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The Epidermal Lamellar Body: a Fascinating Secretory Organelle

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The Epidermal Lamellar Body: a Fascinating Secretory Organelle View metadata, citation and similar papers at core.ac.uk brought to you by CORE See relatedprovided article by Elsevier on page- Publisher 1137 Connector The Epidermal Lamellar Body: A Fascinating Secretory Organelle Manige´ Fartasch Department of Dermatology, University of Erlangen, Germany The topic of the function and formation of the epidermal LAMP-1. Instead, it expresses caveolin—a cholesterol- permeability barrier continue to be an important issue to binding scaffold protein that facilitates the assembly of understand regulation and development of the normal and cholesterol—and sphingolipids into localized membrane abnormal epidermis. A major player in the formation of the domains or ‘‘rafts’’ (Sando et al, 2003), which typically serve barrier, i.e., the stratum corneum (SC), is a tubular and/or as targets for apical transport of vesicles of Golgi origin. To ovoid-shaped membrane-bound organelle that is unique to date, a large body of evidence supports the concept that mammalian epidermis. In the past, this organelle has been LB, which shows morphology ranging from vesicles to embellished largely with descriptive names attributed to tubules on EM, are probably products of the tubulo- its perceived functional properties like membrane coating vesicular elements of the trans-Golgi network (TGN) that granule, keratinosome, cementsoms, and lamellar body/ is a tubulated sorting and delivery portion of the Golgi granule (LB). Over the last decade, data from several apparatus (Elias et al, 1998; Madison, 2003). Recently, laboratories documented that mammalian LB contain not some authors have hypothesized (Norlen, 2001) that LB are only pro-barrier lipids and their respective lipid processing not found as discrete organelles, but rather they comprise enzymes (e.g., b-glucocerebrosidase, acidic sphingomyeli- a branched TGN system with lipid content that unfurls/ nase, secretory phospholipase A2) destined for extrusion unfolds into the extracellular space in a non-energy into the extracellular environment at the apical portion of the dependent, purely physical–chemical manner. But to date flattened stratum granulosum (SG) cell (Menon et al, 1992), there is neither immunoelectron microscopic evidence nor but additionally they contain proteases (SC chymotryptic functional tests with barrier disruption that support this enzyme, cathepsin D, acid phosphatase, glycosidases, model. Moreover, this model does not deal with evidence protease inhibitors). Thus, LB are involved in barrier home- that LB formation and secretion are both energy dependent ostasis, desquamation, formation of the cornified envelope (e.g., LB do not form at 41C) and regulated processes; e.g., and additionally antimicrobial defence (Oren et al, 2003). LB secretion is blocked by classic inhibitors, such as Thus, the heterogeneous content of LB is consistent with brefeldin A and momensin, and further regulated by the host of defensive function mediated by the SC (for a changes in external calcium. review see Elias and Feingold, 2004, in press). In this Issue of the Journal of Investigative Dermatology, The LB transport the pro-barrier lipids (Grayson et al, Ishida-Yamamoto et al try to clarify the localization and 1985) to the apical regions of the outermost SG cell, often timing of LB content formation, providing evidence that forming deep invaginations of the stratum granulosum–SC different content markers are distributed in a separated interface (Elias et al, 1998), facilitating rapid extrusion of population of LB molecules within the upper layers of their contents which is there transformed into barrier lipids. epidermis. In general, the interpretation of immunoelectron In skin diseases with involvement of epidermis and/or microscopy studies regarding LB are difficult to interpret, barrier alterations, either of hereditary or inflammatory as there is not yet a definitive marker for LB other than origin, LB formation, morphology, kinetics of secretion and the demonstration of their internal membrane structure extrusion mechanisms can be disturbed and can be used by osmium tetroxide—or ruthenium tetroxide—staining. A as morphologic markers for diagnosis (Fartasch et al, 1992, combination of criteria that includes size, shape, general 1999; Menon et al, 1992; Elias et al, 2000). Thus, the number structural morphology and their occurrence in the upper of functions linked to this fascinating organelle still stratum spinosum and stratum granulosum is also used to continues to increase. identify LB by immunoelectron microscopy, where preser- The LB is believed to be something of a cross between a vation of the LB membranes still remain suboptimal. In this secretory vesicle and a lysosome (Wolff and Holubar, 1967; study, the authors could show that different functional areas Madison, 2003). While it encapsulates several hydrolases could exist within the branched tubular system that typical of lysosomes, it lacks other classic lysosomal comprise extension of the trans-Golgi network and by markers such as aryl sulfatase A/B and b-glucuronidase. applying different morphologic techniques (immunofluores- Moreover, it lacks lysosomal membrane markers, such as cence microscopy and immunoelectron microscopy on ultrathin cryosections) the authors identified co-localization and localization of a variety of putative lamellar-body- associated antigens which they believe localize to cargo Abbreviation: EM, electron microscopy; LB, lamellar body; SC, stratum corneum; SG, stratum granulosum; TGN, trans-Golgi structures consistent with LB and TGN. Carefully inter- network. preted, this study appears to provide evidence that LB Copyright r 2004 by The Society for Investigative Dermatology, Inc. xi xii FARTASCH THE JOURNAL OF INVESTIGATIVE DERMATOLOGY secretion is a finely tuned, complex mechanism, whereby Fartasch M, Williams ML, Elias PM: Altered lamellar body secretion and stratum assembling of different cargos into LB occurs in a com- corneum membrane structure in Netherton syndrome: Differentiation from other infantile erythrodermas and pathogenic implications. Arch partmentalized fashion. Indeed, the study by Yamamoto Dermatol 135:823–832, 1999 et al provides further evidence that this unique secretory Grayson S, Johnson-Winegar AG, Wintroub BU, Isseroff RR, Epstein EH, Elias system deserves careful study and abundant respect. PM: Lamellar body-enriched fractions from neonatal mice: Preparative techniques and partial characterization. J Invest Dermatol 85:289–294, 1985 DOI: 10.1111/j.0022-202X.2004.22541.x Madison KC: Barrier function of the skin: ‘‘La Raison d’Etre’’ of the epidermis. J Invest Dermatol 121:231–241, 2003 Menon GK, Ghadially R, Williams ML, Elias PM: Lamellar bodies as delivery References systems of hydrolytic enzymes: Implications for normal and abnormal desquamation. Br J Dermatol 126:337–345, 1992 Elias PM, Cullander C, Mauro T, Rassner U, Komuves L, Brown BE, Menon GK: Norlen L: Skin barrier formation: The membrane folding model. J Invest Dermatol The secretory granular cell: The outermost granular cell as a specialized 117:823–829, 2001 secretory cell. J Investig Dermatol Symp Proc 3:87–100, 1998 Oren A, Ganz T, Liu L, Meerloo T: In human epidermis, beta-defensin 2 is Elias PM, Fartasch M, Crumrine D, Behne M, Uchida Y, Holleran WM: Origin of packaged in lamellar bodies. Exp Mol Path 74:180–182, 2003 the corneocyte lipid envelope (CLE): Observation in harlequin ichthyosis Sando GN, Zhu H, Weis JM, Richman JT, Wertz PW, Madison KC: Caveolin and cultured human keratinocytes. J Invest Dermatol 115:765–769, 2000 Expression and localization in human keratinocytes suggest a role in Elias PM, Feingold KR (ed): Cutaneous Barrier Function. New York: Marcel lamellar granule biogenesis. J Invest Dermatol 120:531–541, 2003 Dekker, 2004 Wolff K, Holubar K: Keratinosomes as epidermal lysosomes. Arch Klin Exp Fartasch M, Bassukas ID, Diepgen TL: Disturbed extruding mechnism of lamellar Dermatol 231:1–19, 1967 bodies in dry non-eczematous skin of atopics. Br J Dermatol 221–227, 1992.
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