Characterization and expression of the laminin γ3 chain: A novel, non- basement membrane-associated, laminin chain

Journal of Cell Biology

Volumn 145, Issue 3, 1999, Pages 605-617

  Koch, Manuel ^a   Olson, Pamela F ^a   Albus, Anne ^a   Jin, William ^a   Hunter, Dale D ^b   Brunken, William J ^a   Burgeson, Robert E ^a   Champliaud, Marie France ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Chromosome 9q31 34; Laminin; Lung; Oviduct; Testis

Indexed keywords

LAMININ;

ARTICLE; BASEMENT MEMBRANE; CELL ULTRASTRUCTURE; CHROMOSOME 9Q; DERMOEPIDERMAL JUNCTION; EPITHELIUM CELL; HUMAN; HUMAN CELL; MOLECULAR CLONING; MORPHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; RECEPTOR OCCUPANCY;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODY SPECIFICITY; BASEMENT MEMBRANE; BLOTTING, NORTHERN; CHORIONIC VILLI; CHROMOSOME MAPPING; CHROMOSOMES, HUMAN, PAIR 9; CILIA; CLONING, MOLECULAR; DNA, COMPLEMENTARY; EPITHELIAL CELLS; FALLOPIAN TUBES; FEMALE; HUMANS; IN SITU HYBRIDIZATION; INTEGRINS; LAMININ; LUNG; MALE; MOLECULAR SEQUENCE DATA; PERIPHERAL NERVES; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, COLLAGEN; RNA, MESSENGER; TESTIS;

EID: 0033519298     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.145.3.605     Document Type: Article

References (80)

1. Aebersold, R.H., J. Leavitt, R.A. Saavedra, L.E. Hood, and S.B.H. Kent. 1987. Internal amino acid sequence analysis of proteins separated by one-or two-dimensional gel electrophoresis after in situ protease digestion on nitrocellulose. Proc. Natl. Acad. Sci. USA. 84:6970-6974.
2. Altschul, S.F., W. Gish, W. Miller, E.W. Myers, and D.J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
3. Aumailley, M., C. Battaglia, U. Mayer, D. Reinhardt, R. Nischt, R. Timpl, and J.W. Fox. 1993. Nidogen mediates the formation of ternary complexes of basement membrane components. Kidney Int. 43:7-12.
4. Baker, S., S. Hopkinson, M. Fitchmun, G. Andreason, F. Frasier, G. Plopper, V. Quaranta, and J. Jones. 1996. Laminin-5 and hemidesmosomes: role of the alpha 3 chain subunit in hemidesmosome stability and assembly. J. Cell Sci. 109:2509-2520.
5. Battaglia, C., U. Mayer, M. Aumailley, and R. Timpl. 1992. Basement-membrane heparan sulfate proteoglycan binds to laminin by its heparan sulfate chains and to nidogen by sites in the protein core. Eur. J. Biochem. 208:359-366.
6. Boguski, M.S., T.M. Lowe, and C.M. Tolstoshev. 1993. dbEST-database for "expressed sequence tags." Nat. Genet. 4:332-333.
7. Burgeson, R.E., M. Chiquet, R. Deutzmann, P. Ekblom, J. Engel, H. Kleinman, G.R. Martin, G. Meneguzzi, M. Paulsson, J. Sanes, et al. 1994. A new nomenclature for the laminins. Matrix Biol. 14:209-211.
8. Chait, B.T., and S.B. Kent. 1992. Weighing naked proteins: practical, high-accuracy mass measurement of peptides and proteins. Science. 257:1885-1894.
9. Chen, L., V. Shick, M. Matter, S. Laurie, R. Ogle, and G. Laurie. 1997. Laminin E8 alveolarization site: heparin sensitivity, cell surface receptors, and role in cell spreading. Am. J. Physiol. 272:L494-L503.
10. Cohen, M., C. Jacobson, P. Yurchenco, G. Morris, and S. Carbonetto. 1997. Laminin-induced clustering of dystroglycan on embryonic muscle cells: comparison with agrin-induced clustering. J. Cell Biol. 136:1047-1058.
11. Day, I.N., L.J. Hinks, and R.J. Thompson. 1990. The structure of the human gene encoding protein gene product 9.5 (PGP9.5), a neuron-specific ubiquitin C-terminal hydrolase. Biochem. J. 268:521-524.
12. Deutzmann, R., M. Aumailley, H. Wiedemann, W. Pysny, R. Timpl. and D. Edgar. 1990. Cell adhesion, spreading and neurite stimulation by laminin fragment E8 depends on maintenance of secondary and tertiary structure in its rod and globular domain. Eur. J. Biochem. 191:513-522.
13. Drago, J., V. Nurcombe, and P.F. Bartlett. 1991. Laminin through its long arm E8 fragment promotes the proliferation and differentiation of murine neuroepithelial cells in vitro. Exp. Cell Res. 192:256-265.
14. Durkin, M., F. Loechel, M. Mattei, B. Gilpin, R. Albrechtsen, and U. Wewer. 1997. Tissue-specific expression of the human laminin alpha5-chain, and mapping of the gene to human chromosome 20q13.2-13.3 and to distal mouse chromosome 2 near the locus for the ragged (Ra) mutation. FEBS Lett. 411:296-300.
15. Durr, J., P. Lammi, S.L. Goodman, T. Aigner, and K. von der Mark. 1996. Identification and immunolocalization of laminin in cartilage. Exp. Cell Res. 222: 225-233.
16. Ekblom, P., and R. Timpl. 1996. The Laminins. In Cell Adhesion and Communication. Vol. 2. C. Goridis, editor. Harwood Academic Publishers, The Netherlands. 321 pp.
17. Engel, J. 1992. Laminins and other strange proteins. Biochemistry. 31:10643-10651.
18. Engvall, E. 1993. Laminin variants: why, where and when? Kidney Int. 43:2-6.
19. Engvall, E., D. Earwicker, T. Haaparanta, E. Ruoslahti, and J.R. Sanes. 1990. Distribution and isolation of four laminin variants; tissue restricted distribution of heterotrimers assembled from five different subunits. Cell Regul. 1:731-740.
20. Fox, J.W., U. Mayer, R. Nischt, M. Aumailley, D. Reinhardt, H. Wiedemann, K. Mann, R. Timpl, T. Krieg, J. Engel, et al. 1991. Recombinant nidogen consists of three globular domains and mediates binding of laminin to collagen type IV. EMBO (Eur. Mol. Biol. Organ.) J. 10:3137-3146.
21. Gerecke, D.R., D.W. Wagman, M.F. Champliaud, and R.E. Burgeson. 1994. The complete primary structure for a novel laminin chain, the laminin B1k chain. J. Biol. Chem. 269:11073-11080.
22. Goodman, S.L. 1992. Alpha 6 beta 1 integrin and laminin E8: an increasingly complex simple story. Kidney Int. 41:650-656.
23. Green, T.L., D.D. Hunter, W. Chan, J.P. Merlie, and J.R. Sanes. 1992. Synthesis and assembly of synaptic cleft protein s-laminin by cultured cells. J. Biol. Chem. 267:2014-2022.
24. Harlow, E., and D. Lane. 1988. Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
25. Haaparanta, T., J. Uitto, E. Ruoslahti, and E. Engvall. 1991. Molecular cloning of the cDNA encoding human laminin A chain. Matrix. 11:151-160.
26. Hagg, T., C. Portera-Cailliau, M. Jucker, and E. Engvall. 1997. Laminins of the adult mammalian CNS; laminin-alpha2 (merosin M-) chain immunoreactivity is associated with neuronal processes. Brain Res. 764:17-27.
27. Heimann, P., A. Menke, B. Rothkegel, and H. Jockusch. 1996. Overshooting production of satellite cells in murine skeletal muscle affected by the mutation "muscular dystrophy with myositis" (mdm, Chr 2). Cell Tissue Res. 283: 435-441.
28. Henry, M.D., and K.P. Campbell. 1996. Dystroglycan: an extracellular matrix receptor linked to the cyloskeleton. Curr. Opin. Cell Biol. 8:625-631.
29. Higuchi, M., T. Ohnishi, N. Arita, S. Hiraga, H. Iwasaki, S. Mori, and T. Hayakawa. 1991. Immunohistochemical localization of fibronectin. laminin and fibronectin-receptor in human malignant gliomas - in relation to tumor invasion. No to Shinkei. Brain Nerve (Tokyo). 43:17-23.
30. Hunter, D.D., and W.J. Brunken. 1997. Beta 2 laminins modulate neuronal phenotype in the rat retina. Mol. Cell. Neurosci. 10:7-15.
31. Hunter, D.D., R. Llinas, M. Ard, J.P. Merlie, and J.R. Sanes. 1992a. Expression of s-laminin and laminin in the developing rat central nervous system. J. Comp. Neurol. 323:238-251.
32. Hunter, D.D., M.D. Murphy, C.V. Olsson, and W.J. Brunken. 1992b S-laminin expression in adult and developing retinae: a potential cue for photoreceptor morphogenesis. Neuron. 8:399-413.
33. Iivanainen, A., K. Sainio, H. Sariola, and K. Tryggvason. 1995a. Primary structure and expression of a novel human laminin a4 chain. FEBS Lett. 365:183-188.
34. Iivanainen, A., R. Vuolteenaho, K. Sainio, R. Eddy, T.B. Shows, H. Sariola, and K. Tryggvason. 1995b. The human laminin beta 2 chain (S-laminin): structure, expression in fetal tissues and chromosomal assignment of the LAMB2 gene. Matrix Biol. 14:489-497.
35. Jucker, M., P. Bialobok, T. Hagg, and D.K. Ingram. 1992. Laminin immunohistochemistry in brain is dependent on method of tissue fixation. Brain Res. 586:166-170.
36. Jucker, M., M. Tian, and D. Ingram. 1996a. Laminins in the adult and aged brain. Mol. Chem. Neuropathol. 28:209-218.
37. Jucker, M., M. Tian, D. Norton, C. Sherman, and J. Kusiak. 1996b. Laminin alpha 2 is a component of brain capillary basement membrane: reduced expression in dystrophic dy mice. Neuroscience. 71:1153-1161.
38. Kallunki, P., K. Sainio, R. Eddy, M. Byers, T. Kallunki, H. Sariola, K. Beck, H. Hirvonen, T.B. Shows, and K. Tryggvason. 1992. A truncated laminin chain homologous to the B2 chain: structure, spatial expression, and chromosomal assignment. J. Cell Biol. 119:679-693.
39. Kobayashi, K., Y. Nakahori, M. Miyake, K. Matsumura, E. Kondo-Iida, Y. Nomura, M. Segawa, M. Yoshioka, K. Saito, et al. 1998. An ancient retrotransposal insertion causes Fukuyama-type congenital muscular dystrophy. Nature. 398:388-392.
40. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
41. Langhofer, M., S.B. Hopkinson, and J.C. Jones. 1993. The matrix secreted by 804G cells contains laminin-related components that participate in hemidesmosome assembly in vitro. J. Cell Sci. 105:753-764.
42. Libby, R.T., D.D. Hunter, and W.J. Brunken. 1996. Developmental expression of laminin beta 2 in rat retina. Further support for a role in rod morphogenesis. Investig. Ophthalmol. Vis. Sci. 37:1651-1661.
43. Libby, R.T., Y. Xu, L.M. Selfors, W.J. Brunken, and D.D. Hunter. 1997. Identification and cellular source of laminin β2 in adult and developing vertebrate retinae. J. Comp. Neurol. 389:655-667.
44. Libby, R.T., C. Lavalee, G.W. Balkema, W.J. Brunken, and D.D. Hunter. 1998. Characterization of laminin β2 in retinal function. Investig. Ophthalmol. Vis. Sci. 39:8574.
45. Liu, J., S. Swasdison, W. Xie, R.G. Brewton, and R. Mayne. 1998. Primary structure and expression of a chicken laminin beta chain: evidence for four beta chains in birds. Matrix Biol. 16:471-481.
46. Lunstrum, G.P., L.Y. Sakai, D.R. Keene, N.P. Morris, and R.E. Burgeson. 1986. Large complex globular domains of type VII procollagen contribute to the structure of anchoring fibrils. J. Biol. Chem. 261:9042-9048.
47. Marinkovich, M.P., G.P. Lunstrum, D.R. Keene, and R.E. Burgeson. 1992. The dermal-epidermal junction of human skin contains a novel laminin variant. J. Cell Biol. 119:695-703.
48. Matter, M.L., and G.W. Laurie. 1994. A novel laminin E8 cell adhesion site required for lung alveolar formation in vitro. J. Cell Biol. 124:1083-1090.
49. Mauer, P., and J. Engel. 1996. Structure of laminins and their chain assembly. In The Laminins, Vol. 2. P. Ekblom and R. Timpl, editor. Harwood Academic Publishers, The Netherlands. 27-50.
50. Mayer, U., R. Nischt, E. Poschl, K. Mann, K. Fukuda, M. Gerl, Y. Yamada, and R. Timpl. 1979. A single EGF-like motif of laminin is responsible for high affinity nidogen binding. EMBO (Eur. Mol. Biol. Organ.) J. 12:1879-1885.
51. Mayer, U., E. Poschl, D.R. Gerecke, D.W. Wagman, R.E. Burgeson, and R. Timpl. 1995. Low nidogen affinity of laminin-5 can be attributed to two serine residues in EGF-like motif gamma 2III4. FEBS Lett. 365:129-132.
52. Miner, J.H., B.L. Patton. S.I. Lentz, D.J. Gilbert, W.D. Snider, N.A. Jenkins, N.G. Copeland, and J.R. Sanes. 1997. The laminin a chains: expression, developmental transitions, and chromosomal locations of al-5, identification of heterotrimeric laminins 8-11 and cloning a novel a3 isoform. J. Cell Biol. 137:685-701.
53. Miner, J.H., R.M. Lewis, and J.R. Sanes. 1995. Molecular cloning of a novel laminin chain, alpha 5, and widespread expression in adult mouse tissues. J. Biol. Chem. 270:28523-28526.
54. Mori, S., N.H. Sternberger, M.M. Herman, and L.A. Sternberger. 1992. Variability of laminin immunoreactivity in human autopsy brain. Histochemistry. 97:237-241.
55. Nielsen, H., J. Engelbrecht, S. Brunak, and G. von Heijne. 1997. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10:1-6.
56. Niessen, C.M., F. Hogervorst, L.H. Jaspars, A.A. de Melkar, G.O. Deiwel, E.H. Hulsman, I. Kuikman, and A. Sonnenberg. 1994. The alpha 6 beta 4 integrin is a receptor for both laminin and kalinin. Exp. Cell Res. 211:360-367.
57. Noakes, P.G., M. Gautam, J. Mudd, J.R. Sanes, and J.P. Merlie. 1995. Aberrant differentiation of neuromuscular junctions in mice lacking s-laminin/laminin beta 2. Nature. 374:258-262.
58. Pall, E., K. Bolton, and J. Ervasti. 1996. Differential heparin inhibition of skeletal muscle alpha-dystroglycan binding to laminins. J. Biol. Chem. 271:3817-3821.
59. Pikkarainen, T., R. Eddy, Y. Fukushima, M. Byers, T. Shows, T. Pihlajaniemi, M. Saraste, and K. Tryggvason. 1987. Human laminin B1 chain. A multidomain protein with gene (LAMB1) locus in the q22 region of chromosome 7. J. Biol. Chem. 262:10454-10462.
60. Pikkarainen, T., T. Kallunki, and K. Tryggvason. 1988. Human laminin B2 chain. Comparison of the complete amino acid sequence with the B1 chain reveals variability in sequence homology between different structural domains. J. Biol. Chem. 263:6751-6758.
61. Poschl, E., J.W. Fox, D. Block, U. Mayer, and R. Timpl. 1994. Two non-contiguous regions contribute to nidogen binding to a single EGF-like motif of the laminin gamma 1 chain. EMBO (Eur. Mol. Biol. Organ.) J. 13:3741-3747.
62. Poschl, E., U. Mayer, J. Stetefeld, R. Baumgartner, T. Holak, R. Huber, and R. Timpl. 1996. Site-directed mutagenesis and structural interpretation of the nidogen binding site of the laminin gamma 1 chain. EMBO (Eur. Mol. Biol. Organ.) J. 15:5154-5159.
63. Reinhardt, D., K. Mann, R. Nischt, J.W. Fox, M.L. Chu, T. Krieg, and R. Timpl. 1993. Mapping of nidogen binding sites for collagen type IV. heparan sulfate proteoglycan, and zinc. J. Biol. Chem. 268:10881-10887.
64. Rousselle, P., R. Golbik, M. van der Rest, and M. Aumailley. 1995. Structural requirement for cell adhesion to kalinin (laminin-5). J. Biol. Chem. 270: 13766-13770.
65. Rousselle, P., D.R. Keene, F. Ruggiero, M.F. Champliaud, M. Rest, and R.E. Burgeson. 1997. Laminin 5 hinds the NC-1 domain of type VII collagen. J Cell Biol. 138:719-728.
66. Ryan, M.C., R. Tizard, D.R. VanDevanter, and W.G. Carter. 1994. Cloning of the LamA3 gene encoding the alpha 3 chain of the adhesive ligand epiligrin. Expression in wound repair. J. Biol. Chem. 269:22779-22787.
67. Sugiyama, S., A. Utani, S. Yamada, C.A. Kozak, and Y. Yamada. 1995. Cloning and expression of the mouse laminin gamma 2 (B2t) chain, a subunit of epithelial cell laminin. Eur. J. Biochem. 228:120-128.
68. Tian, M., T. Hagg, N. Denisova, B. Knusel, E. Engvall, and M. Jucker. 1997. Laminin-alpha2 chain-tike antigens in CNS dendritic spines. Brain Res. 764: 28-38.
69. Tian, M., C. Jacobson, S.H. Gee, K.P. Campbell, S. Carbonetto, and M. Jucker. 1996. Dystroglycan in the cerebellum is a laminin alpha 2-chain binding protein at the glial-vascular interface and is expressed in Purkinje cells. Eur. J. Neurosci. 8:2739-2747.
70. Toti, P., C. De Felice, A. Malandrini, T. Megha, C. Cardone, and M. Villanova. 1997. Localization of laminin chains in the human retina: possible implications for congenital muscular dystrophy associated with alpha 2-chain of laminin deficiency. Neuromuscular Disorders. 7:21-25.
71. Verrando. P., B.L. Hsi, C.J. Yen, A. Pisani, N. Serieys, and J.P. Ortonne. 1987. Monoclonal antibody GB3, a new probe for the study of human basement membranes and hemidesmosomes. Exp. Cell Res. 170:116-128.
72. Vuolteenaho, R., M. Nissinen, K. Sainio, M. Byers, R. Eddy, H. Hirvonen, T.B. Shows, H. Sariola, E. Engvall, and K. Tryggvason. 1994. Human laminin M chain (merosin): complete primary structure, chromosomal assignment, and expression of the M and A chain in human fetal tissues. J. Cell Biol. 124: 381-394.
73. Wewer, U., and E. Engvall. 1996. Merosin/laminin-2 and muscular dystrophy. Neuromuscular Disorders. 6:409-418.
74. Wewer, U.M., D.R. Gerecke, M.E. Durkin, K.S. Kurtz, M.G. Mattei, M.F. Champliaud, R.E. Burgeson, and R. Albrechtsen. 1994. Human beta 2 chain of laminin (formerly S chain): cDNA cloning, chromosomal localization, and expression in carcinomas. Genomics. 24:243-252.
75. Xu, H., X.R. Wu, U.M. Wewer, and E. Engvall. 1994. Murine muscular dystrophy caused by a mutation in the laminin alpha 2 (Lama2) gene. Nat. Genet. 8:297-302.
76. Yamamoto, T., N. Shibata, M. Kanazawa, M. Kobayashi, T. Komori, K. Ikeya, E. Kondo, K. Saito, and M. Osawa. 1997. Localization of laminin subunits in the central nervous system in Fukuyama congenital muscular dystrophy: an immunohistochemical investigation. Acta Neuropathol. 94:173-179.
77. Ybot-Gonzalez, P., S. Runswick, N. Smyth, and D. Edgar. 1995. Regulated expression of a novel laminin beta subunit during the development of the chick embryo. Differentiation. 59:215-223.
78. Yurchenco, P.D., and Y.S. Cheng. 1993. Self-assembly and calcium-binding sites in laminin. A three-arm interaction model. J. Biol. Chem. 268:17286-17299.
79. Yurchenco, P.D., and Y.S. Cheng. 1994. Laminin self-assembly: a three-arm interaction hypothesis for the formation of a network in basement membranes. Contrib. Nephrol. 107:47-56.
80. Yurchenco, P.D., Y.S. Cheng, and H. Colognato. 1992. Laminin forms an independent network in basement membranes [published erratum appears in J. Cell Biol. 118:493]. J. Cell Biol. 117:1119-1133.