, Borski RJ (2013) Phylogenetic revision of the claudin gene family. Mar Genomics 11:17–26
Bartolomaeus T, Quast B (2005) Structure and development of nephridia in Annelida and related taxa. Hydrobiologia 535(536):139–165
Bartolomaeus T, Purschke G, Hausen H (2005) Polychaete phylogeny based on morphological data—a comparison of current attempts. Hydrobiologia 535/536:341–356
Baskin DG (1976) Fine structure of polychaete septate junctions. Cell Tissue Res 174:55–67
Bätz T, Förster D, Luschnig S (2014) The transmembrane protein macroglobulin complement-related is essential for septate junction formation and epithelial barrier function in Drosophila. Development 141(4):899–908. doi:10.1242/dev.102160
Baumgartner S, Littleton JT, Broadie K, Bhat MA, Harbecke R, Lengyel JA, Chiquet-Ehrismann R, Prokop A, Bellen HJ (1996) A Drosophila neurexin is required for septate junction and blood-nerve barrier formation and function. Cell 87:1059–1068
Beatty A, Morton D, Kemphues K (2010) The C. elegans homolog of Drosophila Lethal giant larvae functions redundantly with PAR-2 to maintain polarity in the early embryo. Development 137:3995–4004
Beatty A, Morton DG, Kemphues K (2013) PAR-2, LGL-1 and the CDC-42 GAP CHIN-1 act in distinct pathways to maintain polarity in the C. elegans embryo. Development 140(9):2005–2014. doi:10.1242/dev.088310
Behr M, Riedel D, Schuh R (2003) The claudin-like Megatrachea is essential in septate junctions for the epithelial barrier function in Drosophila. Dev Cell 5:611–620
Bénazet-Tambutté S, Allemand D, Jaubert J (1996) Permeability of the oral epithelial layers in cnidarians. Mar Biol 126:43–53
Beyenbach KW, Piermarini PM (2011) Transcellular and paracellular pathways of transepithelial fluid secretion in Malpighian (renal) tubules of the yellow fever mosquito Aedes aegypti. Acta Physiol (Oxf) 202:387–407. doi:10.1111/j.1748-1716.2010.02195.x
Bhat MA (2003) Molecular organization of axo-glial junctions. Curr Opin Neurobiol 13(5):552–559
Bilbaut A (1980) Cell junctions in the excitable epithelium of bioluminescent scales on a polynoid worm: a freeze-fracture and electrophysiological study. J Cell Sci 41:341–368
Bilder D (2004) Epithelial polarity and proliferation control: links from the Drosophila neoplastic tumor suppressors. Genes Dev 18:1909–1925
Bilder D, Perrimon N (2000) Localization of apical epithelial determinants by the basolateral PDZ protein Scribble. Nature 403:676–680
Bilder D, Li M, Perrimon N (2000) Cooperative regulation of cell polarity and growth by Drosophila tumor suppressors. Science 289(5476):113–116
Bleher R, Machado J (2004) Paracellular pathway in the shell epithelium of Anodonta cygnea. J Exp Zool A Comp Exp Biol 301(5):419–427
Boucaud-Camou E (1980) Junctional structures in digestive epithelia of a cephalopod. Tissue Cell 12(2):395–404
Boury-Esnault N, Ereskovsky A, Bezac C, Tokina D (2003) Larval development in the Homoscleromorpha (Porifera, Demospongiae). Invertebr Biol 122:187–202
Brauer EB (1975) Osmoregulation in the fresh water sponge, Spongilla lacustris. J Exp Zool 192:181–192
Brauer EB, McKanna JA (1978) Contractile vacuoles in cells of a fresh water sponge Spongilla lacustris. Cell Tissue Res 192:309–317
Bruce RG (1966) The fine structure of the intestine and hind gut of the larva of Trichinella spiralis. Parasitology 56:359–365
Brusca RC, Brusca GJ (1990) Invertebrates, 2nd edn. Sinauer Associates, Sunderland
Bullivant S, Loewenstein WR (1968) Structure of coupled and uncoupled cell junctions. J Cell Biol 37:621–632
Burghardt RC (1980) Intercellular junctions and exocytosis in the vas deferens of Ascaris. J Ultrastruct Res 71(2):162–172
Byri S, Misra T, Syed ZA, Batz T, Shah J, Boril L, Glashauser J, Aegerter-Wilmsen T, Matzat T, Moussian B, Luschnig S (2015) The triple-repeat protein anaconda controls epithelial tricellular junction formation in Drosophila. Dev Cell 33:535–548
Campbell RD, Iniguez AR, Iniguez AJ, Martinez DE (2013) Hydra of Hawaii: phylogenetic relationships with continental species. Hydrobiologia 713(1):199–205
Caveney S, Podgorski C (1975) Intercellular communication in a positional field. Ultrastructural correlates and tracer analysis of communication between insect epidermal cells. Tissue Cell 7(3):559–574
Cereijido M, Contreras RG, Shoshani L (2004) Cell adhesion, polarity, and epithelia in the dawn of metazoans. Physiol Rev 84:1229–1262
Chaparro OR, Montiel YA, Segura CJ, Cubillos VM, Thompson RJ, Navarro JM (2008) The effect of salinity on clearance rate in the suspension-feeding estuarine gastropod Crepipatella dilatata under natural and controlled conditions. Estuar Coast Shelf Sci 76:861–868
Chapman JA, Kirkness EF, Simakov O, Hampson SE, Mitros T, Weinmaier T, Rattei T, Balasubramanian PG, Borman J, Busam D, Disbennett K, Pfannkoch C, Sumin N, Sutton GG, Viswanathan LD, Walenz B, Goodstein DM, Hellsten U, Kawashima T, Prochnik SE, Putnam NH, Shu S, Blumberg B, Dana CE, Gee L, Kibler DF, Law L, Lindgens D, Martinez DE, Peng J, Wigge PA, Bertulat B, Guder C, Nakamura Y, Ozbek S, Watanabe H, Khalturin K, Hemmrich G, Franke A, Augustin R, Fraune S, Hayakawa E, Hayakawa S, Hirose M, Hwang JS, Ikeo K, Nishimiya-Fujisawa C, Ogura A, Takahashi T, Steinmetz PRH, Zhang X, Aufschnaiter R, Eder M-K, Gorny A-K, Salvenmoser W, Heimberg AM, Wheeler BM, Peterson KJ, Bottger A, Tischler P, Wolf A, Gojobori T, Remington KA, Strausberg RL, Venter JC, Technau U, Hobmayer B, Bosch TCG, Holstein TW, Fujisawa T, Bode HR, David CN, Rokhsar DS, Steele RE (2010) The dynamic genome of Hydra. Nature 464:592–596
Chasiotis H, Kolosov D, Bui P, Kelly SP (2012) Tight junctions, tight junction proteins and paracellular permeability across the gill epithelium of fishes: a review. Resp Physiol Neurobiol 184:269–281
Chaudhari SS, Arakane Y, Specht CA, Moussian B, Boyle DL, Park Y, Kramer KJ, Beeman RW, Muthukrishnan S (2011) Knickkopf protein protects and organizes chitin in the newly synthesized insect exoskeleton. PNAS 108(41):17028–17033
Coimbra J, Machado J (1988) Electrophysiology of the mantle of Anodonta cygnea. J Exp Biol 140:65–88
Costa M, Raich W, Agbunag C, Leung B, Hardin J, Priess JR (1998) A putative catenin-cadherin system mediates morphogenesis of the Caenorhabditis elegans embryo. J Cell Biol 141(1):297–308
Credland PF (1976) A structural study of the anal papillae of the midge Chironomus riparius Miegen (Diptera: Chironomidae). Cell Tissue Res 166(4):531–540
Dallai (1975) Continuous and gap junction in the midgut of Collembola as revealed by lanthanum tracer and freeze-etching techniques. J Submicr Cytol 7:249–257
Dallai R (1976) Septate and continuous junctions associated in the same epithelium. J Submicr Cytol 8:163–174
Dallai R, Bigliardi E, Lane NJ (1990) Intercellular junctions in myriapods. Tissue Cell 22(3):359–369
Danilova LV, Rokhlenko KD, Bodryagina AV (1969) Electron microscopic study on the structure of septate and comb desmosomes. Z Zellforsch Mikrosk Anat 100(1):101–117
Dan-Sohkawa M, Kaneko H, Noda K (1995) Paracellular, transepithelial permeation of macromolecules in the body wall epithelium of starfish embryos. J Exp Zool 271:264–272
Davidson LA (1983) A freeze fracture and thin section study of intestinal cell membranes and intercellular junctions of a nematode, Ascaris. Tissue Cell 15(1):27–37
Del Duca O, Nasirian A, Galperin V, Donini A (2011) Pharmacological characterisation of apical Na+ and Cl− transport mechanisms of the anal papillae in the larval mosquito, Aedes aegypti. J Exp Biol 214:3992–3999
Desser SS, Weller I (1977) Ultrastructural observations on the body wall of the leech, Batracobdella picta. Tissue Cell 9(1):35–42
Dietz TH, Byrne RA, Lynn JW, Silverman H (1995) Paracellular solute uptake by the freshwater zebra mussel Dreissena polymorpha. Am J Physiol 269(Pt 2):R300–R307
Dolmatov IY, Frolova LT, Zakharova EA, Ginanova TT (2011) Development of respiratory trees in the holothurians Apostichopus japonicas (Aspidochirotida: Holothuroidea). Cell Tissue Res 346(3):327–338. doi:10.1007/s00441-011-1280-9
Duperron S, Gaudron SM, Rodrigues CF, Cunha MR, Decker C, Olu K (2013) An overview of chemosynthetic symbioses in bivalves from the North Atlantic and Mediterranean Sea. Biogeosciences 10:3241–3267
Duvert M, Gros D (1982) Further studies on the junctional complex in the intestine of Sagitta setosa. Cell Tissue Res 225:663–671
Duvert M, Gros D, Salat C (1980) The junctional complex in the intestine of Sagitta setosa (Chaetognatha): the paired septate junction. J Cell Sci 42:227–246
Elias-Neto M, Soares MPM, Bitondi MG (2009) Changes in integument structure during the imaginal molt of the honey bee. Apidologie 40:29–39
Epstein ML, Gilula NB (1977) A study of communication specificity between cells in culture. J Cell Biol 75(3):769–787
Fahey B, Degnan BM (2010) Origin of animal epithelia: insights from the sponge genome. Evol Dev 12:601–617
Faivre-Sarrailh C, Banerjee S, Li J, Hortsch M, Laval M, Bhat MA (2004) Drosophila contactin, a homolog of vertebrate contactin, is required for septate junction organization and paracellular barrier function. Development 131:4931–4942
Farquhar MG, Palade GE (1963) Junctional complexes in various epithelia. J Cell Biol 17:375–412
Fautin DG (2009) Structural diversity, systematics, and evolution of cnidae. Toxicon 54(8):1054–1064
Fehon RG, Dawson IA, Artavanis-Tsakonas S (1994) A Drosophila homologue of membrane-skeleton protein 4.1 is associated with septate junctions and is encoded by the coracle gene. Development 120:545–557
Fei K, Yan L, Zhang J, Sarras MP Jr (2000) Molecular and biological characterization of a zonula occludens-1 homologue in Hydra vulgaris, named HZO-1. Dev Genes Evol 210(12):611–616
Fell PE, Knight P, Rieders W (1989) Low-salinity tolerance of and salinity-induced dormancy in the estuarine sponge Microciona prolifera (Ellis et Solander) under long-term laboratory culture. J Exp Mar Biol Ecol 133:195–211
Ferguson JC (1989) Rate of water admission through the madreporite of a starfish. J Exp Biol 145:147–156
Fiandra L, Casartelli M, Giordana B (2006) The paracellular pathway in the lepidopteran larval midgut: modulation by intracellular mediators. Comp Biochem Physiol A Mol Integr Physiol 144:464–473
Filshie BK, Flower NE (1977) Junctional structures in Hydra. J Cell Sci 23:151–172
Finol HJ, Croghan PC (1983) Ultrastructure of the branchial epithelium of an amphibious brackish-water crab. Tissue Cell 15(1):63–75
Fischer FP, Alger M, Ceislar D, Krafczyk H-U (1990) The chiton gill: ultrastructure in Chiton olivaceus (Mollusca, Polyplacophora). J Morphol 204:75–87
Flower NE (1971) Septate and gap junctions between the epithelial cells of an invertebrate, the mollusc Cominella maculosa. J Ultrastruct Res 37(3):259–268
Flower NE (1986) Sealing junctions in a number of arachnid tissues. Tissue Cell 18(6):899–913
Flower NE, Filshie BK (1975) Junctional structures in the midgut cells of lepidopteran caterpillars. J Cell Sci 17(1):221–239
Freire CA, Onken H, McNamara JC (2008) A structure-function analysis of ion transport in crustacean gills and excretory organs. Comp Biochem Physiol A 151:272–304
Froldi F, Ziosi M, Tomba G, Parisi F, Garoia F, Pession A, Grifoni D (2008) Drosophila lethal giant larvae neoplastic mutant as a genetic tool for cancer modeling. Curr Genomics 9:147–154
Funayama N (2010) The stem cell system in demosponges: insights into the origin of somatic stem cells. Dev Growth Differ 52:1–14
Funayama N (2013) The stem cell system in demosponges: suggested involvement of two types of cells: archeocytes (active stem cells) and choanocytes (food-entrapping flagellated cells). Dev Genes Evol 223:23–38
Furuse M, Tsukita S (2006) Claudins in occluding junctions of humans and flies. Trends Cell Biol 16:181–188
Ganot P, Zoccola D, Tambutté E, Voolstra CR, Aranda M, Allemand D, Tambutté S (2015) Structural molecular components of septate junctions in cnidarians point to the origin of epithelial junctions in eukaryotes. Mol Biol Evol 32(1):44–62. doi:10.1093/molbev/msu265
Genova JL, Fehon RG (2003) Neuroglian, Gliotactin, and the Na+/K+ ATPase are essential for septate junction function in Drosophila. J Cell Biol 161:979–989
Georges D (1979) Gap and tight junctions in tunicates. Study in conventional and freeze-fracture techniques. Tissue Cell 11(4):781–792
Gerencser G (1982) Paracellular transport characteristics of Aplysia Juliana intestine. Comp Biochem Physiol A 72(4):721–725
Gilbert MM, Auld VJ (2005) Evolution of clams (cholinesterase-like adhesion molecules): structure and function during development. Front Biosci 10:2177–2192
Gilula NB, Branton D, Satir P (1970) The septate junction: a structural basis for intercellular coupling. Proc Natl Acad Sci USA 67(1):213–220
Ginzberg RD, Morales EA, Spray DC, Bennett MVL (1985) Cell junctions in early embryos of squid (Loligo pealei). Cell Tissue Res 239:477–484
Giribet G, Edgecombe GD (2013) The Arthropoda: A phylogenetic framework. In: Minelli A, Boxshall G, Fusco G (eds) Arthropod biology and evolution—molecules, development, morphology. Springer, Heidelberg, pp 17–40
Giuliani C, Troglio F, Bai Z, Patel FB, Zucconi A, Malabarba MG, Disanza A, Stradal TB, Cassata G, Confalonieri S, Hardin JD, Soto MC, Grant BD, Scita G (2009) Requirements for F-BAR proteins TOCA-1 and TOCA-2 in actin dynamics and membrane trafficking during Caenorhabditis elegans oocyte growth and embryonic epidermal morphogenesis. PLoS Genet 5:e1000675. doi:10.1371/journal.pgen.1000675
Giusti F (1976) Tubular structures in the septate junction of a Gastropod. J Microsc Biol Cell 26:65–68
Gomez-Mendikute A, Elizondo M, Venier P, Cajaraville MP (2005) Characterization of mussel gill cells in vivo and in vitro. Cell Tissue Res 321:131–140
Gomme J (1981) D-Glucose transport across the apical membrane of the surface epithelium in Nereis diversicolor. J Membr Biol 62(1–2):29–46
Graf FC, Noirot-Timothée C, Noirot CH (1982) The specialization of septate junctions in regions of tricellular junctions. I. Smooth septate junctions (=continuous junctions). J Ultrastruct Res 78:136–151
Green CR (1981a) A clarification of the two types of invertebrate pleated septate junction. Tissue Cell 13(1):173–188
Green CR (1981b) A variation of the smooth septate junction in sea spiders (Pycnogonida). Tissue Cell 13(1):189–195
Green CR (1981c) Fixation-induced intramembrane particle movement demonstrated in freeze-fracture replicas of a new type of septate junction in echinoderm epithelia. J Ultrastruct Res 75:11–22
Green CR, Bergquist PR (1979) Cell membrane specialisations in the Porifera. Colloq Int Cent Natl Rech Sci Biol des Spongiaires 291:153–158
Green CR, Bergquist PR (1982) Phylogentic relationships within the invertebrates in relation to the structure of septate junctions and the development of ‘occluding’ junctional types. J Cell Sci 53:279–305
Green CR, Flower NE (1980) Two new septate junctions in the phylum Coelenterata. J Cell Sci 42:43–59
Green CR, Bergquist PR, Bullivant S (1979) An anastomosing septate junction in endothelial cells of the phylum echinodermata. J Ultrastruct Res 68(1):72–80
Green LF, Bergquist PR, Bullivant S (1980) The structure and function of the smooth septate junction in a transporting epithelium: the Malpighian tubules of the New Zealand glow-worm Arachnocampa luminosa. Tissue Cell 12(2):365–381
Green CR, Noirot-Timothee C, Noirot C (1983) Isolation and characterization of invertebrate smooth septate junctions. J Cell Sci 62:351–370
Günzel D, Fromm M (2012) Claudins and other tight junction proteins. Compr Physiol 2:1819–1852. doi:10.1002/cphy.c110045
Günzel D, Yu ASL (2013) Claudins and the modulation of tight junction permeability. Physiol Rev 93:525–569. doi:10.1152/physrev.00019.2012
Halcrow K (1976) The fine structure of the carapace integument of Daphnia magna Straus (Crustacea Branchiopoda). Cell Tissue Res 169(2):267–276
Hall S, Bone C, Oshima K, Zhang L, McGraw M, Lucas B, Fehon RG, Ward RE 4th (2014) Macroglobulin complement-related encodes a protein required for septate junction organization and paracellular barrier function in Drosophila. Development 141(4):889–898. doi:10.1242/dev.102152
Hand AR, Gobel S (1972) The structural organization of the septate and gap junctions of Hydra. J Cell Biol 52(2):397–408
Hanrahan JW (1984) Ionic permeability of insect epithelia. Am Zool 24:229–240
Harrison FW (1972) The nature and role of the basal pinacoderm of Corvomeyenia carolinensis Harrison (Porifera: Spongillidae): A histochemical and developmental study. Hydrobiologia 39(4):495–508
Haszpruner G, Wanninger A (2012) Molluscs. Curr Biol 22(13):R510–R514
Herrera FC, Herrera MI, Lopez I (2000) Further studies on the partial double Donnan. Is isosmotic KCl solution isotonic with cells of respiratory trees of the holothurian Isostichopus badionotus Selenka? J Exp Mar Biol Ecol 247:139–152
Hijazi A, Masson W, Augé B, Waltzer L, Haenlin M, Roch F (2009) boudin is required for septate junction organisation in Drosophila and codes for a diffusible protein of the Ly6 superfamily. Development 136:2199–2209
Hildebrandt A, Pflanz R, Behr M, Tarp T, Riedel D, Schuh R (2015) Bark beetle controls epithelial morphogenesis by septate junction maturation in Drosophila. Dev Biol 400(2):237–247. doi:10.1016/j.ydbio.2015.02.008
Hohagen J, Jackson DJ (2013) An ancient process in a modern mollusc: early development of the shell in Lymnaea stagnalis. BMC Dev Biol 13:27
Holley MC (1985) Changes in the distribution of filament-containing septate junctions as coelenterate myoepithelial cells change shape. Tissue Cell 17(1):1–11
Hori I (1985) A fine structural analysis of the planarian septate junction using ruthenium red staining. J Electron Microsc 34(4):422–426
Hori I (1987) Formation of the septate junction in regenerating planarian gastrodermis. J Morphol 192(205):215
Hortsch M, Margolis B (2003) Septate and paranodal junctions: kissing cousins. Trends Cell Biol 13:557–561
Hudspeth AJ, Revel JP (1971) Coexistence of gap and septate junctions in an invertebrate epithelium. J Cell Biol 50:92–101
Itza EM, Mozingo NM (2005) Septate junctions mediate the barrier to paracellular permeability in sea urchin embryos. Zygote 13(3):255–264
Izumi Y, Furuse M (2014) Molecular organization and function of invertebrate occluding junctions. Semin Cell Dev Biol 36:186–193
Izumi Y, Yanagihashi Y, Furuse M (2012) A novel protein complex, Mesh-Ssk, is required for septate junction formation in the Drosophila midgut. J Cell Sci 125:4923–4933
Jamuar MP (1966) Cytochemical and electron microscope studies on the pharynx and intestinal epithelium of Nippostrongylus brasiliensis. J Parasitol 52:1116–1128
Jarial MS, Kelly-Worden M (2011) Additional ultrastructural observations of the first segments of Malpighian tubules in Cenocorixa bifida (Hemiptera: Corixidae) in relation to reabsorption of solutes. Ann Entomol Soc Am 104(4):768–777. doi:10.1603/AN10055
Jaspers MH, Nolde K, Behr M, Joo SH, Plessmann U, Nikolov M, Urlaub H, Schuh R (2012) The claudin Megatrachea protein complex. J Biol Chem 287:36756–36765
Jesaitis LA, Goodenough DA (1994) Molecular characterization and tissue distribution of ZO-2, a tight junction protein homologous to ZO-1 and the Drosophila discs-large tumor suppressor protein. J Cell Biol 124:949–961
Johnson KE, Perreau L, Charmantier G, Charmantier-Daures M, Lee E (2014) Without gills. Localization of osmoregulatory function in the copepod Eurytemora affinis. Physiol Biochem Zool 87(2):310–324
Josephson RK, Macklin M (1967) Transepithelial potentials in Hydra. Science 156(3782):1629–1631
Josephson RK, Macklin M (1969) Electrical properties of the body wall of Hydra. J Gen Physiol 53:638–665
Juberthie-Jupeu L (1979) Cellular junctions of the midgut in the centipede (Scutigerella pagesi) as revealed by lanthanum tracer and freeze fracture technique. Tissue Cell 11(2):317–323
Kachar B, Christakis NA, Reese TS (1986) The intramembrane structure of septate junctions based on direct freezing. J Cell Sci 80:13–28
Kamenev YO, Dolmatov IY, Frolova LT, Khang NA (2013) The morphology of the digestive tract and respiratory organs of the holothurians Cladolabes schmeltzii (Holothuroidea, Dendrochirotida). Tissue Cell 45:126–139
Khan HR, Saleuddin AS (1981) Cell contacts in the kidney epithelium of Helisoma (Mollusca: Gastropoda)—effects of osmotic pressure and brain extracts: a freeze-fracture study. J Ultrastruct Res 75(1):23–40
Khanna DR, Yadav PR (2005) Biology of Echinodermata. Discovery Publishing House, New Delhi
Knust E, Bossinger O (2002) Composition and formation of intercellular junctions in epithelial cells. Science 298:1955–1959
Kolosov D, Bui P, Chasiotis H, Kelly SP (2013) Claudins in teleost fishes. Tissue Barrier 1:e25391
Kraeuter JN, Setzler EM (1975) The seasonal cycle of scyphozoan and cubozoa in Georgia estuaries. Bull Mar Sci 25(1):66–74
Krumm S, Goebel-Lauth SG, Fronius M, Clauss W (2005) Transport of sodium and chloride across earthworm skin in vitro. J Comp Physiol B 175:601–608
Kukulies J, Komnick H (1983) Plasma membranes, cell junctions and cuticle of the rectal chloride epithelia of the larval dragonfly Aeshna cyanea. J Cell Sci 59:159–182
Kumar KPR (2013) Malpighian tubules of adult flesh fly, Sarcophaga ruficornis Fab. (Diptera: Sarcophagidae): an ultrastructural study. Tissue Cell 45:312–317
Kӧeppen M, Simske JS, Sims PA, Firestein BL, Hall DH, Radice AD, Rongo C, Hardin JD (2001) Cooperative regulation of AJM-1 controls junctional integrity in Caenorhabditis elegans epithelia. Nat Cell Biol 3:983–991
Lake J, Kelly DE (1970) Septate junctions in the gastrodermal epithelium of Phialidium: a fine structural study utilizing ruthenium red. Tissue Cell 2(3):435–441
Lamb RS, Ward RE, Schweizer L, Fehon RG (1998) Drosophila coracle, a member of the protein 4.1 superfamily, has essential structural functions in the septate junctions and developmental functions in embryonic and adult epithelial cells. Mol Cell Biol 9:3505–3519
Lane NJ (1979) Tight junctions in a fluid-transporting epithelium of an insect. Science 204:91–93
Lane NJ, Dilworth (1989) Isolation and biochemical characterization of septate junctions: differences between the proteins in smooth and pleated varieties. J Cell Sci 93:123–131
Lane NJ, Harrison JB (1978) An unusual type of continuous junction in Limulus. J Ultrastruct Res 64:85–97
Lane NJ, Skaer HB (1980) Intercellular junctions in insect tissues. In: Berridge MJ, Treherne JE, Wigglesworth VB (eds) Advances in insect physiology, vol 15. Academic Press, London, pp 35–213
Lane NJ, Dallai R, Burighel P, Martinucci GB (1986) Tight and gap junctions in the intestinal tract of tunicates (Urochordata): a freeze-fracture study. J Cell Sci 84:1–17
Lane NJ, Campiglia SS, Lee WM (1994) Junctional types in the tissues of an onychophoran: the apparent lack of gap and tight junctions in Peripatus. Tissue Cell 26(1):143–154
Lange R (1964) The osmotic adjustment in the echinoderm, Strongylocentrotus droebachiensis. Comp Biochem Physiol 13:205–216
Laval M, Bel C, Faivre-Sarrailh C (2008) The lateral mobility of cell adhesion molecules is highly restricted at septate junctions in Drosophila. BMC Cell Biol 9:38. doi:10.1186/1471-2121-9-38
Ledger PW (1975) Septate junctions in the calcareous sponge Sycon ciliatum. Tissue Cell 7:13–18
Legg DA, Sutton MD, Edgecombe GD (2013) Arthropod fossil data increase congruence of morphological and molecular phylogenies. Nat Commun 4:2485
Legouis R, Gansmuller A, Sookhareea S, Bosher JM, Baillie DL, Labouesse M (2000) LET-413 is a basolateral protein required for the assembly of adherens junctions in Caenorhabditis elegans. Nat Cell Biol 2:415–422
Leik J, Kelly DE (1970) Septate junctions in the gastrodermal epithelium of Phialidium: a fine structural study utilizing ruthenium red. Tissue Cell 2(3):435–441
Lethias C, Garrone R, Mazzorana M (1983) Fine structures of sponge cell membranes: comparative study with freeze-fracture and conventional thin section methods. Tissue Cell 15(4):523–535
Leung B, Hermann GJ, Priess JR (1999) Organogenesis of the Caenorhabditis elegans intestine. Dev Biol 216(1):114–134
Leys SP, Hill A (2012) The physiology and molecular biology of sponge tissues. In: Becerro MA, Uriz MJ, Maldonado M, Turon X (eds) Advances in marine biology, vol 62. Academic Press, London, pp 1–56
Leys SP, Riesgo A (2012) Epithelia, an evolutionary novelty of metazoans. J Exp Zool Mol Dev Evol 318B:438–447
Leys SP, Nichols SA, Adams EDM (2009) Epithelia and integration in sponges. Integr Comp Biol 49:167–177
Llimargas M, Strigini M, Katidou M, Karagogeos D, Casanova J (2004) Lachesin is a component of a septate junction-based mechanism that controls tube size and epithelial integrity in the Drosophila tracheal system. Development 131:181–190
Locke M (1965) The structure of septate desmosomes. J Cell Biol 25:166–169
Lockwood C, Zaidel-Bar R, Hardin J (2008) The C. elegans zonula occludens ortholog cooperates with the cadherin complex to recruit actin during morphogenesis. Curr Biol 18(17):1333–1337. doi:10.1016/j.cub.2008.07.086
Loewenstein WR, Kanno Y (1964) Studies on an epithelial (gland) cell junction. I. Modifications of surface membrane permeability. J Cell Biol 22:565–586
Loh YH, Christoffels A, Brenner S, Hunziker W, Venkatesh B (2004) Extensive expansion of the claudin gene family in the teleost fish, Fugu rubripes. Genome Res 14:1248–1257
Lord BA, DiBona DR (1976) Role of the septate junction in the regulation of paracellular transepithelial flow. J Cell Biol 71(3):967–972
Luquet C, Pellerano G, Rosa G (1997) Salinity-induced changes in the fine structure of the gills of the semiterrestrial estuarian crab, Uca uruguayensis (Nobili, 1901) (Decapoda, Ocypodidae). Tissue Cell 29:495–501
Luquet CM, Genovese G, Rosa GA, Pellerano GN (2002) Ultrastructural changes in the gill epithelium of the crab Chasmagnathus granulates (Decapoda: Grapsidae) in diluted and concentrated seawater. Mar Bio 141:753–760
Ma L, Gu S-H, Liu Z-W, Wang S-N, Guo Y-Y, Zhou J-J, Zhang Y-J (2014) Molecular characterization and expression profiles of olfactory receptor genes in parasitic wasp, Microplitis mediator (Hymenoptera: Braconidae). J Insect Physiol 60:118–126
Mackie GO, Singla CL (1983) Studies on hexactinellid sponges. I Histology of Rhabdocalyptus dawsoni (Lambe, 1873). Philos Trans R Soc Lond B 301:365–400
Maldonado M, Riesgo A (2008) Reproductive output in a Mediterranean population of the homosclerophorid Corticium candelabrum (Porifera, Demospongiae), with notes on the ultrastructure and behavior of the larva. Mar Ecol 29:298–316
Manconi R, Pronzato R (2008) Global diversity of sponges (Porifera: Spongillina) in freshwater. Hydrobiologia 595:27–33
Mashanov VS, Garcia-Arraras JE (2011) Gut regeneration in holothurians: a snapshot of recent developments. Biol Bull 221:93–109
Mather JA, Kuba MJ (2013) The cephalopod specialties: complex nervous system, learning, and cognition. Can J Zool 91(6):431–449
McHugh D (2000) Molecular phylogeny of the Annelida. Can J Zool 78:1873–1884
McMahon L, Legouis R, Vonesch JL, Labouesse M (2001) Assembly of C. elegans apical junctions involves positioning and compaction by LET-413 and protein aggregation by the MAGUK protein DLG-1. J Cell Sci 114:2265–2277
Michaux G, Legouis R, Labouesse M (2001) Epithelial biology: lessons from Caenorhabditis elegans. Gene 277(1–2):83–100
Morris S (2011) Neuroendocrine regulation of osmoregulation and the evolution of air breathing in decapod crustaceans. J Exp Biol 204:979–989
Narasimha M, Uv A, Krejci A, Brown NH, Bray SJ (2008) Grainy head promotes expression of septate junction proteins and influences epithelial morphogenesis. J Cell Sci 6:747–752. doi:10.1242/jcs.019422
Neff JM (1972) Ultrastructure of the outer epithelium of the mantle in the clam Mercenaria mercenaria in relation to calcification of the shell. Tissue Cell 4(4):591–600
Nelson KS, Furuse M, Beitel GJ (2010) The Drosophila claudin Kune-kune is required for septate junction organization and tracheal tube size control. Genetics 185:831–839
Newell PF, Skelding JM (1973) Structure and permeability of the septate junction in the kidney sac of Helix pomatia L. Z Zellforsch 147:31–39
Nguyen H, Donini A (2010) Larvae of the midge possess two distinct mechanisms for ionoregulation in response to ion-poor conditions. Am J Physiol 299:R762–R773
Nichols SA, Dirks W, Pearse JS, King N (2006) Early evolution of animal cell signaling and adhesion genes. Proc Natl Acad Sci USA 103:12451–12456
Nilton A, Oshima K, Zare F, Byri S, Nannmark U, Nyberg KG, Fehon RG, Uv AE (2010) Crooked, coiled and crimpled are three Ly6-like proteins required for proper localization of septate junction components. Development 137:2427–2437
Noirot-Timothee C, Noirot C (1980) Septate and scalariform junctions in arthropods. Int Rev Cytol 63:97–141
Noirot-Timothee C, Smith DS, Cayer ML, Noirot C (1978) Septate junctions in insects: comparison between intercellular and intramembranous structures. Tissue Cell 10(1):125–136
O’Doherty H, Stark RJ (1981) Transmembrane and transepithelial movement of calcium during stimulus-secretion coupling. Am J Physiol 2:G150–G158
O’Donnell MJ, Maddrell SH, Gardiner BO (1984) Passage of solutes through walls of Malpighian tubules of Rhodnius by paracellular and transcellular routes. Am J Physiol 246:R759–R769
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 124:2861–2871
Overton J (1963) Intercellular connections in the outgrowing stolon of Cordylophora. J Cell Biol 17(3):661–671
Padash-Barmchi M, Browne K, Sturgeon K, Jusiak B, Auld VJ (2010) Control of Gliotactin localization and levels by tyrosine phosphorylation and endocytosis is necessary for survival of polarized epithelia. J Cell Sci 123:4052–4062. doi:10.1242/jcs.066605
Padash-Barmchi M, Charish K, Que J, Auld VJ (2013) Gliotactin and Discs large are co-regulated to maintain epithelial integrity. J Cell Sci 126:1134–1143. doi:10.1242/jcs.113803
Pannabecker TL, Hayes TK, Beyenbach KW (1993) Regulation of epithelial shunt conductance by the peptide leucokinin. J Membr Biol 132:63–76
Paul SM, Palladino MJ, Beitel GJ (2007) A pump-independent function of the Na, K-ATPase is required for epithelial junction function and tracheal tube-size control. Development 134:147–155
Pavans de Ceccatty (1986) Cytoskeletal organization and tissue patterns of epithelia in the sponge Ephydatia mülleri. J Morphol 189:45–65
Pespeni MH, Barney BT, Palumbi SR (2013) Differences in the regulation of growth and biomineralization genes revealed through long-term common-garden acclimation and experimental genomics in the prupple sea urchin. Evolution 67(7):1901–1914
Pettitt J, Cox EA, Broadbent ID, Flett A, Hardin J (2003) The Caenorhabditis elegans p120 catenin homologue, JAC-1, modulates cadherin-catenin function during epidermal morphogenesis. J Cell Biol 162:15–22
Phillips JE, Meredith J, Audsley N, Richardson N, Macins A, Ring M (1998) Locust ion transport peptide (ITP): a putative hormone controlling water and ionic balance in terrestrial insects. Am Zool 38:461–470
Poddubnaya LG, Levron C, Gibson DI (2011) Ultrastructural characteristics of the uterine epithelium of aspidogastrean and digenean trematodes. Acta Parasitol 56(2):131–139
Poddubnaya LG, Xylander WER, Gibson DI (2012) Ultrastructural characteristics of the protonephridial terminal organ and associated ducts of adult specimens of the Aspidogastrea, Digenea and Monogenea, with comments on the relationships between these groups. Syst Parasitol 82:89–104
Poirrier MA (1974) Ecomorphic variation in gemmoscleres of Ephydatia fluviatilis Linnaeus (Porifera: Spongillidae) with comments upon its systematic and ecology. Hydrobiologia 44(4):337–347
Porvaznik M, Ribas JL, Parker JL (1979) Rhombic particle arrays in gill epithelium of a mollusc, Aplysia californica. Tissue Cell 11(2):337–344
Primo AL, Marques SC, Falcao J, Crespo D, Pardal MA, Azeiteiro UM (2012) Environmental forcing on jellyfish communities in a small temperate estuary. Mar Environ Res 79:152–159
Prior DJ, Uglem GL (1984) Analysis of contact-rehydration in terrestrial gastropods: absorption of 14C-inulin through the epithelium of the foot. J Exp Biol 111:75–80
Prosser CL (1967) Ionic analysis and effects of ions on contractions of sponge tissues. Z Vergl Physiol 54:109–120
Prusch RD (1977) Solute secretion by the tubefoot epithelium in the starfish Asterias forbesi. J Exp Biol 68:35–43
Purschke G (2002) On the ground pattern of Annelida. Org Divers Evol 2:181–196
Reise Sousa C, Howard JE, Hartley R, Earley FGP, Djamgoz MBA (1993) An insect epidermal cell line (UMBGE-4): structural and electrophysiological characterization. Comp Biochem Physiol A 106(4):759–767
Rose B (1971) Intercellular communication and some structural aspects of membrane junctions in a simple cell system. J Membr Biol 5(1):1–19. doi:10.1007/BF01870823
Sakarya O, Armstrong KA, Adamska M, Adamski M, Wang IF, Tidor B, Degnan BM, Oakley TH, Kosik KS (2007) A post-synaptic scaffold at the origin of the animal kingdom. PLoS ONE 2(6):e506
Satir P, Gilula NB (1970) The cell junction in a lamellibranch gill ciliated epithelium: localization of pyroantimonate precipitate. J Cell Biol 47(2):468–487
Schipp R, Mollenhauer S, von Boletzky S (1979) Electron microscopical and histochemical studies of differentiation and function of the cephalopod gill (Sepia officinalis L.) Zoomorph 93:193–207.
Schnizler M, Krumm S, Clauss W (2002) Annelid epithelia as models for electrogenic Na+ transport. Biochim Biophys Acta 1566(1–2):84–91
Schockaert ER, Hooge M, Sluys R, Schilling S, Tyler S, Artois T (2008) Global diversity of free living flatworms (Platyhelminthes, “Turbellaria”) in freshwater. Hydrobiologia 595:41–48
Schulte J, Tepass U, Auld VJ (2003) Gliotactin, a novel marker of tricellular junctions, is necessary for septate junction development in Drosophila. J Cell Biol 161(5):991–1000
Schulte J, Charish K, Que J, Ravn S, MacKinnon C, Auld VJ (2006) Gliotactin and Discs large form a protein complex at the tricellular junction of polarized epithelial cells in Drosophila. J Cell Sci 119:4391–4401
Segbert C, Johnson K, Theres C, van Fü-rden D, Bossinger O (2004) Molecular and functional analysis of apical junction formation in the gut epithelium of Caenorhabditis elegans. Dev Biol 266:17–26
Shanbhag S, Tripathi S (2009) Epithelial ultrastructure and cellular mechanisms of acid base transport in the Drosophila midgut. J Exp Biol 212:1731–1744
Shivers RR, Chauvin WJ (1977) Intercellular junctions of antennal gland epithelial cells in the crayfish, Orconectes virilis. A freeze-fracture study. Cell Tissue Res 175(4):425–438
Simske JS, Hardin J (2011) Claudin family proteins in Caenorhabditis elegans. Methods Mol Biol 762:147–169. doi:10.1007/978-1-61779-185-7_11
Simske JS, Köppen M, Sims P, Hodgkin J, Yonkof A, Hardin J (2003) The cell junction protein VAB-9 regulates adhesion and epidermal morphology in C. elegans. Nat Cell Biol 5:619–625
Skaer HB, Maddrell SH (1987) How are invertebrate epithelia made tight? J Cell Sci 88:139–141
Skaer HB, Harrison JB, Lee WM (1979) Topographical variations in the structure of the smooth septate junction. J Cell Sci 37:373–389
Skaer HB, Maddrell SH, Harrison JB (1987) The permeability properties of septate junctions in Malpighian tubules of Rhodnius. J Cell Sci 88:251–265
Skelding JM (1973a) The fine structure of the kidney sac of Achatina achatina (L.). Z Zellforsch Mikrosk Anat 147(1):1–29
Skelding JM (1973b) Studies on the renal physiology of Achatina achatina (L.). Malacologia 14:93–96
Spiegel E, Howard L (1983) Development of cell junctions in sea urchin embryos. J Cell Sci 62:27–48
Staehelin LA (1974) Structure and function of intercellular junctions. Int Rev Cytol 39:191–283
Stetak A, Hajnal A (2011) The C. elegans MAGI-1 protein is a novel component of cell junctions that is required for junctional compartmentalization. Dev Biol 350:24–31
Storch V, Welsch U (1977) Septate junctions in the cephalic epidermis of turbellarians (Bipalium). Cell Tissue Res 184:423–425
Strand D, Raska I, Mechler BM (1994) The Drosophila lethal giant larvae tumor suppressor protein is a component of the cytoskeleton. J Cell Biol 127:1345–1360
Suderman RJ, Andersen SO, Hopkins TL, Kanost MR, Kramer KJ (2003) Characterization and cDNA cloning of three major proteins from pharate pupal cuticle of Manduca sexta. Insect Biochem Mol Biol 33:331–343
Sugahara T, Yamashita Y, Shinomi M, Yamanoha B, Iseki H, Takeda A, Okazaki Y, Hayashizaki Y, Kawai K, Suemizu H, Andoh T (2007) Isolation of a novel mouse gene, mSVS-1/SUSD2, reversing tumorigenic phenotypes of cancer cells in vitro. Cancer Sci 98(6):900–908
Tambutté E, Tambutté S, Segonds N, Zoccola D, Venn A, Erez J, Allemand D (2012) Calcein labelling and electrophysiology: insights on coral tissue permeability and calcification. Proc Biol Sci 279(1726):19–27. doi:10.1098/rspb.2011.0733
Tepass U, Tanentzapf G, Ward R, Fehon R (2001) Epithelial cell polarity and cell junctions in Drosophila. Annu Rev Genet 35:747–784
Tiklová K, Senti KA, Wang S, Gräslund A, Samakovlis C (2010) Epithelial septate junction assembly relies on melanotransferrin iron binding and endocytosis in Drosophila. Nat Cell Biol 12:1071–1077
Tyler S (2003) Epithelium – the primary building block for metazoan complexity. Integr Comp Biol 43:55–63
Tyler S, Hooge M (2004) Comparative morphology of the body wall in flatworms (Platyhelminthes). Can J Zool 82:194–210
Tyler S, Tyler MS (1997) Origin of the epidermis in parasitic Platyhelminthes. Int J Parasitol 27(6):715–738
Uglem GL, Just JJ (1983) Trypsin inhibition by tapeworms: antienzyme secretion or pH adjustment? Science 220:79–81
Uglem GL, Prior DJ, Hess SD (1985) Paracellular water uptake and molecular sieving by the foot epithelium of terrestrial slugs. J Comp Physiol B 156:285–289
Van Soest RWM, Boury-Esnault N, Vacelet J, Dohrmann M, Erpenbeck D, De Voogd NJ, Santodomingo N, Vanhoorne B, Kelly M, Hooper JNA (2012) Global diversity of sponges. PLoS One 7(4):e35105
Vanderveken M, O’Donnell MJ (2014) Effects of diuretic hormone 31, drosokinin and allatostatin A on transepithelial K+ transport and contraction frequency in the midgut and hindgut of larval Drosophila melanogaster. Arch Insect Biochem Physiol 85:76–93
Vernet G, Rué G, Gontcharoff M (1979) Studies on the technique of impregnation with lanthanum and the ultrastructure of the body wall epithelium of Lineus ruber (heteronemertine). J Ultrastruct Res 67(2):225–227
Vidolin D, Santos-Gouvea IA, Freire CA (2002) Osmotic stability of the coelomic fluids of a sea cucumber (Holothuria grisea) and a starfish (Asterina stellifera) (Echinodermata) exposed to the air during low tide: a field study. Acta Biol Par 31(1–4):113–121
Ward RE, Lamb RS, Fehon RG (1998) A conserved functional domain of Drosophila Coracle is required for localization at the septate junction and has membrane-organizing activity. J Cell Biol 140:1463–1473
Welsch U, Buchheim W (1977) Freeze fracture studies on the annelid septate junction. Cell Tissue Res 185:527–534
Westermann B, Schipp R (1998) Morphology and histology of the digestive tract of Nautilus pompilius and Nautilus macromphalus (Cephalopoda, Tetrabranchiata). Zoomorphology 117:237–245
Westheide W (1997) The direction of evolution within the Polychaeta. J Nat His 31:1–15
Wolff T (2005) Composition and endemism of the deep-sea hydrothermal vent fauna. Cah Biol Mar 46:97–104
Wood RL (1959) Intercellular attachment in the epithelium of Hydra as revealed by electron microscopy. J Biophys Biochem Cytol 6:343–352
Woods DF, Bryant PJ (1991) The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell 66:451–464
Woods DF, Hough C, Peel D, Callaini G, Bryant PJ (1996) Dlg protein is required for junction structure, cell polarity, and proliferation control in Drosophila epithelia. J Cell Biol 134:1469–1482
Woods DF, Wu JW, Bryant PJ (1997) Localization of proteins to the apico-lateral junctions of Drosophila epithelia. Dev Genet 20(2):111–118
Wright JC, Luke BM (1989) Ultrastructural and histochemical investigations of Peripatus integument. Tissue Cell 21(4):605–625
Wright KA, Lee DL, Shivers RR (1985) A freeze-fracture study of the digestive tract of the parasitic nematode Trichinella. Tissue Cell 17(2):189–198
Wu VM, Schulte J, Hirschi A, Tepass U, Beitel GJ (2004) Sinuous is a Drosophila claudin required for septate junction organization and epithelial tube size control. J Cell Biol 164:313–323
Wu VM, Yu MH, Paik R, Banerjee S, Liang Z, Paul SM, Bhat MA, Beitel GJ (2007) Drosophila Varicose, a member of a new subgroup of basolateral MAGUKs, is required for septate junctions and tracheal morphogenesis. Development 134:999–1009
Xué L, Dallai R (1992) Cell junctions in the gut of Protura. Tissue Cell 24(1):51–59
Yanagihashi Y, Usui T, Izumi Y, Yonemura S, Sumida M, Tsukita S, Uemura T, Furuse M (2012) Snakeskin, a membrane protein associated with smooth septate junctions, is required for intestinal barrier function in Drosophila. J Cell Sci 125:1980–1990
Yu MJ, Beyenbach KW (2001) Leucokinin and the modulation of the shunt pathway in Malpighian tubules. J Insect Physiol 47:263–276
Yu MJ, Beyenbach KW (2002) Leucokinin activates Ca2+-dependent signal pathway in principal cells of Aedes aegypti Malpighian tubules. Am J Physiol 283:F499–F508
Zaidel-Bar R, Joyce MJ, Lynch AM, Witte K, Audhya A, Hardin J (2010) The F-BAR domain of SRGP-1 facilitates cell–cell adhesion during C. elegans morphogenesis. J Cell Biol 191:761–769. doi:10.1083/jcb.201005082
Zerbst-Boroffka I, Bazin B, Wenning A (1997) Chloride secretion drives urine formation in leech nephridia. J Exp Biol 16:2217–2227
Zheng H, Dietz TH (1998) Paracellular solute uptake in the freshwater bivalves Corbicula fluminea and Toxolasma texasensis. Biol Bull 194:170–177
Zhu W, Vandingenem A, Huybrechts R, Vercammen T, Baggerman G, De Loof A, Poulos CP, Valentza A, Breuer M (2001) Proteolitic breakdown of the Neb-trypsin modulating oostatic factor (Neb-TMOF) in the haemolymph of different insects and its gut epithelial transport. J Insect Physiol 47:1235–1242
Acknowledgments
AD and SPK are funded by Natural Sciences and Engineering Research Council (NSERC) discovery grants. SJ is supported by an Ontario Graduate Scholarship.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by I.D. Hume.
Rights and permissions
About this article
Cite this article
Jonusaite, S., Donini, A. & Kelly, S.P. Occluding junctions of invertebrate epithelia. J Comp Physiol B 186, 17–43 (2016). https://doi.org/10.1007/s00360-015-0937-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-015-0937-1