The rod domain is not essential for the function of plectin in maintaining tissue integrity

Molecular Biology of the Cell

Volumn 26, Issue 13, 2015, Pages 2402-2417

  Ketema, Mirjam ^a   Secades, Pablo ^a   Kreft, Maaike ^a   Nahidiazar, Leila ^a   Janssen, Hans ^a   Jalink, Kees ^a   De Pereda, Jose M ^b   Sonnenberg, Arnoud ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BETA4 INTEGRIN; DIMER; ISOPROTEIN; PLECTIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLISTER; CELL MIGRATION; CONTROLLED STUDY; EXON; GENE DELETION; HEMIDESMOSOME; KERATINOCYTE; MICROSCOPY; MOUSE; MUSCULAR DYSTROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; WILD TYPE; WOUND HEALING; ANIMAL; C57BL MOUSE; CYTOSKELETON; EPIDERMOLYSIS BULLOSA SIMPLEX; FEMALE; GENETICS; LIMB GIRDLE MUSCULAR DYSTROPHY; MALE; METABOLISM; PATHOLOGY; PROTEIN TERTIARY STRUCTURE;

MUS;

ANIMALS; CYTOSKELETON; EPIDERMOLYSIS BULLOSA SIMPLEX; FEMALE; HEMIDESMOSOMES; INTEGRIN BETA4; KERATINOCYTES; MALE; MICE; MICE, INBRED C57BL; MODELS, ANIMAL; MUSCULAR DYSTROPHIES, LIMB-GIRDLE; PLECTIN; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY;

EID: 84934311750     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E15-01-0043     Document Type: Article

References (60)

1. Andrä K, Lassmann H, Bittner R, Shorny S, Fässler R, Propst F, Wiche G (1997). Targeted inactivation of plectin reveals essential function in maintaining the integrity of skin, muscle, and heart cytoarchitecture. Genes Dev 11, 3143-3156.
2. Andrä K, Nikolic B, Stöcher M, Drenckhahn D, Wiche G (1998). Not just scaffolding: plectin regulates actin dynamics in cultured cells. Genes Dev 12, 3442-3451.
3. Anton M, Graham FL (1995). Site-specific recombination mediated by an adenovirus vector expressing the Cre recombinase protein: a molecular switch for control of gene expression. J Virol 69, 4600-4606.
4. Auinger S, Small JV (2008). Correlated light and electron microscopy of the cytoskeleton. Methods Cell Biol 88, 257-272.
5. Borradori L, Sonnenberg A (1999). Structure and function of hemidesmosomes: more than simple adhesion complexes. J Invest Dermatol 112, 411-418.
6. Charlesworth A, Gagnoux-Palacios L, Bonduelle M, Ortonne JP, De Raeve L, Meneguzzi G (2003). Identification of a lethal form of epidermolysis bullosa simplex associated with a homozygous genetic mutation in plectin. J Invest Dermatol 121, 1344-1348.
7. Delorenzi M, Speed T (2002). An HMM model for coiled-coil domains and a comparison with PSSM-based predictions. Bioinformatics 18, 617-625.
8. de Pereda JM, Lillo MP, Sonnenberg A (2009). Structural basis of the interaction between integrin alpha6beta4 and plectin at the hemidesmosomes. EMBO J 28, 1180-1190.
9. Eger A, Stockinger A, Wiche G, Foisner R (1997). Polarisation-dependent association of plectin with desmoplakin and the lateral submembrane skeleton in MDCK cells. J Cell Sci 110, 1307-1316.
10. Elliott CE, Becker B, Oehler S, Castañón MJ, Hauptmann R, Wiche G (1997). Plectin transcript diversity: identification and tissue distribution of variants with distinct first coding exons and rodless isoforms. Genomics 42, 115-125.
11. Ervasti JM, Campbell KP (1991). Membrane organization of the dystrophinglycoprotein complex. Cell 66, 1121-1131.
12. Fine JD, Stenn J, Johnson L, Wright T, Bock HG, Horiguchi Y (1989). Autosomal recessive epidermolysis bullosa simplex. Generalized phenotypic features suggestive of junctional or dystrophic epidermolysis bullosa, and association with neuromuscular diseases. Arch Dermatol 125, 931-938.
13. Foisner R, Feldman B, Sander L, Seifert G, Artlieb U, Wiche G (1994). A panel of monoclonal antibodies to rat plectin: distinction by epitope mapping and immunoreactivity with different tissues and cell lines. Acta Histochem 96, 421-438.
14. Foisner R, Feldman B, Sander L, Wiche G (1991). Monoclonal antibody mapping of structural and functional plectin epitopes. J Cell Biol 112, 397-405.
15. Foisner R, Wiche G (1987). Structure and hydrodynamic properties of plectin molecules. J Mol Biol 198, 515-531.
16. Fontao L, Geerts D, Kuikman I, Koster J, Kramer D, Sonnenberg A (2001). The interaction of plectin with actin: evidence for cross-linking of actin filaments by dimerization of the actin-binding domain of plectin. J Cell Sci 114, 2065-2076.
17. Frijns E, Sachs N, Kreft M, Wilhelmsen K, Sonnenberg A (2010). EGF-induced MAPK signaling inhibits hemidesmosome formation through phosphorylation of the integrin b4. J Biol Chem 285, 37650-37662.
18. Fuchs P, Spazierer D, Wiche G (2005). Plectin rodless isoform expression and its detection in mouse brain. Cell Mol Neurobiol 25, 1141-1150.
19. Gache Y, Chavanas S, Lacour JP, Wiche G, Owaribe K, Meneguzzi G, Ortonne JP (1996). Defective expression of plectin/HD1 in epidermolysis bullosa simplex with muscular dystrophy. J Clin Invest 97, 2289-2298.
20. Geerts D, Fontao L, Nievers MG, Schaapveld RQ, Purkis PE, Wheeler GN, Lane EB, Leigh IM, Sonnenberg A (1999). Binding of integrin a6b4 to plectin prevents plectin association with F-actin but does not interfere with intermediate filament binding. J Cell Biol 147, 417-434.
21. Green KJ, Virata ML, Elgart GW, Stanley JR, Parry DA (1992). Comparative structural analysis of desmoplakin, bullous pemphigoid antigen and plectin: members of a new gene family involved in organization of intermediate filaments. Int J Biol Macromol 14, 145-153.
22. Hamelers IH, Olivo C, Mertens AE, Pegtel DM, van der Kammen RA, Sonnenberg A, Collard JG (2005). The Rac activator Tiam1 is required for a3b1-mediated laminin-5 deposition, cell spreading, and cell migration. J Cell Biol 171, 871-881.
23. Hashimoto T, Amagai M, Ebihara T, Gamou S, Shimizu N, Tsubata T, Hasegawa A, Miki K, Nishikawa T (1993). Further analyses of epitopes for human monoclonal anti-basement membrane zone antibodies produced by stable human hybridoma cell lines constructed with Epstein- Barr virus transformants. J Invest Dermatol 100, 310-315.
24. Ketema M, Kreft M, Secades P, Janssen H, Sonnenberg A (2013). Nesprin-3 connects plectin and vimentin to the nuclear envelope of Sertoli cells but is not required for Sertoli cell function in spermatogenesis. Mol Biol Cell 24, 2454-2466.
25. Ketema M, Wilhelmsen K, Kuikman I, Janssen H, Hodzic D, Sonnenberg A (2007). Requirements for the localization of nesprin-3 at the nuclear envelope and its interaction with plectin. J Cell Sci 120, 3384-3394.
26. Koss-Harnes D, Høyheim B, Anton-Lamprecht I, Gjesti A, Jørgensen RS, Jahnsen FL, Olaisen B, Wiche G, Gedde-Dahl T Jr (2002). A site-specific plectin mutation causes dominant epidermolysis bullosa simplex Ogna: two identical de novo mutations. J Invest Dermatol 118, 87-93.
27. Koster J, van Wilpe S, Kuikman I, Litjens SH, Sonnenberg A (2004). Role of binding of plectin to the integrin b4 subunit in the assembly of hemidesmosomes. Mol Biol Cell 15, 1211-1223.
28. Le Rumeur E, Hubert JF, Winder SJ (2012). A new twist to coiled coil. FEBS Lett 586, 2717-2722.
29. Luo J, Deng ZL, Luo X, Tang N, Song WX, Chen J, Sharff KA, Luu HH, Haydon RC, Kinzler KW, et al. (2007). A protocol for rapid generation of recombinant adenoviruses using the AdEasy system. Nat Protoc 2, 1236-1247.
30. Lupas A, van Dyke M, Stock J (1991). Predicting coiled coils from protein sequences. Science 252, 1162-1164.
31. McDonnell AV, Jiang T, Keating AE, Berger B (2006). Paircoil2: improved prediction of coiled coils from sequence. Bioinformatics 22, 356-358.
32. McLean WH, Pulkkinen L, Smith FJ, Rugg EL, Lane EB, Bullrich F, Burgeson RE, Amano S, Hudson DL, Owaribe K, et al. (1996). Loss of plectin causes epidermolysis bullosa with muscular dystrophy: cDNA cloning and genomic organization. Genes Dev 10, 1724-1735.
33. Nakamura H, Sawamura D, Goto M, McMillan JR, Park S, Kono S, Hasegawa S, Paku S, Nakamura T, Ogiso Y, Shimizu H (2005). Epidermolysis bullosa simplex associated with pyloric atresia is a novel clinical subtype caused by mutations in the plectin gene (PLEC1). J Mol Diagn 7, 28-35.
34. Natsuga K, Nishie W, Akiyama M, Nakamura H, Shinkuma S, McMillan JR, Nagasaki A, Has C, Ouchi T, Ishiko A, et al. (2010). Plectin expression patterns determine two distinct subtypes of epidermolysis bullosa simplex. Hum Mutat 31, 308-316.
35. Nikolic B, Mac Nulty E, Mir B, Wiche G (1996). Basic amino acid residue cluster within nuclear targeting sequence motif is essential for cytoplasmic plectin-vimentin network junctions. J Cell Biol 134, 1455-1467.
36. O'Gorman S, Wahl GM (1997). Mouse engineering. Science 277, 1025.
37. Ovesný M, Křížek P, Borkovec J, Švindrych Z, Hagen GM (2014). ThunderSTORM: a comprehensive ImageJ plug-in for PALM and STORM data analysis and super-resolution imaging. Bioinformatics 30, 2389-2390.
38. Pfendner E, Rouan F, Uitto J (2005). Progress in epidermolysis bullosa: the phenotypic spectrum of plectin mutations. Exp Dermatol 14, 241-249.
39. Pfendner E, Uitto J (2005). Plectin gene mutations can cause epidermolysis bullosa with pyloric atresia. J Invest Dermatol 124, 111-115.
40. Pulkkinen L, Smith FJ, Shimizu H, Murata S, Yaoita H, Hachisuka H, Nishikawa T, McLean WH, Uitto J (1996). Homozygous deletion mutations in the plectin gene (PLEC1) in patients with epidermolysis bullosa simplex associated with late-onset muscular dystrophy. Hum Mol Genet 5, 1539-1546.
41. Rabinovitz I, Tsomo L, Mercurio AM (2004). Protein kinase C-alpha phosphorylation of specific serines in the connecting segment of the beta 4 integrin regulates the dynamics of type II hemidesmosomes. Mol Cell Biol 24, 4351-4360.
42. Rezniczek GA, de Pereda JM, Reipert S, Wiche G (1998). Linking integrin a6b4-based cell adhesion to the intermediate filament cytoskeleton: direct interaction between the b4 subunit and plectin at multiple molecular sites. J Cell Biol 141, 209-225.
43. Rodriguez CI, Buchholz F, Galloway J, Sequerra R, Kasper J, Ayala R, Stewart AF, Dymecki SM (2000). High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat Genet 25, 139-140.
44. Schröder R, Fürst DO, Klasen C, Reimann J, Herrmann H, van der Ven PF (2000). Association of plectin with Z-discs is a prerequisite for the formation of the intermyofibrillar desmin cytoskeleton. Lab Invest 80, 455-464.
45. Seifert GJ, Lawson D, Wiche G (1992). Immunolocalization of the intermediate filament-associated protein plectin at focal contacts and actin stress fibers. Eur J Cell Biol 59, 138-147.
46. Smith FJ, Eady RA, Leigh IM, McMillan JR, Rugg EL, Kelsell DP, Bryant SP, Spurr NK, Geddes JF, Kirtschig G, et al. (1996). Plectin deficiency results in muscular dystrophy with epidermolysis bullosa. Nat Genet 13, 450-457.
47. Sonnenberg A, Janssen H, Hogervorst F, Calafat J, Hilgers J (1987). A complex of platelet glycoproteins Ic and IIa identified by a rat monoclonal antibody. J Biol Chem 262, 10376-10383.
48. Sonnenberg A, Liem RK (2007). Plakins in development and disease. Exp Cell Res 313, 2189-2203.
49. Stegh AH, Herrmann H, Lampel S, Weisenberger D, Andrä K, Seper M, Wiche G, Krammer PH, Peter ME (2000). Identification of the cytolinker plectin as a major early in vivo substrate for caspase 8 during CD95- and tumor necrosis factor receptor-mediated apoptosis. Mol Cell Biol 20, 5665-5679.
50. Steinboeck F, Kristufek D (2005). Identification of the cytolinker protein plectin in neuronal cells - expression of a rodless isoform in neurons of the rat superior cervical ganglion. Cell Mol Neurobiol 25, 1151-1169.
51. Sterk LM, Geuijen CA, Oomen LC, Calafat J, Janssen H, Sonnenberg A (2000). The tetraspan molecule CD151, a novel constituent of hemidesmosomes, associates with the integrin a6b4 and may regulate the spatial organization of hemidesmosomes. J Cell Biol 149, 969-982.
52. Touznik A, Lee JJ, Yokota T (2014). New developments in exon skipping and splice modulation therapies for neuromuscular diseases. Expert Opin Biol Ther 14, 809-819.
53. Uitto J, Pulkkinen L, Smith FJ, McLean WH (1996). Plectin and human genetic disorders of the skin and muscle. The paradigm of epidermolysis bullosa with muscular dystrophy. Exp Dermatol 5, 237-246.
54. van der Weyden L, Adams DJ, Harris LW, Tannahill D, Arends MJ, Bradley A (2005). Null and conditional semaphorin 3B alleles using a flexible puroDeltatk loxP/FRT vector. Genesis 41, 171-178.
55. Walko G, Vukasinovic N, Gross K, Fischer I, Sibitz S, Fuchs P, Reipert S, Jungwirth U, Berger W, Salzer U, et al. (2011). Targeted proteolysis of plectin isoform 1a accounts for hemidesmosome dysfunction in mice mimicking the dominant skin blistering disease EBS-Ogna. PLoS Genet 7, e1002396.
56. Wiche G (1998). Role of plectin in cytoskeleton organization and dynamics. J Cell Sci 111, 2477-2486.
57. Wiche G, Becker B, Luber K, Weitzer G, Castañón MJ, Hauptmann R, Stratowa C, Stewart M (1991). Cloning and sequencing of rat plectin indicates a 466-kD polypeptide chain with a three-domain structure based on a central alpha-helical coiled coil. J Cell Biol 114, 83-99.
58. Wiche G, Krepler R, Artlieb U, Pytela R, Denk H (1983). Occurrence and immunolocalization of plectin in tissues. J Cell Biol 97, 887-901.
59. Wilhelmsen K, Litjens SH, Kuikman I, Margadant C, van Rheenen J, Sonnenberg A (2007). Serine phosphorylation of the integrin b4 subunit is necessary for epidermal growth factor receptor induced hemidesmosome disruption. Mol Biol Cell 18, 3512-3522.
60. Wilhelmsen K, Litjens SH, Kuikman I, Tshimbalanga N, Janssen H, van den Bout I, Raymond K, Sonnenberg A (2005). Nesprin-3, a novel outer nuclear membrane protein, associates with the cytoskeletal linker protein plectin. J Cell Biol 171, 799-810.