Biol Cell (1995) 83, 61-68 0 Elsevier, Paris 61 Original article Distribution of actin microfilaments in frog skin epithelial granular cells Kuang-Yi Chou, Willem J Els Department of Anatomy and Cell Biology, University of Cape Town Medical School, Observatory 7925, South Africa (Received 27 January 1995; accepted 7 March 1995) Summary - Microfilaments were localised by … (2003) 22:101–10. This focus is paramount since mucosal epithelia are more prone to pathogen attack, such as that seen in mammalian lung and gut epithelium (12–15). (2017) 8:1168. doi: 10.3389/fimmu.2017.01168, 181. There is difficulty in determining natural physiological parameters of mucus production such as the volume of mucus on the skin, rate of mucus production and discharge, and the ability to determine exact concentrations of skin-secreted compounds in the mucus. J Pep Res. Transepithelial transport is gen- erally viewed as a two-membrane phenomenon, and because the frog skin is a complex, multilay- (2015) 27:111–8. FEMS Micro Ecol. The skin of a frog is water permeable. Ann Rev Immunol. BTC: 1C2d9VtrKVfnEu3fyYUkP8cq2vDFddArSt Eur J Biochem. Forzán MJ, Jones KM, Ariel E, Whittington RJ, Wood J, Markham RJF, et al. (2014) 217(Pt 8):1392–401. doi: 10.2741/4461, 89. doi: 10.1016/j.dci.2017.02.016, 230. In mammals, RIG-I and MDA5 bind viral RNA via the common RNA helicase domain and ligand recognition results in activation of interferon regulatory factor 3 and NF-kB transcription factors to initiate transcription of an anti-viral interferon response (191). Articles, School of Medicine, Emory University, United States, Centre National de la Recherche Scientifique (CNRS), France. Robert J, Abramowitz L, Gantress J, Morales HD. Collectively, PRRs recognize a variety of pathogen-associated molecular patterns (PAMPs), also known as microbial-associated molecular patterns (MAMPs), including lipopolysaccharide, peptidoglycan, lipopeptides, flagellin, single stranded RNA, double stranded RNA, double stranded DNA, carbohydrate structures, as well as other PAMPs (176). Daly JW, Noimai N, Kongkathip B, Kongkathip N, Wilham JM, Garraffo HM, et al. doi: 10.1111/1574-6941.12314, 241. Here, I discuss recent insights into the cell biology of skin. Amino Acids (2012) 43:677–85. Hirata Y, Broquet AH, Menchen L, Kagnoff MF. Xiao XH, Miao HM, Xu YG, Zhang JY, Chai LH, Xu JJ. Microbe-microbe interactions may also contribute to establishment of “healthy microbiomes” and deeper investigation into the metabolic capacities of commensal microbes will likely yield insight into the maintenance of certain microbial communities. The beaker was left undisturbed for 20 minutes. (1968) 38:67–79. They are an important food source for predators and part of the food web dynamics of many of the world's ecosystems. (2018) 60:316–25. Human bone tissue. Majer O, Liu B, Barton GM. Yang W, Molenaar A, Kurts-Ebert B, Seyfert HM. State one advantage of using a stain to study frog skin cells with a microscope. Munoz WA, Kloc M, Cho K, Lee M, Hofmann I, Sater A, et al. Dev Comp Immunol. Development (2014) 141:1514–25. Frog skin has a rich microbiome which is important to their health. doi: 10.1139/cjm-2017-0119, 247. Structural contributions to the intracellular targeting strategies of antimicrobial peptides. The antimicrobial peptide dermaseptin S4 inhibits HIV-1 infectivity in vitro. doi: 10.1002/etc.5620220113, 207. The cationic peptide magainin II is antimicrobial for Burkholderia cepacia-complex strains. Davis BK, Wen H, Ting JP. Leptoglycin: a new Glycine/Leucine-rich antimicrobial peptide isolated from the skin secretion of the South American frog Leptodactylus pentadactylus (Leptodactylidae). Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, et al. Proc. Rota E, Tanteri G, Montori G, Giachi F, Delfino G, Sever DM. The Xenopus embryonic epidermis is a mucociliary epithelium - analogous to that found in mammalian airways. Sperandio B, Fischer N, Sansonetti PJ. Evaluation of the skin peptide defences of the Oregon spotted frog Rana pretiosa against infection by the chytrid fungus Batrachochytrium dendrobatidis. These toxins are being researched for potential pain medications. doi: 10.1529/biophysj.108.133488, 112. Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. (2012) 38:958–65. 102. Critical to the innate immune functions of frog skin are the maintenance of physical, chemical, cellular, and microbiological barriers and the complex network of interactions that occur across all the barriers. Dubaissi E, Rousseau K, Lea R, Soto X, Nardeosingh S, Schweickert A, et al. Denèfle JP, Zhu QL, Lechaire JP. Evidence for a role of tight junctions in regulating sodium permeability in zebrafish (Danio rerio) acclimated to ion-poor water. doi: 10.1016/j.micinf.2015.01.004, 75. Am J Anat. Savage AE, Kiemnec-Tyburczy KM, Ellison AR, Fleischer RC, Zamudio KR. Example Drawing Frog Skin Sample 400x. Cell junctions in amphibian skin. doi: 10.1016/0952-7915(94)90004-3, 36. doi: 10.1038/415389a, 107. doi: 10.1093/intimm/dxv013, 64. (2005) 42:887–93. J Cell Biol. (2008) 45:2333–42. J Anat. (2010) 78:3981–92. (2008) 8:42. doi: 10.1186/1471-2148-8-42, 197. Wang GD, Zhang BL, Zhou WW, Li YX, Jin JQ, Shao Y, et al. Though not largely studied, and thus not often described in studies examining frog integument, resident immune cells responsible for detecting and responding to pathogen exposure have been identified in frog skin (Figure 1). Barrier properties of mucus. doi: 10.1016/0041-0101(87)90265-0, 169. (2006) 30:831–42. Figure 4A.10 Endoplasmic reticulum (ER) in NRK cell labeled with antibodies to ER-resident proteins (from D. Louvard). Nat Biotech. Table 1. doi: 10.1111/exd.12929, 156. Figure provided by Mark Terasaki, University of Connecticut Health Center. Apical cell membranes from Na+-transporting epithelia were identified in centrifugal fractions prepared from homogenates of rainbow trout kidney, gill and frog skin using a spinlabeled, nitroxide derivative of amiloride and electron paramagnetic resonance spectroscopy. It is evident from these findings that the regulation of AMPs and the diversity among the AMP secretome is complex but is shaped by the environment. doi: 10.1042/BCJ20180286, 158. Ludtke SJ, He K, Heller WT, Harroun TA, Yang L, Huang HW. Tight junctions are specially known to contribute to paracellular transport of molecules (i.e., through the intercellular space and across epithelium) and thus integral to epithelial permeability in mammals, fish and frogs (64, 71, 72). doi: 10.1016/j.biocon.2012.03.022, 249. Available online at: www.amphibiaweb.org (2018). Regulation of the Rana sylvatica brevinin-1SY antimicrobial peptide during development and in dorsal and ventral skin in response to freezing, anoxia and dehydration. doi: 10.1084/jem.20101102, 155. 67. Current Protocols in Cell Biology 4A.6 Organelle Atlas. Schock DM, Bollinger TK, Chinchar VG, Jancovich JK, Collins JP. doi: 10.2108/zsj.26.80, 238. Label the structures in the tissues below. doi: 10.1007/s00360-012-0700-9, 73. Nucleic acid-sensing TLRs: trafficking and regulation. Cell Mol Life Sci. For example, increased environmental temperatures (from 5 to 30°C) triggered brevinin-1SY AMP production in R. sylvatica skin tissue (200). The immunology of host defence peptides: beyond antimicrobial activity. Proksch E, Brandner JM, Jensen JM. Science question. 1. Yokoyama H, Kudo N, Todate M, Shimada Y, Suzuki M, Tamura K. Skin regeneration of amphibians: a novel model for skin regeneration as adults. Insulin is known to play a role in keratinocyte function by inducing migration through the PI3-Akt-RhoA network (164). Explain why cells would have differing numbers of these structures. Not surprisingly, the frog skin microbiome is influenced by life stage (253), body region (254, 255), diet (254), capture site (256), habitat, captivity (254, 257), exposure to anthropogenic contaminants (258, 259), and treatment with antibiotics (260). In fact, the most well-characterized frog AMPs to date are of the magainin family, magainin-1 and magainin-2 (105–107). doi: 10.1371/journal.pone.0007699, 208. The amphibious water-sports apparel designed to provide you with warmth, comfort and windchill protection. Nearly 8,000 amphibian species have been discovered to date (88% belonging to order Anura–frogs and toads) and approximately 150 new species are discovered each year (1). A secretory cell type develops alongside multiciliated cells, ionocytes and goblet cells, and provides a protective, antiinfective function in the frog embryonic mucociliary epidermis. They are an important indicator species and their physiology is heavily influenced by the environment (197–199). Warner AE. This non-cellular layer is composed entirely of glycosaminoglycans and glycoconjugates, wherein hyaluronan and dermatan sulphate have been reported as key constituents in various species (29, 30). Horton JD, Horton TL, Ritchie P, Varley CA. Div Distrib. Executive Editor Katherine Brown (virtually) met with the winner of the SDB Conklin Medal, Claude Desplan, and heard about how he first became captivated by Drosophila and neural development, his mentorship style and tips for young scientists. (2017) 28:60–e15. J Chem Ecol. Regulation of innate antiviral defences through a shared repressor domain in RIG-I and LGP2. Talbott K, Wolf TM, Sebastian P, Abraham M, Bueno I, McLaughlin M, et al. doi: 10.1128/JVI.02486-09, 229. Mammalian skin research represents the convergence of three complementary disciplines: cell biology, mouse genetics, and dermatology. Hancock RE, Sahl HG. esculentus) skin. doi: 10.1016/j.virol.2017.06.005, 19. Blog. doi: 10.1016/j.ijantimicag.2003.07.022, 122. Open in figure viewer PowerPoint. Quaranta A, Bellantuono V, Cassano G, Lippe C. Why amphibians are more sensitive than mammals to xenobiotics. Biochim et Biophys Acta (2009) 1788:1593–9. To date, there are no studies on the importance of the mucociliary epithelium in adult frogs. Terms to know!! Exp Dermatol. Yet much remains to be uncovered regarding how the frog host creates a permissive niche for certain microbial species while restricting others. Toxicon (2009) 54:23–32. The frog’s skin may be covered in spots, called chromatophores. Song X, Jin P, Qin S, Chen L, Ma F. The evolution and origin of animal Toll-like receptor signalling pathway revealed by network-level molecular evolutionary analyses. doi: 10.1371/journal.pone.0085563, 255. Martinez-Palomo A, Erlij D, Bracho H. Localization of permeability barriers in the frog skin epithelium. Huang L, Li J, Anboukaria H, Luo Z, Zhao M, Wu H. Comparative transcriptome analyses of seven anurans reveal functions and adaptations of amphibian skin. Austral J Ecotox. Ringø E, Løvmo L, Kristiansen M, Bakken Y, Salinas I, Myklebust R, et al. Pochini KM, Hoverman JT. doi: 10.1089/jamp.2007.0659, 83. Compared to mammalian skin, frog skin has significantly greater uptake potential of xenobiotics that can bioconcentrate and may be detrimental to frog health (207–209). doi: 10.1099/jmm.0.008128-0, 139. In mammalian systems, AMPs can bind cell surface receptors such as formyl peptide receptor-like-1 (FPLR1), purinergic receptors (P2X7), Toll-like receptors (TLRs), chemokine receptors (CCRs), G-protein coupled receptors (GPCRs), and epidermal growth factor receptor (EGFR) to activate downstream signalling pathways to promote wound healing (156). ), while still maintaining a selective barrier to the external environment (2, 3, 9). The diagram below represents a series of events that occur in living cells. 34. Hao X, Yang H, Wei L, Yang S, Zhu W, Ma D, et al. doi: 10.1073/pnas.1713539115. Presence of microbes, whether commensal or pathogenic, triggers an initial upregulation of genes encoding for tight junction proteins, and thus skin barrier strengthening (71, 73). Not surprisingly, the majority of frog skin derived AMPs tested against fungal pathogens of frogs have focused on Bd (Table 4). PLoS Path. 216. Wu J, Yang J, Wang X, Wei L, Mi K, Shen Y, et al. Pesticides Could alter amphibian skin microbiomes and the effects of Batrachochytrium dendrobatidis. Dis Aquatic Org. In general, while these studies are comprehensive at analysing either the impact of contaminants on amphibian skin or effect on ion permeability and pathogen susceptibility, none appear to directly report the regulation of cellular junctions in combination with pathogen susceptibility. Chem Ecol. (2001) 33:311–6. Granular glands appear to be further concentrated in specific regions of the skin, such as the central region of the skin vs. head or leg regions (45, 55). Exp Dermatol. (2016) 21:1341–71. (2007) 43:645–52. Maintenance of amphibian skin integrity is important for overall frog health—both in terms of conducting essential physiological processes and for defence against invading pathogens. (2018) 128:93–103. We briefly discuss the influence of environmental abiotic factors (natural and anthropogenic) and pathogens on the immunocompetency of frog skin defences. The mucous and seromucous glands are easily identifiable as distinct glands. The mucous and seromucous glands are easily identifiable as distinct glands. doi: 10.1016/j.immuni.2017.03.018, 138. Gibb K, Schobben X, Christian K. Frogs host faecal bacteria typically associated with humans. The TLR14 subfamily appears to have expanded in X. tropicalis, and possibly in other frogs, to four TLR14 subfamily members that are hypothesized to form heterodimeric pairs with TLR2, similar to other subfamily members of the TLR2 family (184). (2014) 2:cou032. Ferreira KT, Hill BS. The dermis is largely comprised of connective tissue formed by collagenous fibres (black lines) in two layers, the spongious dermis (4) and the compact dermis (6), connected by collagenous columns (white star). doi: 10.1007/s10393-007-0093-5, 21. They have a 'seat pouch', an area on their bellies which is designed for water absorbtion. Luca V, Stringaro A, Colone M, Pini A, Mangoni ML. Origin and functional diversification of an amphibian defence peptide arsenal. Thus, much of our basis for understanding the role of frog skin epithelial cells to microbial detection is limited to the identification of key pattern recognition molecules in the frog genome and implied conservation of their function based on limited expression data in frog skin tissues. (2011) 7:414–8. Kim JM, Eckmann L, Savidge TC, Lowe DC, Witthoft T, Kagnoff MF. A native mixture of peptides obtained from adult R. catesbaeiana skin was effective at inhibiting trematode cercariae viability at all AMP mixture concentrations tested (Table 5). Sequestered alkaloid defences in the Dendrobatid poison frog oophaga pumilio provide variable protection from microbial pathogens. (2002) 92:1725–42. (See also Blood.) Development (1991) 111:159–69. -What specific cell part is all that remains of the cork cells? 31. Virology (2005) 334:264–75. Ketola-Pirie CA, Atkinson BG. Woodhams DC, Vredenburg VT, Simon M-A, Billheimer D, Shakhtour B, Shyr Y, et al. Skin glands, poison and mimicry in dendrobatid and leptodactylid amphibians. J Histochem Cytochem. Extensive investigation has demonstrated frog AMPs to exert broad-spectrum antimicrobial activity against human pathogens, including bacteria, viruses, fungi and parasites, reviewed in (120, 121, 137, 138). Conservation and divergence in the frog immunome: pyrosequencing and de novo assembly of immune tissue transcriptomes. Despite the exciting advances in the contribution of frog skin microbial communities to innate immune functions of frog skin, much remains to be elucidated in terms of host-microbiome-environment interplay. (2016) 12:e1004570. Frog skin contains three distinct types of exocrine glands: granular (poison), mucous, and seromucous. (2018):2785–99. Cell Res. Infectious disease and amphibian population declines. Becker MH, Richards-Zawacki CL, Gratwicke B, Belden LK. Chang DJ, Hwang YS, Cha SW, Chae JP, Hwang SH, Hahn JH, et al. doi: 10.1897/05-141R.1, 213. The skin: an indispensable barrier. Div Dist. doi: 10.1080/08830185.2017.1365146, 178. (2018) 40:555–65. Immunomodulatory and anti-inflammatory activities of chicken Cathelicidin-2 derived peptides. doi: 10.1016/j.bbrc.2012.12.116, 164. Frog AMPs are effective antimicrobial agents against Aeromonas sp., the causative agents of red-leg, a polymicrobial disease that is characterized by congestion of the skin, ulceration, haemorrhage, bloating, failure to respond to stimuli, and tetanic seizures (150). Toxic alkaloids are primarily involved in predation avoidance, however, a few also participate in defence against microbes (167, 172). doi: 10.1670/16-092, 259. Two papers now identify a final cell type in the frog embryonic skin, the small secretory cell (SSC). Mol Ecol Resour (2014) 14:178–83. Immune defences against Batrachochytrium dendrobatidis, a fungus linked to global amphibian declines, in the South African clawed frog, Xenopus laevis. (2003) 46:445–52. Structure activity analysis of thanatin, a 21-residue inducible insect defense peptide with sequence homology to frog skin antimicrobial peptides. PNAS (1987) 84:5449–53. Microscope Images at Different Magnifications. Innate immune recognition at the epithelial barrier drives adaptive immunity: APCs take the back seat. Kress E, Merres J, Albrecht LJ, Hammerschmidt S, Pufe T, Tauber SC, et al. Dubaissi E, Rousseau K, Hughes GW, Ridley C, Grencis RK, Roberts IS, et al. Comprehensive transcriptomic analyses on the skin of frogs infected with Bd revealed significant transcriptional regulation in the skin with generalized decreases in collagen, fibrinogen, elastin and keratin pathway transcript abundance, which corroborates with the observed disruption in epidermal skin integrity and loss of osmotic balance (236). Both magainins possess an alpha-helical structure and, like most AMPs, are amphipathic (105). The outermost portion of this skin is composed of a single layer of irregularly-shaped, flat (squamous) cells, which gives the tissue its name. FASEB J. Langerhans cells are specialized cells of the immune system that are embedded in your skin. (2017) 54:531–48. (2015) 29:674–82. Chinchar VG, Bryan L, Silphadaung U, Noga E, Wade D, Rollins-Smith L. Inactivation of viruses infecting ectothermic animals by amphibian and piscine antimicrobial peptides. Rollins-Smith LA, Doersam JK, Longcore JE, Taylor SK, Shamblin JC, Carey C, et al. Another environmental factor that has an effect on AMPs is hydration status. The stratum germinativum, which directly connects to the dermis, contains a mixture of cell types including epithelial cells, immune cells (described in the paragraph immediately below) and chromatophores that provide frogs with dynamic pigmentation patterns (26). (1998) 61:162–72. Brizzi R, Delfino G, Pellegrini R. Specialized mucous glands and their possible adaptive role in the males of some species of Rana (Amphibia, Anura). Perez-Iglesias JM, Soloneski S, Nikoloff N, Natale GS, Larramendy ML. doi: 10.1126/science.1103538, 17. doi: 10.1016/j.envpol.2016.11.086. Euro J Pharm. doi: 10.1007/s00726-011-1116-7, 104. A key symptom of FV3 infection in susceptible developmental stages or frog species is the formation of skin lesions, skin shedding, and epidermal cell necrosis (231, 232). Hyaluronan molecules are proposed to reduce water evaporation thereby aiding in the prevention of desiccation, particularly in basking amphibians, since the molecules are highly water retentive (30). Skin is an integral interface between an organism's internal and ext… Anim Conserv. Mol Ecol. Can Immun. Adult X. laevis are relatively resistant to FV3 and generally recover from mild symptoms 3–4 weeks after infection (18, 224, 225), whereas tadpoles are highly susceptible to FV3 infection (226). A plethora of studies in mammalian models describe the impact on barrier integrity, and thus barrier function, in response to various skin diseases or environmental factors (62, 71, 73). doi: 10.1007/BF00218860, 60. Blaustein AR, Romansic JM, Kiesecker JM, Hatch AC. (2010) 84:4912–22. PNAS (2018) 115:726–31. Although these urinary bladder epithelial cells appear to be LPS responsive, unequivocal evidence that TLR4 is responsible for LPS sensing is lacking. Gregorio J, Meller S, Conrad C, Di Nardo A, Homey B, Lauerma A, et al. Oncogene (2006) 25:6749–57. Solar UV radiation reduces the barrier function of human skin. Nat Immunol. Front Micro. BMC Evol Biol. doi: 10.1093/conphys/coy035, 219. Sousa JC, Berto RF, Gois EA, Fontenele-Cardi NC, Honorio JE Jr Konno K, et al. The use of transcriptomic approaches to investigate immune function of frog skin has yielded an effective strategy to identify AMP peptide diversity across frog species, developmental stage, and environmental factors (e.g., abiotic and biotic elements) (123–125). Functional characterization of the mucus barrier on the Xenopus tropicalis skin surface. Read about the actions we are taking at this time. They absorb through capillary action from water or a moist surface. The interplay between UV and chemical exposure on frog skin immunocompetence, however, is not well-studied. The distribution and average size of granular gland in poisonous rock frog, Odorrana hosii. doi: 10.1016/j.toxicon.2009.02.018, 146. Matthijs S, Ye L, Stijlemans B, Cornelis P, Bossuyt F, Roelants K. Low structural variation in the host-defence peptide repertoire of the dwarf clawed frog Hymenochirus boettgeri (Pipidae). Biologically active substances from amphibians: preliminary studies on anurans from twenty-one genera of Thailand. Structure and orientation of the antibiotic peptide magainin in membranes by solid-state nuclear magnetic resonance spectroscopy. Recently, attention has turned to elucidating the contribution of the frog skin microbiome in innate immune defences to emerging infectious diseases of amphibians, and in particular to Bd. doi: 10.3354/dao02823, 120. Matsui T, Amagai M. Dissecting the formation, structure and barrier function of the stratum corneum. J Am Acad Derm. Virology (2017) 511:309–19. Ecology and pathology of amphibian ranaviruses. Please log in to add an alert for this article. Frogs often do not drink through their mouths, but rather absorb moisture through their skin. Skin sloughing may serve to remove skin-associated microbes, including pathogens (79), and the rate of skin sloughing increases with certain infections, perhaps as a mechanism to limit pathogen numbers on the skin (77). doi: 10.1016/j.molimm.2007.11.007, 85. doi: 10.1128/AEM.04147-15, 245. Glucagon and glucagon-like peptide-1 as novel anti-inflammatory and immunomodulatory compounds. Shahin SH, Blankemeyer JT. The first line of defence: insights into mechanisms and relevance of phagocytosis in epithelial cells.
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