Intercellular adhering junctions with an asymmetric molecular composition: Desmosomes connecting Merkel cells and keratinocytes

Cell and Tissue Research

Volumn 346, Issue 1, 2011, Pages 65-77

  Rickelt, Steffen ^a,c   Moll, Ingrid ^b   Franke, Werner Wilhelm ^a,c  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c Progen Biotechnik   (Germany)

Author keywords

Asymmetric junctions; Heterotypic junctions; Keratinocytes; Merkel cells; Plakophilin 2

Indexed keywords

CYTOKERATIN 20; PLAKOPHILIN; PLAKOPHILIN 1; PLAKOPHILIN 2; PLAKOPHILIN 3; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELLULAR DISTRIBUTION; DESMOSOME; FETUS; HUMAN; HUMAN TISSUE; IMMUNOLOCALIZATION; KERATINOCYTE; MERKEL CELL; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT;

ADHERENS JUNCTIONS; ANIMALS; CATTLE; DESMOSOMES; FEMALE; HUMANS; KERATINOCYTES; MERKEL CELLS; MICE; PLAKOPHILINS; RATS; SWINE;

EID: 80755167720     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-011-1260-0     Document Type: Article

References (58)

1. AW Barrett EM Cort P Patel BK Berkovitz 2000 An immunohistological study of cytokeratin 20 in human and mammalian oral epithelium Arch Oral Biol 45 879 887 10973561 10.1016/S0003-9969(00)00050-9 1:CAS:528:DC%2BD3cXmtVCgs78%3D
2. M Barth H Schumacher C Kuhn P Akhyari A Lichtenberg WW Franke 2009 Cordial connections: molecular ensembles and structures of adhering junctions connecting interstitial cells of cardiac valves in situ and in cell culture Cell Tissue Res 337 63 77 19475424 10.1007/s00441-009-0806-x 1:CAS:528: DC%2BD1MXntVSrtrs%3D
3. N Boulais L Misery 2007 Merkel cells J Am Acad Dermatol 57 147 165 17412453 10.1016/j.jaad.2007.02.009 (Pubitemid 46899271)
4. SB Cheng Chew PY Leung 1994 Ultrastructural study of the Merkel cell and its expression of met-enkephalin immunoreactivity during fetal and postnatal development in mice J Anat 185 Pt 3 511 520 7649787
5. Delva E, Tucker DK, Kowalczyk AP (2010) The desmosome. In: Nelson J, Fuchs E (eds) Cold Spring Harbor perspectives in biology. Cold Spring Harbor Laboratory Press, New York, pp 83-99
6. AC Eispert F Fuchs JM Brandner P Houdek E Wladykowski I Moll 2009 Evidence for distinct populations of human Merkel cells Histochem Cell Biol 132 83 93 19319559 10.1007/s00418-009-0578-0 1:CAS:528:DC%2BD1MXmvFGhurc%3D
7. KB English EH Hammond N Stayner 1990 Primary culture of cells arising from a neuroendocrine skin carcinoma Am J Dermatopathol 12 589 597 2267998 10.1097/00000372-199012000-00010 1:STN:280:DyaK3M%2Fps12gug%3D%3D
8. F Fantini O Johansson 1995 Neurochemical markers in human cutaneous Merkel cells. An immunohistochemical investigation Exp Dermatol 4 365 371 8608344 10.1111/j.1600-0625.1995.tb00061.x 1:CAS:528:DyaK28XktVChsA%3D%3D
9. MG Farquhar GE Palade 1963 Junctional complexes in various epithelia J Cell Biol 17 375 412 13944428 10.1083/jcb.17.2.375 1:STN:280: DyaF387js1Whsw%3D%3D
10. GJ Fortman RK Winkelmann 1977 The Merkel cell in oral human mucosa J Dent Res 56 1303 1312 206579 10.1177/00220345770560110201 1:STN:280: DyaE1c7ntF2hsg%3D%3D
11. J Fradette D Larouche C Fugere R Guignard A Beauparlant V Couture L Caouette-Laberge A Roy L Germain 2003 Normal human Merkel cells are present in epidermal cell populations isolated and cultured from glabrous and hairy skin sites J Invest Dermatol 120 313 317 12542538 10.1046/j.1523-1747.2003.12024.x 1:CAS:528:DC%2BD3sXhtVWrsLg%3D (Pubitemid 36513083)
12. Franke WW (2010) Discovering the molecular components of intercellular junctions - a historical view. In: Nelson J, Fuchs E (eds) Cold Spring Harbor perspectives in biology. Cold Spring Harbor Laboratory Press, New York, pp 1-34
13. Franke WW, Rickelt S (2011) Mesenchymal-epithelial transitions: Spontaneous and cumulative syntheses of epithelial marker molecules and their assemblies to novel cell junctions connecting human hematopoietic tumor cells to carcinomatoid tissue structures. Int J Cancer 129:2588-2599
14. WW Franke CM Borrmann C Grund S Pieperhoff 2006 The area composita of adhering junctions connecting heart muscle cells of vertebrates I. Molecular definition in intercalated disks of cardiomyocytes by immunoelectron microscopy of desmosomal proteins Eur J Cell Biol 85 69 82 16406610 10.1016/j.ejcb.2005.11. 003 1:CAS:528:DC%2BD28XisVagsLY%3D (Pubitemid 43137112)
15. WW Franke S Rickelt M Barth S Pieperhoff 2009 The junctions that don't fit the scheme: special symmetrical cell-cell junctions of their own kind Cell Tissue Res 338 1 17 19680692 10.1007/s00441-009-0849-z
16. Garrod D (2010) Desmosomes in vivo. In: Mohoney G, Mueller EJ, Koch PJ (eds) Dermatology research and practice. Desmosomes and desmosomal cadherin function in skin and heart diseases-Advancements in basic and clinical research. Hindawi Publishing Corporation, LaVergne, TN, USA. Article ID 212439
17. D Garrod M Chidgey 2008 Desmosome structure, composition and function Biochim Biophys Acta 1778 572 587 17854763 10.1016/j.bbamem.2007.07.014 1:CAS:528:DC%2BD1cXjtVSqtrc%3D (Pubitemid 351317796)
18. Giberson RT, Demaree RS (2001) Microwave techniques and protocols. Humana Press, Totowa, NJ, USA
19. LM Godsel SN Hsieh EV Amargo AE Bass LT Pascoe-McGillicuddy AC Huen ME Thorne CA Gaudry JK Park K Myung RD Goldman TL Chew KJ Green 2005 Desmoplakin assembly dynamics in four dimensions: multiple phases differentially regulated by intermediate filaments and actin J Cell Biol 171 1045 1059 16365169 10.1083/jcb.200510038 1:CAS:528:DC%2BD2MXhtlCjsr7P (Pubitemid 41815836)
20. VE Gould R Moll I Moll I Lee WW Franke 1985 Neuroendocrine (Merkel) cells of the skin: hyperplasias, dysplasias, and neoplasms Lab Invest 52 334 353 2580118 1:STN:280:DyaL2M7mtFyrtA%3D%3D (Pubitemid 15056792)
21. Hartschuh W, Weihe E, Reinecke M (1984) The Merkel cell. In: Bereiter-Hahn J, Matoltsy AG, Richards KS (eds) Biology of the integument 2-Vertebrates. Springer-Verlag, Berlin, Heidelberg, New York, Tokyo, pp 605-620
22. W Hartschuh E Weihe U Egner 1989 Chromogranin A in the mammalian Merkel cell: cellular and subcellular distribution J Invest Dermatol 93 641 648 2677156 10.1111/1523-1747.ep12319788 1:CAS:528:DyaL1MXmt12ltr4%3D (Pubitemid 19262825)
23. W Hartschuh E Weihe N Yanaihara 1989 Immunohistochemical analysis of chromogranin A and multiple peptides in the mammalian Merkel cell: further evidence for its paraneuronal function? Arch Histol Cytol 52 Suppl 423 431 2510797 10.1679/aohc.52.Suppl-423
24. H Kurzen I Moll R Moll S Schaefer E Simics M Amagai MJ Wheelock WW Franke 1998 Compositionally different desmosomes in the various compartments of the human hair follicle Differentiation 63 295 304 9810708 10.1046/j.1432-0436.1998. 6350295.x 1:CAS:528:DyaK1cXntFGgtrg%3D (Pubitemid 28474949)
25. L Langbein C Grund C Kuhn S Praetzel J Kartenbeck JM Brandner I Moll WW Franke 2002 Tight junctions and compositionally related junctional structures in mammalian stratified epithelia and cell cultures derived therefrom Eur J Cell Biol 81 419 435 12234014 10.1078/0171-9335-00270 1:CAS:528:DC%2BD38XotFGqu7o%3D (Pubitemid 34982270)
26. A Lucarz G Brand 2007 Current considerations about Merkel cells Eur J Cell Biol 86 243 251 17337089 10.1016/j.ejcb.2007.02.001 1:CAS:528: DC%2BD2sXmsFeit7s%3D (Pubitemid 46630212)
27. C Mertens C Kuhn WW Franke 1996 Plakophilins 2a and 2b: constitutive proteins of dual location in the karyoplasm and the desmosomal plaque J Cell Biol 135 1009 1025 8922383 10.1083/jcb.135.4.1009 1:CAS:528:DyaK28XntVarsbw%3D (Pubitemid 26403775)
28. C Mertens C Kuhn R Moll I Schwetlick WW Franke 1999 Desmosomal plakophilin 2 as a differentiation marker in normal and malignant tissues Differentiation 64 277 290 10374264 10.1046/j.1432-0436.1999.6450277.x 1:STN:280:DyaK1Mzgt1Cqtg%3D%3D (Pubitemid 29250934)
29. I Moll 1994 Merkel cell distribution in human hair follicles of the fetal and adult scalp Cell Tissue Res 277 131 138 7519969 10.1007/BF00303089 1:STN:280:DyaK2czjt1yltQ%3D%3D (Pubitemid 24196404)
30. R Moll WW Franke 1985 Cytoskeletal differences between human neuroendocrine tumors: a cytoskeletal protein of molecular weight 46,000 distinguishes cutaneous from pulmonary neuroendocrine neoplasms Differentiation 30 165 175 3007249 10.1111/j.1432-0436.1985.tb00528.x 1:CAS:528: DyaL28XhsVKnsrw%3D (Pubitemid 16153852)
31. I Moll R Moll 1992 Early development of human Merkel cells Exp Dermatol 1 180 184 1365319 10.1111/j.1600-0625.1992.tb00186.x 1:STN:280: DyaK2M%2Fptlyjsg%3D%3D
32. R Moll WW Franke DL Schiller B Geiger R Krepler 1982 The catalog of human cytokeratins: patterns of expression in normal epithelia, tumors and cultured cells Cell 31 11 24 6186379 10.1016/0092-8674(82)90400-7 1:CAS:528: DyaL3sXhtlSjsw%3D%3D (Pubitemid 13215192)
33. R Moll I Moll WW Franke 1984 Identification of Merkel cells in human skin by specific cytokeratin antibodies: Changes of cell density and distribution in fetal and adult plantar epidermis Differentiation 28 136 154 6084624 10.1111/j.1432-0436.1984.tb00277.x 1:STN:280:DyaL2M7ivVWisQ%3D%3D (Pubitemid 15167878)
34. I Moll R Moll WW Franke 1986 Formation of epidermal and dermal Merkel cells during human fetal skin development J Invest Dermatol 87 779 787 3782861 10.1111/1523-1747.ep12458993 1:STN:280:DyaL2s%2FlvFWktA%3D%3D (Pubitemid 17186422)
35. I Moll AT Lane WW Franke R Moll 1990 Intraepidermal formation of Merkel cells in xenografts of human fetal skin J Invest Dermatol 94 359 364 2407788 10.1111/1523-1747.ep12874488 1:STN:280:DyaK3c7ntFKhsw%3D%3D (Pubitemid 20061647)
36. R Moll DL Schiller WW Franke 1990 Identification of protein IT of the intestinal cytoskeleton as a novel type I cytokeratin with unusual properties and expression patterns J Cell Biol 111 567 580 1696264 10.1083/jcb.111.2.567 1:CAS:528:DyaK3cXkvFKqurk%3D (Pubitemid 20239868)
37. I Moll C Kuhn R Moll 1995 Cytokeratin 20 is a general marker of cutaneous Merkel cells while certain neuronal proteins are absent J Invest Dermatol 104 910 915 7769257 10.1111/1523-1747.ep12606183 1:STN:280:DyaK2M3oslSisg%3D%3D
38. I Moll M Roessler JM Brandner AC Eispert P Houdek R Moll 2005 Human Merkel cells-aspects of cell biology, distribution and functions Eur J Cell Biol 84 259 271 15819406 10.1016/j.ejcb.2004.12.023 1:CAS:528:DC%2BD2MXktFCis70%3D (Pubitemid 40353067)
39. R Moll E Sievers B Haemmerling A Schmidt M Barth C Kuhn C Grund I Hofmann WW Franke 2009 Endothelial and virgultar cell formations in the mammalian lymph node sinus: endothelial differentiation morphotypes characterized by a special kind of junction (complexus adhaerens) Cell Tissue Res 335 109 141 19015886 10.1007/s00441-008-0700-y 1:CAS:528:DC%2BD1cXhsVOru7vF
40. KM Morrison GR Miesegaes EA Lumpkin SM Maricich 2009 Mammalian Merkel cells are descended from the epidermal lineage Dev Biol 336 76 83 19782676 10.1016/j.ydbio.2009.09.032 1:CAS:528:DC%2BD1MXhtlyrtr%2FI
41. BL Munger 1965 The intraepidermal innervation of the snout skin of the opossum. A light and electron microscope study, with observations on the nature of Merkel's Tastzellen J Cell Biol 26 79 97 5859024 10.1083/jcb.26.1.79 1:STN:280:DyaF28%2FotVKrug%3D%3D
42. Y Narisawa K Hashimoto H Kohda 1994 Immunohistochemical demonstration of the expression of neurofilament proteins in Merkel cells Acta Derm Venereol 74 441 443 7535501 1:STN:280:DyaK2M3hs1Chug%3D%3D
43. JP Ortonne M Darmon 1985 Merkel cells express desmosomal proteins and cytokeratins Acta Derm Venereol 65 161 164 2408421 1:STN:280: DyaL2M3itFejsw%3D%3D (Pubitemid 15144842)
44. Pieperhoff S, Barth M, Rickelt S, Franke WW (2010) Desmosomal molecules in and out of adhering junctions: normal and diseased states of epidermal, cardiac and mesenchymally derived cells. In: Mohoney G, Mueller EJ, Koch PJ (eds) Dermatology research and practice. Desmosomes and desmosomal cadherin function in skin and heart diseases-Advancements in basic and clinical research. Article ID 139167. Hindawi Publishing Corporation, LaVergne, TN, USA
45. S Rickelt WW Franke Y Doerflinger S Goerdt JM Brandner WK Peitsch 2008 Subtypes of melanocytes and melanoma cells distinguished by their intercellular contacts: heterotypic adherens junctions, adhesive associations, and dispersed desmoglein 2 glycoproteins Cell Tissue Res 334 401 422 18975006 10.1007/s00441-008-0704-7 1:CAS:528:DC%2BD1MXptFKjtw%3D%3D
46. S Rickelt S Winter-Simanowski E Noffz C Kuhn WW Franke 2009 Upregulation of plakophilin-2 and its acquisition to adherens junctions identifies a novel molecular ensemble of cell-cell-attachment characteristic for transformed mesenchymal cells Int J Cancer 125 2036 2048 19551809 10.1002/ijc.24552 1:CAS:528:DC%2BD1MXhtVOms73K
47. S Rickelt S Rizzo Y Doerflinger H Zentgraf C Basso G Gerosa G Thiene R Moll WW Franke 2010 A novel kind of tumor type-characteristic junction: plakophilin-2 as a major protein of adherens junctions in cardiac myxomata Mod Pathol 23 1429 1437 20693980 10.1038/modpathol.2010.138 1:CAS:528: DC%2BC3cXhtlKjtrvK
48. Schaefer S, Nuber UA, Moll R, Franke WW (1997) Desmosomes and hemidesmosomes: differences and similarities in skin and mucosae. In: Pleyer U, Hartmann C, Sterry E (eds) Oculodermal diseases. AEolus Press, Buren, The Netherlands, pp 75-94
49. CJ Schmitt WW Franke S Goerdt B Falkowska-Hansen S Rickelt WK Peitsch 2007 Homo- and heterotypic cell contacts in malignant melanoma cells and desmoglein 2 as a novel solitary surface glycoprotein J Invest Dermatol 127 2191 2206 17495963 10.1038/sj.jid.5700849 1:CAS:528:DC%2BD2sXptVWhtrs%3D (Pubitemid 47258491)
50. Shi SR, Gu J, Taylor CR (2000) Antigen retrieval techniques: Immunohistochemistry and molecular morphology. Eaton Publishing, Natick
51. GS Sidhu P Chandra ND Cassai 2005 Merkel cells, normal and neoplastic: an update Ultrastruct Pathol 29 287 294 16036883 10.1080/01913120590951284 (Pubitemid 40993753)
52. LA Staehelin 1974 Structure and function of intercellular junctions Int Rev Cytol 39 191 283 4611943 10.1016/S0074-7696(08)60940-7 1:STN:280: DyaE2M%2FlvFOmuw%3D%3D
53. T Tachibana 1995 The Merkel cell: recent findings and unresolved problems Arch Histol Cytol 58 379 396 8562130 10.1679/aohc.58.379 1:STN:280: DyaK287lsVeruw%3D%3D
54. T Tachibana T Kamegai N Takahashi T Nawa 1998 Evidence for polymorphism of Merkel cells in the adult human oral mucosa Arch Histol Cytol 61 115 124 9650886 10.1679/aohc.61.115 1:STN:280:DyaK1czht12jtA%3D%3D (Pubitemid 28287655)
55. A van Keymeulen G Mascre KK Youseff I Harel C Michaux N De Geest C Szpalski Y Achouri W Bloch BA Hassan C Blanpain 2009 Epidermal progenitors give rise to Merkel cells during embryonic development and adult homeostasis J Cell Biol 187 91 100 19786578 10.1083/jcb.200907080
56. GN van Muijen SO Warnaar M Ponec 1987 Differentiation-related changes of cytokeratin expression in cultured keratinocytes and in fetal, newborn, and adult epidermis Exp Cell Res 171 331 345 2442018 10.1016/0014-4827(87)90166-2 (Pubitemid 18006686)
57. AM Werling Y Doerflinger JM Brandner F Fuchs JC Becker D Schrama H Kurzen S Goerdt WK Peitsch 2011 Homo- and heterotypic cell-cell contacts in Merkel cells and Merkel cell carcinomas: heterogeneity and indications for cadherin switching Histopathology 58 286 303 21323954 10.1111/j.1365-2559.2011.03748.x
58. SH Woo M Stumpfova UB Jensen EA Lumpkin DM Owens 2010 Identification of epidermal progenitors for the Merkel cell lineage Development 137 3965 3971 21041368 10.1242/dev.055970 1:CAS:528:DC%2BC3MXlsVemtw%3D%3D