Collagen XVII and BP AG1 expression in the retina: Evidence for an anchoring complex in the central nervous system

Journal of Comparative Neurology

Volumn 487, Issue 2, 2005, Pages 190-203

  Claudepierre, Thomas ^a,e   Manglapus, Mary K ^a   Marengi, Nathan ^a   Radner, Stephanie ^a   Champliaud, Marie France ^b,f   Tasanen, Kaisa ^c   Bruckner Tuderman, Leena ^d   Hunter, Dale D ^a   Brunken, William J ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c UNIVERSITY OF OULU   (Finland)

^d UNIVERSITY OF FREIBURG   (Germany)

^e CENTRE DE NEUROCHIMIE   (France)

^f GENEVA UNIVERSITY HOSPITALS   (Switzerland)

Author keywords

CNS development; Extracellular matrix; Hemidesmosomes; Photoreceptor; Synaptogenesis

Indexed keywords

BULLOUS PEMPHIGOID ANTIGEN 1; LAMININ; PROTEIN BP180; UNCLASSIFIED DRUG; ASPARTIC PROTEINASE; AUTOANTIGEN; CALCIUM BINDING PROTEIN; COLLAGEN TYPE 17; COLLAGENASE; KINESIN; KINESIN II; KINESIN-II; LAMININ S; MEMBRANE PROTEIN; MESSENGER RNA; MUSCLE PROTEIN; NERVE PROTEIN; NONFIBRILLAR COLLAGEN; PEANUT AGGLUTININ; PLACENTA PROTEIN; POSTSYNAPTIC DENSITY PROTEINS; PREGNANCY ASSOCIATED GLYCOPROTEIN 1; PREGNANCY-ASSOCIATED GLYCOPROTEIN 1; VIMENTIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COMPARTMENTALIZATION; COMPLEX FORMATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; MOUSE; MUELLER CELL; NONHUMAN; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; RAT; RETINA CONE; RETINA DEVELOPMENT; RETINA ROD; SYNAPSE; SYNAPTOGENESIS; ANIMAL; CATTLE; CELL LINE; CENTRAL NERVOUS SYSTEM; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; CYTOLOGY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; GLIA; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; KERATINOCYTE; METABOLISM; METHODOLOGY; NEWBORN; NORTHERN BLOTTING; PHYSIOLOGY; RETINA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYNAPTOSOME; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; ASPARTIC ENDOPEPTIDASES; AUTOANTIGENS; BLOTTING, NORTHERN; BLOTTING, WESTERN; CALCIUM-BINDING PROTEINS; CATTLE; CELL LINE; CENTRAL NERVOUS SYSTEM; COLLAGENASES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; KERATINOCYTES; KINESIN; LAMININ; MEMBRANE GLYCOPROTEINS; MICE; MODELS, MOLECULAR; MUSCLE PROTEINS; NERVE TISSUE PROTEINS; NEUROGLIA; NON-FIBRILLAR COLLAGENS; PEANUT AGGLUTININ; PREGNANCY PROTEINS; RATS; RETINA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SYNAPTOSOMES; VIMENTIN;

EID: 19544394260     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20549     Document Type: Article

References (63)

1. Aho S, Uitto J. 1998. Direct interaction between the intracellular domains of bullous pemphigoid antigen 2 (BP180) and α4 integrin, hemidesmosomal components of basal keratinocytes. Biochem Biophys Res Commun 243:694-699.
2. Aho S, Rothenberger K, Uitto J. 1999. Human p120ctn catenin: tissue-specific expression of isoforms and molecular interactions with BP180/ type XVII collagen. J Cell Biochem 73:390-399.
3. Anton ES, Sandrock AW Jr, Matthew WD 1994. Merosin promotes neurite growth and Schwann cell migration in vitro and nerve regeneration in vivo: evidence using an antibody to merosin, ARM-1. Dev Biol 164:133-146.
4. Bernier G, Brown A, Dalpe G, De Repentigny Y, Mathieu M, Kothary R. 1995. Dystonin expression in the developing nervous system predominates in the neurons that degenerate in dystonia musculorum mutant mice. Mol Cell Neurosci 6:509-520.
5. Blackshaw S, Fraioli RE, Furukawa T, Cepko CL. 2001. Comprehensive analysis of photoreceptor gene expression and the identification of candidate retinal disease genes. Cell 107:579-589.
6. Brown A, Bernier G, Mathieu M, Rossant J, Kothary R. 1995. The mouse dystonia musculorum gene is a neural isoform of bullous pemphigoid antigen 1. Nat Genet 10:301-306.
7. Claudepierre T, Rodius F, Frasson M, Fontaine V, Picaud S, Dreyfus H, Mornet D, Rendon A. 1999. Differential distribution of dystrophins in rat retina. Invest Ophthalmol Vis Sci 40:1520-1529.
8. Claudepierre T, Dalloz C, Mornet D, Matsumura K, Sahel J, Rendon A. 2000. Characterization of the intermolecular associations of the dystrophin- associated glycoprotein complex in retinal Muller glial cells. J Cell Sci 113:3409-3417.
9. Colognato H, Yurchenco, PD. 2000. Form and function: the laminin family of heterotrimers. Dev Dyn 218:213-234.
10. Dalloz C, Claudepierre T, Rodius F, Mornet D, Sahel J, Rendon A. 2001. Differential distribution of the members of the dystrophin glycoprotein complex in mouse retina: effect of the mdx(SCv) mutation. Mol Cell Neurosci 17:908-920.
11. Dalpe G, Leclerc N, Vallee A, Messer A, Mathieu M, De Repentigny Y. Kothary R. 1998. Dystonin is essential for maintaining neuronal cytoskeleton organization. Mol Cell Neurosci 10:243-257.
12. Duchen LW, Strich SJ. 1963. Clinical and pathological studies of an hereditary neuropathy in mice (dystonia musculorum). Brain 87:367-378.
13. Dunkley PR, Jarvie PE, Heath JW, Kidd GJ, Rostas JA. 1986. A rapid method for isolation of synaptosomes on Percoll gradients. Brain Res 372:115-129.
14. Eckmiller MS. 2000. Microtubules in a rod-specific cytoskeleton associated with outer segment incisures. Vis Neurosci 17:711-722.
15. Favre B, Fontao L, Koster J, Shafaatian R, Jaunin F, Saurat JH, Sonnenberg A, Borradori L. 2001. The hemidesmosomal protein bullous pemphigoid antigen 1 and the integrin β4 subunit bind to ERBIN. Molecular cloning of multiple alternative splice variants of ERBIN and analysis of their tissue expression. J Biol Chem 276:32427-32436.
16. Fernandez-Valle C, Gwynn L, Wood PM, Carbonetto S, Bunge MB. 1994. Anti-beta 1 integrin antibody inhibits Schwann cell myelination. J Neurobiol 25:1207-1226.
17. Foureur N, Descamps V, Lebrun-Vignes B, Picard-Dahan C, Grossin M, Belaich S, Crickx B. 2001. Bullous pemphigoid in a leg affected with hemiparesia: a possible relation of neurological diseases with bullous pemphigoid? Eur J Dermatol 11:230-233.
18. Franzke CW, Tasanen K, Schacke H, Zhou Z, Tryggvason K, Mauch C, Zigrino P, Sunnarborg S, Lee DC, Fahrenholz F, Bruckner-Tuderman L. 2002. Transmembrane collagen XVII, an epithelial adhesion protein, is shed from the cell surface by ADAMs. EMBO J 21:5026-5035.
19. Friedman GC, O'Leary DD. 1996. Retroviral misexpression of engrailed genes in the chick optic tectum perturbs the topographic targeting of retinal axons. J Neurosci 16:5498-5509.
20. Georges-Labouesse E, Messaddeq N, Yehia G, Cadalbert L, Dierich A, Le Meur M. 1996. Absence of integrin alpha 6 leads to epidermolysis bullosa and neonatal death in mice. Nat Genet 13:370-373.
21. Georges-Labouesse E, Mark M, Messaddeq N, Gansmuller A. 1998. Essential role of alpha 6 integrins in cortical and retinal lamination. Curr Biol 8:983-986.
22. Golenhofen N, Drenckhahn D. 2000. The catenin, p120ctn, is a common membrane-associated protein in various epithelial and non-epithelial cells and tissues. Histochem Cell Biol 114:147-155.
23. Gong TW, Besirli CG, Lomax MI. 2001. MACF1 gene structure: a hybrid of plectin and dystrophin. Mamm Genome 12:852-861.
24. Grimpe B, Dong S, Doller C, Temple K, Malouf AT, Silver J. 2002. The critical role of basement membrane-independent laminin γ1 chain during axon regeneration in the CNS. J Neurosci 22:3144-3460.
25. Gumbiner BM. 1996. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84:345-357.
26. Halfter W, Dong S, Yip YP, Willem M, Mayer U. 2002. A critical function of the pial basement membrane in cortical histogenesis. J Neurosci 22:6029-6040.
27. Hashimoto T, Wakabayashi T, Watanabe A, Kowa H, Hosoda R, Nakamura A, Kanazawa I, Arai T, Takio K, Mann DM, Iwatsubo T. 2002. CLAC: a novel Alzheimer amyloid plaque component derived from a transmembrane precursor, CLAC-P/collagen type XXV. EMBO J 21:1524-1534.
28. Helbling-Leclerc A, Zhang X, Topaloglu H, Cruaud C, Tesson F, Weissenbach J, Tome FM, Schwartz K, Fardeau M, Tryggvason K, Guicheney P. 1995. Mutations in the laminin α2-chain gene (LAMA2) cause merosin-deficient congenital muscular dystrophy. Nat Genet 11:216-218.
29. Hopkinson SB, Jones JC. 2000. The N terminus of the transmembrane protein BP180 interacts with the N-terminal domain of BP230, thereby mediating keratin cytoskeleton anchorage to the cell surface at the site of the hemidesmosome. Mol Biol Cell 11:277-286.
30. Hopkinson SB, Baker SE, Jones JC. 1995. Molecular genetic studies of a human epidermal autoantigen (the 180-kD bullous pemphigoid antigen/BP180): identification of functionally important sequences within the BP180 molecule and evidence for an interaction between BP180 and α6 integrin. J Cell Biol 130:117-125.
31. Hunter DD, Shah V, Merlie JP, Sanes JR. 1989. A laminin-like adhesive protein concentrated in the synaptic cleft of the neuromuscular junction. Nature 338:229-234.
32. Hunter DD, Murphy MD, Olsson CV, Brunken WJ. 1992. S-laminin expression in adult and developing retinae: a potential cue for photoreceptor morphogenesis. Neuron 8:399-413.
33. Jones JC, Hopkinson SB, Goldfinger LE. 1998. Structure and assembly of hemidesmosomes. Bioessays 20:488-494.
34. Koch M, Olson PF, Albus A, Jin W, Hunter DD, Brunken WJ, Burgeson RE, Champliaud MF. 1999. Characterization and expression of the laminin γ3 chain: a novel, non-basement membrane-associated, laminin chain. J Cell Biol 145:605-618.
35. Koster J, Geerts D, Favre B, Borradori L, Sonnenberg A. 2003. Analysis of the interactions between BP180, BP230, plectin and the integrin α6β4 important for hemidesmosome assembly. J Cell Sci 116:387-399.
36. Labib RS, Anhalt GJ, Patel HP, Mutasim DF, Diaz LA. 1986. Molecular heterogeneity of the bullous pemphigoid antigens as detected by immunoblotting. J Immunol 136:1231-1235.
37. Lazarus HS, Hageman GS. 1992. Xyloside-induced disruption of interphotoreceptor matrix proteoglycans results in retinal detachment. Invest Ophthalmol Vis Sci 33:364-376.
38. Leung CL, Zheng M, Prater SM, Liem RK. 2001. The BPAG1 locus: Alternative splicing produces multiple isoforms with distinct cytoskeletal linker domains, including predominant isoforms in neurons and muscles. J Cell Biol 154:691-697.
39. Li K, Tamai K, Tan EM, Uitto J. 1993. Cloning of type XVII collagen: Complementary and genomic DNA sequences of mouse 180-kilodalton bullous pemphigoid antigen (BPAG2) predict an interrupted collagenous domain, a transmembrane segment, and unusual features in the 5′-end of the gene and the 3′-untranslated region of the mRNA. J Biol Chem 268:8825-8834.
40. Libby RT, Hunter DD, Brunken WJ. 1996. Developmental expression of laminin β2 in the rat retina. Invest Ophthal Vis Sci 37:1651-1661.
41. Libby RT, Xu Y, Selfors LM, Brunken WJ, Hunter DD. 1997. Identification of the cellular source of laminin β2 in adult and developing vertebrate retinae. J Comp Neurol 389:655-667.
42. Libby RT, Lavallee CR, Balkema GW, Brunken WJ, Hunter DD. 1999. Disruption of laminin β2 chain production causes alterations in morphology and function in the CNS. J Neurosci 19:9399-9411.
43. Libby RT, Champliaud MF, Claudepierre T, Xu Y, Gibbons EP, Koch M, Burgeson RE, Hunter DD, Brunken WJ. 2000. Laminin expression in adult and developing retinae: evidence of two novel CNS laminins. J Neurosci 20:6517-6128.
44. Mainguy G, Montesinos ML, Lesaffre B, Zevnik B, Karasawa M, Kothary R, Wurst W, Prochiantz A, Volovitch M. 2000. An induction gene trap for identifying a homeoprotein-regulated locus. Nat Biotechnol 18:746-749.
45. Masunaga T, Shimizu H, Yee C, Borradori L, Lazarova Z, Nishikawa T, Yancey KB. 1997. The extracellular domain of BPAG2 localizes to anchoring filaments and its carboxyl terminus extends to the lamina densa of normal human epidermal basement membrane. J Invest Dermatol 109:200-206.
46. McGrath JA, Gatalica B, Christiano AM, Li K, Owaribe K, McMillan JR, Eady RA, Uitto J. 1995. Mutations in the 180-kD bullous pemphigoid antigen (BPAG2), a hemidesmosomal transmembrane collagen (COL17A1), in generalized atrophic benign epidermolysis bullosa. Nat Genet 11:83-86.
47. Miceli MV. Newsome DA. 1996. Effects of extracellular matrix and Bruch's membrane on retinal outer segment phagocytosis by cultured human retinal pigment epithelium. Curr Eye Res 15:17-26.
48. Moore SA, Saito F, Chen J, Michele DE, Henry MD, Messing A, Cohn RD, Ross-Barta SE, Westra S, Williamson RA, Hoshi T, Campbell KP. 2002. Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy. Nature 418:422-425.
49. Niessen CM, Hogervorst F, Jaspars LH, de Melker AA, Delwel GO, Hulsman EH, Kuikman I, Sonnenberg A. 1994. The alpha 6 beta 4 integrin is a receptor for both laminin and kalinin. Exp Cell Res 211:360-367.
50. Noakes PG, Gautam M, Mudd J, Sanes JR, Merlie JP. 1995. Aberrant differentiation of neuromuscular junctions in mice lacking s-Iaminin/ Iaminin β2. Nature 374:258-262.
51. Okumura M, Yamakawa H, Ohara O, Owaribe K. 2002. Novel alternative splicings of BPAG1 (bullous pemphigoid antigen 1) including the domain structure closely related to MACF (microtubule actin crosslinking factor). J Biol Chem 277:6682-6687.
52. Olson EC, Walsh CA. 2002. Smooth, rough and upside-down neocortical development. Curr Opin Genet Dev 12:320-327.
53. Patton BL, Chiu AY, Sanes JR. 1998. Synaptic laminin prevents glial entry into the synaptic cleft. Nature. 393:698-701.
54. Patton BL, Cunningham JM, Thyboll J, Kortesmaa J, Westerblad H, Edstrom L, Tryggvason K, Sanes JR. 2001. Properly formed but im properly localized synaptic specializations in the absence of laminin alpha4. Nat Neurosci 4:597-604.
55. Schaapveld RQ, Borradori L, Geerts D, van Leusden MR, Kuikman I, Nievers MG, Niessen CM, Steenbergen RD, Snijders PJ, Sonnenberg A. 1998. Hemidesmosome formation is initiated by the beta4 integrin subunit, requires complex formation of beta4 and HD1/plectin, and involves a direct interaction between beta4 and the bullous pemphigoid antigen 180. J Cell Biol 142:271-284.
56. Schäcke H, Schumann H, Hammami-Hauasli N, Raghunath M, Bruckner-Tuderman L. 1998. Two forms of collagen XVII in keratinpcytes. A full-length transmembrane protein and a soluble ectodomain. J Biol Chem 273:25937-25943.
57. Schumann H, Baetge J, Tasanen K, Wojnarowska F, Schacke H, Zillikens D, Bruckner-Tuderman L. 2000. The shed ectodomain of collagen XVII/ BP180 is targeted by autoantibodies in different blistering skin diseases. Am J Pathol 156:685-695.
58. Soussand J, Jahke R, Simon-Assmann P, Stoeckel ME, Schimchowitsch S. 2001. Tenascin and laminin function in target recognition and central synaptic differentiation. Neuroreport 12:1073-1076.
59. Van der Neut R, Krimpenfort P, Calafat J, Niessen CM, Sonnenberg A. 1996. Epithelial detachment due to absence of hemidesmosomes in integrin beta 4 null mice. Nat. Genet. 13:366-369.
60. Wewer UM, Durkin ME, Zhang X, Laursen H, Nielsen NH, Towfighi J, Engvall E, Albrechtsen R. 1995. Laminin β2 chain and adhalin deficiency in the skeletal muscle of Walker-Warburg syndrome (cerebroocular dysplasia-muscular dystrophy). Neurology 45:2099-2101.
61. Yang B, Jung D, Motto D, Meyer J, Koretzky G, Campbell KP. 1995. SH3 domain-mediated interaction of dystroglycan and Grb2. J Biol Chem 270:11711-11714.
62. Yang Y, Dowling J, Yu QC, Kouklis P, Cleveland DW, Fuchs E. 1996. An essential cytoskeletal linker protein connecting actin microfilaments to intermediate filaments. Cell 86:655-665.
63. Yang Y, Bauer C, Strasser G, Wollman R, Julien JP, Fuchs E. 1999. Integrators of the cytoskeleton that stabilize microtubules. Cell 98: 229-238.